Cyperaceae - RIO Principal - Universidad Pablo de Olavide, de Sevilla

Transcription

Dpto. Biología Molecular
e Ingeniería Bioquímica
The bipolar disjunction in biogeography:
case studies in the genus Carex
(Cyperaceae)
La disyunción bipolar en biogeografía:
casos de estudio en el género Carex
(Cyperaceae)
TESIS DOCTORAL
Tamara Villaverde Hidalgo
Sevilla, 2015
Dpto. Biología Molecular
e Ingeniería Bioquímica
The bipolar disjunction in biogeography:
case studies in the genus Carex
(Cyperaceae)
La disyunción bipolar en biogeografía:
casos de estudio en el género Carex
(Cyperaceae)
Memoria presentada por la licenciada en Biología Tamara Villaverde Hidalgo para
optar al título de Doctora en Estudios Medioambientales (Doctorado Internacional) por
la Universidad Pablo de Olavide de Sevilla.
Sevilla, Julio 2015
Directores
Dr. Modesto Luceño Garcés
Dr. Santiago Martín Bravo
Dr. Marcial Escudero Lirio
Agradecimientos
Para poder llegar hasta el volumen que tienes ahora en las manos, ha sido necesaria la
ayuda de muchas personas. Éste ha sido un camino muy duro, aunque también muy
enriquecedor, que no hubiera sido posible terminar sin las manos prestadas por los
siguientes compañeros de viaje:
Mis directores de tesis. Modesto, muchas gracias por dejarme cumplir un sueño y darme
la oportunidad de crecer profesionalmente. Hacer una tesis sin beca es una de las
situaciones más indeseables para un doctorando. Gracias por creer que merecía la pena
invertir en mí y por darme la posibilidad de estar en las aulas, ha sido una de las
experiencias más gratificantes de mi vida. Siempre te estaré agradecida. Marcial y Santi,
además de prestaros a ser mi brújula y mi mapa, habéis puesto el ímpetu y las ganas
para llegar hasta aquí. Gracias por subiros al barco, cuidarme tanto y darme vuestro
afecto. Ha sido un verdadero placer aprender a vuestro lado. Gracias de todo corazón.
Mis compañeros de laboratorio. Enrique, Inés, Jose, Marcial, Modesto, Mónica, Paco,
Pedro y Santi, sois mi familia en la UPO. Gracias por haber actuado como una válvula
de escape al estrés de la tesis, a veces, volviéndome a poner los pies en la tierra, y otras,
haciéndome reír hasta perder la respiración. He tenido mucha suerte llegando a un grupo
como el vuestro, donde siempre he contado con vuestra ayuda y cariño. ¡Gracias! Sir
Henry, me siento muy afortunada por haberte conocido y por haber encontrado en ti un
hombro (el de un gigante) en el que apoyarme durante este camino. Gracias por ser una
persona
tan
maravillosa
conmigo.
¡MagVilla’s!
También
quiero
darle
las
gracias a esos compañeros que han pasado por el laboratorio y con los que he
pasado uno buenos momentos: Carlos, Carmen, Cristina, Flo, Gloria, Laura,
Manu, Nacho, Paloma, Samuel, Víctor… y a todos los estudiantes del área de botánica
que han estado conmigo estos años.
Compañeros de otros laboratorios. Quiero darle las gracias a todo el equipo de Andrew
Hipp (The Morton Arboretum): Andrew, Bethany, Elisabeth, Marlene, grupo de
voluntarios, Elisabeth Li (biblioteca) y demás compañeros, que han hecho que mi
estancia en Chicago haya sido fabulosa. ¡Gracias por vuestra ayuda y por enseñarme
tantas cosas!
Quiero darle también las gracias a las personas que han recolectado para estos trabajos
(Leo Bruederle, Pedro Jiménez Mejías, Mihai Pusças, Wayne Sawtel, Pablo Vargas,), y
a todos los conservadores de los herbarios que nos han dado acceso a sus
colecciones. También quiero darle las gracias a Paco Rodríguez Sánchez (Estación
Biológica de Doñana – CSIC) por su ayuda y comentarios a los análisis de nicho
ecológico así como a José Luis Blanco Pastor por su ayuda con el programa Maxent.
Gracias a todos los investigadores del Canadian Museum of Nature, Jeff Saarelay
Lynn Gillespie, por ayudarme con los trabajos de morfometría y a Michel Gosselin
por facilitarme mucha bibliografía ornitológica. También a mis compañeros de
laboratorio: Anna, Jocelyn, Katia, Neda, Paul, Roger, Wayne...
Mis amigos. Tengo un grupo de cinco amigas de toda la vida a las que quiero agradecer
que siempre hayan estado, y estén, ahí. Carmen, Campano, María, Martínez y Porti,
gracias por ser mis Malvadas hermanas postizas. Llegar hasta aquí ha sido gracias a
tardes llenas de risas y sabios consejos. Tengo otro grupo de amigos que, aunque hayan
llegado un poco más tarde, son los culpables de ponerme un sonrisote y una cerveza en
la mano estos años de tesis: Cobos, Coco, Vero, Edu, Eli, Elisa, Esteban, Estrella,
Jeovani, Maite, Raquel, Rosa, Paco, compis de la carrera, compis del máster en la UPO,
compis de Toastmaster Sevilla, …
Mi familia. Tengo la familia más molona del mundo mundial. Sois mi refugio, mi
ejemplo de esfuerzo y mi inspiración diaria. Gracias por ser incondicionales y buscar los
medios, las palabras y los abrazos necesarios para animarme a perseguir mis metas en la
vida.
A mis padres.
A mis hermanos.
ÍNDICE
Abstract / Resumen …………………………………………………………… 1
Chapter 1. Introduction ……………………………………………………. 1
Biogeography ……………………………………………………………. Bipolar plant disjunctions ……………………………………………… 22
Hypothesis tested in bipolar disjunctions ……………………………… 23
Molecular markers for biogeographical studies and the need of divergence
analyses ………………………………………………………………… 28
Carex (Cyperaceae), the genus with the greatest number of bipolar
species ……………………………………………………………………. 30
Objetives by chapters …………………………………………………… 36
References ……………………………………………………………… 38
Appendix S1 ……………………………………………………………. 47
Chapter 2. Taxonomy of the Carex capitata complex………………………… 59
Abstract ………………………...……………………………………… 62
Introduction ………………………………………………………………63
Materials and methods …………………………………………..…… 64
Results …………………………………………………………….…… 68
Discussion ……………………………………………………………...... 75
References ……………………………………………………………….. 93
Appendix S1 ……………………………………………………………... 97
Additional Information ……………………………………………...…... 123
Chapter 3. Direct long-distance dispersal best explains the bipolar distribution of
Carex arctogena (Carex sect. Capituligerae, Cyperaceae) ……………………. 155
Abstract ……………………………………………………………...... 154
Introduction ……………………………………………………….....…. 154
Materials and methods ………………………………………………159
Results ………………………………………………………………….... 160
Discussion …………………………………………………………........... 162
Acknowledgements ……………………………………………………. 166
References …………………………………………………………….... 166
Appendix S1 ………………………………………………………….….. 169
Chapter 4. Long-distance dispersal during the middle–late Pleistocene explains
the bipolar disjunction of Carex maritima (Cyperaceae)……………………... 187
Abstract ………………………………………………………………... 189
Introduction ……………………………………………………………. 189
Materials and methods ………………………………………………… 190
Results …………………………………………………………………. 192
Discussion …………………………………………………………….. 195
References ……………………………………………………………... 198
Appendix S1 …………………………………………………………... 201
Appendix S2 …………………………………………………………....... 217
Chapter 5. Two independent dispersals to the Southern Hemisphere to become the
most widespread Carex bipolar species: biogeography of C. canescens Cyperaceae)
…………………………………………………………………………………… 229
Abstract …………………………………………………………………... 232
Introduction ………………………………………………………………. 234
Materials and methods ………………………………………………… 236
Results …………………………………………………………………. 240
Discussion ……………………………………………………………...... 243
References ……………………………………………………………... 248
Appendix S1 ……………………………………………………………... 261
Appendix S2 ……………………………………………………………... 275
Capítulo 6. Discussion and conclusions ……………………………………….. 283
Carex arctogena is a bipolar species …………………………………….. 285
Geological and climatic changes since the Miocene that allowed Northern and
Southern…………………………………………………………………... 292
Direct long-distance dispersal vs. mountain-hopping …………………. 296
North to South long-distance dispersal ………………………………... 297
Means of dispersal ……………………………………………………….. 300
Successful establishment after dispersal in Carex bipolar species………. 305
Conclusions ………………………………………………………………. 308
References ………………………………………………………………... 31 0
Abstract
At a global level, one of the most fascinating plant distribution patterns is the bipolar
disjunction. Bipolar species are defined here as species occurring at very high latitudes
(>55ºN and >52ºS) in both hemispheres, regardless of their distribution in intermediate
areas. Under these criteria, around 30 vascular plant species have such distribution,
being Carex (Cyperaceae) the genus with the largest number of bipolar species (six).
We performed a biogeographic study on three of them (C. arctogena, C. maritima and
C. canescens), based on morphological, molecular and bioclimatic data to shed light on
the origin of their bipolar distribution. The four traditional hypotheses accounting for
this pattern were tested: vicariance, direct long-distance dispersal, mountain hopping
and convergence / parallel evolution. Methods used to accomplish this objective include
molecular phylogenetic and phylogeographic analyses, divergence time estimation
analyses, uni- and multivariate morphometric analyses, and species niche modelling.
The low levels of genetic differentiation found between populations of both Hemisphere
and relatively recent times of diversification allow rejecting all but the long-distance
dispersal hypothesis (including direct long distance dispersal and mountain hopping) for
the studied Carex bipolar species. The studied species probably migrated from the
Northern Hemisphere to the Southern Hemisphere. In the case of C. canescens, two
independent dispersal events were needed to achieve its current distribution.
Resumen
A nivel global, uno de los patrones de distribución más fascinantes corresponde a la
disyunción bipolar. Las especies bipolares se definen en este trabajo como aquellas que
se distribuyen a muy altas latitudes (>55ºN y >52ºS) en ambos hemisferios,
independientemente de tener poblaciones a latitudes intermedias. Bajo estos criterios,
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aproximadamente 30 especies de plantas vasculares presentan esta distribución, siendo
el Carex (Cyperaceae) el género con mayor número de especies bipolares (seis). Hemos
realizado un estudio biogeográfico en tres de ellas (C. arctogena, C. maritima y C.
canescens), basándonos en datos morfológicos, moleculares y bioclimáticos para
aportar evidencias sobre el origen de sus disyunciones bipolares. Testamos las cuatro
hipótesis tradicionalmente propuestas para explicar este patrón: vicarianza, dispersión
directa a larga distancia, saltos entre montañas, y evolución paralela o convergente. Los
métodos usados para alcanzar este objetivo incluyen análisis moleculares filogéneticos y
filogeográficos, análisis de estimación de tiempos de divergencia, análisis
morfométricos uni- y multivariables, y modelización de nicho. Los bajos niveles de
diferenciación genética encontrados entre las poblaciones de ambos hemisferios, así
como los relativos recientes tiempos de diversificación de las especies estudiadas nos
permiten rechazar todas las hipótesis excepto la dispersión a larga distancia (incluyendo
dispersión directa y por salto de montañas). Las especies estudiadas probablemente
migraron del Hemisferio Norte al Hemisferio Sur. En el caso de C. canescens, dos
eventos de dispersión independientes fueron necesarios para alcanzar su distribución
actual.
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Chapter 1
Introduction
17
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Chapter 1. Introduction
Introduction
Biogeography
Darwin (1809 – 1882; 1859, p.1) begins the Origin of the Species concerned about the
information that could be gathered from the historical and geographical distribution of
organisms in the light of his theory. Distribution was an important dimension of Darwin’s
theory of evolution: “When on board of H.M.S. Beagle, as a naturalist, I was much struck
with certain facts in the distribution of the inhabitants of South America, and in the
geological relations of the present to the past inhabitants of that continent. These facts
seemed to me to throw some light on the origin of species”. He did not only find dispersal as
the most plausible explanation for the distribution of organisms [“ …the view of each species
having produced in one area alone, and having subsequently migrated from that area as far
as its power of migration and subsistence under past and present conditions permitted, is the
most probable” (Darwin, 1859, p. 353)], but he also highlighted it as a key element shaping
species range [“…all the grand leading factors of geographical distribution are explicable
on the theory of migration (generally of the more dominant forms of life), together with
subsequent modification and the multiplication of forms. We can then understand that high
importance of barriers, whether of land or water, which separate our several zoological and
botanical provinces” (Darwin, 1859, p. 409)]. He devoted two out of 15 chapters of the
Origin of the Species to the study of the distribution of taxa over geographic space and time,
this is, to biogeography. Therefore, biogeography may be understood as a key element on
Darwin’s theory of evolution. He emphasized three points: (1) barriers to migration allowed
time for the slow process of modification through natural selection; (2) the concept of single
centres of creation was critical; that is, each species was first originated in a single area only,
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and from that centre it would extend as far as its colonization ability would permit; (3)
dispersal was a phenomenon of overall importance.
Alexander von Humboldt (1769 – 1859), often recognized as the father of plant biogeography
(Brown and Lomolino, 1998), and many other illustrious researchers such as Alfred Wallace
(1823 – 1913) or, more recently, Robert MacArthur (1930 – 1972) and Edward Wilson (1929
–) were captivated by this discipline. It started as a descriptive science, mapping the major
vegetation types and their associated fauna, then adding diversity patterns along different
gradients (e.g. latitudinal or elevation) to finally become a multidisciplinary science that links
fields such as systematics, ecology, paleontology or climatology (Morrone, 2009). It has
allowed the designation of the biogeographic realms – those areas into which the Earth can be
divided given the distinct characteristics of flora and fauna found in each area (Figure 1).
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◄ Figure 1. Biogeographical kingdoms and regions of the world from Morrone (2002). 1–2,
Holarctic kingdom (= Laurasia): 1, Nearctic region; 2, Palaearctic region; 3–6, Holotropical
kingdom (= eastern Gondwana): 3, Neotropical region; 4, Afrotropical region; 5, Oriental
region; 6, Australotropical region. 7–12: Austral kingdom (= western Gondwana): 7, Andean
region; 8, Cape or Afrotemperate region; 9, Antarctic region; 10, Neoguinean region; 11,
Australotemperate region; 12, Neozelandic region.
Biogeography may be considered either a synthetic (Brown & Lomolino, 2011) or an
interdisciplinary (Morrone, 2009, Figure 2) discipline, and for this reason, biogeography is
regarded as heterogeneous in its principles and methods, lacking the conceptual unity of other
sciences (Morrone, 2009). Biogeography is divided in two categories: ecological and
historical biogeography (Sanmartín, 2012).
◄ Figure 2. Interdisciplinary
situation of biogeography, at
the intersection of 6 different
disciplines
(modified
from
Morrone, 2009).
Ecological biogeography is concerned with ecological processes occurring over short
temporal and small spatial scales (Myers and Gillers, 1988). In contrast, when dealing with
evolutionary processes that concerns large time scales (i.e. millions of years) and large or
global geographic scales, we run into historical biogeography (Crisci, 2001). Historical
biogeography attempts to reconstruct the origin of taxa, this is, it addresses the how, when,
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and why of species distributions (Jablonski et al., 1985). It is concerned about taxa’s
sequences of dispersal, isolation, and extinction; and to explain how geological events have
shaped their present-day distribution (Myers & Giller, 1988). Important questions are why a
taxon is absent from apparently suitable areas beyond its present range, and how taxa have
become spatially separated or disjunct (Giller et al., 2004). It is hypothesized that such
patterns can be naturally caused by the break-up of a once continuous range (vicariance), by
long-distance dispersal, or through independent origins of the taxon in two or more places
(parallelism or convergence). If we level down to microevolution, we encounter
phylogeography, which concentrates on the geographic distribution of genealogical lineages,
especially those within and among closely related taxa (Avise, 2000). At this level, the
coalescence theory help to model genealogies within populations; in population genetics, it is
applied to several individuals sampled from one population whereas in phylogenetics, only
one individual is often sampled per population (as individuals from the same population are
usually assumed to be genetically similar compared to the differences that exist among
populations or species, Degnan & Rosenberg, 2009).
Bipolar plant disjunctions
Disjunct distribution of species is defined as any discontinuous distribution in which some
parts of the species (or taxa) range are clearly separated from another part (Morrone, 2009).
One of the most fascinating plant distribution patterns concerning the Southern Hemisphere
encompasses the bipolar disjunction. Bipolar species are defined in this work as species
growing at very high latitudes (>55ºN and >52ºS) in both hemispheres, regardless of their
distribution in intermediate areas (Moore & Chater, 1971). Under these criteria, there are only
around 30 vascular plant species from 12 families that could be considered bipolar (Appendix
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S1). Species circumscription in some of these cases are still poorly understood, therefore,
some of them might leave this list after a taxonomic revision, whereas some other might join
it after we gain a broader taxonomic knowledge on the Floras of both hemispheres. From the
compilation of bipolar species by Moore & Chater (1971), there are currently at least seven
species whose bipolar distribution is suspected to have an anthropogenic origin in one of the
Hemispheres (Appendix S1).
The families with the largest number of bipolar species are Poaceae Barnhart (8 species,
26.7%) and Cyperaceae Juss. (6 species, 20%); and the genus with the greatest number of
bipolar species is Carex L. (6 species, 20%; Appendix S1). The majority of the bipolar
species lacks molecular studies comparing Northern and Southern Hemisphere populations.
With the exception of the Carex bipolar species, none of the molecular studies concerning the
remaining species have addressed specifically their bipolar distribution. The following
studies have included at least one population from both hemispheres: Hymenophyllum
tunbrigense (L.) Sm. (Hennequin et al., 2010), Anemone multifida Poir (Ehrendorfer et al.,
2009; Mlinarec et al., 2012), Triglochin palustre L. (von Mering, 2013), Avenella flexuosa
(L.) Dejer (it might be an introduction in South America; Chiapella, 2007) and Phleum
alpinum L. (Boudko, 2014; see Appendix S1 for more details). Thus, these works could serve
as a background to conduct more specific studies addressing the various hypotheses tested in
bipolar distribution.
Hypothesis tested in bipolar disjunctions
Four hypotheses have historically been put forward to account for bipolar disjunctions: (1)
stepwise long-distance dispersal across the equator and via mountain ranges (‘mountainhopping’; (Raven, 1963; Moore & Chater, 1971; Ball, 1990; Heide, 2002; Vollan et al.,
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2006); (2) direct long-distance seed dispersal by birds, wind and/or ocean currents (Cruden,
1966; Muñoz et al., 2004; Nathan et al., 2008); (3) vicariance (Du Rietz, 1940), which
implies a continuous distribution fragmentation dating back to the trans-tropical highland
bridges during the Mesozoic Era (from the early Jurassic, 195 Ma; Scotese et al., 1988); and
lastly, (4) convergent or parallel evolution of the disjunct populations (Scotland, 2011).
Long-distance dispersal
Darwin was so convinced by the hypothesis of migration over long-distances to account for
species distributions, that he undertook a series of experiments to prove it (Darwin, 1859).
Since Darwin, the effectiveness of long-distance methods of seed dispersal has been
documented broadly (e.g. Murray, 1986; De Queiroz, 2005; Nogales et al., 2012; Vargas et
al., 2012). Seed dispersion patterns near sources can be qualitatively different from those far
from sources, because dispersal processes can operate over different ranges of distances
(Nathan & Muller-Landau, 2000). Seed density around a mother plant almost invariably
declines leptokurtically with distance (being more concentrated about the mean than the
corresponding normal distribution), with an extended tail of long-distance dispersal (Harper,
1977; Willson, 1993; Nathan & Muller-Landau, 2000). The limited distances that most seeds
travel are well documented for plants of all growth forms (e.g. Harper, 1977; Howe &
Smallwood, 1982; Willson, 1993a; Cain et al., 1998). Empirical data is mostly acquired for
short-distance events than for rare long-distance dispersal events, due to the difficulty of
sampling the latter (Nathan and Muller-Landau, 2000). However, short-distance dispersals
cannot explain some observed patterns of genetic structure (Cain et al., 2000) or range
expansion rates (Clark, 1998) and therefore, long-distance dispersal deserve its own sampling
effort.
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Typically, several dispersal agents are involved in long-distance dispersal (Gillespie et al.,
2012), as Darwin suggested. Therefore, their seed shadows - the spatial distribution of seeds
dispersed from a single plant (Nathan and Muller Landau, 2000)- are determined by the
combined effects of displacement by all dispersal agents that move seeds from the parent
plant (primary dispersal) or from subsequent locations (secondary dispersal). Wind current
characteristics can be used to explain wind dispersal (e.g. distribution of plants in the
Southern Hemisphere might be affected by the West Wind Drift, Sanmartín et al., 2007, and
references therein); however, animal behaviour, which could depend upon many variables
(e.g. abundances and characteristics of alternate food sources, competing species and
predators), is typically more complex and it limits the understanding of zoochory (Nathan and
Muller-Landau, 2000). For instance, among the birds that void or defecate viable seeds, the
attributes that most influence seed dispersal are behavioural rather than morphological or
physiological (e.g. Howe & Estabrook, 1977; Herrera, 1984a, 1984b). Some authors (Ouborg
et al., 1999; Cain et al., 2000) have emphasized the potential of genetic methods that can
provide evidence of long-distance gene flow, either by comparing the genotypes of seedlings
with potential parents or by examining genetic structure within and among populations
(Ouborg et al., 1999; Jordano & Godoy, 2000). Le Corre et al. (1997) showed that longdistance dispersal events influence the genetic differentiation of populations, leaving a
genetic signature that could persist for long periods of time. Moreover, it has been recently
showed that DNA barcoding can help to identify the source plant of the dispersed seeds and
the frugivore species that contribute to each dispersal event (González-Varo et al., 2014),
which has an extraordinary potential for characterizing long-distance dispersal in plants.
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Direct vs. mountain-hopping long-distance dispersal
The main difference between direct and mountain-hopping long distance dispersal of plants is
the number of “way stations” made before reaching the end of the dispersal process. In the
bipolar disjunction, direct long-distance dispersal implies that the taxa have been carried from
its source in one side of the disjunction to the other, without any stop between these areas.
The mountain-hopping hypothesis (Ball, 1990) proposes a long-distance, stepwise migration
of these taxa using mountains peaks as stepping-stones to cross the tropics. Means of
dispersal in direct long-distance dispersal events could be the same as in mountain-hopping
ones.
Vicariance
Vicariance is defined as the splitting of the continuous geographical range of a group into two
or more parts by the development of some sort of barrier (or barriers) to dispersal (de
Queiroz, 2005). The fossil record can be used to evaluate vicariance and dispersal hypotheses
by dating lineage divergences (nodes). In dated phylogenetic reconstructions, we encounter
two categories of results: (1) a particular evolutionary branching point is estimated to be as
old as or older than the fragmentation event in question, that node is supporting a vicariant
event; (2) a branching point is estimated to be younger than the fragmentation event, then, it
is supporting long-distance dispersal. The biogeographic history of the Southern Hemisphere
is considered a prime example of the vicariance scenario (Sanmartín & Ronquist, 2004). The
disjunct trans-Pacific distributions have been proposed to stem from the sequential breakup of
the southern supercontinent Gondwana during the last 165 million years. This hypothesis has
been long tested in angiosperm groups with Southern Hemisphere distributions (reviewed in
Beaulieu et al., 2013) and it has been supported in some plant groups [e.g. in the genus
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Gunnera (Gunneraceae), Wanntorp & Wanntorp, 2003; in the family Myrtaceae, Sytsma et
al., 2004]. Although dispersal and vicariance are often considered competing hypotheses in
biogeography (Sanmartín and Ronquist, 2004), both are usually claimed to explain Southern
Hemisphere plant distribution (e.g. Nothofagus, Knapp et al., 2005). For bipolar species, we
consider the fragmentation of a continuous distribution dating back to the trans-tropical
highland bridges during the Mesozoic Era (from the early Jurassic, 195-200 Ma; Scotese et
al., 1988; Figure 3). During this time, bipolar species could have had a continuous
distribution from high latitudes in the Northern Hemisphere to high latitudes in the Southern
Hemisphere.
Figure 3. Landmasses in the early Jurassic (ca. 200 Ma; photo taken from Scotese (2004).
After an episode of igneous activity along the east coast of North America and the northwest
coast of Africa, the central Atlantic Ocean opened as North America moved to the northwest.
This movement also gave rise to the Gulf of Mexico as North America moved away from
South America (Scotese, 2002).
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Convergent and parallel evolution
Traditionally, ‘convergent’ has been distinguished from ‘parallel’ evolution as the first
assumes that when a given phenotype evolves, the underlying genetic mechanisms are
different in distantly related species (convergent evolution; Haldane, 1932) but similar in
closely related species (parallel evolution; Haldane 1932). There is still a huge debate
between parallel evolution and convergence (e.g. (Wichman et al., 1999; Cooper et al., 2003;
Fong et al., 2005; Christin et al., 2007; Scotland, 2011). If we assume that homoplasy can be
seen as convergence in a broad sense, then pheonotypic homoplasy can be described as
convergence and genotypic homoplasy as parallelism (Scotland, 2011). However, Stern
(2013; and references therein) showed, on one hand, several examples where the same
phenotype (e.g. coloration in lizards) might evolve among populations within a species by
changes in different genes; on the other hand, he showed examples of similar phenotypes that
might have evolved in distantly related species by changes in the same gene. Therefore, it is
argued that ‘convergent’ and ‘parallel’ evolution represents ends of a continuum and both can
be described with a single term – convergent evolution (Stern, 2013). For bipolar taxa, we
will consider convergent or parallel evolution as synonym hypotheses that can be rejected is
taxa are retrieved as monophyletic.
Molecular markers for biogeographical studies and the need of divergence analyses
When conducting studies in biogeography, ordered markers (DNA sequences) are preferred
rather than unordered ones (e.g. AFLP, ISSR, RAPD) because the first contain records of
their own histories and provide information about genealogical relationships (e.g. Schaal &
Olsen, 2000; Schaal & Leverich, 2001).
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The chloroplast genome has a lower degree of polymorphism than the nuclear genome
(Muse, 2000), however, it can uncover a higher degree of genetic structure. In the chloroplast
genome, genetic drift occurs more rapidly than in the nuclear because it has a lower effective
population size (Louis et al., 1998); thus, genetic drift result in greater genetic differentiation
of fragmented populations, retaining molecular signal of past migrations, dispersal events and
range fragmentation (e.g. Louis et al., 1998; Newton et al., 1999; Hudson & Coyne, 2002;
Rendell & Ennos, 2003; Kadereit et al., 2005; Petit et al., 2005). This difference is due to the
uniparental inheritance of chloroplast DNA (cpDNA), which is maternally inherited in most
angiosperms (Harris & Ingram, 1991). In plant biogeographical studies, as colonization of
new habitats commonly occurs through seeds, the pattern of dispersal is unaffected by
subsequent pollen movements and may be traced with cpDNA markers (Petit et al., 2003).
Moreover, the chloroplast genome is represented by only one DNA molecule where
recombination processes are scarce. Conversely, nuclear markers may contain multiple
different regions of the nuclear genome with more frequent recombination events between
those regions. Therefore, nuclear markers are generally more useful for exploring the recent
history of taxa and gene flow patterns of species (Harpending et al., 1998).
Finally, next-generation sequencing techniques (e.g. restriction-site associated DNA; Baird et
al., 2008) are now being used in biogeographic studies (e.g. Emerson et al., 2010; Lexer et
al., 2013).
Divergence time analysis and the use of local molecular clocks is now a basic tool in
biogeography (Givnish & Renner, 2004). It has allowed to test different hypothesis in plant
disjunctions (e.g. Winkworth et al., 2002; Sytsma et al., 2004; Wen & Ickert-Bond, 2009; Nie
et al., 2012) and discern between dispersal or vicariance, the two main hypotheses tested in
biogeography, in many different groups of angiosperms (e.g. Malpighiaceae, Davis et al.,
2002; Moraceae, Zerega et al., 2005; Ephedra, Ickert-Bond et al., 2009). These studies are
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typically supported by fossil records which are ideal to estimate the ages of lineages (acting
as calibration points) and to support their presence in particular places (Renner, 2005).
However, there are many plant groups lacking reliable fossil records and, therefore,
secondary calibrations are broadly used (e.g. (Valente et al., 2011; Fernández-Mendoza &
Printzen, 2013; Pimentel et al., 2013; Inda et al., 2014). In the case of bipolar species,
divergence time estimates can help to elucidate between the different hypotheses tested.
Carex (Cyperaceae), the genus with the greatest number of bipolar species
One of the families with the largest number of bipolar species is the Cyperaceae. The sedge
family is also among the largest families of flowering plants, occurring on all continents,
except Antarctica. It comprises approximately 104 genera, 14 tribes and 5,400 species
(Goetghebeur, 1996) making it the 7th or 8th largest angiosperm family and the third largest
monocot family after orchids (Orchidaceae Juss.) and grasses (Poaceae). Its species occur in a
great diversity of habitats, ranging from deserts to rainforests (Reznicek, 2011), although they
are predominantly found in wetland habitats such as littoral communities, peat-lands and wet
meadows. Although its economic significance is often at a regional or local level (Simpson &
Inglis, 2001), approximately 10% of its species are used by humanity for food (Chinese water
chestnut, Eleocharis dulcis (Burm.) f. Trin. ex Henschel, or the yellow nut sedge, Cyperus
esculentus L.); for pasture (Carex lyngbyei Hornem.); for construction (Schoenoplectus
californicus (C.A. Mey) Palla); as an elixir (Carex arenaria L.); and even for making paper
(Cyperus papyrus L.), whereas other sedge species, such as Cyperus rotundus L., C.
esculentus L., C. difformis or Fimbristylis miliacea L. are considered to be serious weeds due
to their negative effect on agriculture (Brayson & Carter, 2008).
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Sedge flowers are highly small and evolutionary reduced in size typically with the perianth
lacking or reduced to either bristles or scales. In Carex, a modified bract in the female flower
surrounds the naked gynoecium, enclosing the pistil and later the achene, in a sac-like
structure (Blaser, 1944); known as utricle or perigynium. The flowers are arranged in
structures known as spikelets with the inflorescence consisting of one or many spikelets
arranged on one or more axes. Approximately 40% of all sedge species (ca. 2100 spp.) are
grouped in the cosmopolitan tribe Cariceae Kunth ex Dumort., which has been suggested by
most studies to be sister to tribe Scirpeae or nested within it (e.g. Muasya & Simpson, 1998;
Muasya et al., 2009; Escudero & Hipp, 2013; Hinchliff & Roalson, 2013; Jung & Choi, 2013;
Léveillé-bourret et al., 2014). (Waterway and Starr (2007), using DNA from both nuclear and
plastid genomes, revealed three major clades within Cariceae that roughly corresponded to:
(1) subgenus Vignea, hence named Vignea clade; (2) subgenera Carex and Vigneastra,
named the Core Carex clade; and (3) most unispicate Carex species plus Cymophyllus,
Kobresia, Schoenoxiphium, and Uncinia, named the Caricoid clade (Figure 3). Later on,
Waterway et al., (2009) found that section Siderostictae Franch. ex Ohwi, traditionally
classified in subgenus Carex, formed, together with the Hypolytroides clade (Starr et al.,
2015), a clade sister to all other species in tribe Cariceae; it confirmed that Carex was a
paraphyletic group with all other genera of tribe Cariceae nested within it. For these reasons,
it has been recently agreed by the (Global Carex Group, 2015) to consider a new broader
circumscription of Carex, changing its classification by unifying all genera within it.
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Figure 4. Generalized phylogenetic tree of Cyperaceae tribe Cariceae based on molecular
phylogenetic studies to date (modified from Global Carex Group, 2015). Solid lines show
relationships that are supported by all or most studies; dotted branches show relationships
that are frequently seen but more inconsistent among studies; branches with consistently high
boostrap support are indicated with a grey filled circle.
Therefore, the cosmopolitan genus Carex, the most diverse angiosperm genus of the northern
temperate zone (Escudero et al., 2012b) is the largest genus in the family and it is also one of
the most taxonomically difficult (Starr & Ford, 2009) due to its complex and extremely
reduced morphology. Different potential drivers of diversification have been proposed to
contribute to the extraordinary diversity of Carex [e.g. self-compatibility and high selfing
32
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rates (Arens et al., 2005; Friedman & Barrett, 2009; Escudero et al., 2010b) or chromosome
differentiation (Whitkus, 1988; Hipp, 2007; Escudero et al., 2010b, 2012a, 2012b, 2013a,
2013b; Hipp et al., 2010; Jiménez-Mejías et al., 2012)].
A comprehensive, global taxonomic treatment of the genus is still lacking, and new species
continue to be described. Thus, in the last 20 years, the discovery rate of new Carex species
in North America has been, on average, two per year (Starr & Ford, 2008), which seems to be
a trend that has not yet reached a plateau.
There are six bipolar Carex species (Figure 5): Carex arctogena Harry Sm., C. canescens L.,
C. macloviana D’Urv., C. magellanica Lam., C. maritima Gunn. and C. microglochin
Wahlenb. These species are placed in different lineages within the genus. In the clade
Caricoid, there is C. arctogena and C. microglochin; in the Vignea clade, C. canescens, C.
macloviana, C. maritima; and in the core Carex clade, C. magellanica. Therefore, this
extraordinary geographic disjunction seems to have been achieved independently by Carex
species from different evolutionary lineages. None of this species but C. microglochin present
specialized dispersal devices (a ‘hook’ used for ectozoochory; Savile, 1972); however, it has
been proved that, for instance, epizoic dispersal occurs in other Carex species without having
evident morphological features for it (reviewed in Allessio Leck & Schütz, 2005).
Carex bipolar species generally have a circumboreal distribution and are limited to austral
latitudes in South America (>52º; Figure 5). An exception is C. canescens (sect. Glareosae
G. Don), the single bipolar Carex species that reaches not only the southernmost region of
South America (Tierra del Fuego and Falkland Islands) but also Oceania (including Australia,
Tasmania and New Guinea; Figure 1 and Appendix S1), occurring within five
biogeographical regions (Nearctic, Palearctic, Andean, Neoguinean and Australotemperate;
Morrone, 2002). Carex canescens is therefore the bipolar Carex species with the widest
33
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distribution followed by C. maritima, which has a circumboreal distribution including the
European Alps and the Himalayas in the Northern Hemisphere, while in the Southern
Hemisphere it is distributed from Ecuador to Patagonia (Govaerts et al., 2014).
All species but C. arctogena were studied molecularly by Vollan et al. (2006) and Escudero
et al. (2010a), although with a limited sampling. Both studies found low levels of genetic
differentiation between populations from different Hemispheres, suggesting that either
mountain-hopping or direct long-distance dispersal was the best explanation for the species’
current distributions. However, neither Vollan et al. (2006) nor Escudero et al. (2010) could
determine definitively which hypothesis best explained the distributions of bipolar species.
34
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Figure 5. Distribution maps of the six bipolar Carex species. (a) Carex arctogena; (b) C.
canescens; (c) C. macloviana; (d) C. magellanica; (e) C. marítima; and (f) C. microglochin.
The dark grey regions indicate the distribution obtained from the World Checklist of Selected
Plant Families (http://apps.kew.org/wcsp).
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Objectives by chapters
1. The main goal of Chapter 2 was to resolve taxonomic problems within the C. capitata
complex, especially in relation to the status of the different taxa described within this
complex. Morphological, micromorphological, ecological and geographical data are
studied using more than 450 herbarium specimens.
2. The goal of Chapter 3 was to determine which of the four classic hypotheses used to
account for bipolar taxa could best explain the distribution of C. arctogena. By
evaluating the combined evidence provided by phylogenetic reconstructions and
molecular dating based on nuclear and plastid data together with bioclimatic data
through species’ distribution, biogeographical hypotheses were tested, improving our
understanding of the historical events that promoted the formation of the bipolar
disjunction seen in C. arctogena.
3. The aim of Chapter 4 was to explain the bipolar distribution of C. maritima.
Specifically, the aims were: (i) to clarify the direction of the dispersal (north-to-south
or south-to-north); (ii) in the case of genetic structure, to estimate the timing of
dispersal; and (iii) to test mountain-hopping and direct long-dispersal hypotheses, as
well as the relationship of C. maritima with biotic and abiotic factors that could
explain the bipolar distribution. In order to accomplish this task data on nuclear and
plastid molecular markers and bioclimatic data were combined. Carex maritima
populations were analysed phylogenetic, phylogeographically and ecologically
through its distribution.
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4. The aims of Chapter 5 were to: (i) test the various hypotheses accounting for the
bipolar disjunction of C. canescens; and (ii) to determine whether C. canescens
migrated twice to the Southern Hemisphere or was dispersed from South America to
Australia or vice versa. Phylogenetic reconstructions and phylogeographical analyses
(based on nuclear and plastid regions) as well as bioclimatic data were evaluated in
the total distribution of the species.
5.
In Chapter 6, the objectives were to: (i) to review the hypotheses tested in bipolar
distribution; (ii) to infer the most common direction of dispersal in bipolar species;
(iii) to discuss about the possible means of dispersal that could have promoted bipolar
distribution; and (iv) to highlight the possible characteristics of the bipolar species
that have made them successful in establishment after dispersal.
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Appendix S1
47
Polygonaceae
Koenigia islandica
L.
48
North America and southern South America
(Argentina, Chile); northern Europe; Central
Widespread in the temperate regions of both
hemispheres (Hnatiuk, 1972; Marticorena et al.,
2001; Roux, 2001), Africa (Kenia, South
Africa, Tanzania, Uganda and Marion and
Prince Edward Islands), Australia, South
America and Europe.
Western and Southern Europe, Macaronesia
(Sánchez-Velázquez, 2003), Africa (Gabon,
Kenya, Malawi, Tanzania, Mozambique, South
Africa, Swaziland, Zimbabwe, Madagascar and
Mauritius; Roux, 2001), New Zealand, Central
and South America, Jamaica and in a single
locality in North America (South Carolina;
Farrar, 1993).
Hymenophyllaceae Hymenophyllum
tunbrigense (L.) Sm.
Hymenophyllum
peltatum (Poir.)
Desv.
Northern Hemisphere (North America and
Eurasia), Macaronesia, Australia, Tasmania and
New Zealand (Villar, 1968).
Huperzia selago (L.)
Bernh. ex Schrank &
Mart.
Lycopodiaceae
Distribution
Species
Family
There are no molecular works comparing
populations from both hemispheres.
Larsen et al. (2013) showed genetic differences
only between Southern hemisphere populations.
Therefore, a worldwide study is needed.
Although there is uncertainty about the
circumscription of its populations in Asia,
Mexico, Central and South America (Richards &
Evans, 1972; Farrar, 1993), Hennequin et al.
(2010) showed that Chilean and Tanzanian
populations differed genetically from the
European ones (Asian or Central American
populations were not included).
populations from both hemispheres. A
worldwide taxonomic study is needed due to its
contrasting treatment in different floras (Aiken
et al., 2007)
Status
Appendix S1. Bipolar species list from Moore & Chater (1971). Monocot species distributions have been obtained from Goaverts et al. (2014;
http://apps.kew.org/wcsp/ 2015-05-20.); otherwise, noted.
________________________________________________________________
Chapter 1. ________________________________________________________________
Introduction
Caryophyllaceae
Temperate regions of North and South America
(Moore 1983; Pedersen 1984; Wagstaff and
Taylor 1988; Hoffmann et al. 1997). In southern
South America, it has been described as exotic
and introduced (Brion et al. 1988; Volponi
1990, 1999).
Europe, North of Africa, Southwest Asia,
Macaronesia, South Africa and South America
(Styles, 1962; Zuloaga et al., 2008).
populations from both hemispheres. It is a
morphological complex taxon [treated as several
subspecies in Europe (Tutin et al. 1993); several
forms associated with differences in geographic
distribution in North America (Hitchcock et al.
1977); and it has also been considered as
extremely polymorphic in southern South
America (Moore 1983; Pedersen 1984; Volponi
1990, 1999)]. Although Quiroga et al. (2002)
showed morphological and genetic differences in
the southern Andes populations and suggested
ecotypic variation due to climatic changes
during the Pleistocene, there are no molecular
works supporting this assumption between
hemispheres. Therefore, a worldwide study is
needed.
49
Honckenya peploides Coastal North America and Eurasia. Its
(L.) Ehrh.
distribution in the Southern Hemisphere might
be the result of anthropochorus origin (SánchezVilas, 2007).
Cerastium arvense
L.
Polygonum
maritimum L.
and East Asia (Packer & Freeman, 2005).
________________________________________________________________
Chapter 1. ________________________________________________________________
Introduction
Ranunculaceae
North and southern South America.
Anemone multifida
Poir.
50
Native in the Holarctic; introduced in the
Southern Hemisphere (Cook, 1963;
Whittemore, 1997; Ruiz, 2001; Eichler &
Jeanes, 2007; Lumbreras et al., 2011).
Originally from Europe, it has been introduced
in North America (including Mexico), Central
America (Costa Rica, Guatemala) and South
America (Bolivia and southern Argentina) as
well as in western Asia (Siberia) and Antarctica
(sub-Antarctic Islands; Crow, 2005). It has
invaded 14 out of 22 southern Oceanic Islands
(Shaw et al., 2011) and its eradication in some
of them is been considered (Cooper et al.,
2011).
Ranunculus aquatilis
L.
Sagina procumbens
L.
There are great morphological differences across
its distribution (Hoot et al., 1994). The genetic
differences found between northern and southern
hemispheres (Enhendorfer et al., 2009) might be
the result of an ancestral hybridization and
subsequent polyploidization (Meyer et al.,
2010). It has been hypothesized a migration
from North America to South America during
the Quaternary (Mlinarec et al., 2012). In the
northern hemisphere, allopolyploids were
detected (Hoot et al., 2012; Mlinarec et al.,
2012) as well as a high genetic variability
between alpine vs. lowland ecotypes (McEwen
________________________________________________________________
Chapter 1. ________________________________________________________________
Introduction
Gentiana prostrata
Gentianaceae
51
North America, South America and Eurasia
Predominantly Holarctic and southern South
America (Patagonia)
North America, southern South America and
Australia (Elven et al., 2012).
Hippuris vulgaris L.
Armeria maritima
(Mill.) Willd.
North Africa, temperate Asia, North America
and southern South America (Moore, Williams
and Yates, 1972)
Plantago maritima
L.
Plumbaginaceae
Plantaginaceae
Although it has been widely studied genetically,
ctyogenetically and molecularly (e.g. Weidema
et al., 1996; Coulaud et al., 1999; Fuertes
Aguilar & Nieto Feliner, 2003; Piñeiro et al.,
2011; Abratowska et al., 2012), there are no
molecular works comparing populations from
both hemispheres.
Although Chen et al. (2013) showed genetic
variation between populations in QinghaiTibetan Plateau (China; Chen et al., 2013), there
are no molecular works comparing populations
from both hemispheres.
et al, 2013).
________________________________________________________________
Chapter 1. ________________________________________________________________
Introduction
Temperate areas of Eurasia, North and South
America
Australia, New Zealand, Eurasia, North and
South America
Eurasia and North America; introduced in South There are no molecular works comparing
America (Giussani et al., 2012)
Eurasia, North and South America
Catabrosa aquatica
(L.) P. Beauv.
Trisetum spicatum
(L.) Richt.
Poa glauca Vahl.
Vahlodea
atropurpurea
(Wahlenb.)
Fr. ex Hartm.
[=Deschampsia
atropurpurea
(Wahlenb.) Scheele]
52
Molecular studies based on nuclear (ITS) and
chloroplast regions (rbcL and matk) revealed no
differentiation between northern and southern
hemisphere populations and its distribution is
suggested to be the result of a recent dispersal
(von Mering, 2013).
Poaceae
Temperate areas of Eurasia, North America,
South America and New Zealand.
Triglochin palustre
L.
Juncaginaceae
Australia, North and South America; possibly
introduced in Europe (Wales; Jones, 2011)
Limosella australis
R. Br.
Scrophulariaceae
Haenke
________________________________________________________________
Chapter 1. ________________________________________________________________
Introduction
Boudko (2014) showed no genetic differences
between northern and southern hemisphere
populations.
53
Subarctic and temperate regions of the Northern
Hemisphere (Eurasia and North America),
South America (Guatemala, Argentina and
Chile) and South Georgia
Phleum alpinum L.
Chiapella (2007) shows some degree of
molecular differentiation between northern and
southern hemispheres populations.
Eurasia, Africa (but introduced in Cape
Provinces) North America (introduced in
Hawaii, Aleutian Islands, Alaska, Yukon,
British Columbia, Idaho, Oregon, Washington,
Wyoming, Rhode Island, California, central
Mexico), Central America (introduced in Costa
Rica) and South America [introduced in central
and South Brazil, Trista da Acunha (UK) and
South Georgia (UK)]. Also introduced in North
and South New Zealand.
Avenella flexuosa
(L.) Drejer
[=Deschampsia
flexuosa (L.) Trin.]
Chiapella (2007) shows some degree of
molecular differentiation between northern and
southern hemispheres populations.
Calamagrostis
Temperate and subarctic Northern Hemisphere
stricta (Timm.) Koel. (North America and Eurasia) and South
America Bolivia, Peru and Patagonia)
Subarctic, temperate and tropical mountains of
Eurasia, Africa, (but introduced in Cape
Provinces and Lesotho); Australia (introduced
in South Australia), North America (introduced
in Hawaii) and South America [introduced in
Bolivia, South Brazil, West and South
Argentina, central and south Chile, Macquaire
Islands and South Georgia (UK)]
Deschampsia
cespitosa (L.) P.
Beauv.
________________________________________________________________
Chapter 1. ________________________________________________________________
Introduction
Cyperaceae
North America, Europe, Australasia and
southern South America (Patagonia)
Eurasia, North America (including Hawaii) and
South America (Bolivia, Peru, Argentina and
Chile)
Eurasia, North and South America (Patagonia)
North America, Eurasia and South America
Eurasia, North and South America (Colombia,
Ecuador, Peru, Argentina and Chile)
C. canescens L.
C. macloviana
D’Urv.
C. magellanica Lam.
C. martima Gunn.
C. microglochin
Wahlenb.
54
North America, Europe and southern South
America (Patagonia)
Carex arctogena L.
Escudero et al. (2010) showed no molecular
differences between Northern and Southern
Hemisphere populations.
Escudero et al. (2010) compared Northern and
Southern Hemisphere populations and suggested
a long-distance dispersal as the most plausible
hypothesis explaining its distribution.
Escudero et al. (2010) showed molecular
hemisphere populations and suggested that it has
obtained its distribution by long-distance
dispersal.
Escudero et al. (2010) showed no molecular
Hemisphere populations and concluded that a
long-distance dispersal as the hypothesis that
best explains its distribution.
Vollan et al. (2006) and Escudero et al. (2010)
compared Northern and Southern Hemisphere
and concluded that a long-distance dispersal as
the best hypothesis to explain its bipolar
distribution.
________________________________________________________________
Chapter 1. ________________________________________________________________
Introduction
________________________________________________________________
________________________________________________________________
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57
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________________________________________________________________
58
Chapter 2
Taxonomy of the Carex capitata
complex
59
60
________________________________________________________________
________________________________________________________________
Chapter 2. Taxonomy of the Carex capitata complex
Taxonomy of the Carex capitata complex
Tamara Villaverde1, Santiago Martín-Bravo1 and Julian R. Starr2,3
1
Botany area, Department of Molecular Biology and Biochemical Engineering, Pablo de
Olavide University, ctra. de Utrera km 1, 41013, Seville, Spain, 2Canadian Museum of
Nature, PO Box 3443, Ottawa, ON K1P 6P4, Canada, 3Department of Biology,
Gendron Hall, University of Ottawa, 30 Marie Curie, Ottawa, ON K1N 6N5, Canada.
*Correspondence: Tamara Villaverde, Botany area, Department of Molecular Biology
and Biochemical Engineering, Pablo de Olavide University, ctra. de Utrera km 1,
41013, Seville, Spain.
E-mail: [email protected]
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Abstract
Carex section Capituligerae is a small group placed in the Unispicate clade within the
Caricoid clade that comprises three to four taxa: Carex capitata L., an arctic-alpine
species with a circumpolar distribution; C. oreophila C. A. Mey, an alpine species
found in the mountains of western Asia and C. arctogena Harry Sm., an alpine species
from North America, South America and Eurasia. The taxonomy of the section has
traditionally been controversial, especially concerning the circumscription of the C.
capitata - C. arctogena species group. We performed uni- and multivariate analysis of
macro- and micromorphological characters (28 variables) from 450 specimens of the C.
capitata - C. arctogena species group, covering their morphological and geographical
variability, in order to elucidate its taxonomy. Carex capitata and C. arcotgena are
found to be morphologically different and populations from South America correspond
to C. arctogena. Morphological variability, which also corresponds with geographical
distribution, was found within populations from western North America and we suggest
the description of one species and two subspecies: Carex cayouetteana, C. cayouetteana
subsp. bajasierra and C. cayouetteana subsp. altasierra.
Keywords: arctic-alpine species, Carex arctogena, Carex capitata, Carex section
Capituligerae, species complex, morphology, PCA, taxonomy
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Introduction
Recent molecular studies based on nuclear and plastid DNA sequences (ETS-1f, ITS,
trnL intron, trnL-trnF intergenic spacer) showed that there are four main clades within
the genus Carex (Waterway et al., 2009): (i) Vignea clade, which encloses all species in
the subgenus Vignea; (ii) Core Carex clade, which comprises subgenera Carex and
Vigneastra; (iii) Caricoid clade, which groups subgenus Psyllophora plus genera
Cymophyllus, Kobresia, Schoenoxiphium, and Uncinia; (iv) Siderostictae clade, formed
only by species in section Siderostictae. Later on, Starr et al., (2015) found another
clade, the Hypolytroides clade, sister to the Siderosticatae one, and both sister to all
other species in tribe Cariceae. All these results confirmed that Carex was a
paraphyletic group with all other genera of tribe Cariceae nested within it. For these
reasons, it has been recently agreed by the Global Carex Group (2015) to consider a
new broader circumscription of Carex, changing its classification by unifying all genera
within it. Therfore, the genera Cymophyllus, Kobresia, Schoenoxiphium, and Uncinia
were transferred into Carex. However, clade names are still used for Carex systematics.
Section Capituligerae is a small group placed in the Unispicate clade within the
Caricoid clade (Figure 4 in Chapter 1) that comprises three to four taxa: Carex capitata
L., an arctic-alpine species with a circumpolar distribution; C. oreophila C. A. Mey, an
alpine species found in the mountains of western Asia (Egorova, 1999) and C.
arctogena Harry Sm., an alpine species from North America, South America and
Eurasia, which has been treated as synonym to C. antarctogena Roiv. by Egorova
(1999) and Moore & Chater (1971). Despite its small size, the section possesses several
taxonomic problems concerning the circumscription of its species that should be firstly
resolved in order to not misinterpret posterior results from other studies such as the
following biogeographic ones. Although Carex capitata and C. arctogena are
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recognized as separate species in some taxonomical treatments and online databases
(e.g. Egorova 1999; Jiménez-Mejías & Luceño, 2011; Govaerts et al., 2014), they are
considered as synonyms by other authors (e.g. Murray, 2002; http://www.tropicos.org).
Hybrids involving different members of the C. capitata complex have never been
reported.
The recognition of both taxa as different species is based on the following characters:,
C. capitata is pointed out to have generally longer inflorescences, bigger achenes,
shorter pistillate scales and smooth margins; it forms looser tussocks than C. arctogena
and occurs at lower elevations, in moist or humid areas (Table 1). Carex arctogena’s
distribution in Europe is less widespread (Fig. 2), occurring only in Scandinavian
countries. In North America, it occurs from Greenland to Mexico, where it presents a
considerable morphological and ecological variability, particularly in western North
America. Some authors (Smith, 1940; Egorova, 1999; Cayouette, 2007) stated the
necessity of more detailed studies including specimens from North America. Moreover,
C. arctogena circumscription is also unclear regarding populations found in South
America, which were thought to represent a separate species, C. antarctogena
Roivanen. As stressed by Reinhammar & Bele (2001), only a comprehensive worldwide
study of the complex using morphological, genetic and habitat variation would resolve
the systematics of these taxa.
Therefore, the aims of this study are: (i) to investigate how many taxonomical entities
are found in the C. capitata complex and their appropriate rank; and (ii) to characterize
them morphologically, ecologically and geographically.
Materials and methods
Sampled material
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Owing to the scarcity of herbarium specimens for Carex capitata s.l. from South
America and the western USA, two expeditions were made to collect fresh material: one
to Patagonia (January-February 2010) and a second to the western of United States
(July-August 2010). Samples were collected for a total of 10 populations, covering the
distributional range of the species in those regions (Govaerts et al., 2014). The isotype
for C. arctogena Harry Sm. was obtained from Agriculture and Agri-Food Canada
(DAO, Ottawa) whereas high resolution scans of the holotypes and leptotypes for C.
capitata and C. antarctogena were obtained from the Linnean Society of London
(LINN) and from the University of Helsinki (H), respectively. Four hundred and forty
six herbarium specimens were obtained on loan from the following herbaria
(abbreviations according to Index Herbariorum; Thiers, 2012): A, ALA, BAA, BRY, C,
CAN, CAS, CCO, CHSC, COLO, DAO, GH, H, ICEL, M, MICH, MONTU, O, OSC,
RM, RMS, UBC, UNM, UTEP, WIN and WTU. Carex oreophila has not been studied
as its morphological circunscripcion within the section is not problematic.
Morphological study
Vegetative characters were measured using a standard rule for parts longer than 10 cm
whereas all other quantitative characters were measured to the nearest 0.1 of a
millimeter using a stereoscopic binocular Nikon microscope Olympus SZX12 and a
micrometer. Qualitative states were scored by eye. Twenty nine morphological
characters [28 quantitative (22 cuantitative and 6 discrete) and one qualitative; see Table
2], were measured on a total of 147 specimens (C. capitata, N=43; C. arctogena, N=34,
C. antarctogena, N=6; undetermined specimens N= 63). Summary statistics for all
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characters including means, standard deviations and ranges were calculated for each
group in R v2.15.0 (R Development Core Team, 2011).
The lowermost, mature achene was removed from the terminal spikes of representative
samples of each group (C. capitata, C. arctogena, C. antarctogena and unclassified
specimens). The perigynium surrounding the achene was dissected away and the cell
wall of the epidermal layer of achenes was removed using a 9:1 sulfuric acid - acetic
anhydride solution in order to expose the silica bodies (Starr & Ford, 2001). Scanning
Electron Microscopy (SEM) was then employed to search for taxonomically diagnostic
micromorphological characters on the silica deposit surfaces. Samples were mounted
onto aluminum stubs with conductive carbon adhesive discs, sputter coated with a 20-25
nm layer of a gold/palladium alloy and photographed in high vacuum mode using a
Philips XL-30 ESEM with a 10kV accelerating voltage. Silica body morphology was
described according to the terminology of Schulyer (1971).
Statistical Analysis
Statistical analyses of morphological data were aimed at identifying significantly
distinct groups and diagnostic characters and to test if the studied individuals formed
different groups correlated with the different taxa traditionally recognized within the C.
capitata complex.
Histograms showing interspecific frequency differences between groups were made for
the six discrete variables. Quantitative variables for the five putative taxa were explored
using boxplots. The Shapiro Wilk normality test conducted in the data set showed that
most of the variables were not normally distributed within the putative taxa, thus
intertaxon variation was analyzed using a Kruskal-Wallis one-way ANOVA. A post-hoc
Mann-Whitney U pairwise test was also performed to assess whether differences were
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significant between groups. These analyses were run in R v2.15.0 (R Development Core
Team, 2011).
Principal component analysis (PCA) is primarily used for structure detection within the
studied data, and thus, PCAs were performed to detect groups among all specimens.
These analyses were carried out using R v2.15.0 (R Development Core Team, 2011). A
first PCA was conducted using specimens of C. capitata, C. arctogena and C.
antarctogena and all 22 continuous variables. The analysis was repeated in the same
dataset using a subset of 12 quantitative variables (denoted by asterisks in Table 2) that
included the characters employed by Egorova (1999) to differentiate between C.
capitata and C. arctogena and those determined in a pilot analysis to set apart three
groups within the unclassified specimens. A correlation matrix was studied in order to
discard highly correlated variables (>0.8) within the subset (see Tables S2 and S3 in
Appendix). Although the length of the inflorescence and length of the staminate portion
were highly correlated (0.9), both were retained in the PCA because this correlation was
observed to be inconsistent in C. capitata. Consecutive PCA were performed removing
groups that were distinctly retrieved (Jiménez-Mejías & Cabezas, 2009; Valcárcel &
Vargas, 2010; Jiménez-Mejías et al., 2014).
Geography
All studied specimens were geo-referenced to determine the geographic ranges for each
putative taxon and to reveal whether taxa occur in sympatry or allopatry. Distribution
maps [from Olson et al. (2001) for world maps, and North American Commission for
Environmental Cooperation for North American maps] of all the putative taxa in the
complex were made in ESRI ArcGIS v. 9.2, using all the specimens studied.
Ecology
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For the three populations collected in North America, soil pH measurements using
Cornell pH Test Kit Wide Range (Ithaca, New York) were taken to characterize habitat
conditions. A list of vascular plants associated with the complex (observed within 10 m
of a plant of C. capitata complex) was noted. Habitat characterization of all the putative
taxa in the C. capitata complex was made from field work observations and voucher
label information, unless otherwise noted.
Micromorphological study
Silica bodies are phytoliths produced by some plant species when soluble silica from the
ground water is absorbed by the roots and carried to different parts of the plant through
the vascular system. In sedges, they are found in the achene and leaf epidermal layers
(Toivonen & Timonen, 1976). Micromorphology in angiosperms has been used to
discriminate macromorphologically similar taxa (Stuessy, 2009). Silica bodies were
studied because they can sometimes show significant interspecific variation among
closely related species in Carex (Starr & Ford, 2001; Zhang, 2006). However, some
other micromorphology studies on Carex silica bodies did not help to differentiate
between closely related species (Standley, 1987; Rothrock, 1997).
Results
Raw data from all specimen measurements is available in Appendix S1. All the label
information from the herbarium specimens studied is gathered in a Botanical Research
and
Herbarium
Management
System
database
(http://dps.plants.ox.ac.uk/bol/BRAHMS/Home/Index) that is available upon request
from the author (see Figure 2).
Univariate analysis
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Specimens from South America, previously identified as C. antarctogena, were
compared to specimens of C. arctogena from North America and Europe, resulted in no
statistically significant differences between them (see Table 2). Therefore, those
specimens were included in the C. arctogena group. Despite some overlap in the
measurements for many characters, all taxa present significant differences between
variables (Table 2). Based on Mann-Whitney pairwise comparisons between taxa in the
complex, the best variables to distinguish them are: culm length (overwintered or not),
the length of the staminate flowers portion, leaf length, inflorescence length and width,
perigynium width, and length of the shortest hyaline margin. All taxa can be identified
by a unique set of characters. Based on uni- and multivariate analyses, three new
taxonomic entities are identified within the studied specimens and subsequently
described. Specimens with medium-size culms, the longest pistillate scale and the
widest perigynia were referable a new species herein described as C. cayouetteana sp.
nov. (see section Species descriptions and Figure 15). Specimens with the longest
culms, leaves, inflorescence and staminate flowers portion were referable to a new
subspecies herein described as C. cayouetteana subsp. bajasierra subsp. nov. (see
section Species descriptions and Figure 16). Specimens with short culms and leaves and
the narrowest inflorescence were referable to C. cayouetteana subsp. altasierra subsp.
nov. (see section Species descriptions and Figure 17). Specimens with short culms,
small staminate flowers portion, long hyaline margins, narrow perigynia and with the
smallest staminate scales were referable to C. arctogena, which its morphological
characteristics are consistent with both its holotype and C. antarctogena holotype
(Figures 2.14, A.12 and A.13). Finally, specimens with long culms and leaves, the
widest inflorescence, the narrowest pistillate scales and the longest perigynia were
referable to C. capitata (Figure 2.13). Although discrete characters do not present
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statistically significant differences between taxa (Figure A.1), in general C. arctogena
possesses more teeth along the edges of the perigynium that what is seen in other
species. For instance, C. capitata and C. cayouetteana subsp. bajasierra have smooth
perigynia or possess only a few teeth, generally no more than three, on perigynium
margins whereas C. arctogena often have between four and seven. In general, C.
cayouetteana subsp. altasierra also possess smooth perigynia, but at least one specimen
presented 16 teeth along its margins.
Multivariate analyses
During the analyses of morphological traits, one qualitative character, color of the culm
sheath, was discarded as it could not be reliably scored. Boxplots for each of the twenty
two continuous variables (Figures A.2 and A.3 in Appendix) show interspecic
differences between taxa. Only two characters (achene and leaf width) were not
significantly different among members of the complex (Table A.1 in Appendix). MannWhitney pairwise comparisons reveled the following critical diagnostic characters for
differentiating between species within the complex (Table 2.8 in Appendix): length of
the longest culm overwintered (CLHMT) or from the present year (CLMH), length of
the staminate portion of the inflorescence (MSPL), leaf length (LEAFL), length of the
spike (INFLOL), width of the perigynium (PERIGW), width of the spike (INFLOW)
and length of the narrowest hyaline margin in the pistillate scale (GLUMHC). All taxa
can be identified by a unique set of characters. Specimens with the longest culms,
leaves, inflorescence and staminate flowers portion were referable to C. cayouetteana
subsp. bajasierra (Figure 2.3). Specimens with short culms and leaves and the
narrowest inflorescence were referable to C. cayouetteana subsp. altasierra (Figure
2.4). Specimens with medium-size culms, the longest pistillate scale and the widest
perigynia were referable to ‘C. cayouetteana’ (Figure 2.5). Specimens with short culms,
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small staminate flowers portion, long hyaline margins, and narrow perigynia and with
the smallest staminate scales were referable to C. arctogena, being in consistence with
both its holotype and C. antarctogena holotype (Figures 2.6, A.13 and A.14 in
Appendix). Finally, specimens with long culms and leaves, the widest inflorescence, the
narrowest pistillate scales and the longest perigynia were referable to C. capitata
(Figure 2.7).
A scatter plot of the two first components in a PCA using all C. capitata and C.
arctogena specimens measured and 12 variables was made to study if they could be
clearly differentiated. As shown in Figure 2.9, there is practically no overlap between C.
capitata and C. arctogena, consisting in two distinctive clusters. PCA of the five groups
(C. capitata, C. arctogena, C. cayouetteana subsp. cayouetteana, C. cayouetteana
subsp. bajasierra and C. cayouetteana subsp. altasierra) graphically summarized the
phenetic differences among individuals. Only scatter plots from the PCA with the 12
variables are shown. Similar results are obtained when using the 22 continuous
variables measured (see Figures A.5, A.6, A.7, A.8, A.9 and A.10 in Appendix). When
comparing all specimens of C. arctogena, C. cayouetteana subsp. cayouetteana, C.
cayouetteana subsp. bajasierra and C. cayouetteana subsp. altasierra and using 12
variables, there is a clear separation of C. cayouetteana subsp. bajasierra from all the
other taxa (Figure 2.10). Then, if C. cayouetteana subsp. bajasierra is removed from the
analysis, there is a clear increase in the split of C. cayouetteana subsp. cayouetteana
from C. arctogenaand C. cayouetteana subsp. altasierra (Figure 2.11). Finally,
removing C. cayouetteana subsp. cayouetteana, the scatter plot from the PCA shows a
small overlap between C. arctogena and C. cayouetteana subsp. altasierra, although
two main clusters could be differentiated (Figure 2.12). The first two principal
component axes in PCA using 12 continuous variables, accounted for 28; 53% and 16;
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7% of the total variance. . First components in a PCA using C. arctogena specimens
from North America and Europe and C. antarctogena specimens and the 12 variables
selected showed that there is not a geographical pattern within the samples (see Figure
2.8). Therefore, C. antarctogena specimens were labeled afterwards as C. arctogena.
Micromorphological characters
Silica bodies presented no significant differences between or within putative taxa in the
complex, with all the members possessing a single, circular central body in the middle
of a concave silica platform. Epidermal cell walls were commonly linear, isodiametric
and six-sided (Figure 2.15).
Geographical distribution
Carex capitata presents a circumboreal distribution and it occurs in Eurasia and in
North America (Figure 2.16). In Europe, it occurs in Iceland, Norway, Sweden, Finland,
Germany, Austria, Switzerland and Italy. In Asia, it occurs in Russia from Kola
Peninsula to Chukotka peninsula, occurring south to 50ºN in central eastern Russia.
Raymond (1949) also noted that it occurs in northern Mongolia, but no specimen from
this region was examined during this study. In North America, it occurs in Alaska, the
Yukon Territory, the Northwest Territories, British Columbia (South to ca. 50ºN),
Alberta, Saskatchewan (South to ca. 52ºN), northern Manitoba, northern Ontario and
Greenland (North to ca. 72ºN).
Carex arctogena has a bipolar and amphi-Atlantic distribution with stations in northern
Europe (Scandinavia), North America and South America (Figure 2.1). In North
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America, it occurs in British Columbia (South to ca. 50ºN), northern Saskatchewan,
Manitoba (South to 52ºN), northern Ontario, northern Québec, Newfoundland and
Labrador (South to ca. 52ºN), Nunavut (until South of Victoria Island and Baffin Island,
63.5ºN), New Hampshire (White Mountains and Mt. Washington, 44ºN; Steele &
Hodgon (1973) reported to occur in Mt. Cardigan but that material was not examined)
and its northernmost latitude occurs in Greenland (North to ca. 68ºN). In South
America, it occurs in Argentinian and Chilean Patagonia, from Tierra del Fuego
(Argentina) to Neuquén province (38ºS, Argentina).
Carex cayouetteana subsp. cayouetteana, C. cayouetteana subsp. bajasierra and C.
cayouetteana subsp. altasierra are endemic to North America (Figure A.16 in
Appendix). Carex cayouetteana subsp. cayouetteana occurs only in western North
America with stations in Colorado, Utah, Montana, Wyoming, Nevada, California,
Washington, Alberta and British Columbia (North to ca. 49ºN). C. cayouetteana subsp.
bajasierra occurs only in northern California and southern Oregon (Deschutes, Jackson
and Lake Counties). C. cayouetteana subsp. altasierra is a Californian endemic,
restricted to high elevations in the Sierra Nevada (Inyo, Mono, Tulare and Tuolumne
Counties).
Ecological requirements
Carex capitata is an alpine species. In northern latitudes such as Alaska or the European
Arctic, it is found in tundra and taiga (boreal forest) environments whereas in southern
latitudes, such as central Europe or western Canada, it is found in alpine or subalpine
areas. It occurs in rich and calcareous fens, mires, peat-bog margins, meadows, wet
tundra and other humid or moist habitats, sometimes with moss as also noticed by Smith
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(1940). In Alaska, it is also found in marshes and poplar forest from lowlands (400 m)
to at least 800 meters. In northeastern North America, it is mainly found in areas
adjacent to Hudson Bay, rare or local in alpine summits towards South. Carex capitata
elevational occurrence in Italy is at 1900 - 1980 m (in the South Tyrols). It has been
reported to be strictly a calciphile or calciphilous (Smith, 1940; Nilson, 1991;
Cayouette, 2007), but such information was not taken from the label data from the
specimens examined for this study.
Carex arctogena is an arctic-alpine species. It generally occurs in wind-exposed alpine
heaths, often dominated by Empetrum (Ericaceae) and also in cliffs, ridges, summits
and in dry areas often dominated by rocky or gravelly soil. In northeastern North
America it is found locally in New Hampshire (Alpine Garden and Mt. Cardigan) at
1900 m, one of the highest elevations within its entire distribution together with its
southernmost localities in British Columbia (ca. 2000 m). Similarly, it occurs near this
altitude in northern Patagonia (Neuquén). In southern South America, it occurs in humid
areas such as bogs, wet meadows and eutrophic marshes at low elevations, often in
areas of high floral diversity (Table 2.2). In the southernmost region of Patagonia,
Tierra del Fuego, C. arctogenawas found in a semi-humid grassland, dominated by
tufted grasses interspersed with Empetrum rubrum at low elevations (Table 2.2). It has
been reported to grow in either calciphile, peridotite, gneiss, granite or serpentine soils
(Smith 1940; Nilson 1991) but such information is generally missing in voucher
specimens.
Carex cayouetteana subsp. cayouetteana generally occurs in acidic and rocky soils (see
Table 2.3), in wind-exposed, alpine moist tundra areas and sometimes in dry meadows.
It is found from ca. 2000 m in Washington and California to at least 3500 m in
Colorado and Utah, where it can grow on quartzite soils.
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C. cayouetteana subsp. bajasierra may occur in acidic-neutral pH soils (see Table 2.4),
in wet meadows or mires surrounded by woods. In northern California (Tehama, Plumas
and Butte Counties) and southern Oregon (Lake and Jackson Counties), it occurs at
unusually low elevations for the complex at this latitude (ca. 1400 m). In Sierra and El
Dorado Counties, it occurs in wet marshy meadows and in open Pinus contorta forests
at ca. 1980- 2300 m where it reaches its highest elevation.
C. cayouetteana subsp. altasierra is restricted to the highest elevations in California. It
occurs in non-glaciated plateaus and wet banks. On the North side of Mount Humphries
(‘Humphries Plateau’, Inyo Co.) it grows at 3900 m and also at 3600 m at Mono Mesa
(Inyo Co.); in northeastern Tulare Co., in wet banks at ca. 3400 m. It is found in
Tuolumne Co., in soil formed from metamorphic rocks, in non-glaciated areas at ca.
3800 m
Discussion
There are geographical and ecological differences between the taxa found in this
complex: C. capitata presents a circumboreal distribution whereas C. arctogena
presents a bipolar distribution; Carex cayouettena subsp. cayouetteana is only found in
western North America from (2000 to 3800 m); C. cayouetteana subsp. bajasierra is
restricted to southern Oregon and northern California (1400 - 2300 m); and C.
cayouetteana subsp. altasierra occurs locally at high elevations (3400 - 3900 m) in
California. Only 8 herbarium specimens of C. cayouetteana subsp. altasierra were
observed during the course of this study. Giving the extreme elevation at which this
species occurs, this might indicate that C. cayouetteana subsp. altasierra is rare or that
the habitat in which it occurs has been under collected.
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Although C. antarctogena specimens from South America displayed statistically
significant morphological differences regarding to northern hemisphere specimens of C.
arctogena in some variables, they are not enough to differentiate between northern and
southern specimens. These differences are of a 10% in average and for one variable,
length of the staminate portion is of 38% (but this variable has a standard deviation of
the same order of magnitude as the mean). Thus, C. antarctogena and C. arctogena are
treated as synonyms in this study, which is consistent with the previous morphological
analysis by Moore & Chater (1971). In congruence, in Chapter 3, molecular analyses of
three chloroplast regions (matK, atpF-atpH and rps16; 2297 characters), show no
genetic differences between C. arctogena from the Northern vs. Southern Hemisphere.
On the other hand, some variability was found within C. capitata specimens from
Russia, Austria, Ontario and Alberta, which have culms longer than 41 cm long. This
plasticity within C. capitata was also remarked by Raymond (1949) in some specimens
collected in Québec (Lac De l’Ours). However, in our opinion, this appears to be no
more than a regional trend and it is not correlated with other morphological characters,
so it might not deserve taxonomical recognition. All taxa in the C. capitata complex are
long-lived perennials, wind-pollinated and reproduce sexually. Hybrids between
members of the complex have not been reported.
A large number of new species has been described over the last few decades in North
America North of Mexico (Ertter, 2000). This is especially true for the genus Carex
(Naczi, 1993; Naczi et al., 1998; Saarela & Ford, 2001), with an average of two taxa
described per year over the last 20 years (Ertter 2000). This rich biodiversity in North
America could be due to ecological diversity and historical environmental
transformations due to paleoclimatic changes, especially during Pleistocene climatic
oscillations, as it has been highlighted in many intensive Flora studies (e.g. Ball et al.,
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2002) and should continue to be the focus of research interests in order to better
understand species distributions.
All five species of the C. capitata complex occur in North America and the three new
taxa are endemic to North America, which provides further evidence of the taxonomic
richness that exists within North American Carex. Some other examples include C.
maritima Gunn. species complex, a bipolar species widely distributed in North America,
whose ecological and morphological variability led Kreczetowitcz (1932) to described
twelve different species and some other botanists to describe new taxa [e.g. C.
incurviformis Mack. varieties, C. maritima var.setina (Christ) Fernald or C. maritima
var. misera (Kük.) Fernald]; and forms [e.g. C. maritima f. inflata (Simmons) Polunin].
It is also remarkable the studies made by Naczi et al. (2002) who described seven new
Carex species from North America (C. acidicola Naczi, C. calcifugens Naczi, C.
paeninsulae Naczi, E. L. Bridges & Orzell, C. thornei Naczi, C. kraliana Naczi &
Bryson, C. gholsonii Naczi & Cochrane and C. infirminervia Naczi).
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Taxonomic treatment
The following key helps to identify the species of C. capitata complex recognized in
this study. Mature, complete and well developed specimens are necessary for correct
identifications.
Key to species of the C. capitata complex
1. Tallest culm < 160 mm long, inflorescence < 3 mm wide…. C. cayouetteana
subsp. altasierra .(Y3)
1. Tallest
culm
>
160
mm
long,
inflorescence
>
3
mm
wide……………………….2
2. Inflorescence > 13 mm long…………………………………C. cayouetteana
subsp. bajasierra. (Y2)
2. Inflorescence < 13 mm long……………………………………………….…3
3. Perigynia < 17 mm wide with more than 3 teeth, hyaline margins on
the pistillate scales in a triangular shape…...………………. C. arctogena
3. Perigynia > 17 mm wide with less than 3 teeth, hyaline margins on the
pistillate scales in an inverted V shape…………………………………..4
4. Tallest culm < 230 mm long, staminate portion > 2.4 mm long,
pistillate scales > 2.2 mm long and > 1.5 mm wide .....C.
cayouetteana subsp. cayouetteana. (Y)
4. Tallest culm > 230 mm long, staminate portion < 2.4 mm long,
pistillate scales < 2.2 mm long and < 1.5 mm wide .....C.capitata
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Species descriptions
Carex capitata L., Syst. Nat. (1759) 10th ed., 2:1261. Type: Sweden, Lapponia. Leg.
Solander. Stockholm Linnean Herbarium 378.13 (S-LINN: IDC 378.13) photo!
Herb forming loose to dense tussocks. Roots dark yellow, light brown, yellow or
greyish-yellow. Culms 12-49 cm high and 0.6-1.0 mm wide at the middle, slender, wiry,
more or less dentate on the margins and mainly near the apex. Leaves usually 3-5 per
culm, old leaves persistent, most often shorter than the culm; leaf sheaths dark orangebrown, dark brown-red or dark brown at the base, sparingly filamentose.; blades 11.5-36
cm long and 0.4-1.5 mm wide in the middle, filiform, stiff, erect or recurving, truncate
mouth; ligule very short, obtuse. Spike solitary, androgynous, globose, ovoid or
trigonal, with staminate portions covering 15 % to 34 %, fairly densely packed, of 5.510.3 mm long and 3.3-5.4 mm wide, staminate portions from 0.8-3.5 x 0.5-1.3 mm, 515 staminate flowers, 12-27 pistillate flowers; bract absent or rarely present; staminate
scales erect, obovate or ovate, the body orange, dark yellow-orange or brown-yellow
with hyaline margins located in the distal 1/3 and 0.1-0.2 mm wide, often folded,
glabrous, 1.6-2.9 x 0.6-1.5 mm, incomplete veins, acute apex; stamen with anthers 1.01.5 mm long; pistillate scales ovate or broadly ovate, the body orange, dark orange or
brown, hyaline margins absent or 0.1-0.5 mm in the central portion and 0.1-2.25 mm
along the edges, central nerve rarely present, glabrous, 1.5-2.5 x 0.8-1.8 mm, shorter
than the perigynium body and reaching 1/2 of perigynia body length, narrower than the
perigynia and sometimes not reaching 3/4 of perigynia width; distal perigynia erect or
ascending, mostly spreading or the lowermost descending or retracted in the proximal
part, the body greenish-light yellow in proximal half, yellow to yellow-grayish or brown
with some redness in the distal half, surface often shiny with some red dots, 1.8-3.6 x
1.3-2.2 mm, margins sometimes winged especially in the 1/3 proximal and 0.1-0.2 mm
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wide, smooth (rarely 0-5 teeth), round bases, apex acute, contracting gradually into a
beak; beaks brown or orange-brown, apex orange or hyaline, 0.8-1.7 mm long x 0.2-0.3
mm wide at the base, straight; gynoecium with 2 stigmas; rachilla often visible in relief
on the side of abaxial perigynia, setaceous, as long or slightly longer than achenes;
achenes ellipsoid, broadly ellipsoid or almost orbicular, the body light yellow, yellowgreenish, non-glossy surface, 1.1-2.1 x 1.0-1.5 mm, filling more than 2/3 to 3/4 of the
perigynium, broadly cuneate or rounded at the base, apex acute, obtuse or truncated;
style bases absent or persistent by the bottom of the style.
Notes: C. capitata is easily differentiated from other members of the complex by its
spreading perigynia with the lowermost sometimes even descending, similar to the
morphological condition separating the species pair C. typhina Michaux and C.
squarrosa L. It can also be easily recognized from all other members of the complex by
its pistillate scales, shorter and narrower than the perigynia; its small staminate portion;
the presence of some redness in the perigynia and glabrous perigynia.
Distribution: Europe (ICE, NOR, SWE, FIN, GER, AUT, SWI, ITA); N Russia; N
North America (ASK, YUK, NWT, BRC, ABT, SAS, MAN, ONT, GNL).
Ecology: Tundra, taiga (boreal forest) and alpine and subalpine areas, in various humid
soils (fens, mires, meadows).
Carex arctogena Harry Sm., Acta Phytogeogr. Suecica (1940), 13:193. Type: Sweden,
Torne Lappmark, karesuando, Moskana ca. 1000 m.s.m. 26/7 1933, Harry Sm. (UPS
Holotype) photo! (Fig. A.13 in Appendix)
List of specimens studied: Argentina, Dept. Chos Malal, 2300 m, Boelcke, O., Correa,
M.N.; Bacigalupo, N.M., 30.1.1964, (BAA, 11368). Dept. Chos Malal, 2300 m,
Boelcke, O., Correa, M.N.; Bacigalupo, N.M., 30.1.1964, (BAA, 11368).A, Mendoza,
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Cordillera del Rio Barrancas, Kurtz, F., 16.11.1888, (MICH). Canada, Alberta, Mercoal,
Rousseau, J., 18.7.1947, (COLO, 13811). Alberta, Mercoal, 4300 ft, Malte, M.O.,
Watson, W.R., 8.8.1925, (RM, 280606). British Columbia, Pine Pass, 1402 m, Argus,
G.W., 12.7.1973, (CAN, 372267). British Columbia, 7228 ft, Calder, J., 149035,
Parmelee, J.A.; Taylor, R.L., 8.8.1956, (COLO, 149035). British Columbia, Mount
Apex, 7100 ft, Calder, J., Savile, O., 11.8.1953, (RM, 252249). Manitoba, Fort Chimo,
Rousseau, J., 14.8.1951, (WIN, 22355). Manitoba, Baralzon Lake, Scoggan, H.J.,
22434, Baldwin, W.K.W., 28.7.1950, (WIN, 22434). Manitoba, Hudsons Bay Co.,
Duck Lake, Scoggan, H.J., Baldwin, W.K.W., 10.8.1950, (WIN, 22435). Manitoba, Fort
Chimo, Legault, A., 22.7.1963, (COLO, 491481). Manitoba, Hudsons Bay Co., Duck
Lake, Scoggan, H.J., Baldwin, W.K.W., 10.8.1950, (CAN, 201506). Manitoba,
Baralzon Lake, Scoggan, H.J., Baldwin, W.K.W., 30.7.1950, (CAN, 202500).
Manitoba, Nueltin Lake, Baldwin, W.K.W., 26.7.1951, (CAN, 212816). Manitoba,
Cochrane River, Baldwin, W.K.W., 3.7.1951, (CAN, 212817). Manitoba, Baralzon
Lake, Scoggan, H.J., Baldwin, W.K.W., 28.7.1950, (CAN, 201507). NewfoundlandLabrador, Esker area, 838 m, Mäkinen, Y.,Kankainen, E., 21.7.1967, (CAN, 314758).
Canada, Newfoundland-Labrador, Twin Falls, Hustich, I., 6.7.1967, (CAN, 313311).
Nunavut, Upper Hood River, 100 m, Gould, W..7.1995, (COLO, 475773). Ontario,
Kenora District, Patricia Portion, Riley, J.L., 12.8.1980, (CAN, 462937). Ontario,
Hudson Bay Lowlands, Porsild, A.E., Baldwin, W.K.W., 4.7.1957, (CAN, 278707).
Quebec, Fort Chimo, Sørensen, T., 17.8.1959, (C). Quebec, Baie d'Ungava, Blondeau,
M., 1.8.1993, (WIN, 53902). Quebec, Baie d'Ungava, Rousseau, J., 23.7.1951, (WIN,
22356). Quebec, Lac Jaucourt Region, Lichteneger Lake, 487 m, Argus, G.W.,
16.7.1974, (CAN, 3779977). Quebec, Boatswain Bay, Baldwin, W.K.W.,Hustich, I.;
Kucyniak, J.; Tuomikoski, R., 8.7.1947, (CAN, 17333). Quebec, Lac Payne, Legault,
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A., 2.8.1965, (CCO, 23398). Quebec, Northern Quebec, Lake Payne, Legault, A.,
210789, Brisson, S., 2.8.1965, (COLO, 210789). Quebec, Ungava, Husons Bay, Dutilly,
A., 233644, Lepage, E., 21.3.1945, (RM, 233644). Quebec, Fort Chimo, Calder, J.,
31.7.1948, (RM, 255325). Quebec, Hudson Bay, Cairn Island, Abbe, E.C., Abbe, L.B.;
Marr, J., 30.7.1939, (RM, 252521). Quebec, Hudson Bay, Great Whale River, Calder,
J., Savile, O. Kukkonen, I., 8.8.1959, (RM, 260486). Quebec, Lac Kopeteokash,
Rousseau, J., 18.7.1947, (RM, 228636). Saskatchewan, Vicinity of Patterson Lake,
Argus, G.W., 20.7.1963, (CAN, 282691). Saskatchewan, Northeastern Saskatchewan,
Patterson Lake, Argus, G.W., 20.7.1963, (RM, 277437). Finland, Enontekiö,
Kilpisjärvi, Saana, 750 m, Roivainen, L., 8.7.1935, (H, 127310). Enontekiö, Kilpisjärvi,
Saana, 750 m, Väre, H., 29.7.2004, (H, 805587).A, Enontekiö Lapland, 825 m, Väre,
H., 17.7.2006, (H, 809948). Inari, Vätsäri Wilderness Area, Kulmala, H., 27.7.1996, (H,
717201). Lapponia Imandrae, Lindén, J., 18.7.1891, (H, 325665). Lapponia Imandrae,
Axelson, W.M., Borg, V., 24.7.1901, (H, 325667). Lapponia murmanica, 550 m,
Brotherus, V.F., .8.1887, (H, 325639).A, Petsamo, Cajander, A., 10.7.1927, (H,
325644). Porojärvet, Toskalhar, 950 m, Roivainen, H., Ollila, L., 15.7.1955, (H,
127313).A, Porojärvet, Toskalhar, 910 m, Roivainen, H., 15.7.1966, (H, 179889).
Foutell, C.W., Jalan, M.J., 10.8.1899, (H, 325657). Germany, Altevatn, 500 m,
17.8.1967, (M, 0151943). Greenland, Arfersiorflk, Itjvdljarssuk, 75 m, Fredskild, B.,
Dalgaard, V., 19.7.1987, (COLO, 456814). Groenlandia meridionalis, Kangerdluarssuk,
Hansen, C., Hansen, K.; Petersen, M., 4.7.1962, (CAN, 282521). Nigerdleq, Jørgensen,
L.B., 15.7.1966, (CAN, 311369). Vestgrønland, Pingorssuaq Kitdleq, 400 m, Hanfgarn,
S. 3, 11.8.1983, (C). Tugtilik Lake, 10 m, Elsley, J.E. 15.8.1967, (M, 0151948).
Lagerkranz, J., 2.8.1936, (RMS, 153944). Norway, Finnmark, Sör-Varanger, Bugöynes,
Toivonen, H., 30.7.1971, (H, 1081734). Finnmark, Sör-Varanger, Bugöynes, Toivonen,
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H. 30.7.1971, (H, 1081733). Nordland, Narvik hd., Skjomen, Skifte, O., GRaff, G.;
Spjelkavik, S., 11.8.1973, (H, 1679404). Norland, Sulitjelma, Skifte, O., 1.8.1962,
(DAO, 285800). Sverige, Abisko, Paddas, Lid, J., 1300264, 2.8.1950, (H, 1300264).
Troms, Bardu, Leinavatn, 498 m, Engelskjøn, T., Engelskjøn, E.M., 7.7.1977 (C).
Troms, Bardu, Altevatn, 580 m, 18.8.1967, (M, 0151942). Troms, Bardu, Kampaksla,
780 m, Engelskjøn, T., Skifte, O., 9.8.1978, (H, 1685049). Russia, Petsamo, Petchenga,
Vouvatusjärvi, Piirainen, M., 27.7.1995, (H, 1682990). Sweden, Torne Lappmark,
Karesuando, 1000 m, Smith, H., 26.7.1933, (DAO, 257429). Torne Lappmark,
Karesuando, 1000 m, Smith, H., 26.7.1993, (H, 1652844). Torne Lappmark, Jukkasjärvi
parish, 550 m, Alm, G., Smith, H., 23.7.1939, (H, 1300259). USA, New Hampshire,
Coos Co., Mt. Washington, Hodgon, A.R., Gale, M., 30.6.1950, (DAO, 257427). New
Hampshire, White Mountains, Mt. Washington, Forbes, F., 9.8.1902, (RMS, 242089).
New Hampshire, Alpine Garden, Mt. Washington, Sargent, F.H., 5.7.1942, (BRY,
143916). New Hampshire, Alpine Garden, Mt. Washington, 5000 ft, Löve, A., Löve, D.,
27.7.1958, (COLO, 288736). New Hampshire, Alpine Garden, Mt. Washington, Löve,
A., Löve, D., 3.7.1960, (COLO, 295019). New Hampshire, White Mountains, Mt.
Washington, Forbes, F., 9.8.1902, (RM, 50212). New Hampshire, White Mountains,
Mt. Washington, Eggleston, W.W., 29.7.1899, (RM, 44595). New Hampshire, Alpine
Garden, Mt. Washington, Eggleston, W.W., 29.7.1899, (RM, 23379). New Hampshire,
White Mountains, Faxon, C.E., 1.9.1877, (CAN, 162720).
≡ C. capitata L. ssp. arctogena (Harry Sm.) Hiit., Luonnon YstЉvЉ 48: 52-64. (H)
photo! (≡ C. capitata L. ssp. arctogena (Harry Sm.) Böcher, in Medd. om Grønl.147(9),
1952. Isonym)
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≡ C. capitata L. var. arctogena (Harry Sm.) Hultén, Kungl. Sv. Vet. Ak. Handl. (1958),
4 (7):38. Uppsala. Type: Sweden, Torne Lappmark, Karesuando, Moskana ca. 1000
m.s.m. 26/7 1933, H. Smith. (UPS) photo!
≡ C. capitata f. arctogena Raymond, Contrib. bot. Univ. MontrЋal (1949), 64:38.
= C. capitata f. alpicola Andersson, Bot. Not. (1849), 2.
= Carex antarctogena Roiv., Ann. Soc. Zool. Bot. Fenn. Vanamo (1954), 28 (2): 197198. Type: [Chile, Tierra del Fuego] Estancia Vicuña, in palude. H. Roivanen (H
Holotype) photo!
Carex rahuiensis Kurtz. ex. Kükenth., Bot. Jahrb. (1900), 27:495 - nomen nudum,
according to Smith (1940).
Kurtz based Carex rahuiensis on plants he collected in Argentina (Kükenthal 1900).
According to Smith (1940) it is nomen nudum, although he did not see any specimen
from Kurtz’s collections. Carex antarctogena was described by Roivanen on the basis of
Argentinian specimens which he considered to be more robust in structure and to have a
greater number of staminate flowers and perigynial teeth than C. arctogena from the
northern Hemisphere. The present morphological study does not support these
observations since specimens from South America are not statistically significant bigger
than the North American or European specimens (Table 2.7). Both species will
therefore be considered as synonyms here. In Chapter 3, molecular analyses show no
genetic differences between C. arctogena samples from the northern vs. southern
Hemisphere in the three chloroplast regions and five nuclear loci studied.
Herb forming loose to dense tussocks. Roots sometimes short-creeping, yellow or
reddish. Culms 10-33 cm tall and 0.5-1.1 mm wide in diameter at the middle, slender,
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wiry, more or less dentate on the margins and dense towards the apex. Leaves erect, 3-5
per culm, old leaves persistent, shorter or as long as the culm; leaf sheaths dark red or
brown at the base, sparingly filamentose; blades 9-29 cm and 0.4-1.0 mm wide at the
middle, filiform, stiff, erect or recurving, truncate mouth; ligule very short, obtuse or
nearly truncate. Spike solitary, androgynous, globose, ovoid or trigonal, with staminate
portions covering 20 % to 37 %, fairly densely packed, 5.2-9.8 mm long x 2.9-4.7 mm
wide, staminate flower portion 1.2-3.7 mm long x 0.5-1.3 mm wide, pistillate flowers
portion 3.5-6 mm long, 5-26 staminate flowers, 9-32 pistillate flowers; bract absent,
rarely present; staminate scales erect, obovate, broadly obovate or ovate, the body
yellow or olive-brown with hyaline margins located in the distal 1/3, 0.1-0.2 mm wide,
often folded, glabrous, 1.0 to 2.8 mm long x 0.7 to 1.6 mm wide, with 1-3 veins, apex
acute; stamens with anthers 0.6-1.4 mm long; pistillate scales ovate or broadly ovate,
the body yellow, orange-brown or dark brown with hyaline margins rarely absent and
typically occupying the proximal and distal portions, length of 0.1-1.0 mm in the central
portion and 0.4-2.6 mm along the edges in a triangular shape, no nerve or one,
incomplete, glabrous, 1.0-2.6 x 1.4-3.0 mm shorter than the perigynia and reaching 3/4
of perigynia body length or until the base of the beak, wider or little narrower than
perigynia; distal perigynia erect or ascending, proximal mostly spreading, the body
greenish or yellow on the proximal half and dark grayish, yellow-green or brownish
green in the distal half, surface glossy, 1.5-3.2 x 1.0-2.0 mm, 0.8-1.4 mm, margins
sometimes winged especially in the proximal half and 0.1-0.3 mm wide, almost always
scabrous (1-16 teeth), cuneiform base, abruptly contracted into a beak; beak brown,
dark-brown or olive-brown, apex orange or hyaline, 0.3-0.9 mm long and 0.2-0.3 mm
wide at base, mostly straight, bifid; gynoecium with 2 stigmas; rachilla often visible in
relief on the side of abaxial perigynia, setaceous, as long or slightly longer than the
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achene; achenes ellipsoid, broadly ellipsoid or almost orbicular, the body greyish,
yellow or dark, non-glossy surface, 1.4-1.9 mm long x 0.7-1.7 mm wide, filling more
than 3/4 of the perigynium, broadly cuneate or rounded at the base, apex obtuse or
truncated; style bases absent or persistent by the bottom of the style.
Notes: C. arctogena is differentiated from all other members of the complex by its
pistillate scales, broader and as long or longer than the perigynia; its scabrous perigynia,
and its hyaline margins along pistillate scales, which have a triangular shape and which
can cover up to half of the surface of the scale. It is most similar to C. cayouetteana
subsp. cayouetteana and C. cayouetteana subsp. altasierra but they can be easily
separated by the characters mentioned above.
Distribution: Europe (NOR, SWE, FIN); N Russia; N North America (NUN, BRC,
SAS, MAN, ONT, QUE, NFL, GNL, NWH) and S South America (AGS, CLC).
Ecology: Arctic-alpine areas and wind-exposed alpine heaths, in soils with low water
content.
Carex cayouetteana subsp. cayouetteana
Holotype: Canada, Alberta: Banff National Park, Snow Creek Pass, A.E. Porsild 22673
(CAN-266077).
Paratype: USA, Colorado: Clear Creek Co., Loch Lomond, W.A. Weber, T. Koponen &
P. Nelson s.n. (CAN-374041).
Herb forming loose tussocks. Roots light brown to yellowish. Culms 11-26 cm tall and
0.6-1.1 mm in diameter at the middle, slender, wiry, more or less dentate on the margins
and dense towards the apex. Leaves 3-6(7) per culm, old leaves persistent, shorter than
culm; leaf sheaths yellow or light brown at the base, sparingly filamentose; blades11-19
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cm long and 0.4-0.9 mm wide in the middle; ligules obtuse or nearly truncate. Spike
solitary, androgynous, trigonal to ovoid, lanceolate, with staminate portions wider at the
bottom and covering 50 % to 60 %, densely packed, of 6.1-12.8 mm long x 3.5-6.1 mm
wide, staminate portions from 0.9- 6.7 x 1.5-2.9 mm, pistillate 3.9-6.4 mm long, 15-26
staminate flowers, 17-32 pistillate flowers; bract absent or rarely when present;
staminate scales erect, broadly obovate or ovate, the body dark brown or yellowish,
central bands are not clearly delineated with hyaline margins located in the 1/3 distal
and 0.1-0.15 mm wide, often folded, glabrous, 1.8-3.0 x 0.6-1.9 mm, with 1-2 veins,
apex acute, subacute or rounded; pistillate scales ovate or broadly ovate, the body dark
brown, hyaline margins absent or occupying the distal portions, length of 0.1-1 mm in
the central portion and 0.1-0.5 mm crossing the edges, one nerve clearly marked and
surrounded by light brown or light yellow, glabrous, 1.5-3.4 x 1.2-2.5 mm shorter than
the perigynia and reaching full or 3/4 of body length perigynia, wider or as wide as
perigynia, apex rounded, truncated or obtuse; perigynia distal erect or ascending, most
proximal spreading, the body greenish-yellow in proximal part, dark brown to brown in
the half distal until top of the achene, surface gloss with some redness, 1.5-3.4 x 1.2-2.5
mm, 0.6-1.5 mm, margins sometimes with nerves, almost scabrous (0-5(7) teeth),
obtuse angle at the bottom, acute apex contracted smoothly into a beak; beak dark
brown, apex orange or hyaline, long of 0.9-1.9 mm, mostly straight, teeth acuminate,
bifid, smooth; gynoecium with 2 stigmas; rachilla often visible in relief on the side of
abaxial perigynia, setaceous, as long as or slightly surpassing; achenes ellipsoid, broadly
ellipsoid, the body dark yellow to light brown, glossy surface, 1.0-2.3 x 0.6-1.8 mm,
covering over 3/4 volume perigynia, broadly cuneate, rounded or rotund at the base,
apex obtuse or truncated, wrinkled; beaks marked by the straight base of the style.
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Notes: C. cayouetteana subsp. cayouetteana can be identified by its staminate portion,
as long as the pistillate portion, presenting a cone shape; pistillate scales, broader and as
long as the perigynium beak, or longer than the perigynia; its scabrous perigynia,
usually with 2-3 teeth; its hyaline margins in the pistillate scales, which are around 1
mm wide and go around the edges of the scale, drawing an inverted V shape; its brown
perigynia beak and green perigynia body. Carex arctogena can be easily separated from
C. cayouetteana subsp. cayouetteana by its staminate portion, shorter and cylindrical in
C. arctogena; its hyaline margin with triangular shape; for having more teeth in the
margins of the perigynium and less number of perigynia in the spike.
Distribution: North American endemic (COL, UTA, WYO, NEV, CAL, WAS, ALB,
BRC).
Ecology: Tundra and alpine areas, in dry, acidic and rocky soils. 2000 - 3500 m.
Etymology: This taxon is named after Jacques Cayouette, a passionated botanist who
has spent his life working extensively in North American sedges and particularly in
Québec.
C. cayouetteana subsp. bajasierra
Holotype: USA, California: Butte Co., near Cherry Hill Campground, Lassen National
Forest, J. Starr 10S-054 & T. Villaverde.
Paratypes: USA, California: El Dorado County, Lake Tahoe Basin Management Unit,
J.R. Starr & J. Thibeault 07-44 (CAN). California: Sierra County, Tahoe National
Forest, J.R. Starr & J. Thibeault 07-52 (CAN). California: Butte Co., Lassen National
Forest, Forest Ranch, Cheery Hill meadows, near Cherry Hill campsite. J.R. Starr & J.
Thibeault 06016 (CAN). California: Sierra Co., Yuba Pass-Weber Lake Road, V.H.
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Oswald & L. Ahart 8221 (CHSC-66824). California: Tehama Co., L. Ahart 13.051
(CHSC-94326). Oregon: Deschutes Co., C. Halpern 600 & T. Magge (OSC-159046).
Herb densely caespitose. Roots light brown, orange or dark yellow. Culms 19-54 cm tall
and 0.7-1.0 mm at the middle, slender greenish or yellowish at the base. Leaves 3-5 per
culm; leaf sheaths dark brown to light brown at the base, sparingly filamentose; blades
13-27 cm long and 0.5-0.9 mm wide in the middle; ligules, acute, obtuse or nearly
truncate. Spike solitary, androgynous, trigonal, slender, with staminate portions
covering 50 % to 70 %, loosely packed, of 6.8-16.9 mm x 3.2-4.6 mm, staminate
portions 2- 10.5 x 1-1.5 mm, pistillate 3.5-6 mm long, 30-37 staminate flowers, 815(30) pistillate flowers; bract absent or rarely when present; staminate scales erect,
obovate, broadly obovate or ovate, the body light brown to light yellow in the middle
portion, central bands are clearly delineated, hyaline margins located in the 1/3 distal
and 0.1-0.25 mm wide, often folded, glabrous, 1.6-2.9 x 0.8-1.8 mm, 1 vein, apex
truncate or rounded; stamen with anthers 2-2.6 mm long; pistillate scales ovate or
broadly ovate, the body brown to light brown, orange towards the edges with hyaline
margins absent or occupying the proximal and distal portions, length of 0.1-0.3 mm in
the central portion and 0.1-1.8 mm crossing the edges, one nerve marked, glabrous, 1.22.7 x 1.4-2.2 mm longer, sometimes as long as or shorter than the perigynia, reaching
3/4 of body length perigynia, wider and the bottom, a little narrower or about the same
width as perigynia in the distal portion; perigynia distal erect or ascending, proximal
spreading, the body greenish yellow in 1/2 proximal, dark brown or light brown in the
half distal surface, gloss stinks, 1.5-3.1 x 1-2 mm, 1.2-2.2 mm body length perigynia,
almost always smooth (0-3 teeth), base subacute or rounded, apex contracted smoothly
into a beak; beak brown to dark brown, apex orange or hyaline, mostly straight, teeth
acuminate, bifid; gynoecium with 2 stigmas; rachilla often visible in relief on the side of
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abaxial perigynia, setaceous, as long as or slightly surpassing, 1.2-1.9 x 1 mm; achenes
ovoid or almost orbicular, the body light brown, glossy surface, 1-2 x 0.5-1.4 mm,
covering over 3/4 volume perigynia, rounded at base, apex obtuse or truncated; beaks
absent or marked by the straight base of the style.
Notes: C. cayouetteana subsp. bajasierra is easily differentiated by its staminate
portion, usually longer than the pistillate portion; its perigynia ascending, loosely
packed; its long culms, much longer than the leaves. It occurs in wet meadows at low
elevations in California.
Distribution: Western North American endemic (CAL, ORG).
Ecology: Wet meadows in boreal areas, in soils with high water content. 1400 - 2300 m.
C. cayouetteana subsp. altasierra
Holotype: USA, California: Tulare Co., Sierra Nevada, Army Pass, J.T. Howell s.n.
(DAO-257423).
Paratypes: USA, California: Inyo Co., Mono Mesa, J.T. Howell 22750 (WTU-137524).
California: Northeastern Tulare Co., Sierra Nevada, Central Basin, Lower lake, P.A.
Munz 12669 (WTU-133536).
Herb forming loose to dense tussocks, caespitose. Roots light yellow or light brown.
Culms 8-20 cm tall and 0.7-1.0 mm in diameter at the middle. Leaves 3-4(7) per culm,
90-290 x 0.4-1.0 mm; leaf sheaths brown-dark red or orange, sparingly filamentose;
blades 8-14 cm long and 0.4-0.9 mm wide in the middle; ligules, acute, obtuse or nearly
truncate. Spike solitary, androgynous, ovoid or trigonal, with staminate portions
covering 35 % to 60 %, densely packed, of 6.2-8.5 mm x and 2.5-4.0 mm, staminate
portions from 2.2-4.9 x 1.2-1.7 mm, pistillate 2.0-4.2 mm long, 26-30 staminate
90
________________________________________________________________
________________________________________________________________
flowers, 14-16 pistillate flowers; bract absent or rarely when present; staminate scales
erect, obovate, broadly obovate or ovate, the body pale yellow, light brown to dark
brown, central bands are clearly delineated with hyaline margins located in the 1/3 distal
and 0.1-0.2 mm wide, often folded, glabrous, 1.9-2.5 x 0.9-1.2 mm, with 1 vein, apex
acute to subacute; pistillate scales the body dark brown, light brown to orange towards
the edges, hyaline margins occupying the proximal and distal portions, length of 0.1-0.5
mm in the central portion and 0.1-2.0 mm crossing the edges, central nerve rarely
present, ovate or broadly ovate, glabrous, 1.8-2.1 x 1.15-2.0 mm, as long as or shorter
than the perigynia and reaching 3/4 of body length perigynia until the base of the beak,
wider or as wide as perigynia in the bottom and narrower than perigynia in the distal
part, subacute apex, scarbid; perigynia erect or ascending in the distal part, mostly
spreading in the proximal part, the body greenish or light yellow in 1/2 proximal part
with some redness, dark brown in the half distal portion, not very gloss surface, 2.0-3.8
x 1.1-1.9 mm, 1.4-2.2 mm body length perigynia, almost always smooth (0-1(16) teeth),
rounded to subacute base, beak often abruptly or subacutely contracted; beaks brown to
dark brown, apex orange or hyaline, mostly straight, teeth truncate, smooth, bifid;
gynoecium with 2 stigmas; rachilla often visible in relief on the side of abaxial
perigynia, setaceous, as long as or slightly surpassing; achenes ellipsoid, broadly
ellipsoid, lenticular or almost orbicular, the body grayish to light brown, non-glossy
surface, 1.4-2.6 x 1.0-1.9 mm, covering over 3/4 volume perigynia, at base broadly
truncated or rounded, apex obtuse or truncated; beaks absent or marked by the straight
base of the style.
Notes: C. cayouetteana subsp. altasierra can be differentiated by its short culms, as
long as the leaves; its staminate portion, as long as or slightly longer than the pistillate
portion, presenting a cone shape; its pistillate portion, densely packed. It occurs in high
91
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________________________________________________________________
elevations in California. Carex arctogena can be easily separated from C. cayouetteana
subsp. altasierra for having longer culms, longer spikes, straight tip leaves and for
having its lowermost perigynia horizontally orientated.
Distribution: Southwestern North American endemic (CAL).
Ecology: Non-glaciated plateaus and wet banks. 3400 - 3900 m.
92
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96
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Appendix S1
97
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Supporting Tables
Table 2.1: Diagnostic morphological characteristics used by Smith (1940) and Nilson
(1991) to differentiate C. capitata from C. arctogena (taken from Reinhammar 1999).
Character
Spike size
Carex capitata
6-9 mm long, light brownishgreen
On average 2.5 mm long and
1.8 mm wide
Pear-shaped, with a beak about
1/5 of the total length; smooth
in the upper part
Carex arctogena
3-6 mm long, dark brownish-green
Pistillate
scale length
Beak length
Shorter than the achenes
As long as the achenes
On average 0.4 mm
Leaf length
Leaves shorter than culms
Tussock
density
Habitat
demands
Loose tussocks
On average 0.6 mm; achene more
abruptly contracted into a beak
Leaves as long or longer than the
culms
Dense tussocks
Achene size
Achene
shape
On average 1.9 mm long and 1.5 mm
wide
More rounded, with a beak about 1/3
of the total length; provided with 3-5
small, sharp, teeth in the upper part
In rich mires, and along Wind-exposed heaths in rather dry
riverlets;
calciphilous; habitats; weakly calciphilous, also on
lowlands subalpinelowalpine
serpentine; mostly alpine, but occurs
rarely in subalpine habitats
98
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Table 2.2: Associates of C. arctogena in South America
Locality
Collection
Elevation Associates
No.
(m)
Argentina:Tierra
J.
Starr 60
Erigeron myosotis, Phleum alpinum,
del Fuego, Rio 10015 & T.
Caltha sagittata, Cerastium arvense,
Grande
Villaverde
Carex macloviana and C. canescens
Argentina: Santa J.
Starr 732
Cruz,
Los 10020 & T.
Glaciares National Villaverde
Park
Nothofagus
antartica,
Marsippospermum
grandiorum,
Chiliotrichum diffusum, Escallonia
sp., Carex microglochin, C. banksii,
C. atropicta, C. canescens,C.
decidua,
Gaultheria
pumila,
Empetrum rubrum and Rostkovia
magellanica
Argentina: Santa J.
Starr 449
Cruz,
Los 10023 & T.
Glaciares National Villaverde
Park
Carex microglochin, C. magellanica,
C. canescens, C. barrosii, Schoenus
andinus, Tetroncium magellanicum,
Escallonia sp., Empetrum rubrum,
Juncus sp., Rubus sp., Chiliotrichum
diffusum, Blechnum penna-marina,
Gaultheria pumila and Gavilea sp.
99
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Table 2.3: Associates of C. cayouetteana subsp. cayouetteana.
Locality
Collection
Elevation pH Associates
No.
(m)
U.S.A.: Colorado, J. Starr 10S- 3602
5
Rhodiola sp., Castilleja sp.,
Lake Co., San 030,
W.
Potentilla sp., Salix spp.Bistorta
Isabel National Sawtell & T.
sp.,Caltha
Forest
Villaverde
leptosepala,Pedicularis
groenlandicum and Carex spp.
U.S.A.: Colorado,
Hinsdale
Co.,
Gunnison
National Forest
J. Starr 10S- 3834
033,
W.
Sawtell & T.
Villaverde
-
Kobresia myosuroides
U.S.A.: Montana,
Carbon
Co.,
Custer National
Forest, AbsarokaBeartooth
Wilderness
U.S.A.:
Wyoming, Park
Co.,
Shoshone
National Forest,
Beartooth Plateau
U.S.A.:
Washington,
Whatcom
Co.,
BakerSnoqualmie
National Forest
J. Starr 10S- 3137
047A,
W.
Sawtell & T.
Villaverde
5.4 Carex scirpoidea and Kobresia
myosuroides. It has also been
reported to occur with Cassiope
mertensiana,
Siebbaldia
procumbens and Stellaria spp.
J. Starr 10S- 3291
047B,
W.
Sawtell & T.
Villaverde
-
-
J. Starr 10S- 1984
061,
W.
Sawtell & T.
Villaverde
5
Phyllodoce empetriformis
Table 2.4: Associates of C. cayouetteana subsp. bajasierra.
Locality
Collection
Elevation pH Associates
No.
(m)
U.S.A.:
California, J. Starr 10S- 1441
7.7 Calocedrus
decurrens,
Butte
Co.,
near 054 & T.
Pseudotsuga
menziesii,
Cherry
Hill Villaverde
Pinus ponderosa, Abies
Campground, Lassen
magniffca,
Darlingtonia
National Forest
californica,
Drosera
anglica, and Spiranthes sp.
U.S.A.:
Deschutes
Deschutes
Forest
Oregon, J. Starr 10S- 1927
Co., 057 & T.
National Villaverde
100
5.8 Kobresia myosuroides
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Table 2.5: Morphological characters studied. Continuous characters used by Egorova
(1999) to differentiate between C. capitata and C. arctogena and those used in a pilot
study to differentiate between C. cayouetteana subsp. cayouetteana, C. cayouetteana
subsp. bajasierra and C. cayouetteana subsp. altasierra are denoted by asterisks.
Character
Continuous
variables
CLMHT
Definition
Description
Culm length
distance from the base of the culm to the
base of the spike for the longest culm
present (current and previous years)
CLMH*
Culm length
CULMW
Culm width
LEAFL
Leaf length
LEAFW
Leaf width
INFLOL*
Inflorescence length
INFLOW*
Inflorescence width
same as CLMHT but present year growth
only
width of the longest culm in the medial
portion
longest leaf from the base of the
pseudoculm to the tip
width of the longest leaf in the medial
portion
maximum length from base of the spike to
the bottom of the uppermost perigynium
beak (=PERBKL)
maximum width of the spike from the
base of the perigynium beak (=PERBKL)
MSPL*
Inflorescence staminate length distance from the top of the
portion
proximal staminate scale to the apex
Inflorescence pistillate length distance from the base of the spike
portion
to the base of the most distance pistillate
beak (=PERBKL)
Length of the pistillate longest hyaline margin from the distal
scale hyaline margin
point of the proximal pistillate scale
FPPL*
GLUMH*
GLUMHC*
Length of the pistillate narrowest hyaline margin from the distal
scale hyaline margin
point of the proximal pistillate scale
FSCL*
Length of the pistillate maximum scale length of the proximal
scale
perigynium
Pistillate scale width
maximum scale width of the proximal
perigynium
Maximum
pistillate length distance from FSCW to the base of
scale width
the scale
Perigynium length
maximum length of the perigynium
including the beak
FSCW*
FSCWL
PERIGL*
101
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________________________________________________________________
PERBKL
PERIGW*
PERIWD
ACHL
ACHW
MSCL*
MSCW
Discrete
variables
LEAFN
PSA
PERIGA
Beak length
distance from distal point of the
perigynium to the distal point of the
achene
Perigynium width
maximum width of the perigynium
Maximum perigynium length distance from PERIGW to the base
width
of the perigynium
Achene length
maximum achene length
Achene width
maximum achene width
Staminate scale length maximum scale length at the medial part
of the staminate portion of the
inflorescence
Staminate scale width
maximum scale width at the medial point
of the staminate portion of the
inflorescence
Leaf number
along the longest culm
Angle of the distal edge less than or greater than 45º
of the pistillate scale
CULMD
Perigynium
beak straight or bent
inclination
Perigynium angle
less than or greater than 45º
Perigynium
teeth along the margins of the perigynium
number
Culm teeth number
number within the distal 1mm of the culm
Qualitative
variable
CULMC
Culm sheath colour
PERIGBo
TEETHN
brown, red-brown, red-purple or purplebrown
102
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Table 2.6: Mean ±1 SD and ranges for 22 morphological characters measured for the C.
capitata complex. Character abbreviations correspond to those described in Table 2.5. All
measurements are in millimeters. N = sample size.
Characte
r
CLMHT
CLMH
LEAFL
CULMW
LEAFW
INFLOW
MSPL
GLUMH
GLUMH
C
INFLOL
FPPL
FSCL
FSCW
FSCWL
PERIGL
PERBKL
PERIGW
PERIWD
ACHW
C. capitata
C. arctogena
(N=38)
296.45±70.5
(150-490)
272.10±82.3
(120-490)
205.92±50.0
(115-360)
0.75±0.09
(0.6-1)
0.59±0.19
(0.4-1.5)
4.41±0.48
(3.3-5.4)
1.95±0.65
(0.8-3.5)
0.56±0.62
(0.01-2.25)
0.19±0.15
C.
cayouetteana
subsp.
cayouetteana
(N=35)
(N=28)
204.03±52.1 204.90±30.44
(125.9-335)
(142-260)
168.89±44.74 178.29±39.83
(100-280)
(116-260)
154.64±47.9 157.49±21.11
(90-298)
(115-195)
0.78±0.15
0.89±0.12
(0.5-1.1)
(0.6-1.1)
0.62±0.12
0.64±0.13
(0.4-1)
(0.4-0.9)
3.83±0.39
4.44±0.61
(2.9-4.7)
(3.5-6.1)
2.12±0.68
3.22±1.40
(1.2-3.7)
(0.9-6.65)
0.97±0.49
0.53±0.36
(0.4-2.6)
(0-1)
0.40±0.17
0.23±0.16
C.
cayouetteana
subsp.
bajasierra
(N=24)
354.27±72.37
(225-540)
347.73±75.68
(193-540)
206.97±41.68
(133-270)
0.88±0.08
(0.7-1)
0.65±0.12
(0.5-0.9)
3.86±0.43
(3.2-4.6)
5.36±2.00
(2-10.5)
0.39±0.52
(0.01-1.8)
0.09±0.10
C.
cayouetteana
subsp.
altasierra
(N=6)
58.03±24.75
(140-205)
110.78±22.56
(83-140)
113.08±19.27
(85-140)
0.83±0.12
(0.7-1)
0.58±0.17
(0.4-0.9)
3.07±0.69
(2.5-4)
3.05±1.03
(2.2-4.9)
1.35±0.74
(0.01-2)
0.27±0.18
(0.01-0.5)
7.52±1.20
(5.5-10.3)
4.78±0.89
(2.7-7.2)
2.12±0.25
(1.5-2.5)
1.43±0.21
(0.8-1.8)
0.61±0.16
(0.3-1)
2.99±0.45
(1.8-3.6)
1.28±0.24
(0.8-1.7)
1.79±0.21
(1.3-2.2)
0.94±0.20
(0.5-1.3)
1.21±0.13
(0.1-1)
7.34±1.16
(5.2-9.8)
4.46±0.64
(3.5-6)
2.18±0.29
(1.4-3)
1.77±0.34
(1-2.6)
0.68±0.29
(0.1-1.7)
2.65±0.45
(1.5-3.2)
1.13±0.23
(0.7-1.8)
1.50±0.19
(1-2)
0.82±0.19
(0.5-1.3)
1.18±0.18
(0.01-0.3)
11.25±2.33
(6.8-16.9)
5.08±0.83
(3.9-6.9)
2.18±0.33
(1.2-2.7)
1.74±0.24
(1.4-2.2)
0.65±0.24
(0.2-1)
2.35±0.45
(1.5-3.1)
1.01±0.22
(0.7-1.4)
1.66±0.17
(1.2-2.2)
0.77±0.18
(0.4-1)
1.16±0.16
(0.01-0.5)
7.65±0.87
(6.2-8.5)
3.70±0.84
(2-4.2)
1.93±0.12
(1.8-2.1)
1.53±0.35
(1.15-2)
0.60±0.13
(0.4-0.8)
2.55±0.64
(2-3.8)
0.97±0.35
(0.6-1.6)
1.50±0.26
(1.1-1.9)
0.75±0.14
(0.5-0.9)
1.23±0.35
(0-0.5)
9.11±1.63
(6.1-12.8)
5.00±0.80
(3.9-6.4)
2.43±0.24
(1.9-3)
1.73±0.27
(1.1-2.4)
0.77±0.25
(0.1-1.3)
2.80±0.38
(1.5-3.4)
1.23±0.22
(0.9-1.9)
1.96±0.31
(1.2-2.5)
0.81±0.29
(0.3-1.8)
1.23±0.22
103
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________________________________________________________________
ACHL
MSCL
MSCW
(1-1.5)
1.72±0.21
(1.1-2.1)
2.19±0.26
(1.6-2.9)
1.02±0.23
(0.6-1.5)
(0.7-1.7)
1.61±0.15
(1.4-1.9)
1.86±0.35
(1-2.8)
1.12±0.21
(0.7-1.6)
(0.6-1.8)
1.59±0.24
(1-2.3)
2.28±0.30
(1.8-3)
1.16±0.27
(0.6-1.9)
104
(0.5-1.4)
1.55±0.23
(1-2)
2.24±0.29
(1.6-2.9)
1.23±0.24
(0.8-1.8)
(1-1.9)
1.82±0.43
(1.4-2.6)
2.20±0.20
(1.9-2.5)
1.04±0.10
(0.9-1.2)
________________________________________________________________
________________________________________________________________
Table 2.7: Mean ± 1 SD and ranges for morphological characters measured for C.
arctogena from South America vs. North America and Europe. Character abbreviations
correspond to those described in Table 2.5. All measurements are in millimeters. N =
sample size.
Character
CLMHT
CULMW
CLMH
LEAFL
LEAFW
LEAFN
INFLOW
INFLOL
MSPL
FPPL
GLUMH
GLUMHC
FSCL
FSCW
FSCWL
PERIGL
PERBKL
PERIGW
PERIWD
TEETHN
ACHW
ACHL
MSCL
MSCW
CULMD
C. arctogena from C. arctogena
Europe
North America
(N=10)
(N=23)
179.52 ± 32.28
217.54 ± 58.46
7.70 ± 1.64
8.02 ± 1.47
153.10 ± 34.37
72.52 ± 50.73
130.72 ± 29.53
60.61 ± 45.73
6.00 ± 0.67
6.24 ± 1.35
3.80 ± 0.42
3.52 ± 0.79
36.30 ± 3.68
38.43 ± 3.82
72.80 ± 13.85
71.48 ± 9.76
20.60 ± 7.76
20.04 ± 6.11
42.20 ± 6.71
44.96 ± 6.53
8.90 ± 1.73
9.35 ± 5.36
4.40 ± 0.97
4.13 ± 1.98
22.00 ± 2.16
21.04 ± 2.48
17.40 ± 3.17
16.52 ± 3.10
6.50 ± 2.59
7.26 ± 3.08
25.20 ± 3.05
25.87 ± 4.98
11.67 ± 3.24
10.95 ± 2.08
14.70 ± 1.25
14.83 ± 2.04
6.80 ± 1.69
8.91 ± 2.56
4.56 ± 1.13
4.22 ± 3.15
11.89 ± 1.54
11.41 ± 2.02
15.78 ± 1.56
16.36 ± 1.36
18.50 ± 3.69
18.22 ± 2.52
11.20 ± 2.66
10.89 ± 1.35
5.70 ± 3.13
8.30 ± 4.34
from C. arctogena
South America
(N=6)
221.28 ± 77.22
8.00 ± 2.10
195.99 ± 65.20
94.31 ± 70.21
6.83 ± 1.47
3.33 ± 0.52
43.17 ± 2.79
93.50 ± 20.54
33.17 ± 13.09
51.50 ± 5.47
12.33 ± 4.80
4.00 ± 1.79
24.67 ± 4.46
22.67 ± 2.66
6.50 ± 3.39
30.50 ± 2.59
13.00 ± 1.55
16.83 ± 2.48
9.00 ± 3.16
7.83 ± 3.87
12.67 ± 1.51
15.83 ± 1.72
23.67 ± 5.68
12.83 ± 3.19
7.50 ± 5.01
from
Table 2.8: Mann-Whitney significance for pairwise comparisons of each signifcant
variable from the Kruskal-Wallis test, ordered by its utility to significantly differentiate
between taxa. N denotes no significance, Y denotes significance with p<0.05 and Y*
denotes significance with p <0.01. Variables in bold were included in the Principal
components analysis. Carex capitata (C), C. arctogena (A), C. cayouetteana subsp.
cayouetteana (Y), C. cayouetteana subsp. bajasierra (Y2) and C. cayouetteana subsp.
altasierra (Y3).
105
________________________________________________________________
________________________________________________________________
Variable
CLMH
CLMHT
MSPL
LEAFL
INFLOL
PERIGW
GLUMHC
INFLOW
FSCL
MSCW
FSCW
MSCL
CULMW
GLUMH
ACHL
FPPL
PERIBKL
PERIGL
FSCWL
PERIWD
Y3-Y2
Y
Y
N
Y
Y
N
N
N
N
N
N
N
N
N
N
Y
N
N
N
N
Y3-Y
Y
N
Y
Y
N
N
N
Y
Y
N
N
N
N
N
N
N
N
N
N
N
Y3-A
Y
Y
Y
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
Y3-C
Y
Y
Y
Y
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
106
Y2-Y
Y*
Y*
Y
Y*
Y
Y
Y
Y*
Y
N
N
N
N
N
N
N
Y
Y
N
N
Y2-A
Y*
Y*
Y*
Y*
Y*
Y
Y*
N
N
Y
N
Y*
Y*
Y*
N
Y
N
N
N
N
Y2-C
Y
Y
Y*
N
Y*
Y
Y
Y*
N
Y
Y*
N
Y
N
Y
N
Y
Y
N
Y
Y-A
N
N
Y
N
Y*
Y*
Y
Y*
Y*
N
N
Y*
Y*
Y
N
Y
N
N
N
N
Y-C
Y*
Y*
Y
Y*
Y
Y
N
N
Y*
Y*
Y*
N
N
N
Y
N
N
N
Y
N
A-C
Y*
Y*
N
Y*
N
Y*
Y*
Y*
N
Y
Y*
Y
N
Y
Y
N
Y
Y
N
N
________________________________________________________________
________________________________________________________________
Table 2.9: Percentage of the
total variance explained by
principal component scores of
the variables included in di
erent PCAs. PC = Ordered
principal Component.
PC
All
variables
1
19,401
2
12,4
3
10,989
4
7,6767
5
6,7801
6
6,0676
7
5,2372
8
4,3777
9
3,8413
10
3,4106
11
3,0812
12
2,899
13
2,7171
14
2,2072
15
1,9515
16
1,7454
17
1,3808
18
1,347
19
1,1537
20
1,0073
21
0,21384
22
0,1153
Total 100
12
variables
28,53
16,709
12,48
10,307
7,8787
6,4935
5,0133
4,467
3,0117
2,774
2,1061
0,23034
100
107
________________________________________________________________
________________________________________________________________
Supporting Figures
Figure 1. The distribution of C. arctogena based on all the herbarium specimens
examined in this study. Inset represents the distribution in Scandinavia.
108
________________________________________________________________
________________________________________________________________
Figure 2. Distribution of C. capitata, C. arctogena, C. cayouetteana subsp.
cayouetteana, C. cayouetteana subsp. bajasierra and C. cayouetteana subsp. altasierra
herbarium specimens used in the morphological study.
109
________________________________________________________________
________________________________________________________________
Figure 3. Photographs of herbarium sheets of C. cayouetteana subsp. bajasierra
identified as C. capitata from CHSC. Inset shows spike and perigynium details.
110
________________________________________________________________
________________________________________________________________
Figure 4. Photographs of herbarium sheets of C. cayouetteana subsp. altasierra
identified as C. arctogena from CAL. Inset shows spike and perigynium details.
111
________________________________________________________________
________________________________________________________________
Figure 5. Photographs of herbarium sheets of C. cayouetteana subsp. cayouetteana
identified as C. arctogena from COLO. Inset shows spike and perigynium details.
112
________________________________________________________________
________________________________________________________________
Figure 6. Photographs of herbarium sheets of C. arctogena form H. Inset shows spike
and perigynium details.
113
________________________________________________________________
________________________________________________________________
Figure 7. Photographs of a herbarium sheet of C. capitata from H. Inset shows spike
and perigynium details.
114
________________________________________________________________
________________________________________________________________
Figure 8. PCA scatter plot of the first two principal component using C. arctogena
specimens from Europe (circles), North America (triangles) and South America
(crosses) and 12 quantitative variables.
115
________________________________________________________________
________________________________________________________________
Figure 9. PCA scatter plot of the first two components using all C. arctogena and C.
capitata specimens studied and 12 quantitative variables. Symbols represent C. capitata
(circles), C. arctogena from the Northern Hemisphere (triangles) and C. arctogena from
the Southern Hemisphere (crosses).
116
________________________________________________________________
________________________________________________________________
Figure 10. PCA scatter plot of the first two components using all specimens studied of
C. arctogena (crosses), C. cayouetteana subsp. cayouetteana (dark gray traingles), C.
cayouetteana subsp. bajasierra (medium gray triangles) and C. cayouetteana subsp.
altasierra (light gray trinalges) and 12 quantitative variables.
Figure 11. PCA scatter plot of the first two components using all specimens studied of
117
________________________________________________________________
________________________________________________________________
C. cayouetteana subsp. cayouetteana (dark gray traingles), C. cayouetteana subsp.
bajasierra (medium gray triangles) and C. cayouetteana subsp. altasierra (light gray
trinalges) and 12 quantitative variables.
118
________________________________________________________________
________________________________________________________________
Figure 12. PCA scatter plot of the first two components using all specimens of C.
arctogena (crosses), C. cayouetteana subsp. cayouetteana (medium gray triangles) and
C. cayouetteana subsp. altasierra (light gray triangles) and 12 quantitative variables.
119
________________________________________________________________
________________________________________________________________
Figure 13. PCA scatter plot of the first two components using C. arctogena (crosses)
and C. cayouetteana subsp. altasierra (light gray triangles) specimens and 12
quantitative variables.
120
________________________________________________________________
________________________________________________________________
Figure 14. Scanning electron photographs of silica bodies of all putative taxa in the C.
capitata complex. (A) Carex capitata, A. Dutilly & E. Lepage 16761 (CAN-17332)
from Ontario; (B) C. arctogena, J. Starr 10023 & T. Villaverde (CAN) from Argentina;
(C) C. cayouetteana subsp. cayouetteana, K. H. Lackschewitz 9909 (MONTU-86558)
from Montana;(D) C. cayouetteana subsp. bajasierra, J. Starr & J. Thibeault 07-44
from California (CAN); (E) C. cayouetteana subsp. altasierra, C. W. Sharsmith 2681
(CAN-162869). See Table A.9 for additional specimen voucher information.
121
________________________________________________________________
________________________________________________________________
Figure 15. The distribution of C. capitata based on all the herbarium specimens
examined in this study. Inset represents the distribution in Scandinavia.
122
________________________________________________________________
________________________________________________________________
Additional information
123
________________________________________________________________
________________________________________________________________
Table A.1: Kruskal-Wallis test. Chi-square value,
degrees of freedom (df) and P-value are shown for
each variable.
Variable
KruskalWallis
CLMHT 76.238
CLMH
780.187
LEAFL
447.911
CULMW 299.697
LEAFW 69.523
INFLOW 442.021
MSPL
592.884
GLUMH 28.639
GLUMHC 451.364
INFLOL 549.027
FPPL
179.482
FSCL
28.635
FSCW
334.419
FSCWL
104.719
PERIGL 321.547
PERBKL 237.847
PERIGW 532.796
PERIWD 132.667
ACHW
31.064
ACHL
145.449
MSCL
307.368
MSCW
127.065
chi-square
df
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
p- value
1,09E-12
4,58E-13
4,39E-06
4,96E-03
0.1384
5,83E-06
4,09E-09
9,26E-03
3,73E-06
3,41E-08
0.001263
9,27E-03
9,70E-04
0.03319
1,78E-03
8,82E-02
7,45E-08
0.01004
0.5402
0.005745
3,46E-03
0.01280
124
CLMHT
CLMH
LEAFL
CULMW
LEAFW
INFLOW
MSPL
GLUMH
GLUMHC
INFLOL
FPPL
FSCL
FSCW
FSCWL
PERIGL
PERBKL
PERIGW
PERIWD
ACHW
ACHL
MSCL
MSCW
CLMHT
1,0
0,9
0,8
0,0
0,0
0,1
0,3
0,2
0,3
0,4
0,2
0,0
0,1
0,0
0,0
0,0
0,1
0,0
0,1
0,0
0,2
0,1
CLMH
1,0
0,7
0,0
0,0
0,1
0,4
0,2
0,3
0,4
0,2
0,0
0,0
0,0
0,1
0,0
0,1
0,1
0,0
0,0
0,2
0,1
LEAFL
1,0
0,1
0,1
0,2
0,2
0,1
0,2
0,3
0,2
0,1
0,0
0,0
0,1
0,1
0,1
0,0
0,1
0,0
0,2
0,1
CULMW
1,0
0,2
0,1
0,3
0,2
0,1
0,3
0,2
0,3
0,2
0,2
0,2
0,0
0,2
0,1
0,1
0,0
0,1
0,2
LEAFW
1,0
0,1
0,1
0,1
0,0
0,1
0,1
0,1
0,1
0,0
0,2
0,0
0,1
0,1
0,1
0,1
0,1
0,1
1,0
0,1
0,2
0,9
0,2
0,2
0,3
0,2
0,1
0,1
0,1
0,2
0,0
0,0
0,3
0,4
INFLO
W
MSPL
1,0
0,0
0,1
0,1
0,2
0,5
0,3
0,1
0,0
0,4
0,5
0,5
0,1
0,2
0,1
0,4
0,0
GLUMH
1,0
0,6
0,1
0,2
0,0
0,2
0,0
0,1
0,0
0,2
0,1
0,1
0,1
0,1
0,1
1,0
0,5
0,3
0,3
0,2
0,1
0,1
0,2
0,2
0,0
0,0
0,4
0,4
GLUMH
C
INFLOL
1,0
0,2
0,1
0,1
0,1
0,1
0,1
0,0
0,2
0,0
0,1
0,0
0,2
0,0
FPPL
1,0
0,2
0,2
0,0
0,1
0,2
0,2
0,1
0,0
0,0
0,3
0,0
FSCL
1,0
0,2
0,1
0,1
0,0
0,1
0,0
0,1
0,1
0,3
FSCW
125
1,0
0,4
0,4
0,1
0,2
0,3
0,1
0,1
0,0
0,2
0,2
FSCWL
1,0
0,2
0,0
0,2
0,1
0,1
0,1
0,0
0,2
PERIGL
1,0
0,5
0,4
0,2
0,3
0,2
0,2
0,1
PERBKL
1,0
0,3
0,1
0,2
0,1
0,1
0,1
1,0
0,0
0,3
0,1
0,4
0,1
1,0
0,1
0,0
0,0
0,1
PERIG
W
PERIWD
Table A.2: Correlation matrix for 22 continuous variables used in the morphometric study.
ACHL
ACHW
1,0
0,5 1,0
0,2 0,1 1,0
0,1 0,0 0,2 1
MSCL
________________________________________________________________
Chapter 2. Taxonomy
________________________________________________________________
of the Carex capitata complex
MSCW
________________________________________________________________
________________________________________________________________
Table A.4: Summary statistics for the morphometric analysis of C. arctogena.
Abbreviations: n = sample size; sd = standard deviation; mad = median absolute
deviation; se= standard error.
Variable
n
CLMHT
mean
sd
median
trimmed
mad
min
max
range
skew
kurtosis
se
35 204.03
52.16
190.5
200.03
45.29
125.9
335.05
209.15
0.68
-0.29
8.82
CLMH
35 168.89
44.74
169.0
165.20
38.62
100.7
280.05
179.35
0.64
-0.09
7.56
LEAFL
35 154.64
47.90
145.5
150.61
52.34
90.5
298.70
208.20
0.87
0.32
8.10
CULMW
35 0.78
0.15
0.8
0.78
0.15
0.5
1.10
0.60
0.03
-0.97
0.03
LEAFW
35 0.62
0.12
0.6
0.61
0.15
0.4
1.00
0.60
0.65
0.98
0.02
INFLOW
35 3.83
0.39
3.8
3.83
0.44
2.9
4.70
1.80
-0.02
-0.46
0.07
MSPL
35 2.12
0.68
2.0
2.09
0.74
1.2
3.70
2.50
0.46
-0.95
0.12
GLUMH
35 0.97
0.49
0.9
0.88
0.30
0.4
2.60
2.20
1.70
2.56
0.08
GLUMHC 35 0.40
0.17
0.4
0.40
0.15
0.1
1.00
0.90
0.98
2.64
0.03
INFLOL
35 7.34
1.16
7.4
7.30
1.19
5.2
9.80
4.60
0.41
-0.64
0.20
FPPL
35 4.46
0.64
4.5
4.43
0.74
3.5
6.00
2.50
0.34
-0.51
0.11
FSCL
35 2.18
0.29
2.1
2.17
0.15
1.4
3.00
1.60
0.43
1.15
0.05
FSCW
35 1.77
0.34
1.8
1.77
0.30
1.0
2.60
1.60
0.11
0.04
0.06
FSCWL
35 0.68
0.29
0.6
0.66
0.15
0.1
1.70
1.60
1.22
2.79
0.05
PERIGL
35 2.65
0.45
2.7
2.72
0.44
1.5
3.20
1.70
-1.19
0.81
0.08
PERBKL
35 1.13
0.23
1.2
1.12
0.30
0.7
1.80
1.10
0.50
0.80
0.04
PERIGW
35 1.50
0.19
1.5
1.50
0.15
1.0
2.00
1.00
-0.03
0.58
0.03
PERIWD
35 0.82
0.19
0.8
0.82
0.15
0.5
1.30
0.80
0.26
-0.41
0.03
ACHW
35 1.18
0.18
1.2
1.18
0.15
0.7
1.70
1.00
0.07
1.34
0.03
ACHL
35 1.61
0.15
1.6
1.60
0.15
1.4
1.90
0.50
0.61
-0.55
0.03
MSCL
35 1.86
0.35
1.8
1.86
0.30
1.0
2.80
1.80
0.17
0.41
0.06
MSCW
35 1.12
0.21
1.1
1.11
0.15
0.7
1.60
0.90
0.40
-0.36
0.04
126
________________________________________________________________
________________________________________________________________
Table A.5: Summary statistics for the morphometric analysis of C. capitata. Abbreviations:
n = sample size; sd = standard deviation; mad = median absolute deviation; se= standard
error.
Variable
n
CLMHT
CLMH
mean
sd
median
trimmed
mad
min
max
range
skew
kurtosis
se
38 296.45
70.50
290.05
293.55
70.42
150.05
490.05
340.00
0.49
0.12
11.44
38 272.10
82.37
270.70
268.12
66.72
120.05
490.05
370.00
0.53
-0.14
13.36
LEAFL
38 205.92
50.00
210.38
203.87
43.70
115.05
360.05
245.00
0.64
0.70
8.11
CULMW
38 0.75
0.09
0.70
0.74
0.15
0.60
1.00
0.40
0.45
0.46
0.01
LEAFW
38 0.59
0.19
0.60
0.57
0.15
0.40
1.50
1.10
2.78
10.06
0.03
INFLOW
38 4.41
0.48
4.45
4.43
0.52
3.30
5.40
2.10
-0.14
-0.50
0.08
MSPL
38 1.95
0.65
1.85
1.93
0.74
0.80
3.50
2.70
0.25
-0.77
0.11
GLUMH
38 0.56
0.62
0.50
0.46
0.59
0.01
2.25
2.24
1.39
1.24
0.10
GLUMHC
38 0.19
0.15
0.15
0.18
0.21
0.01
0.50
0.49
0.21
-1.44
0.02
INFLOL
38 7.52
1.20
7.40
7.51
1.33
5.50
10.30
4.80
0.16
-0.90
0.19
FPPL
38 4.78
0.89
4.60
4.71
0.67
2.70
7.20
4.50
0.74
0.92
0.14
FSCL
38 2.12
0.25
2.20
2.14
0.22
1.50
2.50
1.00
-0.72
0.03
0.04
FSCW
38 1.43
0.21
1.40
1.43
0.15
0.80
1.80
1.00
-0.49
0.60
0.03
FSCWL
38 0.61
0.16
0.60
0.60
0.15
0.30
1.00
0.70
0.16
-0.28
0.03
PERIGL
38 2.99
0.45
3.10
3.04
0.30
1.80
3.60
1.80
-1.09
0.69
0.07
PERBKL
38 1.28
0.24
1.30
1.29
0.30
0.80
1.70
0.90
-0.39
-0.74
0.04
PERIGW
38 1.79
0.21
1.80
1.79
0.30
1.30
2.20
0.90
-0.30
-0.52
0.03
PERIWD
38 0.94
0.20
1.00
0.94
0.22
0.50
1.30
0.80
-0.26
-0.86
0.03
ACHW
38 1.21
0.13
1.20
1.21
0.15
1.00
1.50
0.50
0.08
-0.69
0.02
ACHL
38 1.72
0.21
1.70
1.73
0.15
1.10
2.10
1.00
-0.86
0.82
0.03
MSCL
38 2.19
0.26
2.20
2.19
0.15
1.60
2.90
1.30
0.17
0.46
0.04
MSCW
38 1.02
0.23
1.00
1.02
0.30
0.60
1.50
0.90
0.16
-0.81
0.04
127
________________________________________________________________
________________________________________________________________
Table A.6: Summary statistics for the morphometric analysis of Carex cayouetteana subsp.
cayouetteana. Abbreviations: n = sample size; sd = standard deviation; mad = median
absolute deviation; se= standard error.
Variable
n
CLMHT
mean
sd
median
trimmed
mad
min
max
range
skew
kurtosis
se
28 204.90
30.44
205.23
205.15
22.24
142.72
260.50
117.78
-0.09
-0.25
5.75
CLMH
28 178.29
39.83
182.12
177.94
51.32
116.00
260.05
144.05
-0.04
-1.16
7.53
LEAFL
28 157.49
21.11
160.05
157.93
25.39
115.05
195.70
80.65
-0.15
-1.00
3.99
CULMW
28 0.89
0.12
0.90
0.89
0.15
0.60
1.10
0.50
-0.33
-0.34
0.02
LEAFW
28 0.64
0.13
0.60
0.63
0.15
0.40
0.90
0.50
0.29
-0.62
0.02
INFLOW
28 4.44
0.61
4.35
4.39
0.52
3.50
6.10
2.60
1.07
0.61
0.11
MSPL
28 3.22
1.40
3.25
3.13
1.11
0.90
6.65
5.75
0.50
0.05
0.27
GLUMH
28 0.53
0.36
0.50
0.53
0.52
0.00
1.00
1.00
-0.08
-1.43
0.07
GLUMHC 28 0.23
0.16
0.25
0.23
0.22
0.00
0.50
0.50
0.07
-1.27
0.03
INFLOL
28 9.11
1.63
9.40
9.09
1.56
6.10
12.80
6.70
0.04
-0.63
0.31
FPPL
28 5.00
0.80
5.00
4.97
0.96
3.90
6.40
2.50
0.23
-1.34
0.15
FSCL
28 2.43
0.24
2.45
2.42
0.22
1.90
3.00
1.10
0.09
0.27
0.05
FSCW
28 1.73
0.27
1.65
1.72
0.22
1.10
2.42
1.32
0.27
0.09
0.05
FSCWL
28 0.77
0.25
0.77
0.78
0.22
0.10
1.30
1.20
-0.17
0.38
0.05
PERIGL
28 2.80
0.38
2.90
2.84
0.30
1.50
3.40
1.90
-1.45
2.98
0.07
PERBKL
28 1.23
0.22
1.20
1.20
0.15
0.90
1.90
1.00
1.44
1.95
0.04
PERIGW
28 1.96
0.31
1.90
1.99
0.30
1.20
2.50
1.30
-0.59
0.34
0.06
PERIWD
28 0.81
0.29
0.75
0.80
0.37
0.30
1.80
1.50
1.13
2.59
0.05
ACHW
28 1.23
0.22
1.20
1.22
0.15
0.60
1.80
1.20
0.16
2.34
0.04
ACHL
28 1.59
0.24
1.60
1.59
0.15
1.00
2.30
1.30
0.32
1.38
0.05
MSCL
28 2.28
0.30
2.20
2.26
0.30
1.80
3.00
1.20
0.47
-0.31
0.06
MSCW
28 1.16
0.27
1.13
1.16
0.19
0.60
1.90
1.30
0.28
0.75
0.05
128
________________________________________________________________
________________________________________________________________
Table A.7: Summary statistics for the morphometric analysis of C. cayouetteana subsp.
bajasierra. Abbreviations: n = sample size; sd = standard deviation; mad = median absolute
Variable
n
mean
sd
median trimmed mad
CLMHT
28 204.90 30.44 205.23
205.15
22.24 142.72 260.50 117.78 -0.09 -0.25
5.75
CLMH
28 178.29 39.83 182.12
177.94
51.32 116.00 260.05 144.05 -0.04 -1.16
7.53
LEAFL
28 157.49 21.11 160.05
157.93
25.39 115.05 195.70 80.65
-0.15 -1.00
3.99
CULMW
28 0.89
0.12
0.90
0.89
0.15
0.60
1.10
0.50
-0.33 -0.34
0.02
LEAFW
28 0.64
0.13
0.60
0.63
0.15
0.40
0.90
0.50
0.29
-0.62
0.02
INFLOW
28 4.44
0.61
4.35
4.39
0.52
3.50
6.10
2.60
1.07
0.61
0.11
MSPL
28 3.22
1.40
3.25
3.13
1.11
0.90
6.65
5.75
0.50
0.05
0.27
GLUMH
28 0.53
0.36
0.50
0.53
0.52
0.00
1.00
1.00
-0.08 -1.43
0.07
GLUMHC 28 0.23
0.16
0.25
0.23
0.22
0.00
0.50
0.50
0.07
-1.27
0.03
INFLOL
28 9.11
1.63
9.40
9.09
1.56
6.10
12.80
6.70
0.04
-0.63
0.31
FPPL
28 5.00
0.80
5.00
4.97
0.96
3.90
6.40
2.50
0.23
-1.34
0.15
FSCL
28 2.43
0.24
2.45
2.42
0.22
1.90
3.00
1.10
0.09
0.27
0.05
FSCW
28 1.73
0.27
1.65
1.72
0.22
1.10
2.42
1.32
0.27
0.09
0.05
FSCWL
28 0.77
0.25
0.77
0.78
0.22
0.10
1.30
1.20
-0.17 0.38
0.05
PERIGL
28 2.80
0.38
2.90
2.84
0.30
1.50
3.40
1.90
-1.45 2.98
0.07
PERBKL
28 1.23
0.22
1.20
1.20
0.15
0.90
1.90
1.00
1.44
1.95
0.04
PERIGW
28 1.96
0.31
1.90
1.99
0.30
1.20
2.50
1.30
-0.59 0.34
0.06
PERIWD
28 0.81
0.29
0.75
0.80
0.37
0.30
1.80
1.50
1.13
2.59
0.05
ACHW
28 1.23
0.22
1.20
1.22
0.15
0.60
1.80
1.20
0.16
2.34
0.04
ACHL
28 1.59
0.24
1.60
1.59
0.15
1.00
2.30
1.30
0.32
1.38
0.05
MSCL
28 2.28
0.30
2.20
2.26
0.30
1.80
3.00
1.20
0.47
-0.31
0.06
MSCW
28 1.16
0.27
1.13
1.16
0.19
0.60
1.90
1.30
0.28
0.75
0.05
129
min
max
range
skew kurtosis se
________________________________________________________________
________________________________________________________________
Table A.8: Summary statistics for the morphometric analysis of C. cayouetteana subsp.
altasierra. Abbreviations: n = sample size; sd = standard deviation; mad = median absolute
Variable
n mean
sd
median trimmed mad
min
max
range skew kurtosis se
CLMHT
6 158.03 24.75 147.53
158.03
9.25
CLMH
6 110.78 22.56 112.53
110.78
26.39 83.97
140.05 56.08 0.03
LEAFL
6 113.08 19.27 114.03
113.08
CULMW
6 0.83
0.12
0.85
LEAFW
6 0.58
0.17
INFLOW
6 3.07
0.69
MSPL
6 3.05
GLUMH
-0.74
10.10
-2.01
9.21
18.35 85.00
140.05 55.05 -0.07 -1.55
7.87
0.83
0.15
0.70
1.00
0.30
0.04
-1.88
0.05
0.55
0.58
0.07
0.40
0.90
0.50
0.80
-0.86
0.07
2.70
3.07
0.22
2.50
4.00
1.50
0.51
-1.94
0.28
1.03
2.85
3.05
0.82
2.20
4.90
2.70
0.77
-1.06
0.42
6 1.35
0.74
1.45
1.35
0.59
0.01
2.00
1.99
-0.77 -0.99
0.30
GLUMHC 6 0.27
0.18
0.30
0.27
0.22
0.01
0.50
0.49
-0.20 -1.76
0.07
INFLOL
6 7.65
0.87
8.00
7.65
0.52
6.20
8.50
2.30
-0.62 -1.48
0.36
FPPL
6 3.70
0.84
4.00
3.70
0.00
2.00
4.20
2.20
-1.33 -0.13
0.34
FSCL
6 1.93
0.12
1.95
1.93
0.15
1.80
2.10
0.30
0.04
-1.88
0.05
FSCW
6 1.53
0.35
1.46
1.53
0.43
1.15
2.00
0.85
0.23
-1.94
0.14
FSCWL
6 0.60
0.13
0.60
0.60
0.00
0.40
0.80
0.40
0.00
-0.92
0.05
PERIGL
6 2.55
0.64
2.40
2.55
0.22
2.00
3.80
1.80
1.09
-0.48
0.26
PERBKL
6 0.97
0.35
0.95
0.97
0.22
0.60
1.60
1.00
0.72
-0.96
0.14
PERIGW
6 1.50
0.26
1.50
1.50
0.15
1.10
1.90
0.80
0.00
-1.15
0.11
PERIWD
6 0.75
0.14
0.80
0.75
0.07
0.50
0.90
0.40
-0.76 -0.95
0.06
ACHW
6 1.23
0.35
1.10
1.23
0.15
1.00
1.90
0.90
1.05
-0.63
0.14
ACHL
6 1.82
0.43
1.75
1.82
0.30
1.40
2.60
1.20
0.81
-0.89
0.17
MSCL
6 2.20
0.20
2.20
2.20
0.15
1.90
2.50
0.60
0.00
-1.29
0.08
MSCW
6 1.04
0.10
1.04
1.04
0.07
0.90
1.20
0.30
0.10
-1.45
0.04
130
140.50 205.05 64.55 1.01
________________________________________________________________
________________________________________________________________
Studied specimens of C. arctogena
Argentina, Chubut, Los Alerces National Park, Soriano, A., 30.3.1952, (BAA). Dept.
Chos Malal, 2300 m, Boelcke, O., Correa, M.N.; Bacigalupo, N.M., 30.1.1964, (BAA,
11368). Mendoza, Cordillera del Rio Barrancas, Kurtz, F., 16.11.1888, (MICH).
Canada, Alberta, Mercoal, Rousseau, J., 18.7.1947, (COLO, 13811). Alberta,
Mercoal, 4300 ft, Malte, M.O., Watson, W.R., 8.8.1925, (RM, 280606). British
Columbia, Pine Pass, 1402 m, Argus, G.W., 12.7.1973, (CAN, 372267). British
Columbia, 7228 ft, Calder, J., 149035, Parmelee, J.A.; Taylor, R.L., 8.8.1956,
(COLO, 149035). British Columbia, Mount Apex, 7100 ft, Calder, J., Savile, O.,
11.8.1953, (RM, 252249). Manitoba, Fort Chimo, Rousseau, J., 14.8.1951, (WIN,
22355). Manitoba, Baralzon Lake, Scoggan, H.J., 22434, Baldwin, W.K.W., 28.7.1950,
(WIN, 22434). Manitoba, Hudsons Bay Co., Duck Lake, Scoggan, H.J., Baldwin,
W.K.W., 10.8.1950, (WIN, 22435). Manitoba, Fort Chimo, Legault, A., 22.7.1963,
(COLO, 491481). Manitoba, Hudsons Bay Co., Duck Lake, Scoggan, H.J., Baldwin,
W.K.W., 10.8.1950, (CAN, 201506). Manitoba, Baralzon Lake, Scoggan, H.J.,
Baldwin, W.K.W., 30.7.1950, (CAN, 202500). Manitoba, Nueltin Lake, Baldwin,
W.K.W., 26.7.1951, (CAN, 212816). Manitoba, Cochrane River, Baldwin, W.K.W.,
3.7.1951, (CAN, 212817). Manitoba, Cochrane River, Baldwin, W.K.W., 3.7.1951,
(CAN, 212817). Manitoba, Baralzon Lake, Scoggan, H.J.,Baldwin, W.K.W.,
28.7.1950, (CAN, 201507). Newfoundland-Labrador, Esker area, Mäkinen, Y.,
Kankainen, E. 21.7.1967, (CAN, 314758). Newfoundland-Labrador, Esker area, 838
m, Mäkinen, Y.Kankainen, E.21.7.1967, (CAN, 314758). Newfoundland-Labrador,
Twin Falls, Hustich, I., 6.7.1967, (CAN, 313311). Nunavut, Upper Hood River,
Gould, W., 7.1995, (COLO, 475773). Ontario, Kenora District, Patricia PortionRiley,
J.L., 12.8.1980, (CAN). Ontario, Hudson Bay Lowlands, Porsild, A.E., Baldwin,
W.K.W.4.7.1957, (CAN, 278707). Quebec, Fort Chimo, Sørensen, T.H., 17.8.1959,
(C). Quebec, Baie dUngava, Blondeau, M., 1.8.1993, (WIN, 53902). Quebec, Baie
dUngava, Rousseau, J., 23.7.1951, (WIN, 22356). Quebec,Lac Jaucourt Region
Lichteneger Lake,487 m Argus, G.W., 16.7.1974, (CAN, 3779977). Quebec,
Boatswain Bay, Baldwin, W.K.W., 17333, Hustich, I.; Kucyniak, J.; Tuomikoski, R.,
8.7.1947, (CAN, 17333). Quebec, Lac Payne, Legault, A., 23398, 2.8.1965, (CCO,
23398). Quebec, Northern QuebecLake Payne, Legault, A.,Brisson, S. 2.8.1965,
(COLO, 210789). Quebec, Ungava, Husons Bay, Dutilly, A., Lepage, E., 21.3.1945,
(RM, 233644). Quebec, Fort Chimo, Calder, J., 31.7.1948, (RM, 255325).
Quebec,Hudson Bay Cairn Island, Abbe, E.C.,Abbe, L.B.; Marr, J. 30.7.1939, (RM,
252521). Quebec, Hudson Bay,Great Whale River Calder, J.Savile, O.; Kukkonen, I.,
8.8.1959, (RM, 260486). Quebec, Lac Kopeteokash, Rousseau, J., 18.7.1947,
(RM, 228636). Saskatchewan, Vicinity of Patterson Lake, Argus, G.W., 20.7.1963,
(CAN, 282691). Saskatchewan, Vicinity of Patterson Lake, Argus, G.W.,
20.7.1963, (CAN, 282691).Saskatchewan, Northeastern SaskatchewanPatterson
Lake , Argus, G.W., 20.7.1963, (RM, 277437). Enontekiö, KilpisjärviSaana, 750 m
Roivainen, L., 8.7.1935, (H, 127310). Enontekiö, KilpisjärviSaana, 750 mVäre, H.,
29.7.2004, (H, 805587). Enontekiö Lapland, 825 m, Väre, H., 17.7.2006, (H,
809948). Inari, Vätsäri Wilderness Area, Kulmala, H., 27.7.1996, (H, 717201).
Lapponia Imandrae, Lindén, J., 18.7.1891, (H, 325665). Lapponia Imandrae,
Axelson, W.M., Borg, V., 24.7.1901, (H, 325667).Finland, Lapponia murmanica,
550 m, Brotherus, V.F., 8.1887, (H, 325639). PetsamoCajander, A., 10.7.1927, (H,
325644). Porojärvet, Toskalhar950 m,Roivainen, H.Ollila, L. 15.7.1955, (H,
127313). Porojärvet, Toskalhar, 910 m, Roivainen, H., 15.7.1966, (H, 179889).
Foutell, C.W., Jalan, M.J., 10.8.1899, (H, 325657). Altevatn, 500 m, 17.8.1967, (M,
0151943). Groenlandia meridionalis, Kangerdluarssuk, Hansen, C. 282521,Hansen,
K.; Petersen, M. 4.7.1962, (CAN).Nigerdleq, Jørgensen, L.B. 15.7.1966, (CAN,
311369). Greenland, Vestgrønland, Pingorssuaq Kitdleq, 400 mHanfgarn, S.,
11.8.1983, (C). Tugtilik Lake, 10 m, Elsley, J.E. 15.8.1967, (M, 0151948).
Lagerkranz, J., 2.8.1936, (RMS, 153944). Finnmark,Sör-Varanger Bugöynes,
Toivonen, H., 30.7.1971, (H, 1081734). Finnmark, Sör-Varanger, Bugöynes,
Toivonen, H., 1081733, 30.7.1971, (H, 1081733). Nordland, Narvik hd., Skjomen,
Skifte, O., GRaff, G.; Spjelkavik, S., 11.8.1973 (H). Norland, Sulitjelma, Skifte, O.
1.8.1962, (DAO, 285800). Sverige, Abisko, Paddas, Lid, J., 2.8.1950, (H, 1300264).
Norway, Troms, Bardu, Leinavatn, 498 mEngelskjøn, T.,Engelskjøn, E.M. 7.7.1977,
(C).
Troms, Bardu, Altevatn580 m, 18.8.1967, (M, 0151942). Troms,
Bardu,Kampaksla 780 m, Engelskjøn, T.,Skifte, O. 9.8.1978, (H, 1685049). Petsamo,
Petchenga Vouvatusjärvi, Piirainen, M., 27.7.1995, (H, 1682990). Sweden, Torne
131
________________________________________________________________
________________________________________________________________
Lappmark, Karesuando, 1000 m, Smith, H., 26.7.1933, (DAO, 257429). Torne
Lappmark, Karesuando, 1000 m, Smith, H., 26.7.1993, (H, 1652844). Torne
Lappmark, Jukkasjärvi parish, 550 m, Alm, G., Smith, H. 23.7.1939, (H, 1300259).
New Hampshire, Coos Co., Mt. Washington, Hodgon, A.R., Gale, M., 30.6.1950,
(DAO, 257427). New Hampshire, White Mountains, Mt. Washington, Forbes, F.,
9.8.1902, (RMS, 242089). New Hampshire, Alpine Garden, Mt. Washington,
Sargent, F.H., 5.7.1942, (BRY, 143916). New Hampshire, Alpine Garden, Mt.
Washington,5000 ft Löve, A.,Löve, D. 27.7.1958, (COLO, 288736). New
Hampshire, Alpine Garden, Mt. Washington, Löve, A. ,Löve, D. 3.7.1960, (COLO,
295019). New Hampshire, White MountainsMt. Washington, Forbes, F., 9.8.1902,
(RM, 50212).
Studied specimens of C. capitata
Austria, Innsbruck, Seefeld, 1180 m, HöllerJ. s.n., 26.7.1958, (M, 0151923). Tirol,
Seiser Alp, 2000 m, Görz s.n., 27.7.1914, (GH). Canada, Alberta, Ft. Fitzgerald,
Cody, W.J. 4533 and Loan, C.C., 19.7.1950, (RM, 228683). British Columbia,
Bluster Mt., 2133 m, Thompson, J. s.n. and Thompson, M., 14.7.1938, (WTU,
17326). British Columbia, Mt. Tinsdale, 2133 m, Krajina, J. s.n. and Pojar, J.,
13.8.1974, (UBC, 149191). British Columbia, Mount Apex, 2164 m, Calder, J.
11795 and Savile, O., 11.8.1953, (WTU, 170234). British Columbia, Anahim Lake,
1219 m, Calder, J. 18578, Parmelee, J.A.; Taylor, R.L., 9.7.1956, (WTU,
197744). British Columbia, Anahim Lake, 1219 m, Calder, J. s.n., Parmelee, J.A.;
Taylor, R.L., 9.7.1956, (COLO, 158463). British Columbia, Summit Pass, Raup, H.M.
10788 and Correll, D.S., 24.7.1948, (RM, 272042). Manitoba, Fort Churchill,
Ritchie, J. 2104, 5.8.1956, (WIN, 22433). Manitoba, Wapusk National Park, 10 m,
Punter, E. 03-509 and Piercey-Normore, M., 19.7.2003, (WIN, 71429). Manitoba,
Twin Lakes, Ford, A. 02379, Piercey-Normore, M.; Punter, E.; Punter, D., 25.7.2002,
(WIN, 71024). Manitoba, Fort Churchill, Johnson, K. J73-402, 26.8.1973, (WIN,
33557). Manitoba, Fort Churchill, Shay, J. 59-924a, 9.7.1959, (WIN, 64354).
Manitoba, Fort Churchill, Shay, J. 83-60, 11.7.1983, (WIN, 40808). Manitoba, Fort
Churchill, Zbigniewicz, M. 83-237, 5.8.1983, (WIN, 40839). Manitoba, Wapusk
National Park, 15 m, Ford, A. 02-330, Piercey-Normore, M.; Punter, D.; Punter, E.,
21.7.2002, (WIN, 70209). Manitoba, Wapusk National Park, 23 m, Ford, A. 02-306,
Piercey-Normore, M.; Punter, D.; Punter, E., 20.7.2002, (WIN, 70255). Manitoba,
Vicinity of Churchill, Schofield, W. 6862 and Crum, H., 21.7.1956, (CAN, 247332).
Manitoba, Fort Churchill, Ritchie, J. 2104, 5.8.1956, (CAN, 248387). Manitoba,
Open coastal plain 3 miles East of camp, McFarlane, D.M. 239 and Irvine, B.R.,
7.8.1953, (CAN, 322733). Manitoba, Fort Churchill, Brown, D.K. 733, 12.7.1951,
(CAN, 263696). Manitoba, Fort Churchill, Argus, G.W. 425-58, 4.8.1958, (CAN,
281144). Manitoba, Fort Churchill, Rossbach, G.B. 7073, 5.8.1965, (CAN,
329753). Manitoba, Fort Churchill, s.n., 30.7.1910, (CAN, 17340). Northwest
Territories, Aubry Lake, Riewe, R. 225 and Marsh, J., 17.7.1976, (WIN, 32000).
Northwest Territories, Aubry Lake, Riewe, R. 336 and Marsh, J., 4.8.1976, (WIN,
31438). Northwest Territories, Aubry Lake, Riewe, R. 225 and Marsh, G. .M.,
17.7.1976, (CAN, 433230). Northwest Territories, Kakisa river, Thieret, J.W.
MM3 and Reich, R.J., 18.6.1959, (CAN, 298045). Northwest Territories, Sawmill
Bay, Shacklette, H.T. 2970, 13.7.1948, (CAN, 199991). Ontario, Fort Severn,
Hustich, I. 1296, 13.7.1956, (CAN, 242845). Ontario, Winisk, Lundsden, H. s.n.,
(COLO, 448829). Ontario, Kenora District, Riley, J.L. 5848, 23.8.1976, (CAN,
409561). Ontario, Lake River, Dutilly, A. 16550-16807 and Lepage, E., 12.9.1946,
(CAN, 17332). Quebec, Fort Chimo, Calder, J. 2316, 2.8.1948, (RM, 216050).
Saskatchewan, Hwy #2 Waskesim, Hudson, J. 5063, 31.7.1992, (CAN, 565528).
Yukon, Mile 85 on road from Whitehorse to Dawson, 579 m, Calder, J. 25796 and
Gillett, J., 22.6.1960, (ALA, 1124987). Yukon, Kluane Lake Quad, 1036 m, Scotter,
W. 20992 (Y-18), 2.8.1972, (ALA, 1124986). Yukon, Francis Lake, Duman, G. 70805, 28.7.1970, (ALA, 1124985). Yukon, Ogilvie Mountains, Porsild, A.E. 1462,
Porsild, R., 28.6.1968, (CAN, 318349). Yukon, Alaska Highway at milepost 1149,
Welsh, S.L. 7921, Moore, G., 5.7.1968, (BRY, 71334). Yukon, Rink Rapids,
Macoun, 7922, 9.7.1902, (CAN, 17356). Yukon Territory, Dempster Highway,
Porsild, R. 1593, 17.7.1968, (CAN, 318505).Finland, Enontekiö Lapland, Lake
Raittijärvi, 545 m, Väre, H. 11643, 8.8.2001, (H, 737942). Enontekiön Lappi,
Enontekiö, 520 m, Piirainen, M. 2118 and Piirainen, P., 19.7.1991, (H, 668357).
132
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Enontekiön Lappi, Enontekiö, 600 m, Väre, H. 14955, 1.8.2003, (H, 746021).
Enontekiön Lappi, Goaskinjörvi, Kulmala, H. 83/02, 8.8.2001, (H, 744865). Inari
Lapland, Kevo Research Station, Sulkinoja, M. s.n., 12.9.1967, (M, 0151936). Inarin
Lappi, Kietsimäjoki, Kulmala, H. 8/97, 27.7.1997, (H, 720181). Kainuu, YliNäljänkä, 230 m, Ohenoja, M. 11, 8.8.1990, (H, 696101). Karesuando, Karesuando,
Honkell, J.s.n., 9.8.1923, (M, 0151934). Kemi Lapland, Vesmajärvi, 210 m, Kurtto, A.
1778, Vuokko, S., 10.8.1978, (O, 660352). Kittilä, Mustavaara, 202 m, Ulvinen, T.
s.n., Vilpa, E.; Seitapuro, H., 10.7.1997, (H, 720622). Kuusamo, Liikasenvaara,
Ulvinen, T. s.n., 9.8.1962, (O, 539355)., Kuusamo, Liikasenvaara, Ulvinen, T. s.n.,
9.8.1962, (M, 0151946). Kuusamo, Lake Paanajärvi, Laurila, M. s.n., 9.7.1938, (H,
272411). Kuusamo, Liikasenvaara, Kukkonen, I. s.n., 30.8.1966, (RMS, 284390).
Kuusamo, Liikasenvaara, Ulvinen, T. s.n., 9.8.1962, (CAN, 276804). Kuusamo, NEsection, Paanajärv, Savola, J. s.n., 28.7.1985, (H, 616973). Länsi-Suomen Lääni,
Frösön, Mickström s.n., Lagerheim, C.; Sjögren, G., 8.1844, (GH). Lapland, Upper
Kemi-river, Ulvinen, T. s.n., 12.8.1961, (C). Lapland, Poroeno, 540 m, Väre, H.
11651, 9.8.2001, (H, 737950). Lapland, Kivijärvi, 460 m, Väre, H. 11515,
29.7.2001, (H, 737814). Lapland, Upper Kemi-river, Ulvinen, T. s.n., 12.8.1961, (H,
328698). Lapland, Tulppio district, Vuokko, S. 8, 29.7.1975, (H, 449415). Lapponia,
Muornis, Montell, I. s.n., 17.7.14, (GH). Lapponia, Euvntekiensis, Montell, I. s.n.,
9.8.1923, (M, 0151944). Lapponia, Shishe, Montell, I. s.n., 11.7.1909, (M, 0151913).
Lapponia, Kouda, Brotherus, V.F. s.n. and Brotherus, A.H., .8.1872, (H, 244602).
Lapponia orientalis, Tjavauga, Brenner, M. s.n., 4.7.1863, (H, 1037144). Lapponia
Varsugæ, Kihlman, A.O. s.n., 19.8.1889, (H, 328709). Petsamo, Primmanki,
Saxén, U. s.n., 13.7.1930, (H, 328729). Pohjanmaa, Ylitornio, Mellakoski, 137 m,
Ulvinen, T. s.n., 24.7.1980, (COLO, 394339). Pohjois-Pohjanmaa, Pessalompolo,
140 m, Ulvinen, T. s.n., Karjalahti, T., 30.7.1976, (H, 457472). Sompion Lappi,
Petkula, Ohenoja, E. s.n., Melamies, H., 26.7.1996, (H, 722418). Tulijoki, Kainuu,
Lehtonen, L. s.n., 18.7.1933, (DAO, 257434). Tulijoki, Kainuu, Lehtonen, L. s.n.,
18.7.1933, (DAO, 257433). Tuntsa, Ylitornio, Mellakoski, Kämäräinen, H. 1999215, 16.7.1999, (H, 732554). Vaskojoki, Kihlman, A.O. s.n., .8.87, (GH).
Germany, Bavaria, Monacho Bavaria, Brügger, C. s.n., 29.6.1873, (GH, 2275).
Bavaria, Mikalum, Buccarini s.n., (GH). Bavaria, Oberbayern, Seurs 2053,
27.5.1949, (M, 0151919). Bavaria, Oberbayern, Seurs s.n., 22.5.1851, (M, 0151916).
Bavaria, Oberbayern, Leuvs s.n., Seuvnad, 9.6.1851, (M, 0151915). Bavaria,
Deining, Brügger, C. 2275, 29.6.1873, (H, 1093339). Oberbayern, Haspelmoor,
Holler s.n., 6.1872, (M, 0151918). Oberbayern, Deininger Fliz, Ohmüller s.n.,
5.1867, (M, 0151920). Spitzel, V. 379, 1960, (O, 135). Oberschwaben, Schánzle
5.1880, 5.1880, (M, 0151921). Fleischer 18-1900, 1900, (H, 1226126). Greenland,
Vestgrønland, Sydostbugten, 80 m, Møller, M. 1156, 15.7.1981, (C).Vestgrønland,
Akuliarusikavsak, Jakobsen, K. 12291, 11.8.1956, (C). Iceland, Akureyrense,
Skjóldalsárgil, Hg, H. 1529, 20.6.1965, (H, 1226120). Akureyri, Løgumshlid,
Grøntved, J. s.n., 24.7.1928, (GH). Árnessýsla, Votamýri, 60 m, Löve, A. A095,
Löve, D., 25.9.1949, (GH, 095). Belgsá, Fnjóskadal, Kristinnsson, H. 5143,
27.7.1973, (DAO, 288690). Borgarnes, Borgarnes Fjöfdur, Scamman, E. 1260,
22.8.1938, (GH, 1260). Dalfjall, Mývatnssvei, 460 m, Einarsson, E. E6042,
21.8.1974, (ICEL, 04073). Egilsstaðir, Héraði, 80 m, Meyer, Dr. med. G 7146,
27.8.1932, (ICEL, 04083). Egilsstaðir, Vopnafirði, Stefánsson I, S. 256, 4.8.1895,
(ICEL, 04088). Finnsstaðir, Eiðaþinghá, Lagarfljótsrannsóknir 7145, 24.7.1975,
(ICEL, 04082). Hallormsstadur, Egilsstadir, Gøtzsche, H.F. 81.37, 22.7.1981, (C, 8).
Hrísey, Eyjafirði, Garðarsson, A. s.n., 12.8.1967, (ICEL, 04078). Hrísey, Eyjafirði,
Garðarsson, A. s.n., 8.8.1967, (ICEL, 04077). Hvalfjörður, Ingimarsson, Ó. s.n.,
11.8.1951, (DAO, 257458). Lagarfoss, Hróarstungu, Lagarfljótsrannsóknir s.n.,
26.6.1976, (ICEL, 04080). Lagarfoss, Fljótsdals, Magnússon, S.H. s.n., 26.6.1976,
(ICEL, 47380). Lagarfoss, Hróarstungu, Lagarfljótsrannsóknir s.n., 26.6.1976,
(ICEL, 04081). Moldhaugar, Kræklingahlíð, Óskarsson, I. 935, 22.8.1926, (ICEL,
04052). Nes, Höfðahverfi, Óskarsson, I. 681, 30.6.1926, (ICEL, 46472). Öræfi,
Bæjarstaðarskógur Öræfum, Björnsson, H. 9633, 16.10.1947, (ICEL, 04074).
Öræfi, Fagurhólsmýri Öræfum, Björnsson, H. 9638, 7.1947, (ICEL, 04075). Öræfi,
Skaftafell Öræfum, Björnsson, H. 9624, 15.6.1946, (ICEL, 04076). Reykjahlið,
Lake Mývatn, 280 m, Seberg, O. 427, 14.8.1976, (C, 7). Sellátur, Reyðarfirði,
Óskarsson, I. s.n., 14.7.1927, (ICEL, 04051). Skagafjord, Valnsfjall, Sørensen,
T.H. 31/7, 31.7.1930, (O, 539367). Vaglaskógur, Fnjóskadal, Óskarsson, I. 1295,
7.8.1927, (ICEL, 04055). Vesturdalur, Bachufer, Lang, W. s.n., 29.7.1987, (M,
0151937). s.n., 9.7.87, (GH, ). 285 m, Lid, J. s.n., 14.7.1937, (O, 539360). Italy,
South Tirol, Seiser Alm, 1860 m, Bestand, G. s.n., 17.7.1958, (M, 0151928). South
133
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Tirol, 1100 m, Hoock, G. s.n., 3.8.1908, (M, 0151922). South Tirol, Seisseralpe, ,
Koch, J. s.n., 7.7.1955, (M, 0151914). South Tirol, Seiser Alm, 1900 m, Hertel, H.
4324, 27.6.1964, (M, 0151927). South Tirol, Dolomiten, 2370 m, s.n., 15.7.1958,
(M, 0151924). South Tirol, Seisseralpe, 1980 m, Roessler, H. 2519, 25.7.1959, (M,
0151925). South Tirol, Seiser Alm, 2000 m, Dietrich, W. 3283, 28.6.1964, (M,
0151930). South Tirol, Bozen, 1950 m, Dietrich, W. 1963-66, 28.6.1964, (M,
0151929). Südtirol, Feuchstelle, 2200 m, Angerer,O. s.n., 23.7.1976, (M, 0151926).
Norway, Finnmark, Veinesbukt, Skifte, O. s.n., Stellander, O., 6.8.1967, (C).
Finnmark, Kautokeino, 340 m, Kautokeino, N. s.n., Mieron, N.; Moor, 23.8.1967,
(M, 0151938). Finnmark, Bugöynes, 20 m, Toivonen, H. s.n., 3.8.1977, (H,
1471327). Finnmark, Bugöynes, 20 m, Toivonen, H. s.n., 3.7.1977, (H, 1471326).
Finnmark, Bugöynes, 25 m, Toivonen, H. s.n., 3.8.1977, (H, 1468929). Finnmark,
Billefjord, 5 m, Toivonen, H. s.n., 1.8.1972, (H, 1470511). Hamar, Jerkim,
Conradi, F.E. s.n., 15.7.1887, (GH). Hedmark, Gammelsetran, 860 m, Vileid, M.
s.n., 18.8.1998, (O, 235091). Hedmark, Jogåsmyra, 630 m, Kielland-Lund, J. s.n.,
9.7.1967, (O, 176158). Hedmark, Os, 780 m, Elven, R. s.n., (O, 4689). Hedmark,
Folldal, 840 m, Buttle 8066, Gauhl, 19.8.1965, (M, 0151912). Hjerkinn, Stanley
Pease, A. s.n., 21.7.1930, (GH, 20740). Hordaland, Eidfjord, 100 m, Lid, J. s.n.,
26.7.1936, (O, 414980). Kongsvold, Dovrefjeld, Nilsson, S.J. s.n., .8.1898, (GH).
Nordland county, Sørfold, Apold, W. s.n., Brodal, G.; Skifte, O., 8.8.1954, (H,
1013890). Norland, Nordland fylke, , Notø, A. s.n., 6.7.1932, (M, 0151945).
Oppland, Espedal, Berg, R.Y. s.n., 11.8.1973, (O, 260563). Oppland, Lom, 940 m,
Berg, R.Y. s.n., 10.8.1994, (O, 174746). Oppland, Grimsdalen, 900 m, Bratli, H.
s.n., 28.7.1994, (O, 114994). Sör-Tröndelag, Opdal herred, Kongsvoll, Nilsson, S.J.
s.n., .7.1883, (DAO, 257470). Sör-Tröndelag, Oppdal, Near Kongsvoll, Wendelbo,
P. s.n., 17.7.1948, (COLO, 100223). Troms, Stordalen, 250 m, Engelskjøn, T. s.n.,
24.7.1962, (C). Troms, Lulleborg, 360 m, Lye, K.A. 18728, Berg, T., 1.9.1992, (O,
75397). Troms, Fossbakken, Svendsen, S. s.n., 31.7.1967, (O, 92610). Tromsö,
Ringvatso Island, 30 m, Notø, A. s.n., 10.7.1896, (GH). Russia, Chita region, Between
the rivers Nerchei and Kuengoi, Sukatschew, W. s.n., 10.7.1911, (DAO, 142005).
Chukotka national district, Anui upland region, Zimarskaja, E.V. s.n., Korobkov,
A.A.; Yurtsev, B.A., 12.7.1967, (DAO, 139880). Chukotka national district,
Rauchua river, Yurtsev, B.P. s.n., 12.7.1967, (BRY, 122530). Chukotski peninsula,
river Utaveem, , Kozhevnikov, U.P. s.n., Nechaev, A.A.; Yurtsev, B.A., 27.7.1970,
(COLO, 323093). Irkutsk, Balagansk region, Maltsev, I. s.n., 19.6.1905, (GH).
Kamchatka region, Olyutorsky area, Harkevich, S. s.n., 9.8.1975, (GH). Komi
Republic, Syktyvkar, Andreev, V.D. s.n., 21.6.1909, (H, 1037137). Magadan region,
North Even, Hohrjakov, A.P. s.n., 2.8.1976, (CAN, 455497). Republic of Karelia,
Karelia onegensis (Kon), Ruuhijärvi, R. 40/02, 9.7.2002, (H, 744530). Republic of
Karelia, Belomorskiy District, 10 m, Kravchenko, A. s.n., 21.8.2002, (H, 742280).
Republic of Karelia, Karelia pomorica orientalis, Piirainen, M. 5376, 19.8.2004,
(H, 807345). Republic of Karelia, Karelia pomorica orientalis, 20 m, Piirainen, M.
5027, 22.8.2002, (H, 741569). Sakha Republic, Bulunsk region, Yurtsev, B.A. s.n.,
25.6.1960, (DAO, 257437). Taymyr, River Pyasina, Kozhevnikov, U.P. s.n.,
21.8.1982, (CAN, 490439). Between the rivers Nerchei and Kuengoi, Sukachev, V.
s.n., 27.7.1970, (DAO, 139887). Kihlman, A.O. s.n., 18.8.1891, (H, 1226124).
Chersky, Kozhevnikov, U.P. 714, 24.7.1977, (CAN, 455526). Sweden, Dalecarlia,
Morängen, Källström, S. s.n., 7.1887, (GH). Dalecarlia, Fries s.n., (GH). Härjedalen,
Valmåsen, Dusén, K. s.n., 11.8.1879, (DAO, 363985). Jämtland, Paroecia Frösö,
Asplund, E. s.n., 2.6.1925, (GH). Jämtland, Paroecia Frösö, Asplund, E. s.n., (C).
Jämtland, Nyhem, 280 m, s.n., 4.7.1977, (M, 0151939). Jämtland, Häggenås, 400 m,
s.n., 3.7.1977, (M, 0151940). Jämtland, Mosjön, 305 m, s.n., 5.7.1977, (M,
0151941). Jämtland Ås, Ahlqvist, A. s.n., 28.6.1902, (GH). Kilpisjärvi, Saana, 50
m, Roivainen, L. s.n., 14.7.1958, (DAO, 257436). Lule Lappmark, Avvakkotunturi, 500 m, Hertel, H. 7248b, 21.7.1967, (M, 0151935). Scandinavia, s.n.,
1887, (M, 0151938). Sverige, Torne Lappmark, Pederson, T.M. 5615, 15.7.1960,
(O, 314293). Torne Lappmark, Torne Träsk, Torlöf, A. s.n., 12.8.1958, (GH). Torne
Lappmark, Låktatjakko, 700 m, Alm, G. 449, 11.8.1935, (GH, 449). Torne
Lappmark, Jukkasjärvi, 333 m, Alm, G. s.n., 8.8.1935, (GH, 442). Torne
Lappmark, Abisko, Selander, S. s.n., 9.7.1905, (GH). Torne Lappmark, Lake
Torneträsk District, 450 m, Alm, G. s.n., 9.8.1958, (O, 539346). Torne Lappmark,
Abisko, Hertel, H. 22918, 8.8.1980, (M, 0151931). Torne Lappmark, Abisko, s.n.,
13..8, (M, 0151947). Torne Lappmark, Abisko, Hiitonen, I. s.n., 22.7.1950, (H,
1693670). Torne Lappmark, Abisko, 400 m, Alm, G. s.n., 6.8.1958, (H, 1226056).
USA, Alaska, Old John Lake Area, Holmen, K. 61-1227, 13.7.1961, (C, 61-1227).
134
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________________________________________________________________
Alaska, Wiseman, Anderson, J.F. 5970, Gasser, G.W., 3.8.1939, (ALA, 1125027).
Alaska, Shaw Creek Flats, Elven, R. s.n., Solstad, H., 28.7.2001, (ALA, 1125006).
Alaska, Euchre Moutain, 3868 ft, Bennett, B. 194/13273, Loomis, P., 20.6.2003,
(ALA, 1125007). Alaska, Smith Lake, Parker, C.L. 15339, 7.8.2003, (ALA,
1125008). Alaska, Central Noatak R. Valley, 100 m, Parker, C.L. 15128, Elven,
R.; Solstad, H., 23.7.2003, (ALA, 1124990). Alaska, Kilikmak Cr., 8 m, Parker,
C.L. 14722, Elven, R.; Solstad, H., 13.7.2003, (ALA, 1124991). Alaska, Mt. Hayes,
419 m, Duffy, M. 98-201, 15.7.1998, (ALA, 1124993). Alaska, Endicott
Mountains, 900 m, Parker, C.L. 12108, Elven, R.; Solstad, H.; Bennett, B.A.,
19.7.2002, (ALA, 1124994). Alaska, Neacola Moutains, Caswell, P. 96-205,
19.6.1996, (ALA, 1124995). Alaska, Mt. Michelson, 861 m, Batten, A. 686,
26.7.1973, (ALA, 1124996). Alaska, Howard Pass, 700 m, Parker, C.L. 7648, ,
27.7.1997, (ALA, 1124998). Alaska, Table Mountain, 622 m, Mouton, M.A.
MM79279, 30.6.1979, (ALA, 1125000). Alaska, Imiaknikpak Lake, 581 m,
Murray, D.F. 4314, 27.7.1973, (ALA, 1124970). Alaska, Baird Mountains, 85 m,
Parker, C.L. 15299, Elven, R.; Solstad, H., 29.7.2003, (ALA, 1124972). Alaska,
Charley River, 850 ft, Larsen, A. 02-2430, Batten, A., 25.7.2002, (ALA, 1124973).
Alaska, Bering Land Bridge NPreserve, 250 m, Kelso, T. 87-319, 7.7.1987, (ALA,
1124975). Alaska, McKinley River, 1900 ft, Viereck, L.A. 1613, 30.7.1956, (ALA,
1124982). Alaska, Arctic National Wildlife Range, 430 m, Murray, D.F. 3350,
26.7.1970, (ALA, 1124984). Alaska, Alaska Range, 750 m, Duffy, M. MD02-240,
16.8.2002, (ALA, 1125011). Alaska, Alaska Range, 725 m, Roland, C. 4519,
Batten, A.; Goeking, S., 7.1.2000, (ALA, 1125012). Alaska, Solomon, 85 m, s.n.,
14.7.2000, (ALA, 1125013). Alaska, Seward Peninsula, 37 m, Murray, D.F. 11077,
Yurtsev, B.A.; Kelso, T., 26.7.1992, (ALA, 1125015). Alaska, Kokrine Hills, 275 m,
Foote, J. JF4208, 24.6.1980, (ALA, 1125016). Alaska, Fort Wainwright Military
Reservation, 115 m, Duffy, M. 95-624, Lipkin, R., 10.7.1995, (ALA, 1125017).
Alaska, Jago Lake, Cantlon, J.E. 57- 1613, Gillis, W.T., 28.7.1957, (ALA, 1125021).
Alaska, Tanana River, Spetzman, L. 11868, 7.8.1957, (ALA, 1125022). Alaska,
Bendeleben Quad, 100 m, Kelso, T. 82-190, 10.8.1982, (COLO, 387320). Alaska,
Mt. Mckinley Natl. Park Teklanika River, 792 m, Viereck, L.A. 7427, 3.8.1964, (ALA,
1125025). Alaska, Mt. Mckinley Natl. Park Teklanika River, 792 m, Viereck, L.A.
7427, 3.8.1964, (RMS, 430206). Alaska, Mt. Mckinley Natl. Park Teklanika River,
792 m, Viereck, L.A. 7427, 3.8.1964, (CAN, 362141).
Studied specimens of C. cayoutteana subsp. cayouetteana
Snow Creek Pass, 7400 ft, Calder, J. 23957, 24.7.1959, (COLO, 148926). Alberta,
Snow Creek Pass, 7000 ft, Porsild, A.E. 22673, 29.7.1960, (RM, 529780). British
Columbia, Bluster Mt., 2133 m, Thompson, J. s.n., Thompson, M., 14.7.1938,
(WTU, 48964). British Columbia, Chipuin Mt., 1828 m, Thompson, J. s.n.,
Thompson, M., 21.7.1938, (WTU, 17893). British Columbia, Quiniscoe Lake, 2316 m,
Calder, J. 19594, Parmelee, J.A.; Taylor, D., 2.8.1956, (WTU, 199618). British
Columbia, 7100 ft, Calder, J. 11795, Savile, O., 11.8.1953, (COLO, 118024).
British Columbia, Ashnola Range, 7600 ft, Calder, J. 19594, Parmelee, J.A.;
Taylor, R.L., 2.8.1958, (RM, 260491). Mexico, Pacheco, Chihuahua, Hartman, C.V.
s.n., 10.6.1891, (MICH, 1132452). USA, California, Anderson Mdw., 1950 m,
Gierisch, R. 3493, Esplin, D., 25.6.1969, (RMS, 430207). California, Anderson Mdw.,
6400 ft, Gierisch, R. 3493, Esplin, D., 25.6.1969, (COLO, 246761). California,
Anderson Mdw., Gierisch, R. 3493, Esplin, D., 25.6.1969, (CAS, 690732).
California, South Warner Mountains, 9000 ft, Otting, N. NAD27, Lytjen, D.,
2.9.2004, (OSC, 219450). Colorado, Bill Moore Lake, 3627 m, Lederer, N. 4257,
31.8.1993, (COLO, 00263731). Colorado, Loch Lomond, 3395 m, Weber, W.A.
s.n., Koponen, T.; Nelson, P., 8.8.1972, (CAN, 374041). Colorado, San Juan
National Forest, 11900 ft, Rink, G. 3668, 25.7.4, (BRY, 467234). Colorado, Loch
Lomond, 11140 ft, Weber, W.A. s.n., Koponen, T.; Nelson, P., 8.8.1972, (COLO,
259883). Colorado, Hagerman Pass, 11980 ft, Hartman, E.L. 6718, Rottman, M.L.,
29.8.1986, (COLO, 428741). Colorado, Fraser Exp. Forest, 12000 ft, Weber, W.
8621, Dahl, E., 31.7.1953, (COLO, 76204). Colorado, Mesa Seco, 12300 ft, Johnson,
K. J64-117, (COLO, 232659). Montana, Sweet Grass County, 2956 m, Lesica, P.
7663, 27.7.1998, (MONTU, 122991). Montana, Sweet Grass County, 2743 m, Lesica,
P. 7362, 10.8.1996, (MONTU, 122399). Montana, Sweet Grass County, 2743 m,
Lackshewitz, H. 9909, 15.8.1981, (MONTU, 86558). Montana, Carbon County,
135
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________________________________________________________________
2999 m, Ramsden, J. 1625, 10.7.1987, (MONTU, 118978). Montana, Carbon
County, 2987 m, Lesica, P. 5583, 15.8.1991, (MONTU, 115081). Montana, Carbon
County, 3048 m, Lesica, P. 4483, 11.8.1987, (MONTU, 108435). Montana, Park
County, Ramsden, J. 85542, 9.7.1980, (MONTU, 85542). Montana, Carbon
County, 3017 m, Lackshewitz, H. 7790, 11.8.1977, (MONTU, 78793). Montana,
Sweet Grass County, 2743 m, Lackshewitz, H. s.n., 15.8.1981, (COLO, 355226).
Montana, Stillwater County, 2767 m, Evert, E. 24076, 27.7.1992, (RMS, 780026).
Montana, Carbon County, 3048 m, Evert, E. 19835, 23.7.1990, (RMS, 619855).
Montana, Carbon County, 2987 m, Lackshewitz, H. 7000, 14.9.1976, (WTU, 272540).
Montana, Carbon County, 3017 m, Lackshewitz, H. 7790, 11.8.1977, (WTU,
288770). Montana, 9800 ft, Lackschewitz, K.H. 7035, 15.9.1976, (RM, 367206).
Montana, Beartooth Pass, 11000 ft, Hermann, F.J. 20079, 20.7.1965, (RMS,
430211). Montana, 9000 ft, Evert, E. 18434, 9.8.1989, (RM, 579301). Montana,
Lackschewitz, K.H. 9909, 15.8.1981, (RM, 521779). Montana, 9900 ft, Lackschewitz,
K.H. 7790, 11.8.1977, (RM, 367094). Montana, Sweet Grass County, 9000 ft,
Lackschewitz, K.H. s.n., 15.8.1981, (GH). Nevada, Browns Cr., 2590 m, Lewis, E.
448, 17.7.1955, (RMS, 390545). Nevada, Browns Cr., 2590 m, Lewis, E. 17.7.1955,
(CAN, 550536). Utah, Uinta Mountains, Lewis, E. 512, 15.8.1955, (RMS, 368032).
Utah, Gilbert Bench, 3505 m, Goodrich, S. 25583, Huber, A.; Prescott, D.,
20.8.1996, (BRY, 392186). Utah, Gilbert Creek, 3493 m, Huber, A. 440, Goodrich,
S., 25.8.1993, (BRY, 368578). Utah, Uinta Mountains, Lewis, E. 512, 15.8.1955,
(CAN, 515168). Utah, Gilbert Bench, 12100 ft, Goodrich, S. 26303, Huber, A.;
Frandsen, J.; Bartlett, F., 9.8.2000, (BRY, 437123). Utah, Ridge saddle, 12600 ft,
Huber, A. 4134, 3.8.1999, (BRY, 426752). Utah, Ashley Forest, 11850 ft, Goodrich,
S. 23530, Bartlett, F.; Atwood, D.; Nelson, D., 19.8.1991, (BRY, 350794).
Washington, Chowder Ridge, 6800 ft, Douglas, G. 4345, Douglas, G., 3.8.1972,
(DAO, 621358). Washington, Rocky Mt., 2365 m, Douglas, G. 2887, 19.7.1971,
(RMS, 430209). Wyoming, 10700 ft, Mosquin, T. 4817, 2.8.1962, (DAO, 257425).
Wyoming, 3279 m, Mellmann-Brown, S. 2575, 7.8.1996, (RMS, 644114). Wyoming,
Elk Peak, 3566 m, Hartman, L. 24223, Poll, T., 9.8.1988, (RMS, 533361).
Wyoming, 3474 m, Hartman, L. 31265, 19.8.1991, (RMS, 589096). Wyoming,
Neely, B. 2435, 18.8.1984, (COLO, 399492). Wyoming, Beartooth Plateau, 3300 m,
Weber, W. s.n., 18.8.1973, (COLO, 270915). Wyoming, Beartooth Plateau, 9800 ft,
Lackshewitz, H. s.n., 14.9.1976, (COLO, 306544). Wyoming, Cascade Creek, 10300
ft, Evert, E. 18305, 3.8.1989, (COLO, 449077). Wyoming, Lamar River, 10300 ft,
Nelson, B.E. 12725, Hartman, R.L., 22.7.1985, (RM, 482304). Wyoming,
Beartooth Plateau, 9800 ft, Lackschewitz, K.H. 7000, 14.9.1976, (RM, 367209).
Wyoming, Beartooth Plateau, 9800 ft, Dorn, R.D. 3590, 12.8.1980, (RM, 330260).
Wyoming, Francs Fork, 11150 ft, Hartman, L. 16805, 14.8.1983, (RM, 558454).
Wyoming, Beartooth Plateau, 10800 ft, Mellmann-Brown, S. 2470, 22.7.1996, (RM,
612812). Wyoming, Eastern Wind River Range, 10240 ft, Mills, S. 232a, 18.8.1995,
(RM, 603492). Wyoming, Head Elk Creek, 11500 ft, Johnson, W.M. 140,
29.8.1961, (RMS, 401425). Wyoming, Northern Wind River Range, 10240 ft, Mills,
S. 230b, 18.8.1995, (RM, 603491). Wyoming, Bug Creek Pass, Absarokas, 11000
ft, Johnson, W.M. 270, 8.8.1962, (RM, 189438-s). Wyoming, Bug Creek Pass,
Absarokas, 11000 ft, Johnson, W.M. 270, 8.8.1962, (RMS, 401298). Wyoming,
Absaroka Mountains, 10000 ft, Kirkpatrick, R.S. 5901, Kirkpatrick, R.E.B.,
14.8.1984, (RM, 558456). Wyoming, Cascade Creek, 10300 ft, Evert, E. 18305,
3.8.1989, (RM, 579204). Wyoming, Absaroka Mountains, 11150 ft, Kirkpatrick, R.S.
5910, Kirkpatrick, R.E.B., 21.8.1984, (RM, 558455). Wyoming, Absaroka Mountains,
10200 ft, Evert, E. 18249, 3.8.1989, (RM, 579080). Wyoming, Absaroka Mountains,
9800 ft, Evert, E. 9608, 20.8.1985, (RM, 623052). Wyoming, Absaroka Mountains,
10000 ft, Hartman, R.L. 19105, 21.8.1984, (RM, 558453). Wyoming, Absaroka
Mountains, 11750 ft, Hartman, R.L. 19289, 22.8.1984, (RM, 558452). Wyoming,
Absaroka Mountains, 10700 ft, Hartman, R.L. 23927, Poll, T., 5.7.1988, (RM,
536641). Wyoming, West Slope Wind River Range, 10400 ft, Hartman, R.L.
31278, 19.8.1991, (RM, 589095). Wyoming, Absaroka Mountains, 10500 ft, 4416,
20.7.1984, (RM, 558457). Wyoming, Beartooth Plateau, 9570 ft, Fertig, W. 15202,
23.7.1994, (RM, 602345). Wyoming, Mellmann-Brown, S., 24.8.1996, (RM,
615036).
Studied specimens of C. cayouetteana subsp. bajasierra
136
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USA, California, El Dorado Co., Echo Summit, Howell, J.T. 257424, , 1.9.1946, (DAO,
257424). California, El Dorado Co., El Dorado National Forest, 2350 m, Toivonen, H.
661914, Norris, D.H.; Pykälä, J., 23.7.1987, (DAO, 661914). California, El Dorado
Co., El Dorado National Forest, 2350 m, Pykälä, J. 6, Norris, D.H.; Toivonen, H.,
23.7.1987, (C, 6). California, El Dorado Co., Freel Peak quad, 2292m, Janeway, L.
73322, Schroder, E., 2.9.1998, (CHSC, 73322). California, Plumas County, Blucks
Lake quad, 481 m, Janeway, L. 78722, 7.7.2000, (CHSC, 78722). California, Tehama
County, Yellow Pine Forest, 1540 m, Ahart, L. 94326, 19.7.2006, (CHSC, 94326).
California, Sierra County, Yuba Pass- Weber Lake Rd., 2194 m, Oswald, H. 66824,
Ahart, L., 19.8.1996, (CHSC, 66824). California, Nevada County, University of
California Trout Lab, 6500 ft, Langenheim, J. 272099, 19.7.1957, (CAN, 272099).
California, Nevada County, University of California Trout Lab, 6500 ft, Nisbet, W.A.
272091, 20.7.1957, (CAN, 272091). California, Nevada County, Sagehen Creek, 6300 ft,
True, G.H. 845706, Howell, J.T., 29.8.1966, (CAS, 845706). California, Nevada
County, University of California Trout Lab, 6500 ft, Langenheim, J. 845707, 19.7.1957,
(CAS, 845707). California, Lassen Volcanic National Park, Badger Flat, 6275 ft, Leschke,
H. 136120, 10.8.1960, (OSC, 136120). California, Nevada County, Truckee, 2035 m,
Naczi, R.F.C., 3.8.2006, (NYBG). California, Nevada County, Truckee, 1980 m, Naczi,
R.F.C., 4.8.2006, (NYBG). California, Tulare County, Kaweah Meadows, Howell, J.T.
17724, 5.8.1942, (GH, 17724). Oregon, Lake County, Sycan Marsh, 1524 m, Christy, A.
188302, 23.8.1980, (OSC, 188302). Oregon, Deschutes County, 1981 m, Wilson, B.
178855, 9.8.1990, (OSC, 178855). Oregon, Jackson County, Cascade Mountains, 1636
m, Otting, N. 210656, 28.6.2001, (OSC, 210656). Oregon, Deschutes County, 1926 m,
Halpern, C. 159046, Magee, T., 30.8.1982, (OSC, 159046).
Studied specimens of C. cayouetteana subsp. altasierra
USA, California, Tulare Co., Sierra Nevada, 12000 ft, Howell, J.T. s.n., 5.8.1949,
(DAO, 257423). California, Inyo County, Mount Humphreys, 12880 ft, Sharsmith, C.W.
3116, 11.8.1937, (DAO, 257428). California, Inyo County, Mono Mesa, 3657 m, Howell,
J.T. s.n., 26.7.1946, (WTU, 137524). California, Mono County, Mt. Dana Plateau, 3505
m, Taylor, D. 7550, 25.7.1979, (COLO, 330874). California, Sierra Nevada, Central
Basin, 3444 m, Munz, A. 12669, 26.7.1948, (WTU, 133536). California, Tuolumne
County, Kuna Peak, 12500 ft, Sharsmith, C.W. 2681, 21.7.1937, (CAN, 162869).
California, Mono County, White Mountains, 11800 ft, Morefield, J.D. 4829, Perala, C.,
27.7.1988, (MICH). California, Mono County, Dunderberg Peak, 11800 ft, Taylor, D.
5291, 27.7.1975, (CAS, 856994). California, Fresno County, 11192 ft, Quibell, C.H.
4162, 7.8.1954, (OSC, 96143). California, Inyo County, Mono Mesa, 12000 ft, Howell,
J.T. s.n., 26.7.1946, (GH, 12750).
137
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APPENDIX S2
Figure A.1: Histograms of the six discrete variables scored for the morphometric study. C.
capitata (C), C. arctogena (A), C. cayouetteana subsp. cayouetteana (Y), C. cayouetteana
subsp. bajasierra (Y2) and C. cayouetteana subsp. altasierra (Y3). X axis represents the
measurements and Y axis the number of specimens.
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139
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Figure A.2: Boxplots showing mean interspecific differences between C. capitata (C), C.
arctogena (A), C. cayouetteana subsp. cayouetteana (Y), C. cayouetteana subsp.
bajasierra (Y2) and C. cayouetteana subsp. altasierra (Y3) for twenty two quantitative and
continuous variables. Asterisks to the left of each box denote level of statistical significance
based on a Kruskal-Wallis ANOVA. Blue denotes P<0.01 and red P<0.05. Characters are
alphabetically arranged. A full description of the characters is given in Table 2.5.
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141
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142
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143
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Figure A.3: Pistillate scales (above) and periginia (below) of C. capitata (C), C.arctogena
(A), C. cayouetteana subsp. cayouetteana (Y), C. cayouetteana subsp. bajasierra (Y2) and
C. cayouetteana subsp. altasierra (Y3).
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Figure A.4: Holotype of C. capitata L. at LINN.
145
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Figure A.5: Holotype of C. arctogena Harry Sm. at DAO
146
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Figure
A.6:
Holotype
of
C.
147
antarctogena
Roivanen
at
H.
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Figure A.7: The distribution of C. capitata (circles), C. arctogena (squares), C.
cayouetteana subsp. cayouetteana (triangles), C. cayouetteana subsp. bajasierra (crosses)
and C. cayouetteana subsp. altasierra (stars) based on all the herbarium specimens
examined in this study.
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Figure A.8: The distribution of C. capitata (circles), C. arctogena (squares), C.
cayouetteana subsp. cayouetteana (triangles), C. cayouetteana subsp. bajasierra (crosses)
and C. cayouetteana subsp. altasierra (stars) in North America based on all the herbarium
specimens examined in this study.
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Figure A.9: The distribution of Carex capitata and C. arctogena in Europe based on all
specimens examined in this study.
150
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Figure A.10: The distribution of C. cayouetteana subsp. cayouetteana based on all the
herbarium specimens examined in this study.
151
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Figure A.11: The distribution of C. cayouetteana subsp. bajasierra based on all the
.
152
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Figure A.12: The distribution of C. cayouetteana subsp. altasierra based on all the
153
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154
Chapter 3
Direct long-distance dispersal best
explains the bipolar distribution of
Carex arctogena (Carex sect.
Capituligerae, Cyperaceae)
155
156
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Chapter 3. Direct long-distance
________________________________________________________________
dispersal best explains the bipolar distribution of Carex arctogena
Journal of Biogeography (J. Biogeogr.) (2015)
ORIGINAL
ARTICLE
Direct long-distance dispersal best
explains the bipolar distribution of
Carex arctogena (Carex sect.
Capituligerae, Cyperaceae)
Tamara Villaverde1*, Marcial Escudero2, Santiago Martın-Bravo1,
Leo P. Bruederle3, Modesto Luce~
no1 and Julian R. Starr4,5
1
Botany area, Department of Molecular
Biology and Biochemical Engineering, Pablo
de Olavide University, 41013 Seville, Spain,
2
Department of Integrative Ecology, Estacion
Biologica de Do~
nana (EBD – CSIC), 41092
Seville, Spain, 3Department of Integrative
Biology, University of Colorado Denver,
Denver 80217–3364, USA, 4Canadian
Museum of Nature, Ottawa K1P 6P4,
Canada, 5Department of Biology, Gendron
Hall, University of Ottawa, Ottawa K1N 6N5,
Canada
ABSTRACT
Aim The bipolar disjunction, a biogeographical pattern defined by taxa with a
distribution at very high latitudes in both hemispheres (> 55° N; > 52° S), is
only known to occur in about 30 vascular plant species. Our aim was to use
the bipolar species Carex arctogena to test the four classic hypotheses proposed
to explain this exceptional disjunction: convergent evolution, vicariance, mountain-hopping and direct long-distance dispersal.
Location Arctic/boreal and temperate latitudes of both hemispheres.
Methods A combination of molecular and bioclimatic data was used to test
phylogeographical hypotheses in C. arctogena. Three chloroplast markers
(atpF–atpH, matK and rps16) and the nuclear ITS region were sequenced for
all species in Carex sections Capituligerae and Longespicatae; Carex rupestris,
C. obtusata and Uncinia triquetra were used as outrgroups. Phylogenetic relationships, divergence-time estimates and biogeographical patterns were inferred
using maximum likelihood, statistical parsimony and Bayesian inference.
Results Carex sections Capituligerae and Longespicatae formed a monophyletic
group that diverged during the late Miocene. Two main lineages of C. arctogena were inferred. Southern Hemisphere populations of C. arctogena shared the
same haplotype as a widespread circumboreal lineage. Bioclimatic data show
that Southern and Northern Hemisphere populations currently differ in their
ecological regimes.
*Correspondence: Tamara Villaverde, Botany
area, Department of Molecular Biology and
Biochemical Engineering, Pablo de Olavide
University, Ctra. de Utrera km 1 s/n, 41013
Seville, Spain.
Main conclusions Two of the four hypotheses accounting for bipolar disjunctions may be rejected. Our results suggest that direct long-distance dispersal, probably southwards and mediated by birds, best explains the bipolar
distribution of C. arctogena.
Keywords
Biogeography, bipolar distribution, Capituligerae, Carex, climatic niche,
Cyperaceae, divergence-time estimation, long-distance dispersal.
INTRODUCTION
Arctic taxa are often widely distributed, their distributions
usually fitting into one of three patterns: circumpolar, amphiAtlantic or amphi-Beringian. When Arctic taxa also occur at
very high latitudes in the Southern Hemisphere (> 52° S),
they achieve what is known as a bipolar distribution (Moore
& Chater, 1971). This remarkable biogeographical pattern
provides some of the greatest biological disjunctions known
and it has inspired authors in biogeography since the 19th
ª 2015 John Wiley & Sons Ltd
century (e.g. Darwin, 1859). However, resolving the biogeographical and evolutionary origins of bipolar taxa has been
challenging due to the scale of their distributions. Four main
mechanisms have been proposed to account for bipolar taxa:
(1) vicariance (Du Rietz, 1940), implying fragmentation of a
continuous distribution that would date back to the transtropical highland bridges of the Mesozoic (c. 195 million years
ago, Ma; Scotese et al., 1988); (2) convergent or parallel evolution of disjunct populations that have independent origins
but similar phenotypes through adaptation to comparable
http://wileyonlinelibrary.com/journal/jbi
doi:10.1111/jbi.12521
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1
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T. Villaverde et al.
environmental pressures (Scotland, 2011); (3) stepwise longdistance dispersal across the equator via mountain ranges
(‘mountain-hopping’, Moore & Chater, 1971; Heide, 2002;
Vollan et al., 2006) during the last cold periods of the Pliocene
and Pleistocene that extended the polar regions of both hemispheres (Raven, 1963); and (4) direct long-distance seed dispersal by birds, wind or ocean currents (Nathan et al., 2008;
and references therein). These hypotheses can now be tested
objectively by examining the distribution of haplotypes and by
dating molecular phylogenies to better assess the possible
evolutionary, climatic and geological changes at the origin of
biogeographical patterns (Crisp et al., 2011).
Most recent studies addressing the origin of bipolar plants
have focused on supraspecific groups (e.g. Euphrasia, Gussarova et al., 2008; Empetrum, Popp et al., 2011) and used
molecular data only. Nonetheless, these studies estimated
that the divergence of bipolar lineages occurred a maximum
of 10 million years ago, and concluded that the best explanation for bipolar distributions was long-distance dispersal. Of
the approximately 30 bipolar vascular species that are known
(Moore & Chater, 1971), six are found in Carex L., a diverse
genus (> 2000 species) that is most common in the cold and
temperate regions of the Northern Hemisphere (Reznicek,
1990). Because most Carex species, and especially the bipolar
species, live under long-day conditions, Heide (2002) tested
whether the plants could reproduce under the short-day conditions seen in the tropics, in an attempt to refute the
hypothesis of trans-equatorial mountain-hopping. Heide’s
results showed that, at least for Carex canescens L. and Ca-
rex magellanica Lam., cool, short-day conditions are sufficient to induce flowering. The few molecular studies that
have focused on bipolar Carex are consistent with Heide’s
(2002) results. Both Vollan et al. (2006) and Escudero et al.
(2010) found low levels of genetic differentiation in five of
the six known bipolar species of Carex, suggesting that either
mountain-hopping or direct long-distance dispersal was the
best explanation for the species’ current distributions. However, neither Vollan et al. (2006) nor Escudero et al. (2010)
could determine definitively which hypothesis best explained
the distributions of bipolar species. The only remaining
bipolar Carex not to have been studied using molecular
markers is Carex arctogena Harry Sm. (in Carex sect. Capituligerae K€
uk.), a species that reaches both the Canadian
Arctic Archipelago in the Northern Hemisphere and the
southernmost region of South America, Tierra del Fuego
(Fig. 1). Carex sect. Capituligerae includes two other species:
the alpine Carex oreophila C. A. Mey, a species confined to
the mountains of south-western Asia, and the circumboreal
Carex capitata L. (Egorova, 1999).
Although morphological, ecological and molecular data
clearly separate C. arctogena from its sister species, C. capitata,
in northern Europe (Reinhammar, 1999; Reinhammar & Bele,
2001), these differences are less clear in North America, where
these species are considered to form a complex (Murray,
2002). Ecological factors could be influencing the geographical
distribution of C. arctogena and C. capitata and may therefore
constitute a key element in determining their distributional
patterns. The integration of phylogeographical inferences from
Figure 1 Distribution map of sampled populations of species in Carex sections Capituligerae and Longespicatae (Cyperaceae). Black
circles, C. arctogena A; white circles, C. arctogena B; white triangles, C. capitata A; black triangles, C. capitata B; squares,
C. monostachya; cross, C. oreophila; diamond, C. runssoroensis. The dark grey and the dashed regions indicate the distribution of
C. arctogena and C. capitata, respectively, obtained from the World Checklist of Selected Plant Families (http://apps.kew.org/wcsp).
Journal of Biogeography
2
158
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Bipolar disjunction in Carex arctogena
DNA sequences with bioclimatic data could thus be valuable
in clarifying the evolutionary history of this bipolar species.
The goal of this study was to determine which of the four
classic hypotheses used to account for bipolar taxa could best
explain the distribution of C. arctogena. By evaluating the
combined evidence provided by phylogenetic reconstructions,
molecular dating and bioclimatic data, we will be able to test
biogeographical hypotheses and to improve our understanding of the historical events that promoted the formation of
the bipolar disjunction seen in C. arctogena.
MATERIALS AND METHODS
Sampling
known to blur signals of migration and isolation (Schaal &
Olsen, 2000). Consequently, this region was used for phylogenetic purposes alone and was only amplified for a subset
of samples.
Nuclear and plastid regions were amplified and sequenced
following the conditions described by Escudero et al. (2008)
and Starr et al. (2009), respectively. Minor adjustments (e.g.
reagent concentrations or annealing temperature) were sometimes necessary in order to obtain suitable amplification
products. Sequence data were assembled and edited using Sequencher 4.10 (Gene Codes, Ann Arbor, MI, USA) and
subsequently submitted to GenBank (Appendix S1).
Sequences were automatically aligned with muscle (Edgar,
2004) and manually adjusted using Geneious 6.1.7 (Biomatters, Auckland, New Zealand).
Carex arctogena has a circumboreal distribution, with its
range limited to Patagonia in the Southern Hemisphere
(Fig. 1). It is a wind-pollinated herbaceous hemicryptophyte
that generally occurs in arctic–alpine habitats and windexposed heaths where the soil water content is low. We
obtained plant material representing the entire range of
C. arctogena (55 populations), as circumscribed by Egorova
(1999). We also included 36 populations of C. capitata and
one population of C. oreophila. Two East African species
from Carex sect. Longespicatae K€
uk., Carex runssoroensis K.
Schum. and Carex monostachya A. Rich., were also sampled
(one and two populations, respectively; Fig. 1, and see
Appendix S1 in Supporting Information), because molecular
studies suggest that C. sect. Longespicatae is sister to C. sect.
Capituligerae (e.g. Starr & Ford, 2009). Finally, we used Carex obtusata Lilj., Carex rupestris All. and Uncinia triquetra
K€
uk. as outgroups (Starr & Ford, 2009). For all species, one
individual per population was sampled, except for five populations of C. arctogena that consisted of two individuals each
(Appendix S1). Samples used for the molecular study were
obtained from silica-dried leaf material collected in the field
and from herbarium specimens (Appendix S1). Vouchers for
new collections have been deposited in the herbaria CAN, SI
and UPOS.
Nucleotide diversity (p; Nei, 1987) and haplotype diversity
(Hd; Nei & Tajima, 1983) were calculated for the amplified
chloroplast regions of C. arctogena and C. capitata in DnaSP
5.10 (Librado & Rozas, 2009). DnaSP was also used to test
for molecular selection in atpF–atpH, rps16 and matK with
Tajima’s D (Tajima, 1989) and Fu and Li’s D* and F* (Fu &
Li, 1993) neutrality tests. Selective pressure on matK was
evaluated using the codon-based Z test (Nei & Gojobori,
1986). To test the null hypothesis of neutral selection, the
number of synonymous substitutions per synonymous site
(dS), the number of non-synonymous substitutions per nonsynonymous site (dN), and their variances (estimated by
bootstrap over 10,000 pseudoreplicates) were calculated for
each pair of sequences in Mega 4 (Tamura et al., 2007).
Gaps or missing data were deleted in the pairwise distance
estimation. Because they showed incongruence due to positive selection, we removed the matK sequences of C. monostachya and C. runssoroensis from subsequent phylogenetic
analyses (see Results), mirroring the removal by Gehrke et al.
(2010) of ITS sequences that showed incongruence between
samples.
PCR amplification and sequencing
Phylogenetic analyses
All regions were amplified by polymerase chain reaction
(PCR) from total genomic DNA extracted as described by
Starr et al. (2009). We amplified the nuclear ITS region
(using the primers ITSA and ITS4; White et al., 1990; Blattner, 1999) and three chloroplast DNA (cpDNA) regions: the
atpF–atpH spacer, using primers atpF and atpH (Fazekas
et al., 2008); a portion of the matK gene, using primers
matK 2.1f_J and matK 5r_J (Plant Working Group, Royal
Botanical Gardens Kew, http://www.kew.org/barcoding/protocols.html modified by Chouinard, 2010), and the rps16
intron, using primers rps16F and rps16R (Shaw et al., 2005).
The ITS region has been one of the most useful markers for
inferring plant phylogenies at low taxonomic levels, but
concerted evolution within this multicopy gene family is
We obtained a total of 19 sequences of ITS, 87 of atpF–atpH,
85 of matK and 49 of rps16 (Appendix S1). The ITS region
was only analysed in combination with the plastid regions
due to the low number of sequences obtained. The three
plastid loci were analysed independently, to check for incongruence, and in combination using maximum likelihood
(ML) and Bayesian inference (BI). The combined nuclear
and plastid matrix consisted of 107 sequences with 2835 sites
(see Appendix S1). Maximum-likelihood analyses were performed using RAxML 7.2.6 (Stamatakis, 2006), with a
GTRGAMMA model of sequence evolution and node support
assessed via 1000 bootstrap (BS) pseudoreplicates. Bayesian
analyses were executed in MrBayes 3.2 (Ronquist et al.,
2012) using the most appropriate nucleotide substitution
Genetic variation, neutrality and selection tests
3
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________________________________________________________________
model for each partition as chosen by jModelTest (Posada,
2008) under the Akaike information criterion (AIC). The
selected nucleotide substitution models were HKY for atpF–
atpH, HKY+I for matK, GTR for rps16, HKY+I for ITS1, JC
for ITS 5.8S and GTR for ITS2 (Appendix S1). The Markov
chain Monte Carlo (MCMC) search was run for five million
generations with one tree sampled every 1000 generations
and two simultaneous analyses (‘Nruns = 2’) each of four
Markov chains (‘Nchains = 4’) started from different random
trees. The first 20% of trees were discarded from each run as
burn-in. A Bayesian majority-rule consensus tree was calculated in MrBayes with posterior probability (PP) values as a
measure of clade support. Trees were edited using FigTree
1.3.1 (http://tree.bio.ed.ac.uk/software/figtree/).
Haplotype network
We obtained the genealogical relationships among all three
cpDNA haplotypes using the plastid matrix and statistical
parsimony as implemented in tcs 1.21 (Clement et al.,
2000). The maximum number of differences resulting from
single substitutions among haplotypes was calculated with
95% confidence limits. The only informative indel (atpF–
atpH region) was coded as a presence/absence character for
analysis. Gaps due to mononucleotide repeat units (poly-T
and poly-A) are considered to be highly homoplastic (Kelchner, 2000) and were therefore treated as missing data.
Divergence-time estimation
Dated phylogenies were estimated for the nuclear and plastid
matrix in beast 1.7.5 (Drummond et al., 2012). All matK
sequences were excluded because run convergence was hampered by incongruence in matK, which showed a significant
departure from neutrality (Appendix S1). The analysed
matrix therefore consisted of 94 ITS, atpF–atpH and rps16
sequences with an aligned length of 2089 sites. All phylogenies were estimated using an uncorrelated log-normal relaxed
clock model. A normal age prior with a mean of 13.20 Ma
2.5 Myr was applied to the crown node, based on the previous estimate for the divergence of Carex sections Capituligerae and Longespicatae from the outgroups in the analysis of
Escudero & Hipp (2013). Analyses were conducted using two
independent MCMC runs of 40 million generations each,
assuming a birth–death tree prior with a mean substitution
rate set at 1.0. Run convergence and burn-in were assessed
in Tracer 1.5 (Rambaut & Drummond, 2009). Maximumclade-credibility (MCC) trees were calculated with
TreeAnnotator 1.7.2 (Drummond & Rambaut, 2007) using
a posterior probability limit of 0.9 and the mean heights
option.
Climatic environment – ecological niche
Carex arctogena and C. capitata are known to have different
ecological preferences in Scandinavia (Reinhammar & Bele,
2001). Because the range limits of species and lineages can
be influenced by spatial variation in ecological factors
(Wiens, 2011), we obtained values for 19 bioclimatic variables (Appendix S1) as described by Escudero et al. (2013)
for each sampled population of species in Carex sections Capituligerae and Longespicatae. To characterize the climatic
niche space occupied by each species, we performed a principal components analysis (PCA) of the climatic dataset using
the ‘prcomp’ function (sdev, rotation, centre and scale
options were set as TRUE) and a phylogenetic PCA using
the ‘phyl_pca’ function in the phytools package (assuming
Brownian motion and covariance matrix option; Revell,
2009) in R (R Development Core Team, 2014). A phylogenetic size-correction was performed in our dataset for
non-independence among the observations for lineages. We
represented the data associated with the most important
bioclimatic variables retained in the PCA for C. arctogena in
boxplots.
RESULTS
Haplotype diversity and neutrality tests
The number of cpDNA haplotypes and haplotype diversity
were highest in matK (Nh, 6; Hd, 0.746; nucleotide diversity,
p, 0.00397), whereas nucleotide diversity was highest in
atpF–atpH (Nh, 5; Hd, 0.725; p, 0.00442; Appendix S1). The
number of segregating sites was eight in both matK and
atpF–atpH, twice that in rps16. A significant departure from
neutrality was found in matK sequences (F*-test, P < 0.05;
Appendix S1). Estimates of the average within-group nucleotide substitution rates for matK revealed significant positive
selection (dN > dS) in C. monostachya and C. runssoroensis.
The matK sequences for these species were therefore eliminated from the subsequent analyses as they could affect the
results of phylogenetic reconstructions. Selective pressure has
also been detected on matK in other plant groups (e.g.
McNeal et al., 2009) and in other chloroplast regions (e.g.
Kapralov & Filatov, 2007).
Phylogenetic reconstruction
Bayesian-inference (BI) and ML analyses revealed strong support (97% BS / 1.00 PP, Fig. 2) for a clade including both
sections. Carex monostachya was poorly supported as sister
to a large polytomy composed of C. runssoroensis plus C.
sect. Capituligerae. Carex sect. Capituligerae was retrieved as
an unresolved group with four main lineages (see below).
Neither C. arctogena nor C. capitata was resolved as a monophyletic taxon; instead, two different geographically defined
lineages were detected for each species: (1) C. arctogena lineage A (90% BS / 0.71 PP) includes samples from Europe and
North and South America; (2) C. arctogena lineage B (91%
BS / 0.90 PP) only includes samples from western North
America; (3) C. capitata lineage A (88% BS / 0.78 PP)
includes samples from Russia; and (4) C. capitata lineage
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Uncinia triquetra ARG
C. obtusata WYO 1
C. obtusata WYO 2
C. obtusata WYO 3
C. rupestris SPA
1
98
0.96
69
94
1
97
Sect.
Capituligerae
+ Longespicatae
0.73
Outgroups
C. monostachya KEN 1
C. monostachya KEN 2
C. runssoroensis KEN
C. oreophila TUR
C. capitata MAG 1
0.78
C. capitata MAG 2
C. capitata MAG 3
88
C. capitata YAK 4
C. arctogena ARG 1
C. arctogena ARG 2
C. arctogena ARG 3
C. arctogena ARG 4
C. arctogena ARG 5
C. arctogena ARG 6
C. arctogena ARG 7
C. arctogena ARG 8
C. arctogena ARG 9
C. arctogena ARG 10
C. arctogena MAN 11
0.71
C. arctogena MAN 12
C. arctogena MAN 13
90
C. arctogena BRC 14
C. arctogena QUE 15
C. arctogena QUE 16
C. arctogena QUE 17
C. arctogena LAB 18
C. arctogena SAS 19
C. arctogena ONT 20
C. arctogena ONT 21
C. arctogena NWH 22
C. arctogena GNL 23
C. arctogena GNL 24
C. arctogena FIN 25
90
C. arctogena QUE 26
87
C. capitata MAG 5
C. capitata RUN 6
C. capitata FIN 7
C. capitata FIN 8
C. capitata FIN 9
C. capitata SWE 10
C. capitata SWE 11
C. capitata SWE 12
C. capitata SWE 13
C. capitata NOR 14
C. capitata ICE 15
C. capitata ICE 16
C. capitata ICE 17
C. capitata ICE 18
C. capitata ASK 23
0.92
C. capitata BRC 21
C. capitata BRC 22
97
C. capitata ALB 19
C. capitata MAN 23
C. capitata MAN 24
C. capitata MAN 25
C. capitata MAN 26
C. capitata MAN 27
C. capitata MAN 28
C. capitata MAN 29
C. capitata ONT 30
C. capitata ONT 31
C. capitata YUK 32
C. capitata YUK 33
C. capitata YUK 34
C. capitata NWT 35
C. capitata NWT 36
60 C. capitata SAS 37
C. arctogena ORE 27
C. arctogena ORE 28
C. arctogena WYO 29
C. arctogena ALB 30
C. arctogena WAS 31
C. arctogena WAS 32
C. arctogena MNT 33
C. arctogena MNT 34
C. arctogena MNT 35
C. arctogena UTA 36
C. arctogena UTA 37
C. arctogena NEV 38
C. arctogena COL 39
C. arctogena COL 40
C. arctogena COL 41
C. arctogena COL 42
0.9
C. arctogena COL 43
91
C. arctogena COL 44
C. arctogena CAL 45
C. arctogena CAL 46
C. arctogena CAL 47
C. arctogena CAL 48
C. arctogena CAL 49
C. arctogena CAL 50
C. arctogena CAL 51
C. arctogena CAL 52
C. arctogena CAL 53
C. arctogena CAL 54
C. arctogena CAL 55
C. arctogena CAL 56
C. arctogena CAL 57
C. arctogena CAL 58
C. arctogena CAL 59
87
C. arctogena CAL 60
C. arctogena CAL 61
C. capitata A Russia
C. arctogena A
Northern &
Southern
Hemispheres
C. capitata B
Northern
Hemisphere
C. arctogena B
W North America
0.003
Figure 2 Majority-rule (50%) consensus tree from the Bayesian analysis of nuclear and chloroplast sequences from Carex sections
Capituligerae and Longespicatae (Cyperaceae). Uncinia triquetra, Carex rupestris and C. obtusata were used as outgroups. Numbers above
branches represent Bayesian posterior probabilities (> 0.7 PP); numbers below branches represent bootstrap values (> 60% BS) from the
maximum-likelihood analyses. The grey rectangle highlights C. arctogena samples from the Southern Hemisphere. Abbreviations after
names correspond to geographical regions of the world (Brummitt, 2001) followed by population number.
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0.19–1.66 Ma, Table 1). The grouping of Carex arctogena A
with C. runssoroensis did not receive statistical support in the
MCC tree above 0.9.
B (97 BS / 0.92 PP) comprises samples from North America,
Europe and Russia.
Haplotype network
Climatic environment
The cpDNA haplotype network (Fig. 3) revealed 10 haplotypes and five missing haplotypes. Geographical structure
was detected in most lineages, similar to that found in the
phylogenetic reconstruction. We found one unique haplotype
in C. arctogena lineage A, four in C. arctogena lineage B, one
in C. capitata lineage A and two in C. capitata lineage B.
There is a haplotype shared by eight samples of C. arctogena
A, C. oreophila, C. monostachya and one individual of
C. capitata B. Carex runssoroensis occupied a central position
in the network. The 10 C. arctogena samples from the Southern Hemisphere shared the same haplotype as the 10 Northern Hemisphere samples of C. arctogena A.
The PCA of the climatic dataset from 94 total populations
consisting of C. arctogena (53 individuals; two populations
had missing data in the WorldClim database), C. capitata
(35), C. oreophila (3), C. monostachya (2) and C. runssoroensis (1) showed that principal component 1 (PC1) explained
98.99% of variance and PC2 explained 0.78% (Fig. 5). The
variables with the highest loadings on PC1 were temperature
seasonality (BIO4), the mean temperature of the coldest
quarter (BIO11), the minimum temperature of the warmest
month (BIO6) and isothermality (BIO3; Appendix S1). Maxima and minima for each lineage are shown in Table 2. Similar results were obtained when the analysis was not
corrected for the phylogeny (results not shown). Northern
and Southern Hemisphere samples of C. arctogena A were
clearly separated into two groups. The boxplots of the variables with the highest loadings revealed that northern populations of C. arctogena A tolerate greater temperature
oscillations through the year and a wider range of minimum
temperatures during the coldest month than populations
from the Southern Hemisphere (Table 2, Fig. 6a,b).
Estimation of divergence times
The dating analyses produced a partly incongruent topology
with respect to the BI and ML analyses presented above
(Fig. 4, Table 1). The divergence time of the clade comprising Carex sections Capituligerae and Longespicatae was
6.76 Ma (95% highest posterior density interval, HPD, 3.05–
11.29 Ma), which falls in the late Miocene to early Pliocene.
The diversification of the clade consisting of C. arctogena,
C. capitata, C. oreophila and C. runssoroensis is estimated to
have begun 5.0 Ma (95% HPD 2.10–8.03 Ma). The crown
nodes of the main lineages obtained in the phylogeny
were placed in the late Pleistocene (C. monostachya: 0.13 Ma,
95% HPD 0–0.51 Ma; C. capitata A plus C. oreophila:
0.37 Ma, 95% HPD 0.01–1.17 Ma; C. capitata B: 0.68 Ma,
95% HPD 0.14–1.39 Ma; C. arctogena B: 0.81 Ma, 95% HPD
C.
arctogena
B
(3)
C.
arctogena
B
(12)
DISCUSSION
Origin of the bipolar distribution of C. arctogena
Our study provides strong evidence for a recent origin of the
bipolar disjunction in C. arctogena lineage A. The divergence
time for the clade comprising Carex sections Capituligerae
C.
arctogena
B
(13)
W North America
North
America &
Eurasia
C.
capitata
A
(4)
C.
capitata
B
(4)
C.
capitata
B
(22)
C.
runssoroensis
(1)
C. monostachya
(2)
C. oreophila
(1)
C. arctogena A
(8)
C. capitata B
(1)
C.
arctogena
B
(1)
C.
arctogena A
(20)
North & South
America
Eurasia, North
America & Africa
Figure 3 tcs haplotype network of
concatenated cpDNA sequences of Carex
sections Capituligerae and Longespicatae
(Cyperaceae). Circles represent haplotypes,
lines represent single mutational steps and
small black circles are missing haplotypes.
Circle shades indicate species, and numbers
in parentheses indicate the number of
samples per haplotype. Shaded and dashed
squares represent the geographical
distributions of lineages.
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3.84
Outgroups
0.13
C. monostachya Kenya
6.76
Sect.
Capituligerae
+
Longespicatae
0.37
C. capitata A (Russia) +
C. oreophila Turkey
5.00
C. arctogena A (North &
*
South America) +
2.18
C. runssoroensis Kenya
0.68
C. capitata B (North
America & Eurasia)
0.81
C. arctogena B (W North
America)
MIOCENE
15.0
12.5
10.0
PLIOCENE
7.5
5.0
PLEISTOCENE
0.0 Ma
2.5
Figure 4 Maximum-credibility-clade phylogeny from the Bayesian divergence-time analysis of Carex sections Capituligerae and
Longespicatae (Cyperaceae) using a combined matrix of ITS and atpF–atpH and rps16. Node bars represent the 95% highest posterior
density intervals for the divergence-time estimates of nodes with posterior probabilities above 0.9. See Table 1 for posterior probabilities
and ages inferred for clades. The asterisk denotes that the C. arctogena and C. runssoroensis clade has a posterior probability below 0.5.
Table 1 Divergence dates of clades resolved in Carex sections Capituligerae and Longespicate (Cyperaceae), presented as posterior
probabilities, mean and median time to the most common recent ancestor in millions of years (Ma) and 95% highest posterior density
(HPD) interval obtained from the divergence time analyses of the combined nuclear (ITS) and plastid (atpF–atpH and rps16) matrix.
Clade
Posterior probability
Mean (Ma)
Median (Ma)
95% HPD interval
Carex sect. Capituligerae + Longespicatae
C. monostachya
C. runssoroensis + C. oreophila
+ C. arctogena + C. capitata
C. oreophila + C. capitata A
C. capitata B
C. arctogena B
1.00
0.96
0.64
6.76
0.13
5.00
6.44
0.05
4.81
3.05
0.00
2.31
11.29
0.51
8.03
0.61
0.51
0.96
0.37
0.68
0.81
0.22
0.60
0.72
0.01
0.14
0.19
1.17
1.39
1.66
and Longespicatae (crown node: 6.76 Ma, 95% HPD 3.05–
11.29 Ma; Fig. 4, Table 1) is far younger than the trans-tropical highland bridges (c. 195 Ma; Scotese et al., 1988) and we
therefore reject the vicariance hypothesis for the bipolar disjunction of C. arctogena (Du Rietz, 1940). If convergent evolution could explain the bipolar distribution of C. arctogena,
northern and southern populations of the species would not
share an immediate common ancestor. In contrast, our phylogenetic results place all C. arctogena A samples in a single
clade (Fig. 2) and our haplotype data demonstrate that populations from both hemispheres share identical cpDNA haplotypes over the 2207 bp of three chloroplast markers
(Fig. 3). This clearly suggests that C. arctogena A is a bipolar
monophyletic clade, so we reject a hypothesis of convergent
evolution (Stern, 2013).
The bipolar disjunction is best explained by long-distance
dispersal, which may have been either by mountain-hopping
(‘stepping stones’) or by a direct event (a ‘giant leap’). This
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-8
-6
-4
PC2
-2
0
2
4
C. arctogena A NH
C. arctogena A SH
C. arctogena B
C. capitata A
C. capitata B
C. monostachya
C. oreophila
C. runssoroensis
-2
0
2
4
6
8
PC1
Table 2 Maximum and minimum values for climatic variables
with the highest loadings on principal component 1 by groups
of Carex arctogena and C. capitata: BIO4, temperature
seasonality; BIO6, minimum temperature of the coldest month;
BIO11, mean temperature of the coldest quarter; BIO3,
isothermality.
C. arctogena A
C. arctogena B
C. capitata A
C. capitata B
C. arctogena A Northern
Hemisphere
C. arctogena A Southern
Hemisphere
min.
max.
min.
max.
min.
max.
min.
max.
min.
max.
min.
max.
BIO4
BIO6
BIO11
BIO3
31.15
150.98
51.78
96.09
153.45
205.98
37.44
148.76
64.38
150.98
31.15
51.98
34.8
1.7
20.5
0.6
47.1
34.8
33.9
4.9
34.8
13.9
5.1
1.7
27.9
4.8
12.9
7.2
42.0
29.2
29.0
1.7
27.9
10.3
0.1
4.8
17%
51%
31%
46%
16%
20%
16%
36%
17%
27%
45%
51%
could have occurred during some of the last cold periods at
the end of the Pliocene or in the Pleistocene, which
expanded the polar regions in both hemispheres (Raven,
1963; Ball, 1990), or even at present times. Given that all
other taxa in Carex section Capituligerae and all but one
haplotype are found in the Northern Hemisphere, our data
suggest that this dispersal occurred from the Northern to the
Southern Hemisphere.
The remaining question is: which mechanism better
explains the bipolar disjunction – mountain-hopping or
direct long-distance dispersal? The mountain-hopping
hypothesis (Ball, 1990) proposes a stepwise long-distance
migration by mountain peaks as stepping-stones for polar
and temperate taxa to cross the ecological barrier presented
by the tropics. A route connecting North and South America
through the American Cordillera has been in place since
the late Miocene (Smith, 1986). For species of Carex, no
10
Figure 5 Scatter plot of the first two
principal components, which explain
99.78%, from the principal components
analysis depicting the position of the
samples of Carex sections Capituligerae and
Longespicatae (Cyperaceae) in climatic niche
space.
ecophysiological adaptations to crossing the short-day conditions of the tropical alpine environment seem to be necessary
(Heide, 2002), but we are not aware of any published fossil
records or any other evidence for the occurrence of C. arctogena in areas between northern North America and southern
South America. If C. arctogena had migrated to South America by the slow and gradual means predicted by mountainhopping, we would expect that such a process would leave a
trace of genetic differences in the plastid loci of populations
from both hemispheres (Brochmann et al., 2003; Scotland,
2011), as has been shown for other bipolar species (Vollan
et al., 2006; Escudero et al., 2010). Although we cannot completely reject the mountain-hopping hypothesis, the absence
of genetic variability between populations of C. arctogena A
from both hemispheres fits better with a recent and direct
long-distance dispersal. Direct long-distance dispersal has
been shown to be remarkably frequent in some other species
of Cyperaceae (e.g. Viljoen et al., 2013).
The utricle surrounding Carex fruit can show some features
for wind-dispersal, as seen in Carex physodes (Egorova, 1999)
or for animal-dispersal as seen in Carex microglochin (Savile,
1972). However, with the exception of the bladder-like utricle,
fruits and surrounding fruit structures of Carex generally lack
any obvious morphological features for dispersal by abiotic or
biotic forces. The perigynia of Carex arctogena do not have any
apparent mechanism for dispersal; even the aculeolate teeth on
the margin of the perigynia are variable in number, sometimes
being entirely absent. We suggest that relatively unspecialized
structures for dispersal might play a role in the distribution of
C. arctogena. We regard the hypothesis of non-standard vector-mediated dispersal, either by abiotic or biotic forces, as a
possible explanation of the bipolar disjunction of C. arctogena.
It is possible that populations of C. arctogena in the Southern Hemisphere may have been the result of an accidental
anthropogenic introduction. In this scenario, adaptation to
local environmental conditions, biotic interactions and
demographic processes of this species would all have been
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Figure 6 Carex arctogena boxplots
comparing the four bioclimatic variables
with the highest loadings on the first
component of the bioclimatic PCA for the
different lineages found (A and B) and for
Northern and Southern Hemisphere samples
(A NH and A SH, respectively). (a)
Temperature seasonality (BIO4); (b)
minimum temperature of the warmest
month (BIO6); (c) mean temperature of the
coldest month (BIO11); (d) isothermality
(BIO3). Each box represents the
interquartile range which contains 50% of
the values and the median (horizontal line
across the box). The whiskers extending
from the box represent the highest and
lowest values observed, excluding outliers
(dots).
(a)
(b)
(c)
(d)
established relatively quickly (Theoharides & Dukes, 2007).
Populations of C. arctogena in Patagonia occur in well-conserved habitats and most are only accessible on foot. Specimens of C. arctogena from Patagonia are few in the South
American herbaria BA, BAA, BAB, BCRU, HIP and SI, with
some dating to the late 1880s, when the human influence in
the southernmost parts of South America was very limited.
Although we cannot rule out an anthropogenic introduction
of this species to South America, it seems unlikely.
Bird-mediated direct long-distance dispersal from North
America has already been used to explain a bipolar disjunction in crowberries (Empetrum; Popp et al., 2011). Most
migratory birds that disperse seeds live in temperate and
boreal regions (Wheelwright, 1988). For birds to act as vectors for seed dispersal by endo- or ectozoochory, the seeds
must have morphological features for association with these
animals, and must be able to maintain their viability after
intestinal transit to allow for establishment in new environments (Gillespie et al., 2012). Although Carex arctogena
fruits lack obvious morphological features for zoochorous
dispersal, other structures or features that are not directly
related with dispersal syndromes may be involved, including
anatomical features such as deposits of silica in the pericarp
that harden seeds (Graven et al., 1996; Prychid et al., 2004).
These silica deposits could protect seeds when passing
through birds’ alimentary tracts (Graven et al., 1996) but
could also make the seeds as hard as pebbles and useful for
grinding other organic material in bird gizzards. Carex fruits
could therefore be doubly preferred by birds – both as nourishment and as gastroliths (Alexander et al., 1996).
Some birds from North America, such as the pectoral
sandpiper, Calidris melanotos (Holmes & Pitelka, 1998), and
the lesser yellowlegs, Tringa flavipes (Tibbitts & Moskoff,
1999), are known to feed in sedge meadows before migrating
southwards to their wintering grounds in South America.
Their breeding ranges closely match the current distribution
of C. arctogena A in both hemispheres (Fig. 1). Although
current bird migratory patterns do not necessarily coincide
with past migrations, these observations suggest that the
bipolar disjunction in C. arctogena may have originated via
bird-mediated long-distance dispersal. Additionally, dispersal
may occur through accidental displacement – vagrant birds
or migrants, such as those flying to Australia or New Zealand, deviating widely from their normal route (Battley et al.,
2012). With satellite telemetry, Gill et al. (2009) recorded
transoceanic flights of bar-tailed godwits (Limosa lapponica
baueri) from Alaska to New Zealand and showed that they
can fly 10,153 km ( 1043 SD) non-stop in 7.8 days ( 1.3
SD). This extraordinary flight, combined with species that
can be preferentially chosen for fuel, could help species such
as C. arctogena to achieve a bipolar distribution by means of
direct long-distance dispersal.
Climatic regime differentiation
Theoretically, C. arctogena A is most likely to become established at the high latitudes and elevations in the Southern
Hemisphere that have similar climatic conditions to those of
northern populations (Carlquist, 1966). Although our results
from the bioclimatic data show that Southern Hemisphere
populations currently differ from Northern Hemisphere populations of C. arctogena A in their climatic niches (Fig. 6),
differences in community assembly, which suggest differences
in competitive interactions, may explain how C. arctogena A
was able to establish itself in South America after one or
more initial dispersal events (Waters, 2011). Such differences
could have allowed C. arctogena to shift into new habitats
and climate zones (Broennimann et al., 2007). Alternatively,
establishment could have taken place at a time when both
areas had similar climatic conditions.
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CONCLUSIONS
Evidence from multiple analytical approaches was used to
infer the possible mechanisms underlying the distribution of
a bipolar species. Bioclimatic data, phylogenetic and phylogeographical analyses and divergence-time estimates have
been integrated to test hypotheses that are traditionally used
to account for the origin of bipolar distributions at the species level. Our study highlights the importance of long-distance dispersal in explaining this extraordinary pattern of
plant distribution, although further comparative studies
using multiple bipolar species are necessary to test the same
explanation in other phylogenetically independent cases.
ACKNOWLEDGEMENTS
We thank the staff of the following herbaria for giving us
access to their collections and providing plant material: A,
ALA, BA, BAA, BAB, BCRU, BRY, C, CAN, CAS, CCO,
CHSC, COLO, DAO, E, GH, H, HIP, ICEL, M, MICH,
MONTU, MOR, O, OSC, RM, RMS, SI, UBC, UNM, UPOS,
UTEP, WIN and WTU. Thanks are also due to three anonymous referees and to the editor Robert Whittaker. We
would also like to thank E. Maguilla (Universidad Pablo de
Olavide, Seville, Spain; UPO) for his help with map editing,
M. Gosselin (Canadian Museum of Nature, Ottawa, Canada;
CMN) for providing information related to bird dispersal,
W. Sawtell (University of Ottawa, Canada) and P. Vargas
(Real Jardın Botanico de Madrid, Spain) for assistance in
plant collections, and R. Bull (CMN), M. Mıguez and F. J.
Fernandez (UPO) for technical support. In addition, we are
grateful to University of Ottawa undergraduate students A.
Ginter for translations of Russian label data and J. E. Pender
for assistance with databasing label data and DNA sequencing. This research was supported by a Natural Sciences and
Engineering Research Council of Canada (NSERC) Discovery
Grant to J.R.S. and by a Talentia Scholarship from the
Regional Ministry of Economy, Innovation, Science and
Employment of Andalusia awarded to T.V. for MSc research
at the University of Ottawa. Further support was provided
by the Spanish Ministry of Science and Technology through
project CGL2012-38744 and from the Regional Ministry of
Economy, Innovation, Science and Employment of Andalucia
through the project RNM-2763.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article:
Appendix S1 Studied material, molecular characteristics of
the amplified regions, and results from the principal components analysis of 19 bioclimatic variables from the
WorldClim database, both corrected for phylogeny and
uncorrected.
BIOSKETCH
Tamara Villaverde is a PhD student at Pablo de Olavide
University, Seville (Spain). Her research is focused on the
evolution and phylogeography of angiosperms, with special
interest in the biogeography and systematics of the genus Carex (Cyperaceae).
Authors contributions: M.E., M.L., L.P.B. and J.R.S. conceived the idea; T.V., S.M.-B., L.P.B., M.L. and J.R.S. collected the plant material; T.V., M.E. and S.M.-B. carried out
the lab work and analysed the data; T.V., M.E. and S.M.-B.
led the writing and drafted the manuscript, and all authors
contributed to its preparation.
Editor: Robert Whittaker
12
168
Table S7 Bioclimatic variables used.
169
Table S6 Loadings matrix obtained by the principal components analysis corrected by phylogeny of 19 bioclimatic variables on Carex
sections Capituligerae and Longespicatae.
Table S5 Loadings matrix obtained by the principal components analysis not corrected by phylogeny of 19 bioclimatic variables on Carex
Table S4 Average within-group nucleotide substitution estimates for the matK gene of the complete dataset.
Table S3 Locus information for the regions amplified in the study.
Table S2 Characteristics of the DNA regions sequenced.
Table S1 List of material studied.
Appendix S1 Studied material, molecular characteristics of the amplified regions and results from the principal components analysis of
19 bioclimatic variables from the WorldClim database, uncorrected and corrected for phylogeny.
Tamara Villaverde, Marcial Escudero, Santiago Martín-Bravo, Leo P. Bruederle, Modesto Luceño and Julian R. Starr
Direct long-distance dispersal best explains the bipolar distribution of Carex arctogena (Carex sect. Capituligerae, Cyperaceae)
________________________________________________________________
Chapter 3. Direct long-distance dispersal best explains
________________________________________________________________
the bipolar distribution of Carex arctogena
FIN
25
GNL
23
GNL
24
LAB
18
MAN
11
MAN
12
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
BRC
14
Pop.
code
C. arctogena
Species
58.06000
60.00000
51.88333
64.05000
67.90000
68.22200
55.61667
Latitude
Ϋ͸ͺǤ͵ͻͻͲͲ
Ϋͻ͸Ǥͺ͵͵͵͵
Ϋ͸ͷǤͻͷͲͲͲ
ΫͶͻǤͻͷͲͲͲ
ΫͶͻǤͶͳ͸͸͹
23.62700
ΫͳʹʹǤ͸ͷͲͲͲ
Longitude
Coordinates
170
Canada, British Columbia, Pine Pass. G.
W. Argus 8831. 12/7/1973. (CAN372267)
Finland, Enontekiö. H. Väre 17177.
17/7/2006. (H-809948)
Greenland, Arfersoprflk. B. Fredskild
& V. Dalgaard s.n. 19/8/1987. (COLO456814)
Greenland, Pingorssuaq kitdleq. S.
Hanfgam 83-175. 11/7/1983. (C17/2009N3)
Canada, Labrador, Esker area. Y.
Mäkinen & E. Kankainen s.n.
21/7/1967. (CAN-314758)
Canada, Manitoba, Baralzon Lake. H. J.
Scoggan 22434 & W. K. W. Baldwin.
18/7/1950. (WIN, 22434)
Canada, Quebéc, Fort Chimo. A.
Legault 6782. 22/7/1963. (COLO491481)
Voucher
arctogena A
NH
arctogena A
NH
arctogena A
NH
arctogena A
NH
arctogena A
NH
arctogena A
NH
arctogena A
NH
Clade
—
—
—
KP984471
—
KP984469
—
ITS
KP996281
KP996284
KP996287
—
KP996285
—
KP996286
atpF–atpH
KP996368
KP996371
KP996375
—
KP996372
—
KP996374
matK
GenBank accession numbers
—
—
KP996451
—
—
—
—
rps16
Table S1 List of material studied of Carex arctogena, C. capitata, C. monostachya, C. oreophila, C. runssoroensis, C. rupestris, C. obtusata and
Uncinia triquetra including population code, coordinates, voucher information, corresponding clade and GenBank accessions for
markers used for molecular studies. Population codes correspond to geographical regions of the world (Brummitt, 2001) and population
number.
________________________________________________________________
________________________________________________________________
ONT
20
ONT
21
QUE
15
QUE
16
QUE
17
QUE
26
SAS
19
ARG
1
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
MAN
13
Pop.
code
C. arctogena
Species
ΫͷͶǤ͵͵͵ʹͲ
59.91667
58.15000
52.75000
52.87400
59.26667
55.11160
54.36280
59.36667
Latitude
Ϋ͸͹ǤͶͶͻ͸Ͳ
ΫͳͲͳǤ͸͸͸͸͹
Ϋ͸ͺǤͶͳͲͲͲ
Ϋ͹͵Ǥͺͺ͵͵͵
ΫͺʹǤͺ͵͹ͲͲ
Ϋ͹ʹǤͷͺ͵͵͵
Ϋͻ͵Ǥ͵ͷͷͻͲ
ΫͺͶǤͶ͹ͻͷͲ
Ϋͻ6.23333
Longitude
Coordinates
171
Canada, Manitoba, Hudsons Bay Co.,
Duck Lake. H. J. Scoggan 8288 & W. K.
W. Baldwin. 19/8/1950. (CAN201506)
Canada, Ontario, Kenora District,
Patricia Portion. J. L. Riley 11856.
12/8/1980. (CAN-462937)
Canada, Ontario, Hudson Bay
Lowlands. A. E. Porsild et al. 19898.
4/7/1957. (CAN-278707)
Canada, Quebec, Lac Payne. A. Legault
A7849. 2/8/1965. (CCO-23398)
Canada, Quebec, Boatswain Bay. W. K.
W. Baldwin 406 et al. 8/7/1947. (CAN17333)
Canada, Quebéc, Lac Jaucourt Region,
Lichteneger Lake. G. W. Argus 9221.
16/7/1974. (CAN-3779977)
Canada, Quebec, Fort Chimo. T. Sorensen 293. 17/7/1959. (C15/2009N4)
Canada, Saskatchewan, vicinity of
Patterson Lake. G. W. Argus s.n.
20/7/1963. (CAN-282691)
Argentina, Tierra del Fuego, Tolhuin.
S. Martín-Bravo et al. 40SMB10(1).
14/1/2010. (UPOS-4271)
Voucher
arctogena A
SH
arctogena A
NH
arctogena A
NH
arctogena A
NH
arctogena A
NH
arctogena A
NH
arctogena A
NH
arctogena A
NH
arctogena A
NH
Clade
KP984465
—
KP984474
—
—
—
—
—
—
ITS
—
KP996290
—
KP996288
KP996283
KP996280
KP996282
KP996354
KP996289
atpF–atpH
KP996361
KP996378
—
KP996376
KP996370
KP996367
KP996369
—
KP996377
matK
KP996445
KP996454
—
KP996452
—
—
—
—
KP996453
rps16
________________________________________________________________
________________________________________________________________
ARG
2
ARG
3
ARG
4
ARG
5
ARG
6
ARG
7
ARG
8
ARG
9
ARG
10
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
Pop.
code
C. arctogena
Species
Ϋ͵ͷǤʹͺ͵͵͵
ΫͶͻǤʹ͸͸͸͹
ΫͶͺǤͺʹͳ͵͸
Ϋͷ͵Ǥͻ͵ʹ͵Ͳ
ΫͶͺǤͺʹͳ͵͸
ΫͶͺǤ͹ͳͲͷ͸
ΫͶͺǤ͹ͳͲͷ͸
Ϋͷ͵Ǥͻ͵ͲͲͲ
ΫͷͶǤ͵ͷͳ͸Ͳ
Latitude
Ϋ͸ͻǤͷ͵͵͵͵
Ϋ͹ͳǤ͸͸͸͸͹
Ϋ͹ͳǤͲͷʹͷͲ
Ϋ͸ͺǤͲͺͺ͹Ͳ
Ϋ͹ͳǤͲͷʹͷͲ
Ϋ͹ͳǤͲͷͲ81
Ϋ͹ͳǤͲͷͲͺͳ
Ϋ͸ͺǤͲͺͺͲͲ
Ϋ͸͹Ǥ͸ͷͲͲͲ
Longitude
Coordinates
172
Argentina, Tierra del Fuego, Tolhuin.
S. Martín-Bravo et al. 35SMB10(1).
12/1/2010. (UPOS-4272)
Argentina, Tierra del Fuego, Río
Grande. J. Starr 10015 & T. Villaverde.
13/1/2010. (CAN)
Argentina, Santa Cruz, Los Glaciares
National Park. J. Starr 10020 & T.
Villaverde. 21/1/2010. (CAN)
Argentina, Tierra del Fuego, Río
Grande. J. Starr 10015 & T. Villaverde.
13/1/2010. (CAN)
Argentina, Santa Cruz, Sierra Baguales,
M. K. Arroyo 85201. 16/1/1985. (HIP10500)
Argentina, Neuquén, Chos Malal. O.
Boeckle et al. s.n. 30/1/1964. (BAA11368)
Voucher
arctogena A
SH
arctogena A
SH
arctogena A
SH
arctogena A
SH
arctogena A
SH
arctogena A
SH
arctogena A
SH
arctogena A
SH
arctogena A
SH
Clade
—
—
—
—
—
—
—
—
KP984466
ITS
KP996353
KP996350
KP996349
KP996348
KP996279
KP996278
KP996277
KP996276
—
atpF–atpH
—
—
—
—
KP996366
KP996365
KP996364
KP996362
KP996362
matK
—
KP996485
KP996484
KP996483
KP996450
KP996449
KP996448
KP996447
KP996446
rps16
________________________________________________________________
________________________________________________________________
ALB
30
CAL
45
CAL
46
CAL
47
CAL
48
CAL
49
CAL
51
CAL
52
CAL
53
CAL
54
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
CAL
36
Pop.
code
C. arctogena
Species
39.41917
39.42472
39.49500
39.50191
40.10400
39.47800
40.12739
40.10222
40.10253
51.61000
41.24700
Latitude
ΫͳͳͻǤ͹Ͷ͵͵͵
ΫͳʹͲǤʹͷ͸͸͹
ΫͳʹͲǤͶͳͳͲͲ
ΫͳʹͲǤͳͺ͵ʹͷ
ΫͳʹͳǤͷͲʹͲͲ
ΫͳʹͲǤʹͻʹͲͲ
ΫͳʹͲǤͷͲͻͲ͵
ΫͳʹͲǤͶͻͻͳ͹
ΫͳʹͲǤͶͻͻͻʹ
ΫͳͳͷǤͺʹͳͲͲ
ΫͳʹͳǤ͹ͷ500
Longitude
Coordinates
173
USA, California, Siskiyou Co. J. D.
Jokerst 1823. 5/7/1983. (CHICO38999)
Canada, Alberta, Snow Creek Pass, A.
E. Porsild 22673. 29/7/1960. (CAN266077)
USA, California, Butte Co., J. Starr 10S054 & T. Villaverde. 6/8/2010. (CAN)
USA, California, Butte Co., J. Starr
06018 & J. Thibeault. 3/8/2006. (CAN)
USA, California, Tehama Co., Yellow
Pine Forest. L. Ahart 94326.
19/7/2006. (CHSC-94326)
USA, California, Sierra Co., Anderson
Mdw. R. K. Gierischerisch 3493 & D.
Esplin. 25/6/1969. (COLO-246761)
USA, California, Butte Co. J. Starr 10S054 & T. Villaverde. 6/8/2010. (CAN)
USA, California, Sierra Nevada Co. W.A.
Nisbet 45. 20/7/1957. (CAN-272091)
USA, California, Sierra Co. H. Oswald
8221 & L. Ahart. 19/8/1996. (CHSC66824)
USA, California, Nevada Co. R. Naczi
11420. 3/8/2006. (US-3534689)
USA, California, Nevada Co. R. Naczi
11420. 3/8/2006. (CHICO-99406)
Voucher
arctogena B
arctogena B
arctogena B
arctogena B
arctogena B
—
KP984464
—
—
—
—
—
arctogena B
—
—
—
arctogena B
ITS
KP984467
arctogena B
arctogena B
arctogena B
arctogena B
Clade
—
—
KP996329
KP996343
KP996322
KP996333
KP996320
KP996319
KP996323
KP996347
—
atpF–atpH
KP996358
KP996359
KP996418
KP996432
KP996411
KP996422
KP996409
KP996408
KP996412
KP996436
—
matK
KP996443
—
KP996468
—
KP996464
—
KP996463
KP996462
KP996465
KP996481
KP996482
rps16
________________________________________________________________
________________________________________________________________
CAL
59
CAL
60
CAL
61
COL
39
COL
40
COL
41
COL
42
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
CAL
55
CAL
57
CAL
58
Pop.
code
C. arctogena
Species
38.02547
38.02547
39.80700
39.83400
34.49900
ΫͳͲ͸Ǥ͹ͷͻͻʹ
ΫͳͲ͸Ǥ͹ͷͻͻʹ
ΫͳͲͷǤ͹ͳͲͲͲ
ΫͳͲͷǤ͸͹ͺͲͲ
ΫͳͳͺǤʹͶͺͲͲ
ΫͳͳͻǤʹͳͶͲͲ
ΫͳͳͻǤʹͳͶͲͲ
37.92100
37.92200
ΫͳͳͺǤͶ͹͵ͲͲ
ΫͳͳͺǤͲͶͳ͸͹
ΫͳʹͳǤͷͷͲͲͲ
Longitude
36.65800
38.79167
40.07700
Latitude
Coordinates
174
USA, California, Butte Co. L. P. Janeway
3111. 29/7/1988. (CHICO-44118)
USA, California, El Dorado Co. J. Pykäla
et al. s.n. 23/7/1987. (H-15/2009N6)
USA, California, Tulare Co. S. Brush & J.
Oliphant 155. 24/8/1991. (CAS857890)
USA, California, Mono Co., Mt. Dana
Plateau. D. Taylor 7550. 25/7/1979.
(COLO-330874)
USA, California, Mono Co., Mt. Dana
Plateau. D. Taylor 7550, 25/7/1979.
(COLO-330874)
USA, California, Tulare Co., Sierra
Nevada. J. T. Howell s.n. 5/8/1949.
(DAO-257423)
USA, Colorado, Clear Creek Co. W. A.
Weber et al. s.n. 8/8/1972. (CAN374041)
USA, Colorado, Clear Creek Co., Bill
Moore Lake. N. Lederer s.n.
31/8/1993. (COLO-00263731)
USA, Colorado, Hinsdale Co., Gunnison
National Forest. J. Starr 10S-033 & T.
USA, Colorado, Hinsdale Co., Gunnison
Voucher
arctogena B
arctogena B
arctogena B
arctogena B
—
—
—
—
—
—
arctogena B
—
KP984468
—
arctogena B
ITS
KP984463
arctogena B
arctogena B
arctogena B
arctogena B
Clade
KP996337
KP996338
KP996330
KP996346
KP996328
KP996327
KP996326
—
—
—
atpF–atpH
KP996426
KP996427
KP996419
KP996435
KP996417
KP996416
KP996415
KP996360
—
KP996357
matK
KP996474
KP996475
KP996469
KP996480
—
—
—
KP996444
—
KP996442
rps16
________________________________________________________________
________________________________________________________________
COL
43
COL
44
MNT
33
MNT
34
MNT
35
NEV
38
ORE
27
ORE
28
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
Pop.
code
C. arctogena
Species
44.11400
44.11467
40.81100
44.97142
45.03203
45.05800
39.26528
39.26528
Latitude
ΫͳʹͳǤ͸ʹʹͲͲ
ΫͳʹͲǤ͵͹ͷͻͶ
ΫͳͳͲǤ͵͵ͳͲͲ
ΫͳͲͺǤͷ͹ͻʹͺ
ΫͳͲͺǤͷͳͶͻ͹
ΫͳͲͻǤͶ͹͸ͲͲ
ΫͳͲͷǤͷʹͲ͸͹
ΫͳͲͷǤͷʹͲ͸͹
Longitude
Coordinates
175
USA, Colorado, Lake Co., San Isabel
USA, Colorado, Lake Co., San Isabel
USA, Montana, Carbon Co. H.
Lackshewitz 7790. 11/8/1977. (WTU288770)
USA, Montana, Carbon Co., Custer
National Forest J. Starr 10S-047A & T.
USA, Wyoming, Park Co. J. Starr 10S047B & T. Villaverde. 31/7/2010.
(CAN)
USA, Utah, Duchesne Co., Uinta
Mountains. E. Lewis 512. 15/8/1955.
(CAN-515168)
USA, Oregon, Deschutes Co.,
Deschustes National Forest. J. Starr
10S-057 & T. Villaverde. 9/8/2010.
(CAN)
USA, Oregon, Deschutes Co. C. Halpern
159046 & T. Magee. 30/8/1982. (OSC159046)
Voucher
arctogena B
arctogena B
arctogena B
arctogena B
arctogena B
arctogena B
arctogena B
arctogena B
Clade
—
—
—
—
—
—
—
—
ITS
KP996321
KP996325
KP996344
KP996340
KP996339
KP996334
KP996336
KP996335
atpF–atpH
KP996410
KP996414
KP996433
KP996429
KP996428
KP996423
KP996425
KP996424
matK
—
KP996467
KP996479
—
KP996476
—
KP996473
KP996472
rps16
________________________________________________________________
________________________________________________________________
UTA
36
NEV
37
NWH
22
WAS
31
WAS
32
WYO
29
MAG
1
MAG
2
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. arctogena
C. capitata
C. capitata
C. arctogena
ORE
50
Pop.
code
C. arctogena
Species
68.00000
66.00000
45.05200
48.84233
48.84233
42.27083
39.38800
40.77800
44.11467
Latitude
167.00000
171.00000
ΫͳͲͻǤͷ͹ͶͲͲ
ΫͳʹͲǤͳͶʹʹͷ
ΫͳʹͲǤͳͶʹʹͷ
Ϋ͹ͳǤ͵ͲͷͷͲ
ΫͳͳͻǤ͹ͻʹͲͲ
ΫͳͳͲǤʹ͵͹ͲͲ
ΫͳʹͲǤ͵͹ͷͻͶ
Longitude
Coordinates
176
USA, Utah, Duchesne Co., Gilbert
Creek. A. Huber 440 & S. Goodrich.
25/8/1993. (BRY-368578)
USA, Nevada, Washoe Co. M. E. Lewis
448. 17/7/1955. (CAN-550536)
USA, New Hampshire, Alpine Garden,
Mt. Washington. W. W. Eggleston
1681. 29/7/1989. (RM-23379)
USA, Washington, Whatcom Co. J. Starr
10S-061 & T. Villaverde. 11/8/2010.
(CAN)
USA, Washington, Whatcom Co. J. Starr
10S-061 & T. Villaverde. 11/8/2010.
(CAN)
USA, Wyoming, Park Co., Beartooth
Plateau. B. Neely s.n. 18/8/1984.
(COLO-399492)
Russia, Chukotski Peninsula. U. P.
Kozhevnikov et al. s.n. 27/7/1970.
(DAO-139887)
Russia, Chukotka, Anui upland region.
E. V. Zimarskaja et al. s.n. 12/7/1967.
(DAO-139880)
USA, Oregon, Deschutes Co.,
Deschustes National Forest. J. Starr
10S-057 & T. Villaverde. 9/8/2010.
(CAN)
Voucher
capitata A
capitata A
arctogena B
arctogena B
arctogena B
arctogena B
arctogena B
arctogena B
arctogena B
Clade
—
—
—
—
—
—
—
—
—
ITS
KP996308
KP996304
KP996332
KP996341
KP996342
—
KP996345
KP996331
KP996324
atpF–atpH
KP996397
KP996393
KP996421
KP996430
KP996431
KP996373
KP996434
KP996420
KP996413
matK
—
—
KP996471
KP996477
KP996478
—
—
KP996470
KP996466
rps16
________________________________________________________________
________________________________________________________________
MAG
3
YAK
4
ALB
19
ASK
23
BRC
21
BRC
22
FIN 7
FIN 8
FIN 9
ICE
15
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
Pop.
code
C. capitata
Species
65.14400
66.36700
66.36700
69.08800
52.46667
52.46667
68.06300
58.98333
69.41667
68.00000
Latitude
ΫͳͶǤ͵ͻͶͲͲ
29.53300
29.53300
21.92800
ΫͳʹͶǤ͸ͺ͵͵͵
ΫͳʹͶǤ͸ͺ͵͵͵
ΫͳͶͷǤͲͻ͵ͲͲ
ΫͳͳͲǤͳ͸͸͸͹
130.66667
167.00000
Longitude
Coordinates
177
Russia, Sakha Republic, Bulnsk region.
B. Yurtsev s.n. 25/6/1960. (DAO257437)
Canada, Alberta, Ft. Fitzgerald. W. J.
Cody 4533 & C. C. Loan. 19/7/1950.
(RM-228683)
USA, Alaska, Old John Lake Area. K.
Holmen 61-1227. 13/7/1961. (CAN271116)
Canada, British Columbia, Anahim
Lake. J. Calder 18578 et al. s.n.
9/7/1956. (COLO-158463)
Canada, British Columbia, Anahim
Lake. J. Calder 18578. J. A. Parmelee &
R. L. Taylor s.n. 9/7/1956. (WTU197744)
Finland, Enontekiö lapland. H. Väre
11515. 29/7/2001. (H-737814)
Finland, Kuusamo, Liikasenvaara. T.
Ulvinen s.n. 9/8/1962. (CAN-276804)
Finland,Kuusamo, Liikasenvaara. T.
Ulvinen s.n. 9/8/1962. (CAN-276804)
Iceland, Hallormsstadhur. H. F.
Gotzsche HFG81-37. 22/7/1981. (C15/2009)
Russia, Western Chukotka. E. V.
Zimarskaja et al. s.n. 12/7/1967.
(BRY-122530)
Voucher
capitata B
capitata B
capitata B
capitata B
capitata B
capitata B
ITS
KP984472
—
—
KP984470
—
—
—
—
capitata B
capitata B
—
—
capitata A
capitata A
Clade
—
KP996305
KP996316
—
KP996307
KP996301
KP996312
KP996300
KP996352
KP996310
atpF–atpH
—
KP996394
KP996405
—
KP996396
KP996390
KP996401
KP996389
—
KP996399
matK
—
—
KP996460
—
—
—
KP996456
—
—
—
rps16
________________________________________________________________
________________________________________________________________
ICE
17
ICE
18
MAG
5
MAN
23
MAN
24
MAN
25
MAN
26
MAN
27
MAN
29
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
ICE
16
Pop.
code
C. capitata
Species
58.75500
58.63700
57.83000
58.75500
58.74700
58.63500
62.20000
65.65700
66.00000
66.05000
Latitude
ΫͻͶǤͲ͹ͺͲͲ
Ϋͻ͵Ǥͺʹ͹ͲͲ
ΫͻʹǤͺͲͶ͵Ͳ
ΫͻͶǤͲ͹ͺͲͲ
ΫͻͶǤͳ͸ͷͲͲ
-94.13000
33.78333
Ϋͳ͸ǤͺͳͷͲͲ
ΫͳͺǤ͵ͺ͵ͲͲ
Ϋʹ͵Ǥͳ͵͵ͲͲ
Longitude
Coordinates
178
Iceland, Hrísey, Eyjafirði. A.
Garðarsson s.n. 12/8/1967. (ICEL04078)
Iceland, Dalfjall, Mývatnssvei. E.
Einarsson s.n. 21/8/1974. (ICEL04073)
Russia, Magadan region, North Even
area. A.P. Hohrjakov s.n. 2/8/1976.
(CAN- 455497)
Canada, Manitoba, Churchill, south of
Fort. K. Johnson J73-402. 26/8/1973.
(WIN-33557)
Canada, Manitoba, Fort Churchill. J.
Shay 83-60. 11/7/1983. (WIN-40808)
Ritchie 2104. 5/8/1956. (WIN-22433)
Canada, Manitoba, Wapusk National
Park. E. Punter 03-509 & M. PierceyNormore. 19/7/2003. (WIN-71429)
Canada, Manitoba, Twin Lakes. A. Ford
02379 et al. 25/7/2002. (WIN-71024)
Ritchie 2104. 5/8/1956. (CAN248387)
Iceland, Lagarfoss, Hróarstungu,
Lagarfljótsrannsóknir s.n. 26/6/1976.
(ICEL-04081)
Voucher
capitata B
capitata B
capitata B
capitata B
capitata B
capitata B
—
—
—
—
—
—
—
—
capitata B
capitata B
—
—
capitata B
capitata B
Clade
ITS
KP996313
KP996297
KP996296
KP996294
KP996292
—
KP996314
KP996299
KP996298
KP996306
atpF–atpH
KP996402
KP996385
KP996384
KP996382
KP996380
KP996387
KP996403
KP996388
KP996386
KP996395
matK
KP996457
—
—
—
—
—
KP996458
—
—
—
rps16
________________________________________________________________
________________________________________________________________
NOR
14
NWT
35
NWT
36
ONT
30
ONT
31
RUN
6
SAS
37
SWE
10
SWE
11
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
C. capitata
MAN
30
Pop.
code
C. capitata
Species
63.18100
68.32700
54.06667
62.20000
55.98000
55.13420
67.33333
65.71700
60.07900
58.76667
Latitude
14.75100
18.83800
ΫͳͲͶǤͲͷͻͶͶ
33.78333
Ϋͺ͹Ǥ͸ͶͶͲͲ
ΫͺʹǤ͵ͳʹͺͲ
ΫͳʹͷǤͷͺ͵͵͵
ΫͳͳͺǤͺ͵͵ͲͲ
10.03300
Ϋͻ͵Ǥͺ͵333
Longitude
Coordinates
179
Norway, Folldal Gammelsetran. M.
Vileid s.n. 18/8/1998. (O-235091)
Canada, Northwest Territories,
Sawmill Bay. H. T. Shacklette 2970.
13/7/1948. (CAN-199991)
Canada, Northwest Territories, Aubry
Lake. R. Riewe 225 & M. G. Marsh.
17/7/1976. (CAN-433230)
Canada, Ontario, Kenora District. J. L.
Riley 5848. 23/8/1976. (CAN409561)
Canada, Ontario, Fort Severn. I.
Hustich 1296. 13/7/1956. (CAN242845)
Russia, Karelia Republic. Ruuhijävi 4002. 9/7/2002. (H-744530)
Canada, Saskatchewan, Waskesim. J.
Hudson 5063. 31/7/1992. (CAN565528)
Sweden, Torne, Gemeinde Kiruna. H.
Hertel 22918. 8/8/1980. (M0151931)
Sweden, Jämtland, Paroecia Frösö. E.
Asplund s.n. 2/6/1925. (C15-2009N2)
Canada, Manitoba, vicinity of
Churchill. W. Schofield 6862 & H.
Crum. 21/7/1956. (CAN-247332)
Voucher
capitata B
capitata B
capitata B
capitata B
capitata B
capitata B
capitata B
capitata B
capitata B
capitata B
Clade
KP984476
KP984477
—
—
—
—
—
—
KP984473
—
ITS
—
—
KP996311
KP996309
KP996351
KP996302
KP996318
KP996291
—
KP996315
atpF–atpH
—
—
KP996400
KP996398
—
KP996391
KP996407
KP996379
—
KP996404
matK
—
—
KP996455
—
—
—
KP996461
—
—
KP996459
rps16
________________________________________________________________
________________________________________________________________
YUK
32
YUK
33
YUK
34
KEN
1
KEN
2
TUR
WYO
1
C. capitata
C. capitata
C. capitata
C. monostachya
C. monostachya
C. oreophila
C. obtusata
C. capitata
SWE
12
SWE
13
Pop.
code
C. capitata
Species
44.98930
37.75100
ΫͲǤͳ͸ͷ͸ͳ
ΫͲǤͳ͸ʹͷ͸
61.86667
64.36700
64.36700
68.56667
68.56667
Latitude
ΫͳͳͲǤ͹͸͸͹
44.31600
37.24197
37.20828
Ϋͳ͵ͷǤͺͺ͵͵͵
Ϋͳ͵͹Ǥʹ͸͹ͲͲ
Ϋͳ͵͹Ǥʹ͸͹ͲͲ
18.34167
19.50000
Longitude
Coordinates
180
Canada, Yukon Territory, Dempster
Highway. R. Porsild 1593. 17/7/1968.
(CAN-318505)
Canada, Yukon, Ogilvie Mountains. A.
E. Porsild 1462 & R. Porsild.
28/6/1968. (CAN-318349)
Canada, Yukon, Dawson. J. Calder
25796 & J. Gillett. 22/6/1960. (ALA43436)
Kenya, Mt. Kenya National Park. Naro
Moru route. M. L. Buide 114UPO-K.
28/7/2007. (UPOS3304-111)
Kenya, Mt. Kenya National Park, Naro
Moru route. M. L. Buide 114UPO-K.
28/7/2007. (UPOS3306-462)
Turkey. Hakkari Province, Kara Dag.
Davis & Polunim 24438. 16/8/1954.
(E-00353688)
USA, Wyoming, Park Co., Yellowstone
National Park. E. F. Evert 38901.
9/7/2001. (MOR0060897-164295)
Sweden, Soland, Torne. C. G. Alm s.n.
9/8/1958. (V-539346)
Sweden, Torne Lappmark, Abisko. G.
Alm s.n. 6/8/1958. (H-1226056)
Voucher
Outgroup
oreophila
monostachya
KP984459
KP984462
—
—
—
capitata B
—
—
—
monostachya
ITS
KP984475
capitata B
capitata B
capitata B
capitata B
Clade
KP996270
—
KP996273
KP996274
KP996295
KP996317
KP996293
KP996303
—
atpF–atpH
—
—
—
—
KP996383
KP996406
KP996381
KP996392
—
matK
KP996437
KP996441
—
KP996440
—
—
—
—
—
rps16
________________________________________________________________
________________________________________________________________
WYO
2
WYO
3
SPA
KEN
ARG
C. obtusata
C. rupestris
C. runssoroensis
Uncinia
triquetra
Pop.
code
C. obtusata
Species
Ϋͷ͵ǤͳͷͻͷͲ
ΫͲǤͳ͵͵͸ͻ
42.68350
43.77250
43.81930
Latitude
Ϋ͹ͳǤͳ͹͸ͳͲ
37.23439
0.07240
ΫͳͲͻǤͳͻͺͷͲ
ΫͳͲͻǤͲ͸͵͵
Longitude
Coordinates
181
Spain, Huesca, Parque Nacional de
Ordesa y Monte Perdido. M. L. Buide
57MBR04 & J. M. Marín. 30/7/2004.
(UPOS-168)
Kenya, Mt. Kenya National Park, Naro
Moru route. M. L. Buide et al. 113UPOK. 28/7/2007.(UPOS3305-461)
Chile, Punta Arenas, Reserva forestal
de Magallanes. M. Luceño 185ML05 &
R. Álvarez. 28/12/2005. (UPOS-1803)
USA, Wyoming, Hot Springs Co.,
Shoshone National. Forest. E. Evert
39259. 2/7/2002. (MOR-0060899162917)
USA, Wyoming, Hot Springs Co.,
Absaroka Mountains. E. Evert 38141.
29/6/2000. (MOR-0060898-161081)
Voucher
Outgroup
runssoroensis
Outgroup
Outgroup
Outgroup
Clade
—
—
—
KP984461
KP984460
ITS
KP996268
KP996275
KP996269
KP996272
KP996271
atpF–atpH
KP996355
—
KP996356
—
—
matK
—
—
—
KP996439
KP996438
rps16
________________________________________________________________
________________________________________________________________
Total number of sequences in the alignment
Aligned length (bp)
Ungapped length range
Identical sites
Pairwise identity
Variable characters
Parsimony-informative
characters
Number of informative
indels
Mean G+C content
Substitution model
References
Description of regions
Primers
atpF / atpH
matk 2.1f_J /matk 5r_J
rps16F / rps16R
1
13
47.90%
27.90%
HKY+I (ITS 1)/ JC
HKY
(5.8S)/ GTR (ITS 2)
605
516–601
579 (97.7%)
99.30%
17
14
628
616–624
571 (91.8%)
64.50%
51
36
182
28.90%
HKY+I
0
746
693–746
722 (96.8%)
99.50%
21
12
27.10%
GTR
0
856
643–856
833 (97.3%)
99.50%
34
14
Intergenic spacer
Internal transcribed Intergenic spacer Chloroplast gene of a maturase protein
of chloroplast
spacers 1 and 2 and of chloroplast
region
5.8S ribosomal RNA region
White (1990) and
Fazekas et al.
Plant Working Group, Royal Botanical Gardens Shaw et al.
Blattner (1999)
(2008)
Kew, http://www.kew.org/barcoding/protoc (2005)
ols.html, modified by Chouinard (2010)
19
87
89
49
ITS-4 / ITS-A
Table S2 Characteristics of the DNA regions sequenced for complete datasets including all species in Carex sections Capituligerae and
Longespicatae and outgroups.
________________________________________________________________
________________________________________________________________
________________________________________________________________
________________________________________________________________
Table S3 Locus information for the regions amplified in the study including samples
sizes, summary statistics. Nh, number of haplotypes (gaps were excluded); Hd,
haplotype diversity; SǡǢɎǡucleotide diversity.
Locus
atpF–atpH
rps16
matK
Nh
5
4
6
Hd
S
0.725
0.729
0.746
8
4
8
Ɏ
0.00442
0.00245
0.00397
Tajima’s D
Fu & Li’s D*
1.27151n.s.
1.63220n.s.
1.85050n.s.
1.27758n.s.
1.01718n.s.
1.28088n.s.
Fu & Li’s F*
1.50645n.s.
1.40374n.s.
1.73597*
*P < 0.05; n.s., not significant.
Table S4 Average within-group nucleotide substitution estimates for the matK gene of
the complete dataset. dS, number of synonymous sites; dN, number of non-synonymous
sites.
Selection hypothesis tested
Species
Outgroups
C. monostachya
and C. runssoroensis
C. capitata A
C. capitata B
C. arctogena A
C. arctogena B
Neutrality
Positive
Purifying
Probability ΫdN
Probability dSΫdN
Probability dSΫdN
0.508n.s.
0.040*
ΫͲǤ͸͸Ͷ
2.081
1.000n.s.
0.019*
ΫͲǤ͸͸͹
2.106
0.252n.s.
1.000n.s.
0.670
ΫʹǤͲͻ͵
1.000n.s.
0.304n.s.
1.000n.s.
0.297n.s.
0 .000
1.031
0.000
ΫͳǤͲͶͺ
1.000n.s.
0.154n.s.
1.000n.s.
0.150n.s.
0.000
1.022
0.000
1.039
1.000n.s.
1.000n.s.
1.000n.s.
1.000n.s.
0.000
ΫͳǤͲ͵ͺ
0.000
ΫͳǤͲ͵Ͳ
*P < 0.05; n.s., not significant.
183
PC1
PC2
PC3
bio1
ΫͲǤʹͺ͸ ΫͲǤʹͳͻ ΫͲǤͲ͸ͻ
bio2
ΫͲǤͳͳͲ ΫͲǤʹͻͶ
0.187
bio3
ΫͲǤ͵Ͳͺ ΫͲǤͲͻ͵ ΫͲǤͲʹ͹
bio4
0.328
0.009
0.209
bio5
ΫͲǤͲ͸ͻ ΫͲǤ͵͹ͷ
0.209
bio6
ΫͲǤ͵ʹʹ ΫͲǤͳͲͷ ΫͲǤͳ͹͵
bio7
0.293 ΫͲǤͲ͹ͷ
0.277
bio8
0.152
0.008
0.125
bio9
ΫͲǤʹͻͺ ΫͲǤͳͻͲ ΫͲǤͲͻ͹
bio10
ΫͲǤͲ͸Ͷ ΫͲǤ͵͸Ͷ
0.150
bio11
ΫͲǤ͵ʹ͵ ΫͲǤͳ͵ʹ ΫͲǤͳ͵ͻ
bio12
ΫͲǤʹͶͶ
0.252
0.265
bio13
ΫͲǤʹ͵ͳ
0.178
0.378
bio14
ΫͲǤͳͷͲ
0.351 ΫͲǤͳͲͳ
bio15
0.014 ΫͲǤͳ͸ͳ
0.496
bio16
ΫͲǤʹ͵ͳ
0.172
0.384
bio17
ΫͲǤͳͺʹ
0.344 ΫͲǤͲ͵Ͷ
bio18
ΫͲǤͲͶ͸
0.346
0.141
bio19
ΫͲǤʹͷͶ
0.048
0.244
% of
41.900% 26.940% 14.340%
variance
Variable
0.217
ΫͲǤͲ͵͹
0.093
ΫͲǤͲͳͺ
0.157
0.083
ΫͲǤͲͲͺ
0.658
ΫͲǤͳʹͳ
0.308
0.107
ΫͲǤͲͲͻ
0.005
0.101
ΫͲǤͲͻͷ
ΫͲǤͲͶ͸
0.120
0.420
ΫͲǤ͵ͺͳ
7.699%
PC4
ΫͲǤͲͷʹ
0.570
0.053
0.113
0.273
ΫͲǤͳ͸͵
0.297
ΫͲǤʹͺ͸
0.031
0.072
ΫͲǤͲͺͲ
0.028
ΫͲǤͳͳ͹
0.340
ΫͲǤ͵͵Ͷ
ΫͲǤͳͲ͹
0.318
0.127
ΫͲǤͲͷͲ
4.640%
PC5
ΫͲǤͳͶͷ
0.339
0.601
ΫͲǤͳͳʹ
ΫͲǤͳͻͶ
ΫͲǤͲͷͶ
ΫͲǤͲ͵ͻ
ΫͲǤͲ͵͵
ΫͲǤͲ͸͵
ΫͲǤͶͲͳ
ΫͲǤͲʹͷ
ΫͲǤͳͲͶ
0.064
ΫͲǤʹͳͲ
0.230
ΫͲǤͲʹͷ
ΫͲǤͲͻ͵
0.179
ΫͲǤ͵͸Ͳ
2.338%
PC6
ΫͲǤͲͻͳ
0.330
0.083
ΫͲǤͲͷͻ
ΫͲǤͳͲͳ
ΫͲǤͲͷ͵
0.004
0.580
ΫͲǤͲ͸ʹ
ΫͲǤʹʹͻ
ΫͲǤͲͳͷ
0.069
ΫͲǤͲʹͺ
ΫͲǤͳͳͷ
ΫͲǤͶͲ͵
0.056
ΫͲǤͲͺʹ
ΫͲ.285
0.441
0.915%
PC7
ΫͲǤͳͻͳ
0.076
ΫͲǤͲ͸ͳ
0.035
ΫͲǤͲ͹ʹ
0.014
ΫͲǤͲͶͻ
0.317
0.499
ΫͲǤͳͲ͵
ΫͲǤͲͶ͹
ΫͲǤͳͳʹ
ΫͲǤͳ͸͸
0.405
0.501
ΫͲǤʹͳͻ
0.231
ΫͲǤͳͷ͸
0.044
0.511%
PC8
184
ΫͲǤͳͲͷ
ΫͲǤͲ͸ʹ
ΫͲǤͳ͵͸
0.071
ΫͲǤͲͲ͹
ΫͲǤͳͲ͸
0.104
0.029
0.754
ΫͲǤͲ͹Ͳ
ΫͲǤͲͻͻ
ΫͲǤͲͲ2
0.164
Ϋ0.290
ΫͲǤ͵Ͳͻ
0.137
ΫͲǤͳͷ͸
0.298
ΫͲǤͳʹ͹
0.312%
PC9
ΫͲǤͳͳͲ
ΫͲǤ͵͹ͺ
0.652
0.394
0.008
ΫͲǤͲͶ͵
0.048
0.007
0.103
0.274
ΫͲǤʹʹʹ
0.058
0.062
0.053
ΫͲǤͳͷͻ
ΫͲǤͲʹͳ
0.118
ΫͲǤʹ͹͵
0.039
0.213%
PC10
0.286
0.008
0.150
0.064
ΫͲǤ͵ͷͶ
ΫͲǤʹͲ͹
0.038
ΫͲǤͲ͸ͷ
0.048
0.180
ΫͲǤͲ͵͹
0.017
ΫͲǤͶͳͶ
ΫͲǤͳ͵͸
0.112
ΫͲǤʹͳͳ
ΫͲǤͲͶͲ
0.463
0.467
0.063%
PC11
ΫͲǤͷ͵ͳ
ΫͲǤͲͷͺ
0.023
0.058
0.395
0.400
ΫͲǤʹͳͶ
ΫͲ.020
ΫͲǤͲͻͳ
ΫͲǤͲʹ͹
ΫͲǤͲʹ͸
ΫͲǤͳͷʹ
ΫͲǤͳͲͶ
ΫͲǤʹ͸ʹ
0.001
ΫͲǤͳͶ͵
0.174
0.323
0.286
0.053%
PC12
0.062
0.045
ΫͲǤͳʹͶ
ΫͲ.007
ΫͲǤͳͳ͵
ΫͲǤͲͷ͹
0.003
0.018
0.028
0.033
0.045
0.359
ΫͲǤͲͻͲ
ΫͲǤͷͷͺ
0.063
ΫͲǤͳͳ͹
0.646
ΫͲǤʹͲ͹
ΫͲǤͳͺͳ
0.031%
PC13
ΫͲǤͲʹͻ
0.145
ΫͲǤͲͺͲ
0.021
ΫͲǤ͵ʹ͹
ΫͲǤͲͺͶ
ΫͲǤͲ͹͵
ΫͲǤͲʹͷ
ΫͲǤͲͶͷ
0.282
0.080
ΫͲǤͷ͸ͺ
0.575
ΫͲǤͲ͹ʹ
ΫͲǤͲͶ͸
ΫͲǤͳ͹͸
0.236
ΫͲǤͲͲͶ
0.124
0.017%
PC14
0.377
ΫͲǤ͵ͳ͸
0.105
ΫͲǤͳ͸ʹ
0.379
ΫͲǤͳ͸Ͳ
0.347
0.044
0.007
ΫͲǤͶͷʹ
ΫͲǤͲͲ͸
ΫͲǤ͵͵͹
0.083
ΫͲǤͲ͹ͳ
0.035
ΫͲǤͲͷ͸
0.253
0.008
0.176
0.015%
PC15
ΫͲǤͲͳͻ
ΫͲǤͲͷ͵
0.000
ΫͲǤͲͷͳ
0.100
ΫͲǤͲʹͻ
0.078
ΫͲǤͲͲͳ
ΫͲǤͲͲͳ
ΫͲǤͲͺͳ
0.072
0.430
0.391
0.044
ΫͲǤͲͲ͵
ΫͲǤ͹ͷʹ
ΫͲǤʹ͵ͷ
0.042
0.054
0.010%
PC16
0.464
0.185
ΫͲǤͳͳʹ
0.447
0.021
0.331
ΫͲǤ͵ʹ͸
ΫͲǤͲͲͶ
ΫͲǤͲͲͷ
ΫͲǤʹ͵͸
ΫͲǤͶͻ͹
ΫͲǤͲͳ͵
0.115
ΫͲǤͲͳ͵
ΫͲǤͲͲͳ
ΫͲǤͲ͹ͳ
0.006
0.018
ΫͲǤͲʹʹ
0.003%
PC17
PC19
0.033 0.000
0.009 0.000
ΫͲǤͲͳͻ 0.000
0.650 0.000
ΫͲǤͲͳ͹ ΫͲǤ͵ʹ͵
ΫͲǤͲͳͳ 0.674
0.003 0.665
ΫͲǤͲͲ͵ 0.000
ΫͲǤͲͲʹ 0.000
ΫͲǤʹ͵ͻ 0.000
0.718 0.000
ΫͲǤͲͳͺ 0.000
ΫͲǤͲʹʹ 0.000
0.006 0.000
ΫͲǤͲͲ͵ 0.000
0.032 0.000
ΫͲǤͲͳ͸ 0.000
0.025 0.000
0.000 0.000
0.001% 0.000%
PC18
Table S5 Loadings matrix obtained by the principal components analysis not corrected by phylogeny of 19 bioclimatic variables on Carex
________________________________________________________________
________________________________________________________________
PC1
Ϋ0.286
Ϋ0.110
Ϋ0.308
0.328
Ϋ0.069
Ϋ0.322
0.293
0.152
Ϋ0.298
Ϋ0.064
Ϋ0.323
Ϋ0.244
Ϋ0.231
Ϋ0.150
0.014
Ϋ0.231
Ϋ0.182
Ϋ0.046
Ϋ0.254
98.993%
Variables
bio1
bio2
bio3
bio4
bio5
bio6
bio7
bio8
bio9
bio10
bio11
bio12
bio13
bio14
bio15
bio16
bio17
bio18
bio19
% of
variance
Ϋ0.219
Ϋ0.294
Ϋ0.093
0.009
Ϋ0.375
Ϋ0.105
Ϋ0.075
0.008
Ϋ0.190
Ϋ0.364
Ϋ0.132
0.252
0.178
0.351
Ϋ0.161
0.172
0.344
0.346
0.048
0.786%
PC2
Ϋ0.069
0.187
Ϋ0.027
0.209
0.209
Ϋ0.173
0.277
0.125
Ϋ0.097
0.150
Ϋ0.139
0.265
0.378
Ϋ0.101
0.496
0.384
Ϋ0.034
0.141
0.244
0.126%
PC3
0.217
Ϋ0.037
0.093
Ϋ0.018
0.157
0.083
Ϋ0.008
0.658
Ϋ0.121
0.308
0.107
Ϋ0.009
0.005
0.101
Ϋ0.095
Ϋ0.046
0.120
0.420
Ϋ0.381
0.052%
PC4
Ϋ0.052
0.570
0.053
0.113
0.273
Ϋ0.163
0.297
Ϋ0.286
0.031
0.072
Ϋ0.080
0.028
Ϋ0.117
0.340
Ϋ0.334
Ϋ0.107
0.318
0.127
Ϋ0.050
0.023%
PC5
Ϋ0.145
0.339
0.601
Ϋ0.112
Ϋ0.194
Ϋ0.054
Ϋ0.039
Ϋ0.033
Ϋ0.063
Ϋ0.401
Ϋ0.025
Ϋ0.104
0.064
Ϋ0.210
0.230
Ϋ0.025
Ϋ0.093
0.179
Ϋ0.360
0.008%
PC6
Ϋ0.091
0.330
0.083
Ϋ0.059
Ϋ0.101
Ϋ0.053
0.004
0.580
Ϋ0.062
Ϋ0.229
Ϋ0.015
0.069
Ϋ0.028
Ϋ0.115
Ϋ0.403
0.056
Ϋ0.082
Ϋ0.285
0.441
0.006%
PC7
Ϋ0.191
0.076
Ϋ0.061
0.035
Ϋ0.072
0.014
Ϋ0.049
0.317
0.499
Ϋ0.103
Ϋ0.047
Ϋ0.112
Ϋ0.166
0.405
0.501
Ϋ0.219
0.231
Ϋ0.156
0.044
0.004%
PC8
185
Ϋ0.105
Ϋ0.062
Ϋ0.136
0.071
Ϋ0.007
Ϋ0.106
0.104
0.029
0.754
Ϋ0.070
Ϋ0.099
Ϋ0.002
0.164
Ϋ0.290
Ϋ0.309
0.137
Ϋ0.156
0.298
Ϋ0.127
0.001%
PC9
Ϋ0.110
Ϋ0.378
0.652
0.394
0.008
Ϋ0.043
0.048
0.007
0.103
0.274
Ϋ0.222
0.058
0.062
0.053
Ϋ0.159
Ϋ0.021
0.118
Ϋ0.273
0.039
0.000%
PC10
0.286
0.008
0.150
0.064
Ϋ0.354
Ϋ0.207
0.038
Ϋ0.065
0.048
0.180
Ϋ0.037
0.017
Ϋ0.414
Ϋ0.136
0.112
Ϋ0.211
Ϋ0.040
0.463
0.467
0.000%
PC11
Ϋ0.531
Ϋ0.058
0.023
0.058
0.395
0.400
Ϋ0.214
Ϋ0.020
Ϋ0.091
Ϋ0.027
Ϋ0.026
Ϋ0.152
Ϋ0.104
Ϋ0.262
0.001
Ϋ0.143
0.174
0.323
0.286
0.000%
PC12
0.062
0.045
Ϋ0.124
Ϋ0.007
Ϋ0.113
Ϋ0.057
0.003
0.018
0.028
0.033
0.045
0.359
Ϋ0.090
Ϋ0.558
0.063
Ϋ0.117
0.646
Ϋ0.207
Ϋ0.181
0.000%
PC13
Ϋ0.029
0.145
Ϋ0.080
0.021
Ϋ0.327
Ϋ0.084
Ϋ0.073
Ϋ0.025
Ϋ0.045
0.282
0.080
Ϋ0.568
0.575
Ϋ0.072
Ϋ0.046
Ϋ0.176
0.236
Ϋ0.004
0.124
0.000%
PC14
0.377
Ϋ0.316
0.105
Ϋ0.162
0.379
Ϋ0.160
0.347
0.044
0.007
Ϋ0.452
Ϋ0.006
Ϋ0.337
0.083
Ϋ0.071
0.035
Ϋ0.056
0.253
0.008
0.176
0.000%
PC15
Ϋ0.019
Ϋ0.053
0.000
Ϋ0.051
0.100
Ϋ0.029
0.078
Ϋ0.001
Ϋ0.001
Ϋ0.081
0.072
0.430
0.391
0.044
Ϋ0.003
Ϋ0.752
Ϋ0.235
0.042
0.054
0.000%
PC16
0.464
0.185
Ϋ0.112
0.447
0.021
0.331
Ϋ0.326
Ϋ0.004
Ϋ0.005
Ϋ0.236
Ϋ0.497
Ϋ0.013
0.115
Ϋ0.013
Ϋ0.001
Ϋ0.071
0.006
0.018
Ϋ0.022
0.000%
PC17
PC19
0.033 0.000
0.009 0.000
Ϋ0.019 0.000
0.650 0.000
Ϋ0.017 Ϋ0.323
Ϋ0.011 0.674
0.003 0.665
Ϋ0.003 0.000
Ϋ0.002 0.000
Ϋ0.239 0.000
0.718 0.000
Ϋ0.018 0.000
Ϋ0.022 0.000
0.006 0.000
Ϋ0.003 0.000
0.032 0.000
Ϋ0.016 0.000
0.025 0.000
0.000 0.000
0.000% 0.000%
PC18
Table S6 Loadings matrix obtained by the principal components analysis corrected by phylogeny of 19 bioclimatic variables on Carex
________________________________________________________________
________________________________________________________________
________________________________________________________________
________________________________________________________________
Table S7 Bioclimatic variables used. Units of bioclimatic variables are °C × 10 for
temperature (excluding BIO4, which was calculated based on K × 10 to deal with
negative temperatures) and mm for precipitation.
Bioclimatic variable
BIO1
BIO2
BIO3
BIO4
BIO5
BIO6
BIO7
BIO8
BIO9
BIO10
BIO11
BIO12
BIO13
BIO14
BIO15
BIO16
BIO17
BIO18
BIO19
Description
annual mean temperature
mean diurnal temperature range [mean of monthly (maximum temperature Ϋ
minimum temperature)]
isothermality (BIO2 / BIO7 × 100)
temperature seasonality (standard deviation of monthly temperature)
maximum temperature of the coldest month
minimum temperature of the warmest month
temperature range (BIO6 Ϋ BIO5)
mean temperature of the wettest quarter
mean temperature of the driest quarter
mean temperature of the warmest quarter
mean temperature of the coldest quarter
annual precipitation
precipitation of the wettest month
precipitation of the driest month
precipitation seasonality (coefficient of variation of monthly precipitation)
precipitation of the wettest quarter
precipitation of the driest quarter
precipitation of the warmest quarter
precipitation of the coldest quarter
REFERENCES
Blattner, F.R. (1999) Direct amplification of the
entire ITS region from poorly preserved plant
material using recombinant PCR. Biotechniques,
27, 1180–1186.
Brummitt, R.K. (2001) World geographical scheme
for recording plant distributions, 2nd ed. Hunt
Institute for Botanical Documentation, Pittsburgh, PA.
Chouinard, B.N. (2010) DNA Barcodes for the Cariceae (Carex & Kobresia, Cyperaceae) of North
America, north of Mexico. University of Ottawa,
Ottawa, ON.
Fazekas, A.J., Burgess, K.S., Kesanakurti, P.R.,
Graham, S.W., Newmaster, S.G., Husband, B.C.,
Percy, D.M., Hajibabaei, M. & Barrett, S.C.H.
(2008) Multiple multilocus DNA barcodes from
the plastid genome discriminate plant species
equally well. PLoS ONE, 3, 1–12.
Miller, J., Siripun, K.C., Winder, C.T., Schilling, E.,
& Small, R.L. (2005) The tortoise and the hare
II: relative utility of 21 noncoding chloroplast
DNA sequences for phylogenetic analysis. American Journal of Botany, 92, 142–166.
White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990)
Amplification and direct sequencing of fungal
ribosomal RNA genes for phylogenetics. PCR
protocols: a guide to methods and applications
(ed. by M. Innis, D. Gelfand, D. Sninsky and T.
White), Academic Press.
186
Chapter 4
Long-distance dispersal during the
middle–late Pleistocene explains the
bipolar disjunction of Carex maritima
(Cyperaceae)
187
188
Chapter 4. Long-distance dispersal during the middle–late Pleistocene explains the bipolar
________________________________________________________________
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disjunction of Carex maritima
Journal of Biogeography (J. Biogeogr.) (2015)
ORIGINAL
ARTICLE
Long-distance dispersal during the
middle–late Pleistocene explains the
bipolar disjunction of Carex maritima
(Cyperaceae)
Tamara Villaverde1*, Marcial Escudero2, Modesto Luce~
no1 and
1
Santiago Martın-Bravo
1
Botany area, Department of Molecular
Biology and Biochemical Engineering, Pablo
de Olavide University, Seville, Spain,
2
Department of Integrative Ecology, Estacion
Biologica de Do~
nana (EBD – CSIC), Seville,
Spain
ABSTRACT
Aim We set out to explain the bipolar distribution of Carex maritima, clarifying the direction and timing of dispersal. We also tested mountain-hopping
and direct long-distance dispersal hypotheses, as well as the relationship of C.
maritima with biotic and abiotic factors that could explain the bipolar distribution.
Location Arctic/boreal latitudes of both hemispheres.
Methods Molecular and bioclimatic data were obtained for C. maritima and
related species from section Foetidae. We sequenced two (rps16 and 50 trnK
intron) plastid DNA regions (cpDNA) and the external and internal transcribed spacers (ETS and ITS) of the nuclear ribosomal gene region (nrDNA)
and inferred phylogenetic relationships, divergence time estimates and biogeographical patterns using maximum likelihood, statistical parsimony, Bayesian
inference and ecological niche modelling.
Results Carex maritima populations from the Southern Hemisphere were
genetically and ecologically differentiated from their northern counterparts and
formed a monophyletic group nested within a paraphyletic C. maritima. Divergence time analysis estimated a middle–late Pleistocene divergence of the
southern lineage (0.23 Ma; 95% highest posterior density: 0.03–0.51 Ma).
Southern Hemisphere populations are more stenotopic than the Northern
Hemisphere ones, which tolerate harsher conditions.
*Correspondence: Tamara Villaverde, Botany
area, Department of Molecular Biology and
Biochemical Engineering, Pablo de Olavide
University, ctra. de Utrera km 1 s/n, 41013
Seville, Spain.
Main conclusions Our results point to a middle–late Pleistocene migration
of C. maritima by long-distance dispersal, either directly or via mountain-hopping, from the Northern Hemisphere to the Southern Hemisphere.
Keywords
Biogeography, bipolar distribution, Carex, climatic niche, Cyperaceae,
divergence time estimation, Foetidae, long-distance dispersal.
INTRODUCTION
Darwin (1872) studied some potential mechanisms underlying the disjunctions of arctic–alpine plant species to refute
the idea of multiple creations (Gmelin, 1747) in favour of
the hypothesis of a single origin and subsequent migrations.
He compiled evidence about the time in which these plants
could have initiated their migrations, together with the
means and directions of colonization (e.g. seed survival in
oceans or seed dispersal by birds), making use of data to
explain the similarities between the floras of very distant
mountain ranges spread throughout the world. He invoked
signs of an Ice Age in the high latitudes of the Northern
Hemisphere to argue that these plants could have migrated
southwards and descended from the mountain summits during the glacial epoch. As the climate subsequently warmed
up in the high latitudes of the Northern Hemisphere, plants
would have recolonized northwards, as well as moved to
higher elevations in the mountainous regions of the lower
latitudes of the Northern Hemisphere. When the Southern
Hemisphere experienced a glacial period, these isolated populations would have been able to spread, in time reaching
http://wileyonlinelibrary.com/journal/jbi
doi:10.1111/jbi.12559
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1
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the scattered locations in the high latitudes of the Southern
Hemisphere where they persist. Nearly a century and a half
later, the ideas and hypotheses proposed by Darwin to
explain bipolar disjunctions are still admired as having been
well ahead of their time (Donoghue, 2011). Nowadays, a
combination of bioclimatic and molecular data can help us
to better assess the possible evolutionary, climatic and geological changes at the origin of the biogeographical patterns
(Crisp et al., 2011).
Historical biogeography has been dominated over the past
few decades by investigations of shared distribution patterns
among taxa (e.g. Sanmartın et al., 2001; Posadas et al.,
2006). Organism distributions in the Southern Hemisphere,
together with the underlying causes, have long been analysed
(e.g. Raven, 1963; Raven & Axelrod, 1974; Wen & IckertBond, 2009; reviewed in Sanmartın & Ronquist, 2004).
One of the most fascinating plant distribution patterns
concerning the Southern Hemisphere encompasses the bipolar disjunction (> 55 N and > 52 S), achieved only by c. 30
vascular plant species (Moore & Chater, 1971). Four hypotheses have historically been put forward to account for bipolar
disjunctions: (1) convergent or parallel evolution of the disjunct populations (Scotland, 2011); (2) vicariance (Du Rietz,
1940), which implies a continuous distribution fragmentation dating back to the trans-tropical highland bridges during the Mesozoic Era (from the early Jurassic, 195 Ma;
Scotese et al., 1988); (3) stepwise long-distance dispersal
across the equator and via mountain ranges (‘mountain-hopping’; Raven, 1963; Moore & Chater, 1971; Ball, 1990; Heide,
2002; Vollan et al., 2006); and lastly (4) direct long-distance
seed dispersal by birds, wind and/or ocean currents (Cruden,
1966; Mu~
noz et al., 2004; Nathan et al., 2008).
Six out of the c. 30 bipolar vascular plant species known
belong to the genus Carex L. (Moore & Chater, 1971), a species-rich genus (> 2000 species) found especially in the temperate and cold regions of the Northern Hemisphere
(Reznicek, 1990). Molecular studies focused on bipolar Carex
species (Vollan et al., 2006; Escudero et al., 2010a; Villaverde
et al., 2015) determined low levels of genetic differentiation
between the disjunct populations, suggesting either mountain-hopping or direct long-distance dispersal, yet none of
these studies could determine which hypothesis best
explained the observed distributions of the bipolar species.
Carex maritima Gunn. [sect. Foetidae (Tuckerm. ex L.H. Bailey) K€
uk.] is an arctic–alpine species with a circumboreal distribution including the European Alps and the Himalayas in
the Northern Hemisphere, while in the Southern Hemisphere
it is distributed from Ecuador to Patagonia (Govaerts et al.,
2014; see Fig. 1). It is a wind-pollinated herbaceous hemicryptophyte or rhizome geophyte, which generally colonizes
water-influenced habitats (e.g. lake, river, ocean shores or
snowmelt water areas) and hydromorphic soils (e.g. beaches,
fens, alluviums). Recent morphological and taxonomical
studies of C. maritima (Moore & Chater, 1971; Reznicek,
2002) did not reveal any infraspecific taxa. Although Escudero et al. (2010a) detected some degree of genetic differen-
tiation between Northern and Southern Hemisphere
populations of C. maritima, no North American populations
were included in their analyses.
Although the vicariance hypothesis (Du Rietz, 1940) has
traditionally been considered in explanation of Carex bipolar
distribution (e.g. Villaverde et al., 2015), it can now easily be
rejected for Carex bipolar species as the age of the diversification of the Cyperaceae family is younger than the transtropical highland bridges (82.6 Ma, 95% highest posterior
density, HPD: 75.9–85.6 Ma; Escudero & Hipp, 2013). We
can also discard parallel evolution for C. maritima because
Escudero et al. (2010a) showed that populations from the
Northern Hemisphere and the Southern Hemisphere were
part of the same clade.
The aim of the present study was to explain the bipolar
distribution of C. maritima. Specifically, our aims were: (1)
to clarify the direction of the dispersal (north-to-south or
south-to-north); (2) in the case of genetic structure, to
estimate the timing of dispersal; and (3) to test mountainhopping and direct long-distance dispersal hypotheses, as
well as the relationship of C. maritima with biotic and abiotic factors that could explain the bipolar distribution. In
order to accomplish this task we combined a wide sampling
of the species’ range with data from nuclear and plastid
molecular markers and bioclimatic data. We analysed the
phylogenetic and phylogeographical relationships of C. maritima populations and compared its ecological niche throughout its distribution.
Sampling
We obtained plant material representing the geographical
range of C. maritima (42 populations) as circumscribed by
Egorova (1999). Samples used for the molecular study were
obtained from fresh leaf material collected in the field and
dried in silica gel, and from herbarium specimens (see
Appendix S1 in Supporting Information). Vouchers for new
collections are deposited in CAN, COLO, SI and UPOS
herbaria (abbreviations according to Index Herbariorum;
http://sciweb.nybg.org/science2/IndexHerbariorum.asp). We
emphasized the sampling of the most northern Southern
Hemisphere populations and we were able to obtain material
from northern parts of Argentina. We were not, however,
able to sample other more northerly populations in the
Southern Hemisphere, from Ecuador and Bolivia (Govaerts
et al., 2014). We also included four other species from
Carex sect. Foetidae [10–15 species in total, including C.
maritima; Reznicek, 2002; eMonocot Cyperaceae (http://
cyperaceae.e-monocot.org, accessed 3 December 2014)]: C.
incurviformis Mack. (two populations), C. pseudofoetida K€
uk.
(two populations), C. sajanensis V. I. Krecz. (four populations) and C. vernacula L. H. Bailey (three populations). As
outgroups, we included taxa from the subgenus Vignea
(P. Beauv. ex Lestib. f.) Perterm. (Hendrichs et al., 2004;
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Bipolar disjunction in Carex maritima
Figure 1 Distribution map of the sampled
populations of Carex maritima, C.
incuviformis and C. pseudofoetida. Carex
maritima populations (46; some populations
overlap in the map, see Appendix S1 for
more details) are depicted by black circles,
white diamonds represent C. incurviformis
(two populations) and grey triangles
indicate C. pseudofoetida samples (two
populations). The dashed region denotes the
distribution of C. maritima, obtained from
the World Checklist of Cyperaceae (Govaerts
et al., 2014).
Escudero & Hipp, 2013): C. stenophylla Wahlenb. from section Divisae H. Christ ex K€
uk. (three populations), C. remota
L. from section Remotae (Ascherson) C. B. Clarke (one population), C. canescens L. from section Glareosae G. Don (one
population) and C. paniculata L. from section Heleoglochin
Dumort. (one population; see Fig. 1 and Appendix S1). For
all species, one individual per population was sampled except
for four populations of C. maritima, for which two individuals were included (Yukon, Nunavut, Iceland and Argentina;
see Appendix S1).
PCR amplification and sequencing
Total DNA was extracted using DNeasy Plant Mini Kit (Qiagen, Valencia, CA, USA). Forward and reverse primers were
used for amplifications of the internal transcribed spacer
(ITS) region (ITS-A, ITS-4; White et al., 1990; Blattner,
1999), external transcribed spacer (ETS) region (ETS-1f, 18SR; Starr et al., 2003), 50 trnK intron (50 trnKCarexF, 50 trnKCarexR; Escudero & Luce~
no, 2009) and rps16 intron (rps16–
rps16R; Shaw et al., 2005). Thermal cycling was carried out
in a Perkin Elmer PCR-system 9700 (Foster City, CA) under
the conditions specified by Escudero et al. (2010a) for ITS
and rps16; and Starr et al. (2003) and Escudero & Luce~
no
(2009) for the ETS region and 50 trnK intron, respectively.
Polymerase chain reaction (PCR) products were cleaned and
sequenced following Escudero et al. (2008). Sequences were
edited, automatically aligned with muscle (Edgar, 2004) and
manually adjusted using Geneious 6.1.7 (Biomatters, Auckland, New Zealand).
Phylogenetic and haplotype analyses
We used a total of 44 sequences of ITS (six from GenBank),
43 of ETS (one from GenBank), 48 of 50 trnK (one from
GenBank) and 51 of rps16 (two from GenBank; see Appendix S1). Each locus was analysed independently and in combination using maximum likelihood (ML) and Bayesian
inference (BI). The combined nuclear and plastid aligned
matrix consisted of 197 sequences from 64 individuals and
2699 sites (Appendix S1).
There are two main strategies for inferring phylogenies
from multiple DNA regions: (1) the total evidence approach,
in which phylogeny is reconstructed from as much data as
possible to obtain the dominant signal (Kluge, 1989); (2)
gene-by-gene strategy, in which it is often possible to identify
and explain gene tree incongruences (Rannala & Yang,
2008). In the last few years, coalescent species tree methods
have been used to reconcile population history with incongruent phylogenies derived from different DNA regions (Degnan & Rosenberg, 2009). Because of the absence of
incongruences between DNA regions (results not shown) and
the little genetic variation found in them, we have used the
total evidence strategy in the current study.
Maximum likelihood analyses of the unpartitioned combined matrix were performed using RAxML 7.2.6 (Stamatakis, 2006) with a GTR-GAMMA model of sequence
evolution and node support assessed with 1000 bootstrap
(BS) replicates. Bayesian inference analyses were executed in
MrBayes 3.2 (Ronquist et al., 2012). The most appropriate
nucleotide substitution model for each partition was chosen
using the Akaike information criterion (AIC) in jModelTest
(Posada, 2008). Selected nucleotide substitution models were
GTR+I, HKY and GTR+G for ITS1, 5.8S and ITS2, respectively; HKY+I for ETS; F81 + I for 50 trnK and GTR for rps16
(Appendix S1). The Markov chain Monte Carlo (MCMC)
search was run for five million generations with a tree sampled every 1000 generations and two simultaneous analyses
started from different random trees (Nruns = 2), each with
four Markov chains (Nchains = 4). The first 20% of the trees
were discarded from each run as the burn-in. A Bayesian
majority-rule consensus tree was calculated in MrBayes with
posterior probability (PP) values as a measure for clade support.
We estimated the genealogical relationships among the
two cpDNA haplotypes using the plastid 50 trnK–rps16 matrix
and statistical parsimony as implemented in tcs 1.21 (Clement et al., 2000). Owing to the polyphyly of the section (see
Results), this analysis was only performed for the core Foetidae, which comprises all sampled members of section Foetidae except for C. vernacula. The maximum number of
differences resulting from single substitutions among
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________________________________________________________________
haplotypes was calculated with 95% confidence limits. Two
informative indels in 50 trnK and one in rps16 were coded as
a presence–absence character for analysis. Gaps due to
mononucleotide repeat units (poly-T and poly-A), which are
considered to be highly homoplasic (Kelchner, 2000), were
treated as missing data. We estimated completeness of haplotype (50 trnK–rps16) sampling using a Stirling probability distribution as described by Dixon (2006), which calculates a
posterior probability distribution of the total number of
haplotypes (sampled or not).
Divergence time estimation
Dated phylogenies were estimated for the combined nuclear
and plastid matrix in beast 1.7.5 (Drummond et al., 2012).
Phylogeny was estimated using an uncorrelated lognormal
relaxed clock model. A normal age prior with a mean of
14.82 Ma 2.5 Myr was applied to the root of the tree
based on the previous estimate for the divergence of the subgenus Vignea (Escudero & Hipp, 2013). Analyses were conducted using two independent MCMC runs of 60 million
generations each, assuming the birth–death tree prior with a
mean substitution rate set at 1.0. Run convergence and
burn-in were assessed in Tracer 1.5 (Rambaut & Drummond, 2009). Maximum clade credibility trees were calculated with TreeAnnotator 1.7.2 (Drummond & Rambaut,
2007) using a posterior probability limit of 0.7 and the mean
heights option.
Climatic environment – ecological niche
We obtained bioclimatic data for the localities of our molecular sampling (56 samples of core Foetidae: 47 of C. maritima, two each of C. incurviformis and C. pseudofoetida, and
five of C. sajanensis; ‘reduced data set’ from here on) in
order to study the ecological factors influencing species’
range. We compiled a new data set (‘full data set’) and also
obtained bioclimatic data. This new data set was completed
by adding: (1) three additional populations from Austria,
Italy and Sweden for which we failed to amplify any loci
(Appendix S1); and (2) species occurrence data between
1950 and 2000 downloaded from the Global Biodiversity
Information Facility data portal (http://www.gbif.org/, downloaded 22 December 2014) after pruning for likely incorrect
identification or georeferencing (e.g. occurrences in oceans)
and removing duplicate records from the same locality to
reduce the effects of spatial autocorrelation (847 new presence data from preserved specimens of C. maritima). Finally,
our full second data set included 894 populations in total
(see Appendices S1 and S2). For each sampled population in
our data sets we obtained values for 19 bioclimatic variables
(Appendix S1) as described by Escudero et al. (2013). We
ran principal components analyses (PCA) using the full and
reduced climatic data sets, as Villaverde et al. (2015). The
phylogenetic size-correction was performed in our reduced
data set for non-independence among the observations for
lineages. We represented data associated with the most
important bioclimatic variables retained in the phylogenetic
PCA for C. maritima in boxplots. In order to compare climate regime similarities and differences of the species of core
Foetidae we included the samples of C. incurviformis, C.
pseudofoetida and C. sajanensis in the PCA of the climatic
environment.
Past and present distribution under climatic change
scenarios
Species distribution modelling was performed to reconstruct
the potential ranges of C. maritima under present climatic
conditions and for two historical periods, the Last Interglacial (LIG; 120–140 ka) and the Last Glacial Maximum
(LGM; 21 ka), with Maxent 3.3.3k (Phillips et al., 2006).
Neither C. incurviformis nor C. pseudofoetida was included in
the model with C. maritima because their different ecological
requirements may confound C. maritima distribution modelling. Carex incurviformis is distributed only in North America
and its ecology differs from that of C. maritima in this
region (Reznicek, 2002). Moreover, the partial molecular differentiation (see Results) and their distinctive morphology
(Reznicek, 2002) also support this decision. Settings were
established following Blanco-Pastor et al. (2013). We performed a correlation analysis with the variance inflation factor (VIF) using the ‘vif’ function in the usdm package in R
(R Core Team, 2014) and a correlation threshold of 0.7.
Only three variables were uncorrelated and consequently
included in the analyses: BIO1 (annual mean temperature),
BIO6 (minimum temperature of the warmest month) and
BIO12 (annual precipitation). Replicate runs (500) were performed by using the bootstrap run type. All 19 of these variables have a grid size of 30 arc seconds for present and LGM
conditions but 2.5 arc minutes for LIG scenarios. These grid
size differences required us to omit 82 data points from the
C. maritima full data set from the model, leaving a total of
812 points. Analyses were performed for all populations of
C. maritima and separately for Northern and Southern
Hemisphere populations of C. maritima. We partitioned all
the locality data into training and testing data sets (75% vs.
25%, respectively) in order to build niche models and to
evaluate the quality of the model. Nonetheless, projections to
past scenarios have to be interpreted with caution due to the
absence of fossils to validate the model and the low number
of existing localities in the Southern Hemisphere. Similar
results were obtained when modelling the climatic niche of
C. maritima using the reduced data set (results not shown).
RESULTS
BI and ML analyses revealed a lack of monophyly both for
Carex sect. Foetidae and C. maritima. Strong support (100%
BS/1 PP; Fig. 2) was obtained for the core Foetidae, including
4
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C. canescens ROM
0.96
C. paniculata GRC
C. remota YUG
C. vernacula YUK
1
C. vernacula ORE
100
C. vernacula CAL
C. stenophylla RU
C. stenophylla TAJ
86
C. stenophylla TCS
C. sajanensis CHI_1
1
C. sajanensis CHI_2
92
C. sajanensis CHI_3
C. sajanensis NEP_1
0.98
77 C. sajanensis EHM_1
63
C. pseudofoetida TAJ_1
C. pseudofoetida TAJ_2
C. maritima ASK_1
C. maritima YUK_1a
C. maritima YUK_1b
C. maritima YUK_2
C. maritima YUK_3
C. maritima NWT_1
C. maritima NWT_2
C. maritima NWT_3
C. maritima NWT_4
C. maritima NWT_5
C. maritima SAS_1
C. maritima NUN_1a
C. maritima NUN_1b
C. maritima NUN_2
C. maritima MAN_1
C. maritima MAN_2
C. maritima NFL_1
C. maritima NFL_2
C. maritima GNL_1
0.99
C. maritima GNL_2
97
C. maritima GNL_3
C. maritima GNL_4
C. maritima GNL_5
C. maritima ICE_1
C. maritima ICE_2a
C. maritima ICE_3
C. maritima ICE_4
C. maritima ICE_5
C. maritima WSB_1
C. maritima SWI_1
C. maritima SWI_2
C. maritima NOR_1
C. maritima NOR_2
C. maritima NOR_3
C. maritima NOR_4
C. maritima RUE_1
C. maritima RUW_1
C. maritima RUC_1
C. maritima ICE_2b
C. maritima RUW_2
0.90
C. incurviformis COL_1
75
C. incurviformis COL_2
C. maritima CLN_1
65
C. maritima CLN_2
0.99 C. maritima CLS_1
93 C. martitima AGS_1a
C. maritima AGS_1b
C. maritima AGS_3
0.0030
1
100
1
100
0.98
1
100
Figure 2 Majority rule (50%) consensus
tree derived from the Bayesian analysis of
Carex maritima and the related species in
section Foetidae inferred from the combined
nuclear (ITS and ETS) and chloroplast
(50 trnK and rps16) matrix; C. remota, C.
canescens and C. paniculata were used as
outgroups. Numbers above and below the
branches represent the Bayesian posterior
probability (> 0.9 PP) and bootstrap
(> 60% BS) values of the maximum
likelihood analysis, respectively. A grey
rectangle highlights the C. maritima samples
of the Southern Hemisphere. Vertical bars
indicate supraspecific taxa from the same
taxonomic group. Abbreviations after the
names correspond to the geographical
regions of the world (Brummitt, 2001) and
to the population number. The scale bar
indicates substitutions per site.
all sampled section Foetidae species except C. vernacula. Nevertheless, several species from section Foetidae, not sampled in
the current study, could potentially also be part of the core
Foetidae. A strongly supported (100% BS/1 PP) monophyletic
C. stenophylla (sect. Divisae) was sister to the core Foetidae
(100% BS/1 PP). Within the latter, C. sajanensis was retrieved
as monophyletic (92% BS/1 PP) and sister to a strongly supported clade (97% BS/0.99 PP), including C. pseudofoetida, C.
incurviformis and C. maritima. Two different subclades were
detected: (1) a strongly supported lineage comprising all C.
maritima samples from South America (93% BS/0.99 PP); and
(2) C. incurviformis (75% BS/0.90 PP).
Haplotype network
The cpDNA haplotype network obtained for the core Foetidae (Fig. 3) revealed seven haplotypes and five missing haplotypes. A probability of 81% that all haplotypes have been
sampled is given by Dixon’s (2006) method. Five haplotypes
Sect. Remotae
Sect. Foetidae
Sect. Divisae
Sect.
Foetidae
(Core
Foetidae)
were found within the sampled C. maritima populations.
Two of them were widely distributed but geographically
overlapping in part: one of them was shared by 10 samples
of C. maritima from Russia, Canada and Greenland (H1),
and the other by 26 samples of C. maritima from northern
North America and Europe (H2). In addition, H1 was also
shared with one population of C. incurviformis and two of C.
pseudofoetida. Interestingly, all C. maritima samples from
South America (5) shared the same exclusive haplotype
(H3). We found unique haplotypes for C. maritima samples
from Norway (H4; one sample) and for samples from eastern
Russia (H5; two samples). Finally, C. sajanensis displayed
two haplotypes (H5–H6) separated by four mutational steps
from C. maritima haplotypes.
Estimation of divergence times
The dating analyses produced a congruent topology with
respect to BI and ML analyses presented above (Fig. 4,
5
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________________________________________________________________
H4
C. marima
(1)
Norway
H1
C. marima (5)
South America
C. pseudofoeda (2)
India
C. incurviformis (1)
Colorado
C. marima (10)
North and Central Russia, Northwest
Territories & Greenland
H3
C. marima (2)
Eastern Russia
H5
H7
H2
C. sajanensis
(1)
C. marima (26)
Alaska, Canada &
Europe
C. sajanensis
(4)
H6
Table 1). The divergence time of the clade comprising core
Foetidae was 2.85 Ma (95% HPD: 0.93–5.01 Ma), which falls
in the late Pliocene to middle Pleistocene. The diversification
of the clade consisting of C. maritima, C. incurviformis and
C. pseudofoetida could have occurred during the middle–late
Pliocene to early–middle Pleistocene (1.61 Ma; 95% HPD:
0.61–2.96 Ma). Finally, the divergence of the clade consisting
of C. maritima samples from South America could have
begun during the middle–late Pleistocene (0.23 Ma; 95%
HPD: 0.03–0.51 Ma). While the age of the core Foetidae
could experience some variation after including some of the
missing species from section Foetidae, the estimated age for
C. maritima clade (the clade including all C. maritima samples) is reliable and should experience little or no variation
after including unsampled species even if one or several of
those fell nested within the C. maritima clade.
The phylogenetic PCA of the reduced climatic data set
showed that PC1 explained 50.35% of the variance whereas
PC2 explained 22.29% (see Fig. 5). The variables with the
highest loadings in PC1 were temperature seasonality
(BIO4), temperature range (BIO7) and minimum temperature of the coldest month (BIO6; see Appendix S1). Maximum and minimum values for each variable are shown by
groups (Table 2). Similar results were obtained when the
analysis is not corrected with the phylogeny (results not
shown). Northern and Southern Hemisphere samples of C.
maritima were clearly separated into two groups, probably
revealing some degree of ecological differentiation. The boxplots of the variables with the highest loadings revealed that
C. maritima populations from the Northern Hemisphere
occur in localities with greater temperature oscillations
through the year and a wider range of minimum tempera-
Figure 3 Haplotype network of
concatenated cpDNA sequences of Carex
maritima, C. pseudofoetida, C. incurviformis
and C. sajanensis. Circles represent the seven
haplotypes found (H1–H7), lines represent
single mutational steps, and small black
circles represent missing haplotypes.
Numbers of samples per haplotype are
indicated in parentheses.
tures during the coldest month than populations from the
Southern Hemisphere (Table 2, Fig. 6). The PCA of the full
climatic data set showed that PC1 explained 65.9% of the
variance whereas PC2 and PC3 explained 14.7% and 9.4%,
respectively (Appendix S1). A clear separation between
Northern and Southern Hemisphere samples of C. maritima
is also obtained when plotting PC1 and PC3 or PC2 and
PC3 (Appendix S2).
Past and present distribution under climatic change
scenarios
Current conditions
Our results show that the modelled ecological niche of C.
maritima, including Northern and Southern Hemisphere
samples, predicts suitable areas in both hemispheres. Values
for AUC were all above 0.9, which indicate a good fit of the
models. The average AUC values for each group and the
most important environmental variables detected in each
analysis are reported in Appendix S1. Scatter diagrams of the
variables used in Maxent analyses also depicted clear differences between Northern and Southern Hemisphere populations of C. maritima (Appendix S2). The modelled ecological
niche of C. maritima including only the Northern Hemisphere populations predicts suitable habitats also in the
Southern Hemisphere (Appendix S2). By contrast, the modelled ecological niche of C. maritima including only Southern
Hemisphere populations does not predict suitable habitats in
the Northern Hemisphere.
Past conditions
The projection of suitable environments to past conditions
in all lineages revealed a wider distribution range in LGM
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________________________________________________________________
C. paniculata
C. canescens
C. remota
0.81
8.05
1
C. vernacula
1.80
Figure 4 Maximum credibility clade
phylogeny of the Bayesian divergence time
analysis considering Carex maritima and
other related species in section Foetidae
carried out on a combined matrix of
nuclear (ITS and ETS) and plastid (50 trnK
and rps16) sequences. Carex remota, C.
canescens, C. paniculata and C. stenophylla
were used as outgroups. Node bars
represent the 95% highest posterior density
intervals of the divergence time estimates
linked to nodes with posterior probabilities
above 0.75 (values above branches) with
mean ages inferred for clades in million
years (below branches).
1
C. stenophylla
0.54
0.83
1
9.04
0.63
C. sajanensis
1
C. incurviformis
2.85
C. maritima
Southern Hemisphere
1
0.87
1.61
0.09
0.76
0.23
MIOCENE
15.0
12.5
scenarios than at the present time and in the LIG scenarios
(Appendix S2). Although suitable environments are predicted
in the Southern Hemisphere for C. maritima populations
from the Northern Hemisphere, when Southern Hemisphere
populations are analysed alone these areas are considerably
reduced in LGM scenarios and absent in the LIG scenario
(Appendix S2). These results have to be interpreted with
caution due to the absence of fossils to validate the model.
DISCUSSION
Pleistocene north-to-south long-distance dispersal
Haplotypes H1 and H2 are widely distributed throughout
the Northern Hemisphere (North America, Europe and Asia)
and comprise the highest number of haplotype connections
(Fig. 3), implying under the coalescent theory that they
amount to the ancestral haplotypes (Posada & Crandall,
2001). South American C. maritima populations are monophyletic and nested with a strong statistical support within
the Northern Hemisphere accessions (Figs 2 & 3). In addition, the haploid genotype diversity pattern consisting of
four different haplotypes found in relation to the C. maritima populations of the Northern Hemisphere (H1, H2, H4,
H5), whilst a single haplotype was detected for the southern
populations (H3; Fig. 3), suggests a migration event from
the Northern Hemisphere to the Southern Hemisphere as
the most plausible explanation. This evidence, together with
the fact that 11 out of the 15 species in Carex sect. Foetidae
(eMonocot Cyperaceae; http://cyperaceae.e-monocot.org,
accessed 3 December 2014) are also distributed in the Northern Hemisphere, supports the hypothesis that C. maritima
originated in the Northern Hemisphere, according to our
10.0
PLIOCENE
7.5
5.0
PLEISTOCENE
2.5
C. maritima
Northern Hemisphere +
C. pseudofoetida
0.0 Ma
analysis during the middle–late Pliocene and early–middle
Pleistocene (Table 1, Fig. 4).
The other five bipolar Carex species manifest most of their
distribution in the Northern Hemisphere (Govaerts et al.,
2014). At least C. arctogena, C. macloviana and C. maritima
display a higher morphological variation in North America
than in South America (Moore & Chater, 1971), which could
also support the idea that the bipolar species generally
migrated southwards (Raven, 1963; Moore & Chater, 1971).
Studies of other bipolar taxa have also suggested a north-tosouth dispersal as the most plausible migration direction
(e.g. Moore & Chater, 1971; Vollan et al., 2006; Popp et al.,
2011). The C. maritima biogeographical history elucidated in
our study appears to be congruent with the predominantly
inferred pattern, and it seems that Northern Hemisphere to
South Hemisphere dispersal is predominant in plant dispersals (reviewed in Wen & Ickert-Bond, 2009). However, other
plant genera present the opposite direction of dispersal. For
example, the centre of origin of the genus Larrea (Zygophyllaceae) is located in South America and this genus was
inferred to have migrated to North America during the late
Neogene by long-distance dispersal, using way stations in
Peru and Bolivia and probably mediated by birds (Lia et al.,
2001). Likewise, the Rubiaceae family was inferred to have
migrated from South to North America during the late Palaeocene–early Eocene using land bridges (Antonelli et al.,
2009), as was Hoffmannseggia glauca (Fabaceae) via birds
during the late Miocene or later (Simpson et al., 2005).
Mountain-hopping or direct long-distance dispersal?
The subsequent question arises of how the inferred northto-south middle–late Pleistocene long-distance dispersal
7
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________________________________________________________________
Table 1 Divergence times of clades in Carex sect. Foetidae and outgroups presented as the posterior probability followed by the mean
time to the most recent common ancestor in million years and the 95% highest posterior density (HPD) interval obtained from the
divergence time analysis of the combined nuclear (ITS and ETS) and plastid (50 trnK intron and rps16) regions. Carex maritima
populations of the Northern Hemisphere (NH) and Southern Hemisphere (SH), respectively, are indicated.
Clade
6
C. remota + C. vernacula
C. vernacula
C. stenophylla + Core Foetidae
(C. sajanensis + C. incurviformis + C. maritima + C. pseudofoetida)
C. stenophylla
Core Foetidae
(C. sajanensis + C. incurviformis + C. maritima + C. pseudofoetida)
C. sajanensis
C. incurviformis + C. maritima NH + C. maritima SH + C. pseudofoetida
C. incurviformis
C. maritima SH
-2
0
PC2
2
4
C. maritima Northern Hemisphere
C. maritima Southern Hemisphere
C. incurviformis
C. pseudofoetida
C. sajanensis
-2
0
PC1
2
4
6
Figure 5 Scatter plot of the first two components explaining up
to 72.64% of the observed variance, derived from the principal
components analysis as corrected by phylogeny and depicting
the position in a climate-niche space of Northern and Southern
Hemisphere samples of Carex maritima (black and white circles,
respectively), C. pseudofoetida (triangles), C. incurviformis
(diamonds) and C. sajanensis (crosses).
Table 2 Maximum and minimum values of the variables with
the highest loadings for principal component 1 for the Northern
Hemisphere populations (NH) and Southern Hemisphere
populations (SH) of Carex maritima. Bioclimatic variables
correspond to temperature seasonality (BIO4, SD), the
temperature range (BIO7 = BIO6 – BIO5, C), the minimum
temperature during the coldest month (BIO6, C) and the
maximum temperature during the coldest month (BIO5).
C. maritima HN
C. maritima SH
min.
max.
min.
max.
BIO4
BIO7
BIO6
35.33
177.28
24
32.78
14.2
58
15.4
25.4
44.9
3.5
9.6
0.6
could have occurred. According to our data, the current C.
maritima distribution can be explained by either of two
hypotheses: (1) Northern Hemisphere populations could
Posterior
probability
Mean (Ma)
95% HPD
interval (Ma)
0.81
1
0.83
8.0522
1.8038
9.0452
2.7638
0.2665
3.6505
13.1959
3.7436
14.2733
1
1
0.5365
2.8456
0.0291
0.9327
1.2872
5.0077
1
1
0.87
0.76
0.6275
1.6110
0.0884
0.2266
0.0440
0.6062
0
0.0286
1.4295
2.9603
0.3099
0.5092
have migrated stepwise by mountain-hopping all the way
through the Andes, with a posterior extinction of most of
the intermediate populations; or (2) Northern Hemisphere
populations could have been disseminated by a direct longdistance dispersal to South America, where they subsequently
colonized northwards or southwards until reaching their current distribution (Fig. 1).
The mountain-hopping hypothesis (Ball, 1990) proposes a
long-distance, stepwise migration of arctic and temperate
taxa using mountains peaks as stepping-stones to cross the
tropics. A route connecting North and South America
through the American cordillera has been in place since the
late Miocene epoch (Smith, 1986). Then, a gradual uplift of
the cordillera during the late Pliocene created the high
mountainous environment with a much colder climate later
on during the Pleistocene compared to that occurring today
at the same latitudes and elevations (van der Hammen,
1974). According to our results, from the Last Interglacial
(LIG; c. 120 ka) to the present time similar ecological niches
could have existed that were suitable for C. maritima in
South America (although these results should to be taken
with caution, see Results; Appendix S2). Therefore, we cannot rule out the mountain-hopping migration since the early
Pleistocene, with a subsequent extinction of most of the
northern South American intermediate populations. In addition, the sister relationship between C. maritima of the
Southern Hemisphere and C. incurviformis (present in western North America yet reaching southern latitudes) could
also support this hypothesis (nonetheless see lack of clade
support; Fig. 2). As already demonstrated by Heide (2002),
changes in flowering requirements would not have been necessary for the other bipolar Carex species to migrate across
of the tropical belt, still making mountain-hopping a plausible premise.
Alternatively, C. maritima could have reached the Southern Cone by a direct long-distance dispersal event, with a
subsequent genetic differentiation in the South American
continent and a northward or southward colonization along
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________________________________________________________________
(a)
BIO7 (°C)
BIO4 (SD)
(c)
NH
SH
NH
SH
NH
SH
BIO6(°C x 10)
Figure 6 Carex maritima boxplots
comparing the three bioclimatic variables
with the highest loadings regarding the first
component of the bioclimatic principal
components analysis (PCA) taking into
account the Northern and Southern
Hemisphere samples (NH and SH). (a)
Temperature seasonality (BIO4), (b) annual
temperature range (BIO7, i.e. minimum
temperature during the warmest month
minus maximum temperature during the
coldest month, BIO6 – BIO5), and (c)
minimum temperature during the warmest
month (BIO6). Each box represents the
interquartile range which contains 50% of
the values and the median (horizontal line
across the box); the whiskers are the lines
that extend from the box to the highest and
lowest values, excluding outliers (o).
(b)
the Andes, as suggested for the bipolar C. arctogena (Villaverde et al., 2015). The molecular data in this study, without
genetic structure between northern and southern populations
within each hemisphere, but strong genetic structure between
both hemispheres, could support the direct long-distance dispersal hypothesis and subsequent genetic differentiation.
Nevertheless, more information is still needed to confirm
either the mountain-hopping or the direct long-distance dispersal hypothesis.
Breeding system, dispersal syndrome and the bipolar
disjunction
Some self-fertilization is a reproductive characteristic displayed by many species with disjunct populations in the temperate zones (Carlquist, 1983). This attribute could favour
local survival and establishment after long-distance dispersal
events, given that a single propagule of self-compatible
individuals could in principle be sufficient to start a sexually
reproducing colony (Baker, 1955). In congruence, Carex species are predominantly monoecious and in general highly
self-pollinated (Friedman & Barrett, 2009), which has been
inferred from studies based on hand pollinations, isozyme
work (e.g. Ohkawa et al., 2000; Friedman & Barrett, 2009)
and microsatellite data (e.g. Escudero et al., 2010b, 2013).
This characteristic could explain, at least in part, the often
successful colonization of Carex species after a long-distance
dispersal event (Moore & Chater, 1971; Ball, 1990; Escudero
et al., 2009).
Carex maritima inhabits water-influenced areas (e.g. lakes,
river, ocean shores or snowmelt water areas) or else populates hydromorphic soils (e.g. beaches, fens, alluviums), and
seed dispersal of C. maritima could be mediated by birds,
wind or ocean currents. Except for their small size, fruits of
C. maritima lack the evident morphological features for a
long-distance dispersal, unlike other bipolar species (C.
microglochin; Savile, 1972). On the one hand, species with
small seeds and from water-influenced habitats are often
highly dispersible taxa (McGlone et al., 2001). On the other
hand, the long-distance dispersal of seeds might not necessarily be driven by standard dispersal vectors inferred from
plant morphology (as described by Higgins et al., 2003) or
by regular events; in fact, great long-distance dispersals
(> 100 km) are usually associated with stochastic events
(unusual behaviour of regular events or a combination of
vectors; Nathan et al., 2008). Thus, arctic species have been
demonstrated to migrate enormous distances despite the lack
of specific syndromes (Abbott & Brochmann, 2003).
Considering the extreme dispersal distance, together with
the shape and structure of the C. maritima propagules, we
consider that its dispersal was more likely to have been mediated by migratory animals than by wind or ocean currents,
which seem insufficient for such an enormous task. Some
birds which migrate from North America to temperate zones
of South America have already been pointed out as the most
likely dispersal agents of the several disjunct plant groups
(Cruden, 1966, and references therein; Popp et al., 2011).
Moreover, arrivals of Carex species to newly formed islands
have predominantly been reported to happen when seeds
were embedded in mud attached to birds’ feet or else when
eaten and carried inside by birds (Carlquist, 1967). Therefore, we consider it plausible that C. maritima could have
acquired its bipolar distribution by means of bird-mediated
dispersal.
CONCLUSIONS
This study contributes to the general knowledge regarding
biogeographical patterns of bipolar taxa whilst presenting a
combination of multiple approaches (phylogenetic and
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________________________________________________________________
phylogeographical analyses, together with divergence time
estimates and bioclimatic data) to test the traditional
hypotheses used to understand the distribution of bipolar
species. Carex maritima populations of the Southern Hemisphere were retrieved as a monophyletic lineage within a
paraphyletic C. maritima. The phylogeographical structure
found within C. maritima suggests that the bipolar disjunction could be explained by a middle–late Pleistocene longdistance dispersal derived from the Northern Hemisphere.
Our study highlights the importance of long-distance dispersal mechanisms to explain this fascinating plant distribution pattern.
ACKNOWLEDGEMENTS
The authors thank all staff from herbaria CAN, COLO, E,
M, MSB, SI, UPOS and WIN for granting us access to their
collections and for providing plant material; E. Maguilla
(Universidad Pablo de Olavide, UPO) and Francisco
Rodrıguez-Sanchez (Estaci
on Biol
ogica de Do~
nana, EBDCSIC) for their help with the Maxent analyses and map
editing; L.P. Bruederle (University of Colorado, Denver) and
P. Vargas (Real Jardın Botanico de Madrid) for assistance in
plant collections; and M. Mıguez and F.J. Fernandez (UPOS)
for technical support. We also thank the University of
Helsinki master’s student A. Ginter for translations of
Russian data labels. This research was supported by the
Spanish Ministry of Science and Technology through the
project CGL2012-38744. Further support was also provided
by the Regional Ministry of Economy, Innovation, Science
and Employment through project RNM-2763.
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reconstructions of the Cretaceous and Cenozoic ocean
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Scotland, R.W. (2011) What is parallelism? Evolution and
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Miller, J., Siripun, K.C., Winder, C.T., Schilling, E.E. &
Small, R.L. (2005) The tortoise and the hare II: relative
utility of 21 noncoding chloroplast DNA sequences for
phylogenetic analysis. American Journal of Botany, 92,
142–166.
Simpson, B.B., Tate, J.A. & Weeks, A. (2005) The biogeography of Hoffmannseggia (Leguminosae, Caesalpinioideae,
Caesalpinieae): a tale of many travels. Journal of Biogeography, 32, 15–27.
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the 5 and 3 ends of intergenic spacer (IGS) of rDNA in
the Cyperaceae: new sequences for lower-level phylogenies
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Villaverde, T., Escudero, M., Martın-Bravo, S., Bruederle,
P.L., Luce~
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Additional Supporting Information may be found in the
online version of this article:
Appendix S1 Supplementary tables. Studied material of Carex maritima, related species and outgroups (Table S1);
molecular characteristics of the amplified regions (Table S2);
results from the principal components analysis of 19 bioclimatic variables from the WorldClim database, uncorrected
(on full and reduced data sets) and corrected for phylogeny
(Tables S3–S5); description of bioclimatic variables (Table
S6); and AUC values from Maxent analyses (Table S7).
Appendix S2 Supplementary figures. Distribution map of
Carex maritima (Fig. S1); ecological niche models of C.
maritima groups fitted to current climatic conditions from
Maxent analyses (Fig. S2), and projections of the models to
Last Glacial Maximum (18–21 ka; MIROC and CCSM models) and Last Interglacial Period (c. 120–140 ka) (Fig. S3);
scatter plots of the uncorrelated bioclimatic variables used in
Maxent analyses (Fig. S4); and scatter plot of the three first
components from the principal components analysis of the
full data set (Fig. S5).
BIOSKETCH
Tamara Villaverde is a PhD student at Pablo de Olavide
University, Seville (Spain). Her research is focused on the
evolution and phylogeography of angiosperms, with special
interest in the systematics and biogeography of the genus
Carex (Cyperaceae).
Author contributions: M.E. and M.L. conceived the idea;
T.V., S.M-B and M.L. collected the plant material; T.V., M.E.
and S.M-B, carried out the lab work and analysed the data;
T.V., M.E. and S.M-B led the writing and drafted the manuscript, although all authors contributed to its preparation.
Editor: Liliana Katinas
12
200
201
bioclimatic variables (Table S6); and AUC values from MAXENT analyses (Table S7).
WorldClim database, uncorrected (on full and reduced data sets) and corrected for phylogeny (Tables S3–S5); description of
characteristics of the amplified regions (Table S2); results from the principal components analysis of 19 bioclimatic variables from the
Appendix S1 Supplementary tables. Studied material of Carex maritima, related species and outgroups (Table S1); molecular
Tamara Villaverde, Marcial Escudero, Modesto Luceño and Santiago Martín-Bravo
Long-distance dispersal during the middle–late Pleistocene explains the bipolar disjunction of Carex maritima (Cyperaceae)
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
GRC
ROM
YUG
CAL
YUK
ORE
C. paniculata
subsp. paniculata
C. canescens
C. remota
C. vernacula
C. vernacula
C. vernacula
-
61.28698
38.44445
19.09025
45.60321
21.22555
Pop. code Latitude
Species
-
-138.52892
-119.32149
43.15227
24.61613
39.78673
Longitude
world (Brummitt, 2001) and population number.
202
USA, California, Wheeler Peak. Bell 1459.
(WS s.n.)
Canada, Yukon. Kluane Lake. L. P.
Bruederle 08142010_01c. 14/VIII/2010.
(COLO s.n.)
USA, Oregon. Mason 9130. (POM s.n.)
Greece, Epiro, Ioannina, Kambos Despoti.
M. Luceño 0808ML, 23/VI/2008.
(UPOS3419)
Romania, Carpathians, Bâle Lake. M.
Pusças s.n., 20/07/2013. (Personal
collection)
Montenegro, High Dinarics, Durmitor
National Park. P. Jiménez-Mejías
198PJM10, 17/VII/2010. (UPOS4006)
Label information
/AF285022/-/-
-/ KR827099 / KR827144 /-
-/EU001077/-/-
KR827053/ KR827096 /
KR827141 / KR827192
KR827051/ KR827094 /
KR827139 / KR827190
GenBank accession
ETS/ITS/rps16/trnK
KR827052/ KR827095 /
KR827140 / KR827191
clade and GenBank accessions for markers used for molecular studies. Population codes correspond to geographical regions of the
stenophylla, C. canescens, C. remota and C. paniculata, including population code, coordinates, voucher information, corresponding
Table S1 List of material studied of Carex maritima, C. incurviformis, C. pseudofoetida, C. sajanensis, C. vernacula and the outgroups C.
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
TCS
TAJ
RU
CHI_1
CHI_2
CHI_3
EHM_1
NEP_1
TAJ_1
TAJ_2
C. stenophylla
C. stenophylla
C. stenophylla
C. sajanensis
C. sajanensis
C. sajanensis
C. sajanensis
C. sajanensis
C. pseudofoetida
C. pseudofoetida
38.61667
38.48333
27.90611
27.93333
30.30000
33.55000
30.30000
-
38.68333
40.42275
72.86667
74.31667
86.70556
88.63333
90.60000
91.35000
90.60000
-
73.71667
44.23447
203
Tajikistan, Gorno-Badakhshan, East Pamir.
B. Dickoré 17842, 09/IX/2002.
(MSB162332)
India, Sikkim, Chuu Valey. Edinburgh
Expedition to Northern Sikkim (1996) 364,
20/VII/1996. (E00047590)
Nepal, Sagarmatha, Machhermo Kola. First
Darwin Nepal Fieldwork Training
Expedition 171. 15/V/2004. (E00229251)
Tajikistan, Gorno-Badakhshan, Murgab. B.
Dickoré 18037, 12/IX/2009. (MSB162329)
China, Qinghai, Tibet. B. Dickoré 4409,
24/VIII/1989. (MSB140876)
China, Xizang Zizhiqu, Dangxiong Xian. B.
Dickoré 4010, 14/VIII/1989. (MSB142360)
China, Xizang Zizhiqu, Dangxiong Xian. B.
Dickoré 3765, 11/VIII/1989. (MSB140868)
Tajikistan, Gorno-Badakhshan, East Pamir.
B. Dickoré 18239, 16/IX/2002.
(MSB162331)
Russia. (MO04981469)
Armenia, Aragatsotn Province, Mt. Aragats.
G. Fayuush 07-1385, 23/VI/2007. (NY s.n.)
-/-/ KR827150 / KR827199
-/ KR827102 / KR827151 /
KR827200
KR827057/ KR827101 /
KR827149 / KR827198
KR827056/ KR827100 /
KR827148 / KR827197
KR827055/-/ KR827147 /-
-/-/ KR827146 / KR827196
-/-/ KR827145 / KR827195
EU001224/EU001070/-/-
-/ KR827097 / KR827142 /
KR827193
KR827054/ KR827098 /
KR827143 / KR827194
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
COL_1
COL_2
AGS_1a
AGS_1b
AGS_2
CLN_1
CLN_2
CLS_1
ASK_1
GNL_1
C. incurviformis
C. incurviformis
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
65.45000
68.19472
-52.76021
-20.98333
-28.61667
-54.05803
-53.34667
-53.34666
39.19275
38.86297
-52.55000
-152.74750
-69.02174
-68.55000
-69.86667
-67.39000
-68.27930
-68.27933
-105.45410
-105.37929
204
Greenland, Kangerdluarssuk, Qivaqe. S.
Holt 785, 15/VIII/1977. (CAN488203)
Chile, Iquique, Pica. S. Teillier 3258,
24/I/1994. (MIN934751)
Chile, Región Magallanes-Antártica, Tierra
del Fuego. M. Luceño 18ML06, 6/I/2006.
(UPOS1830)
USA, Alaska, Chandler Lake. B. A. Benett
02-393, 23/VII/2002. (CAN589262)
Chile, Atacama, El Tránsito. S. Teillier 4953,
15/II/2002. (MIN934748)
USA, Colorado, Park County, Pike National
Forest, Horseshoe Cirque area. Tallent 517.
(MICH s.n.)
Argentina, Tierra del Fuego, Río Grande. S.
Martín-Bravo 42SMB10, 15/I/2010.
(UPOS4277)
Argentina, Tierra del Fuego, Río Grande. S.
Martín-Bravo 42SMB10, 15/I/2010.
(UPOS4274)
Argentina, Tierra del Fuego, Río Grande. J.
Starr P9-1 10013. 12/I/2010 (UPOS3930)
USA, Colorado, Park County. D. Randolph
17402, 23/VII/1984. (CAN499701)
KR827062/ KR827107 /-/
KR827205
-/ KR827113 / KR827160 /
KR827212
KR827061/ KR827106 /-/
KR827204
KR827066/ KR827112 /
KR827158 / KR827210
KR827059/ KR827104 /
KR827153 / KR827202
KR827077/ KR827121 /
KR827171 / KR827221
KR827076/ KR827120 /
KR827170 / KR827220
KR827073/-/ KR827167 /
KR827218
-/DQ115186/-/-
KR827058/ KR827103 /
KR827152 / KR827201
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
GNL_2
GNL_3
GNL_4
GNL_5
ICE_1
ICE_2a
ICE_2b
ICE_3
ICE_4
ICE_5
NFL_1
NFL_2
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritime
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
47.61587
47.38583
64.39412
63.55043
65.81401
65.01748
65.01748
64.07082
61.16096
61.00098
72.86333
73.20404
-58.86786
-54.69931
-16.78246
-19.34967
-16.37628
-19.21685
-19.21685
-16.97465
-45.41469
-46.44850
-25.13333
-24.49918
205
Iceland, Vatnajökull. M. Luceño 5206ML,
8/VIII/2006. (UPOS1963)
Canada, Newfoundland and Labrador,
Burnt Island. B. S. Hay 87329, 25/VII/1987.
(CAN545627)
Canada, Newfoundland and Labrador,
Pointe Riche Peninsula. A. Bouchard 91022,
30/VII/1991. (CAN564151)
Greenland, Narsarsuaq, Kieqtotsermiat
glacier. M. Luceño 9307ML, 16/VIII/2007.
(UPOS4512)
Iceland, Skaftafell N.P. M. Guzmán s.n.,
15/Vlll/2005. (UPOS706)
Iceland, My vatnn. G. Kaule s.n.,
18/VIII/1970. (M0177749)
Iceland, My vatnn. G. Kaule s.n.,
9/VIII/1970. (M0177749)
Iceland, Dettifoss. M. Guzmán s.n.,
22/VIII/2005. (UPOS00707)
Iceland, Vik, Drangshliðardalur. M. Luceño
4706ML, 7/VIII/2006. (UPOS1957)
Greenland, Ymer Island, Botanikerbugten.
T. Sørensen 3087, 17/VIII/1932.
(CAN17509)
Greenland, Ella Island, Cape Oswald. T.
Sørensen 316, 24/VII/1932. (CAN17503)
Greenland, Qaleragdlit fjord. M. Luceño
4707ML, 5/VIII/2007. (UPOS4484)
KR827080/ KR827125 /
KR827175 /-
KR827079/ KR827123 /
KR827173 / KR827223
-/-/ KR827188 /-
KR827090/ KR827134 /
KR827184 / KR827233
KR827093/ KR827138 /
KR827187 / KR827236
KR827084/-/ KR827179 /
KR827227
-/-/KR869806/-
-/EU541874/-/-
KR827086/ KR827130 /
KR827181 / KR827229
KR827074/ KR827119 /
KR827168 / KR827219
KR827069/-/ KR827162 / -
KR827067/-/ KR827159 /
KR827211
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
MAN_1
MAN_2
NOR_1
NOR_2
NOR_3
NOR_4
NUN_1a
NUN_1b
NUN_2
NWT_1
NWT_2
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
64.63998
79.89869
64.31868
63.73333
63.73333
78.21307
71.02708
68.19203
70.23601
57.84694
58.39004
-84.11801
-90.97104
-96.01683
-68.45000
-68.45000
15.66346
-8.39625
13.70330
24.94370
-92.76806
-94.36161
206
Canada, Nunavut, Baker Lake. S. A. Edlund
350, 31/VII/1983. (CAN495360)
Canada, Northwest Territories, Axel
Heiberg Island. A. E. Porsild 18643,
1/VIII/1953. (CAN223325)
Canada, Northwest Territories,
Southampton Island. D. K. Brown s.n.,
20/VII/1952. (CAN258613)
Canada, Nunavut, Baffin Island. S. G. Aiken
86-346, 16/VIII/1986. (CAN518226)
Norway, Longyearbyen, Spitzbergen. F.
Hörl s.n., 14/VIII/1961. (M0177748)
Canada, Nunavut, Baffin Island. S. G. Aiken
86-431, 19/VIII/1986. (CAN518311)
Norway, Lofoten Islands. M. Escudero
44ME09. 27/VII/2009. (UPOS s.n.)
Norway, Havhestberget, Jan Mayen Island.
J. Lid s.n., 10/VIII/1930. (CAN281858)
Canada, Manitoba, Wapusk National Park.
E. Punter (03-711), 21/VII/2003.
(CAN591811)
Norway, Lapland, Stabbursnes. M. Luceño
7305ML, 8/VIII/2005. (UPOS00370)
Canada, Manitoba, Churchill. H.
Doppelbaur 134, 29/VII/1965. (M0177754)
KR827063/ KR827109 /
KR827156 / KR827207
KR827091/ KR827135 /-/
KR827234
-/ KR827108 / KR827155 /
KR827206
KR827085/ KR827129 /
KR827180 / KR827228
KR827078/ KR827122 /
KR827172 / KR827222
-/-/ KR827189 / KR827237
KR827071/ KR827116 /
KR827164 / KR827215
KR827072/ KR827117 /
KR827165 / KR827216
KR827068/ KR827114 /
KR827161 / KR827213
-/DQ115214/-/-
-/ KR827136 / KR827185 /
KR827235
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
NWT_3
NWT_4
NWT_5
RUC_1
RUE_1
RUW_1
RUW_2
SAS_1
SWI_1
SWI_2
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
46.00715
46.52271
59.46133
68.48859
66.28633
72.95000
57.62112
72.00000
69.06200
79.15114
7.74323
9.88484
-109.81917
37.08493
36.80000
121.66667
60.67165
-125.00000
-105.10000
-75.17893
207
Switzerland, Engadine, Punt Muragl. J.
Höller s.n., 2/VIII/1965. (M0177741)
Switzerland, Zermatt, Trockener Steg. M.
Luceño 25ML12 2/2, 11/VIII/2012.
(UPOS4997)
Canada, Saskatchewan, Lake Athabasca. G.
W. Argus 8193, 28/VII/1972. (CAN351228).
Canada, Northwest Territories, Banks
Island. J. M. Gillett 18833, 25/VII/1981.
(CAN464428)
Russia, Taymyr. Matveeva et al. s.n. ,
15/VII/1965. (CAN327344)
Russia, Sakha Republic. A. Tolmatsheur
s.n., 25/VII/1956. (CAN256245)
Russia, Murmansk Oblast, Murmansk. E.
Pobedimova, s.n., 29/VIII/1958.
(CAN377158)
Russia, Murmansk Oblast, Murmansk. E.
Pobedimova s.n. 20/VIII/1958. (M0177753)
Canada, Northwest Territories, Ellesmere
Island. J. M. Gillett 18344A, 21/VII/1979.
(CAN454023)
Canada, Northwest Territories, Victoria
Island. L. J. Gillespie 1120, 26/VII/1997.
(CAN582314)
KR827082/ KR827127 /
KR827177 / KR827225
KR827075/-/ KR827169 /-
KR827083/ KR827128 /
KR827178 / KR827226
KR827088/ KR827132 /
KR827182 / KR827231
KR827060/ KR827105 /
KR827154 / KR827203
-/ KR827118 / KR827166 /
KR827217
KR827092/ KR827137 /
KR827186 /-
KR827087/ KR827131 /-/
KR827230
KR827070/ KR827115 /
KR827163 / KR827214
KR827064/ KR827110 /-/
KR827208
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
YUK_2
YUK_3
Not
47.15778
included
in
molecular
analyses
Not
58.29501
included
in
molecular
analyses
Not
46.50523
included
in
molecular
analyses
C. maritima
C. maritima
C. maritima
C. maritima
C. maritima
YUK_1b
C. maritima
-
60.73167
61.28698
61.28698
YUK_1a
C. maritima
70.67088
WSB_1
C. maritima
11.37101
11.64168
10.58944
-
-135.06500
-138.52892
-138.52892
70.13672
208
Italia, Bolzano, Schlernhaus. Thomas et al.
s.n., 19/VII/2006. (BOZ-PVASC9171)
Sweden, Bohuslän. Skee s.n., 19/VIII/1948.
(UPOS s.n.)
Russia, Tyumen, Yamal Peninsula. O.
Rebristaja s.n., 12/VIII/1983. (E00639424)
Bruederle 07142010 02. 14/VII/2010.
(COLO s.n.)
Bruederle 07142010 01. 14/VII/2010.
(COLO s.n.)
Canada, Yukon, Kishwoot Island. B. A.
Benett 06-033, 3/VII/2006. (CAN589263)
Canada, Yukon. Waterway et al. 96.098
(MTMG s.n.)
Austria, Tirol, Zams. M. Hellweger s.n.
VI/1875.
-
-
-
KR827089/ KR827133 /
KR827183 / KR827232
-/AY757421/-/-
KR827081/ KR827126 /
KR827176 / KR827224
KR827065/ KR827111 /
KR827157 / KR827209
-/ KR827124 / KR827174 /-
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
Blattner (1999) and White
(1990)
52
References
38
0
67.30%
96.60%
90
57
0
60.50%
GTR + I (ITS1) / HKY (5.8s) /
GTR + G (ITS2)
% Identical sites
% Pairwise identity
Variable characters
characters
Number of informative indels
Mean % G+C content
Substitution model
209
HKY + I
53.10%
78
97.90%
79.10%
307-547
481-610
551
612
45
Starr et al. (2003)
External transcribed
spacer of ribosomal
RNA
ETS1f – 18S-R
Aligned length (bp)
Total number of sequences in the
alignment
Internal transcribed
spacers 1 and 2 and 5.8S
ribosomal RNA
Description
ITS1/ 5.8S/ ITS2
F81 + I
22.00%
2
4
14
98.10%
88.70%
614-639
654
48
Escudero & Luceño (2009)
5′trnKCarexF–
5′trnkCarexR
intron of plastid region
Complete data set
GTR
24.20%
2
9
39
92.30%
56.70%
786-875
878
52
Shaw et al. (2005)
Intergenic spacer of
plastid region
rps16F–rpsR
Table S2 Characteristics of the DNA regions sequenced for complete data sets including Carex maritima, related species in section
Foetidae and outgroups.
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
0.335
0.310
0.356
-0.191
0.296
0.219
-0.091
0.295
0.216
0.280
0.275
-0.165
-0.112
-0.179
0.189
-0.133
-0.177
-0.096
-0.177
-0.226
0.121
-0.109
0.252
0.016
-0.272
0.266
0.084
-0.256
-0.058
-0.258
-0.293
-0.268
-0.287
0.151
-0.276
-0.288
-0.253
-0.292
50.35
BIO1
BIO2
BIO3
BIO4
BIO5
BIO6
BIO7
BIO8
BIO9
BIO10
BIO11
BIO12
BIO13
BIO14
BIO15
BIO16
BIO17
BIO18
BIO19
%
Variance
22.29
PC2
PC1
14.69
-0.062
-0.210
-0.112
-0.156
0.104
-0.109
-0.153
-0.130
0.108
-0.449
0.119
-0.393
-0.294
0.117
-0.458
-0.285
0.273
-0.029
-0.067
PC3
8.00
0.006
-0.326
-0.008
-0.269
-0.570
-0.014
-0.320
-0.085
0.068
0.182
0.106
0.050
-0.123
0.162
0.082
-0.002
-0.209
-0.484
0.101
PC4
1.88
-0.253
0.292
-0.176
0.089
0.191
-0.172
0.152
-0.073
0.101
-0.059
-0.322
0.467
-0.251
0.156
-0.256
-0.120
-0.193
-0.418
0.049
PC5
1.08
0.027
-0.203
-0.213
0.175
0.430
-0.234
0.219
-0.030
0.015
0.208
0.416
-0.343
0.025
0.004
0.073
0.050
-0.424
-0.248
0.099
PC6
0.84
0.205
-0.229
0.282
-0.184
0.572
0.325
-0.247
0.069
0.013
0.178
-0.355
-0.050
-0.052
0.089
0.085
0.068
0.154
-0.294
0.034
PC7
0.39
0.128
0.013
0.211
-0.225
0.216
0.213
-0.197
0.000
-0.057
-0.217
0.546
0.499
0.011
-0.096
-0.201
-0.031
-0.297
0.104
-0.100
PC8
0.28
-0.322
0.420
0.157
-0.150
0.042
0.152
-0.341
-0.101
0.169
0.081
-0.123
-0.369
-0.022
0.041
0.044
-0.177
-0.464
0.237
0.167
PC9
210
0.12
0.212
-0.505
-0.025
0.124
-0.033
-0.028
0.108
0.149
0.185
-0.212
-0.354
0.130
-0.082
0.127
0.097
-0.261
-0.432
0.373
0.031
PC10
0.04
-0.020
-0.205
0.069
-0.034
-0.087
0.168
0.218
-0.193
0.083
0.486
-0.077
0.019
-0.024
-0.244
-0.644
0.094
-0.017
0.195
0.242
PC11
0.02
0.562
0.240
-0.295
0.029
0.009
-0.284
-0.397
0.187
-0.015
-0.021
-0.090
0.009
0.113
-0.192
-0.174
0.000
-0.004
-0.002
0.420
PC12
0.02
-0.467
-0.250
0.098
0.408
0.003
0.165
-0.187
0.222
-0.048
-0.266
0.053
0.063
0.221
-0.236
-0.012
-0.026
0.082
-0.153
0.467
PC13
0.01
-0.131
-0.055
0.041
0.426
0.016
-0.176
-0.443
0.331
0.009
0.296
0.062
0.038
-0.266
0.197
-0.194
0.230
0.002
0.172
-0.369
PC14
0.00
-0.075
-0.016
0.588
-0.259
0.010
-0.572
0.161
0.176
-0.134
-0.107
-0.025
-0.025
-0.108
0.099
-0.034
0.255
-0.020
0.064
0.272
PC15
0.00
0.158
0.007
0.032
0.334
-0.012
0.140
-0.089
-0.576
-0.400
-0.159
-0.010
0.005
-0.259
0.297
0.060
0.279
-0.050
0.114
0.257
PC16
variables on Carex maritima, C. incurviformis, C. pseudofoetida and C. sajanensis using the reduced data set.
0.00
-0.157
0.004
-0.439
-0.346
0.007
0.308
0.142
0.467
-0.286
-0.046
0.018
-0.044
-0.225
0.223
-0.030
0.286
-0.050
0.133
0.200
PC17
0.00
-0.031
-0.024
0.065
0.000
0.003
-0.078
-0.012
0.087
-0.705
0.269
-0.010
0.011
-0.018
0.010
-0.023
-0.640
0.011
0.006
-0.017
PC18
Table S3 Loadings matrix obtained by the principal components analysis uncorrected by phylogeny of 19 bioclimatic
0.00
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.695
0.664
-0.278
0.000
0.000
0.000
0.000
PC19
100.0
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
-0.191
0.135
0.053
-0.008
-0.241
-0.124
0.017
0.001
-0.072
-0.299
-0.114
-0.611
-0.606
-0.625
0.250
-0.618
-0.619
-0.649
-0.555
0.729
-0.481
0.789
-1.000
-0.211
0.943
-0.980
-0.331
0.875
0.015
0.925
0.791
0.751
0.754
-0.605
0.763
0.762
0.685
0.810
50.35
BIO1
BIO2
BIO3
BIO4
BIO5
BIO6
BIO7
BIO8
BIO9
BIO10
BIO11
BIO12
BIO13
BIO14
BIO15
BIO16
BIO17
BIO18
BIO19
%
Varia
nce
22.29
PC2
PC1
14.69
0.098
-0.125
0.078
-0.051
-0.060
0.088
-0.083
0.023
-0.356
-0.938
-0.344
-0.840
-0.129
-0.274
-0.934
0.000
-0.188
-0.476
-0.648
PC3
8.00
0.129
-0.225
0.022
-0.046
-0.093
0.016
-0.056
0.002
-0.017
-0.025
0.313
-0.347
0.044
-0.044
0.007
0.000
0.118
0.179
-0.019
PC4
1.88
-0.061
0.150
-0.060
0.109
0.403
-0.065
0.147
-0.004
-0.062
-0.143
0.073
0.015
0.108
-0.124
-0.020
0.000
0.326
0.557
-0.072
PC5
1.08
-0.009
-0.088
-0.151
0.133
0.111
-0.159
0.177
0.001
0.010
0.016
0.001
-0.068
-0.058
0.047
-0.032
0.000
-0.128
-0.274
0.008
PC6
0.84
-0.021
0.084
-0.006
-0.007
-0.429
-0.013
0.014
-0.002
-0.027
-0.067
0.080
0.112
-0.065
0.011
-0.130
0.000
-0.228
-0.281
-0.050
PC7
0.39
-0.046
0.063
0.012
0.011
-0.207
0.004
-0.036
-0.002
0.015
0.058
0.000
-0.213
0.006
0.016
0.049
0.000
-0.190
-0.076
0.035
PC8
0.12
0.043
0.030
-0.028
-0.004
-0.088
-0.031
0.004
-0.003
-0.001
0.002
-0.009
-0.012
0.003
0.005
0.018
0.000
0.132
0.049
0.000
PC10
211
0.28
-0.018
-0.041
-0.024
0.004
-0.381
-0.023
-0.015
0.005
-0.006
-0.020
-0.013
0.032
0.031
-0.023
0.023
0.000
0.019
0.062
0.010
PC9
0.04
0.004
-0.006
0.028
0.018
-0.067
0.028
0.047
-0.003
0.001
0.002
-0.002
0.002
-0.005
0.009
0.010
0.000
0.095
0.073
-0.021
PC11
0.02
0.006
0.000
0.007
0.009
-0.016
0.013
-0.004
-0.002
0.006
0.021
-0.002
0.001
-0.005
-0.016
-0.048
0.000
0.003
0.015
0.043
PC12
0.02
-0.007
0.000
-0.006
-0.007
-0.002
-0.013
-0.004
0.001
0.008
-0.002
0.001
-0.006
-0.010
0.004
-0.015
0.000
0.234
0.095
-0.002
PC13
0.01
0.001
0.000
0.002
0.007
0.004
-0.002
-0.034
0.000
-0.007
-0.025
0.001
0.002
-0.002
0.005
0.007
0.000
0.050
0.009
0.010
PC14
Carex maritima, C. incurviformis, C. pseudofoetida and C. sajanensis using the reduced data set.
0.00
-0.001
0.000
0.002
-0.005
0.001
-0.009
0.027
0.000
-0.006
-0.015
0.000
-0.002
0.000
0.002
0.004
0.000
0.048
-0.005
0.015
PC15
0.00
0.000
0.000
-0.001
0.001
0.000
0.020
0.000
0.000
0.000
0.002
0.000
0.000
0.001
-0.001
0.001
0.000
0.160
-0.024
-0.001
PC16
0.00
0.000
0.000
0.002
0.001
0.000
-0.014
0.000
0.000
0.007
-0.012
0.000
0.000
0.001
-0.001
0.000
0.000
0.024
-0.013
-0.001
PC17
0.00
0.000
0.000
-0.002
0.000
0.000
0.021
0.002
0.000
0.003
-0.010
0.000
-0.001
0.000
0.001
0.001
0.000
-0.047
0.006
0.001
PC18
0.0
0
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
PC1
9
Table S4 Loadings matrix obtained by the principal components analysis corrected by phylogeny of 19 bioclimatic variables on
10
0.0
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
% of
Varia
nce
BIO19
BIO18
BIO17
BIO16
BIO15
BIO14
BIO13
BIO12
BIO11
BIO10
BIO9
BIO8
BIO7
BIO6
BIO5
BIO4
BIO3
BIO2
BIO1
0.341
0.032
0.127
0.554
-0.001
0.178
0.498
0.030
0.458
0.032
-0.012
0.027
-0.063
0.143
0.034
-0.048
0.091
-0.068
0.151
-0.174
0.255
-0.080
-0.268
0.252
0.023
-0.260
-0.159
-0.266
-0.264
-0.251
-0.264
0.202
-0.254
-0.265
-0.249
-0.262
14.7
0.166
-0.258
65.9
PC2
PC1
9.4
0.230
0.272
0.228
0.314
0.296
0.206
0.324
0.263
-0.236
-0.054
-0.220
-0.007
0.220
-0.220
-0.026
0.265
-0.315
-0.046
-0.207
PC3
4.7
0.094
0.060
0.088
0.020
0.113
0.082
0.062
0.053
-0.059
-0.211
-0.008
-0.249
0.093
-0.099
-0.031
-0.014
0.657
0.620
-0.090
PC4
2.3
0.106
-0.088
0.047
-0.068
-0.438
0.016
-0.046
0.007
-0.072
0.249
0.139
-0.640
0.193
-0.083
0.336
0.160
-0.274
0.160
0.004
PC5
1.7
0.046
-0.277
-0.111
0.071
0.732
-0.142
0.088
-0.017
0.099
0.217
0.140
-0.425
-0.073
0.107
0.118
-0.012
0.059
-0.185
0.121
PC6
0.4
-0.090
0.202
-0.219
0.186
0.063
-0.304
0.201
-0.014
0.044
-0.251
0.559
0.016
-0.032
-0.013
-0.141
-0.171
-0.399
0.379
0.014
PC7
0.3
-0.302
0.592
-0.197
0.124
-0.021
-0.298
0.010
-0.022
0.091
0.014
-0.507
-0.290
-0.096
0.133
0.131
-0.113
0.025
-0.027
0.083
PC8
0.2
0.270
-0.403
-0.230
0.331
-0.295
-0.501
0.396
0.122
-0.033
-0.001
-0.218
0.100
0.006
-0.002
0.012
0.041
0.165
-0.056
-0.037
PC9
212
0.1
-0.485
0.143
-0.153
0.192
-0.129
0.070
0.202
-0.061
-0.180
0.162
0.386
-0.035
0.155
-0.173
-0.075
0.279
0.367
-0.351
-0.115
PC10
0.1
-0.491
-0.374
-0.002
0.209
-0.044
0.407
0.303
-0.040
0.138
0.106
-0.270
-0.055
-0.048
-0.011
-0.186
-0.108
-0.187
0.278
0.215
PC11
0.0
0.103
0.040
0.000
0.401
-0.010
-0.128
-0.541
0.150
-0.011
0.355
-0.002
-0.013
0.004
-0.151
-0.480
0.153
0.011
0.125
0.277
PC12
0.0
-0.294
-0.221
0.193
0.465
0.009
-0.023
-0.410
0.290
-0.012
-0.349
0.055
0.011
0.020
0.105
0.406
-0.115
-0.006
-0.065
-0.199
PC13
0.0
0.268
0.039
-0.760
0.197
-0.012
0.485
-0.155
-0.047
-0.067
-0.102
-0.018
0.002
-0.061
0.098
0.129
0.025
-0.004
0.002
-0.052
PC14
0.0
0.058
0.009
-0.073
-0.029
0.009
0.019
-0.005
0.023
0.081
-0.277
-0.015
-0.007
0.494
-0.444
0.104
-0.307
0.050
-0.212
0.559
PC15
0.0
-0.106
-0.029
-0.037
-0.206
-0.001
-0.028
0.048
0.345
-0.335
-0.296
0.024
-0.003
-0.224
0.231
0.049
0.478
-0.008
0.037
0.535
PC16
0.0
0.138
0.022
0.255
0.352
-0.017
0.004
-0.005
-0.773
-0.035
-0.224
-0.004
-0.002
-0.072
0.100
0.100
0.258
0.004
-0.017
0.223
PC17
0.0
0.004
-0.014
0.061
0.048
0.010
-0.001
0.008
-0.107
-0.817
0.187
-0.004
0.001
-0.078
0.078
0.010
-0.512
0.003
0.003
0.074
PC18
0.0
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
-0.677
-0.703
0.216
0.000
0.000
0.000
0.000
PC19
100.
0
Table S5 Loadings matrix obtained by the principal components analysis of 19 bioclimatic variables on Carex maritima full data set.
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
BIO1
BIO2
BIO3
BIO4
BIO5
BIO6
BIO7
BIO8
BIO9
BIO10
BIO11
BIO12
BIO13
BIO14
BIO15
BIO16
BIO17
BIO18
BIO19
213
Description
mean diurnal temperature range [mean of monthly (maximum temperature - minimum temperature)]
isothermality (BIO2 / BIO7 x 100)
maximum temperature of the coldest month;
temperature range (BIO6 - BIO5)
calculated based on K × 10 to deal with negative temperatures) and mm for precipitation.
Table S6 Bioclimatic variables used. Units of bioclimatic variables are °C × 10 for temperature (excluding BIO4 which was
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
0.941 ± 0.002
0.942 ± 0.002
0.997 ± 0.003
C. maritima from both
hemispheres
C. maritima from Northern
Hemisphere
C. maritima from Southern
Hemisphere
AUC ± SD
minimum temperature
of the warmest month
(BIO6)
BIO1
Annual mean
temperature (BIO1)
Environmental
variables that
contributed most
214
BIO6
BIO1
BIO1
The most important
environmental
variable when used
alone
WorldClim database layers and the most important when used alone, for each group of Carex maritima.
Table S7 Area under the curve (AUC) ± standard deviation (SD) and the variables that contributed the most to explain MAXENT models under
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
215
White T.J., Bruns T., Lee S., & Taylor J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for
phylogenetics. PCR protocols: a guide to methods and applications (ed. by M. Innis, D. Gelfand, D. Sninsky and T. White), pp.
315–322. Academic Press, San Diego, CA.
Starr J.R., Harris S.A., & Simpson D.A. (2003) Potential of the 5 and 3 ends of intergenic spacer (IGS) of rDNA in the Cyperaceae:
new sequences for lower-level phylogenies in sedges with an example from Uncinia Pers. International Journal of Plant
Sciences, 164, 213–227.
Shaw J., Lickey E.B., Beck J.T., Farmer S.B., Liu W., Miller J., Siripun K.C., Winder C.T., Schilling E.E. & Small R.L. (2005) The
tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal
of Botany, 92, 142–166.
Escudero M. & Luceño M. (2009) Systematics and evolution of Carex sects. Spirostachyae and Elatae (Cyperaceae). Plant
Brummitt R.K. (2001) World geographical scheme for recording plant distributions, 2nd edn. Hunt Institute for Botanical
Documentation, Pittsburgh, PA.
Blattner F.R. (1999) Direct amplification of the entire ITS region from poorly preserved plant material using recombinant PCR.
Biotechniques, 1180–1186.
REFERENCES
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
216
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
components analysis of the full data set (Fig. S5).
217
bioclimatic variables used in MAXENT analyses (Fig. S4); and scatter plot of the three first components from the principal
(18–21 ka; MIROC and CCSM models) and Last Interglacial Period (c. 120–140 ka) (Fig. S3); scatter plots of the uncorrelated
fitted to current climatic conditions from MAXENT analyses (Fig. S2), and projections of the models to Last Glacial Maximum
Appendix S2 Supplementary figures. Distribution map of Carex maritima (Fig. S1); ecological niche models of C. maritima groups
Tamara Villaverde, Marcial Escudero, Modesto Luceño and Santiago Martín-Bravo
Long-distance dispersal during the middle–late Pleistocene explains the bipolar disjunction of Carex maritima (Cyperaceae)
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
218
and removing duplicate records from the same locality to reduce the effects of spatial autocorrelation.
downloaded 22 December 2014) after pruning for likely incorrect identification or georeferencing (e.g. occurrences in oceans)
between 1950 and 2000, downloaded from the Global Biodiversity Information Facility data portal (http://www.gbif.org/,
Figure S1 Distribution map of Carex maritima (894 preserved specimens) depicted by black circles, obtained from occurrence data
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
(b)
(a)
219
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
Hemisphere.
220
Carex maritima; (b) C. maritima populations of the Northern Hemisphere; (c) C. maritima populations of the Southern
analyses. Colours correspond to a continuous prediction with values ranging from 0 to 1 (from white to red, respectively). (a)
Figure S2 Ecological niche model of Carex maritima groups fitted to current climatic conditions (c. 1950–2000) from MAXENT
(c)
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
from 0 to 100 (from blue to red, respectively).
221
shown) and Last Interglacial Period (LIG, c. 120–140 ka). Colours correspond to a continuous prediction with values ranging
Hemispheres). MAXENT projections of the model to the Last Glacial Maximum (LGM, 18–21 ka; MIROC and CSSM model
Figure S3 Maps of predicted environmental suitability for Carex maritima and population groups (Northern and Southern
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
(a)
222
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
(b)
223
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
224
warmest month (BIO6); (b) BIO1 and annual precipitation (BIO12); and (c) BIO6 and BIO12.
Hemisphere samples (grey and red circles, respectively): (a) annual mean temperature (BIO1) and minimum temperature of the
Figure S4 Scatter plots of the uncorrelated bioclimatic variables used in MAXENT analyses of Carex maritima Northern and Southern
(c)
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
(a)
225
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
(b)
226
disjunction
________________________________________________________________
________________________________________________________________
of Carex maritima
227
and principal component 2 (PC2); (b) PC1 and principal component 3 (PC3); and (c) PC2 and PC3.
Carex maritima Northern and Southern Hemisphere samples (grey and red circles, respectively): (a) principal component 1 (PC1)
the principal components analysis of the full data set (894 populations) and depicting in a climate-niche space the position of
Figure S5 Scatter plots of the first three components explaining up to 90% of the observed variance (see Appendix S1), derived from
(c)
disjunction
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of Carex maritima
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disjunction
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of Carex maritima
Chapter 5
Two independent dispersals to the
Southern Hemisphere to become the
most widespread Carex bipolar species:
biogeography of C. canescens
(Cyperaceae)
229
230
Chapter 5. Two independent dispersals to the Southern Hemisphere to become the most widespread
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Carex bipolar species: biogeography of C. canescens
Two independent dispersals to the Southern Hemisphere to become the most
widespread Carex bipolar species: biogeography of C. canescens (Cyperaceae)
Tamara Villaverdea, Marcial Escuderob,c, Santiago Martín-Bravoa and Modesto Luceñoa
a
Department of Molecular Biology and Biochemical Engineering, Pablo de Olavide
University, Seville, Spain. bDepartment of Integrative Ecology, Estación Biológica de
Doñana (EBD-CSIC), Seville, Spain. cDepartment of Plant Biology and Ecology,
University of Seville, Seville, Spain.
*Correspondence: Tamara Villaverde. Department of Molecular Biology and
Biochemical Engineering, Pablo de Olavide University, carretera de Utrera Km 1 sn
41013 Seville, Spain. email: [email protected]
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Abstract
Aim: To test the various hypotheses accounting for the bipolar disjunction of Carex
canescens and to elucidate if it migrated twice to the Southern Hemisphere or if it
dispersed from South America to Australia (or vice versa).
Location: Arctic/boreal latitudes of both hemispheres.
Methods: We obtained and analysed DNA sequences for the nuclear internal and
external transcribed spacers (ITS and ETS) and for the plastid 5′ trnK and rps16 introns
from 56 populations of C. canescens and 8 populations from its sister species and
outgroups. We also climatically characterized the species distribution by adding 1,995
species presence data points from the Global Biodiversity Information Facility and
using the climatic information stored in the WorldClim database.
Results: Although the internal phylogenetic resolution of C. canescens was poor and
populations were embedded in a polytomy independently of their geographical origin,
genetic structure was detected between South America and Australia, which did not
share any of the sampled haplotypes. The diversification of C. canescens occurred
during the Pleistocene (1.17 Ma; 95% HPD 0.34 – 2.17 Ma). Southern Hemisphere
populations occupy a more restricted climatic niche than in the Northern Hemisphere
but falling within the general ecological conditions tolerated by the species, which seem
to be very wide.
Main conclusions: Carex canescens dispersed twice from the Northern Hemisphere to
South America and Australia. Recent divergence times and the lack of genetic
differentiation between disjunct populations did not allow us to discern between direct
dispersal and mountain-hopping or a combination of both, to explain the colonization of
the Southern Hemisphere. Long-distance dispersal is claimed as a widespread
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phenomenon in bipolar Carex species, possibly facilitated by rare processes or unusual
behaviour of vectors.
Keywords: Biogeography, climatic niche, Cyperaceae, divergence time estimation,
Glareosae, long-distance dispersal.
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INTRODUCTION
Interest in establishing the relations between floras in the Southern Hemisphere has
been fostered by their similarities with floras of the Northern Hemisphere (e.g., Raven,
1963; Raven, 1972; Wen & Ickert-Bond, 2009; Leslie et al., 2012). Around 75-85% of
families present in Tasmania and South America (south of ca. 40º S) also occur in the
Northern Hemisphere, whereas ca. 20-27% of the genera are shared between New
Zealand-South America and the Northern Hemisphere (Moore, 1972). Plant disjunctions
between hemispheres are formidable when species reach very high latitudes at both
sides of the Equator, regardless of its occurrence at intermediate latitudes, thus
achieving the so-called bipolar distribution (Moore & Chater, 1971). About 30 vascular
plant species are known to have such a distribution, which are mainly restricted to
alpine and polar regions (Moore & Chater, 1971).Bipolar disjunctions have historically
been explained by four hypotheses: (1) vicariance (Du Rietz, 1940), which implies a
continuous distribution fragmentation during the Mesozoic Era (Scotese et al., 1988);
(2) convergent or parallel evolution of the disjunct populations (Hofsten, 1916;
Scotland, 2011); (3) stepwise long-distance dispersal across the Equator via mountain
ranges (“mountain-hopping”; Raven, 1963; Moore & Chater, 1971; Ball, 1990; Vollan
et al., 2006); and (4) direct long-distance seed dispersal by birds, wind and/or ocean
currents (Cruden, 1966; Muñoz et al., 2004; Nathan et al., 2008; Gillespie et al., 2012).
The genus Carex L., which consists of c. 2000 species (Reznicek, 1990), has the
greatest number of bipolar taxa (6), which generally have a circumboreal distribution
and are limited to austral latitudes in South America (>52º). An exception is C.
canescens (sect. Glareosae G. Don), the single bipolar Carex species that reaches not
only the southernmost region of South America (Tierra del Fuego and Falkland Islands)
but also Oceania (including Australia, Tasmania and New Guinea; Fig. 1 and Appendix
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S1), occurring within five biogeographical regions (Nearctic, Palearctic, Andean,
Neoguinean and Australotemperate; Morrone, 2002). Carex canescens is therefore the
bipolar Carex species with the widest distribution.
The great morphological variability within C. canescens across its wide
distribution has motivated the description of more than 40 infraspecific taxa, of which
only Carex canescens subsp. disjuncta (Fernald) Toivonen (that occurs in eastern North
America) and C. canescens var. robustior Blytt ex Andersson (that is distributed in
Patagonia and Falkland Islands) are currently accepted (Govaerts et al. 2014). Carex
canescens var. robustior is also considered an ecotype of C. canescens from the
mountainous regions in North America, but this taxon is not currently accepted in North
America (Toivonen, 2002). A morphological study of C. canescens covering its total
range found slight differences between Northern and Southern Hemisphere populations,
which only deserved varietal recognition (Moore & Chater, 1971). In general, Southern
Hemisphere plants tend to be greater than their Northern Hemisphere counterparts for
various parts (e.g., stem diameter, leaf size and utricle width), although there is some
overlapping (Moore & Chater, 1971). Moore (1972) interpreted that these
morphological differences between hemispheres could suggest a transtropical migration
in the Americas and subsequent circum-Antarctic dispersal. Nelmes (1951) proposed
that C. canescens populations from Malaysia are intermediate forms between Australian
and European forms based on the number and conspicuously (or not conspicuously)
nerved utricles, and suggested a southward migration and adaptation of southern
populations (Moore, 1972). In C. canescens, as well as in other temperate sedges, leaf
elongation has been proven to increase with temperature (Heide, 1997, 2000) and might
not have a genetic origin. Vollan et al. (2006) analysed samples of C. canescens from
Europe (only Norway), South America (Chile) and Australia using amplified fragment
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length polymorphisms (AFLPs) and found genetic differentiation between Northern and
Southern Hemisphere populations. They hypothesized a Northern Hemisphere origin
and a single colonization of the Southern Hemisphere, followed by secondary dispersal
from Australia to South America or vice versa. Escudero et al. (2010a) found that the
genetic distance between populations of C. canescens from North and South America
was lower than between some populations from the Northern Hemisphere, which could
indicate a more recent connection between North America and Patagonia than among
some areas of the Northern Hemisphere. However, sampling was limited in both of
these studies, including only six or seven populations and lacking samples from North
America (Vollan et al., 2006) or Australia (Escudero et al., 2010a). For bipolar Carex
species, the vicariance hypothesis (Du Rietz, 1940) is rejected as the origin of the family
Cyperaceae (82.6 Ma, 95% highest posterior density: 75.9–85.6 Ma; Escudero & Hipp,
2013) is placed during the Cretaceous, which is well after the fragmentation of the
trans-tropical highland bridges that occurred during the Mesozoic Era (195 Ma; Scotese
et al., 1988).
Here we aimed to: (i) test the various hypotheses accounting for the bipolar
disjunction of C. canescens; and (ii) to determine whether C. canescens migrated twice
to the Southern Hemisphere or was dispersed from South America to Australia or vice
versa.
Study species and sampling
Carex canescens is distributed in the temperate areas of both hemispheres, with a
circumpolar range in the Northern Hemisphere, whereas its range is limited to Patagonia
and south-eastern Australia in the Southern Hemisphere (Fig. 1). Potential C. canescens
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herbarium specimens from New Guinea were depauperate and infertile, precluding a
confident
identification.
Carex
canescens
is
a
wind-pollinated
herbaceous
hemicryptophyte that usually grows in persistently wet, base-poor sites (e.g., sphagnum
bogs), moist coniferous forests, woodlands, meadows, lakeshores, rivers and other fresh
water bodies. We obtained plant material representing the entire range of C. canescens
subsp. canescens (58 populations) as circumscribed by Egorova (1999) and Toivonen
(2002). We also included one population each of C. canescens subsp. disjuncta
(Fernald) Toivonen, C. lachenalii Schkuhr, C. glareosa Schkuhr ex Wahlenb., C. furva
Webb and C. arcta Boott from section Glareosae. We use C. macloviana d’Urv., C.
maritima Gunn., C. paniculata subsp. paniculata L. and C. remota L. as outgroups
(Waterway et al. 2009). For all species one individual per population was sampled.
Samples used for the molecular study were obtained from silica-dried leaf material
collected in the field and from herbarium specimens (Appendix S1). Vouchers for new
collections are deposited in the following herbaria: CAN, SI and UPOS (abbreviation
following Index Herbariorum).
PCR amplification and sequencing
Total DNA was extracted using DNeasy Plant Mini Kit (Qiagen, California). Forward
and reverse primers were used for amplifications of the internal transcribed spacer
region (ITS: ITS-A, ITS-4; White et al., 1990; Blattner, 1999), external transcribed
spacer regions (ETS: ETS-1f, 18S-R; Starr et al., 2003), 5′trnK intron (5′trnKCarexF,
5′trnKCarexR; Escudero & Luceño, 2009) and rps16 intron (rps16F-rps16R; Shaw et
al., 2005). Amplifications were obtained in a Perkin Elmer PCR-system 9700
(California) under the conditions specified by Escudero et al. (2010a) for ITS and
rps16, Starr et al. (2003) for ETS, and Escudero & Luceño (2009) for 5′trnK intron.
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Polymerase chain reaction (PCR) products were cleaned and sequenced following
Escudero et al. (2008). Sequences were edited, automatically aligned with MUSCLE
(Edgar, 2004) and manually adjusted using GENEIOUS v6.1.7 (Biomatters, Auckland,
New Zealand). We coded three informative indels for the 5′trnK region following the
simple gap coding method by Simmons & Ochoterena (2000).
Phylogenetic analyses
We obtained a total of 56 sequences of ITS (six from NCBI GenBank), 41 of ETS (four
from NCBI GenBank), 43 of rps16 (two from NCBI GenBank) and 47 of 5′trnK (one
from NCBI GenBank; Appendix S1). Each of the four loci was analysed independently
and in combination using Maximum Likelihood (ML) and Bayesian inference (BI). The
combined nuclear and plastid matrix consisted of 64 combined sequences with 2,635
sites (see Appendix S1). Maximum likelihood and Bayesian analyses were performed as
described by Villaverde et al. (2015a). Selected nucleotide substitution models under
the Akaike Information Criterion (AIC) in jModeltest (Posada, 2008) were GTR+G for
ITS1 and ITS2, HKY for ITS 5.8s; GTR for rps16 and HKY+I for 5′trnK (Appendix
S1).
Haplotype network and divergence time estimation
We obtained the genealogical relationships among ptDNA haplotypes using the plastid
combined matrix and statistical parsimony as implemented in TCS v1.21 (Clement et
al., 2000) and described in Villaverde et al. (2015a). We estimated completeness of
haplotype (5′trnK - rps16) sampling using a Stirling probability distribution, as
described by Dixon (2006), which calculates a posterior probability distribution of the
total number of haplotypes (sampled or not).
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Dated phylogenies were estimated for the nuclear and plastid matrix in
BEAST
v1.7.5 (Drummond et al., 2012). All phylogenies were estimated using an uncorrelated
log-normal relaxed clock model. A normal age prior with a mean of 14.82 million years
ago (Ma) ± 2.5 million years (Myr) was applied to the root of the tree based on previous
estimates (Escudero & Hipp, 2013). Analyses were conducted using two independent
MCMC runs of 40 million generations each, assuming the Birth Death tree prior with a
mean substitution rate set at 1.0. Run convergence and burn-in were assessed in TRACER
v1.5 (Rambaut & Drummond, 2009). Maximum Clade Credibility (MCC) trees were
calculated with TREEANNOTATOR v1.7.2 (Drummond & Rambaut, 2007) using a
posterior probability limit of 0.7 and the mean heights option.
We obtained values for 19 bioclimatic variables (Appendix S1) as described by
Escudero et al. (2013) for each sampled population of C. canescens, except for one
population from the USA (Wisconsin) lacking precise geographic coordinates. This data
set was completed by adding: (i) five additional populations from Australia for which
we failed to amplify any loci (see Appendix S1); (ii) 1,992 species occurrence records
originated from herbarium specimens, collected between 1950 and 2014, and
downloaded from the Global Biodiversity Information Facility data portal
(http://www.gbif.org/, downloaded 12 February 2015). This dataset was refined by
removing likely incorrectly identified (e.g., occurrences outside of the distribution range
defined by Monocot checklist, Govaerts et al. 2014) or incorrectly georeferenced
populations (e.g., occurrences in oceans) and duplicate records from the same locality to
reduce the effects of spatial autocorrelation. Our final data set included a total of 2,057
populations (Appendix S2). To characterize its climatic niche space, we performed a
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principal components analysis (PCA) of the climatic dataset using the prcomp function
(sdev, rotation, centre and scale options were set as TRUE) in R (R Core Team, 2014).
Ecological niche model
A species distribution modeling was performed to reconstruct the potential ranges of C.
canescens under present clime with MAXENT v3.3.3k (Phillips et al., 2006). We
performed a correlation analysis with the Variance Inflation Factor (VIF) using the vif
function in the usdm package in R (R Development core Team, 2014) and a correlation
threshold of 0.7 (Dormann et al., 2013) . Only three variables were uncorrelated and
consequently included in the analyses: bio1 (annual mean temperature), bio6 (minimum
temperature of the warmest month) and bio12 (annual precipitation). Replicate runs
(500) were performed using the bootstrap run type. Analyses were performed for all
populations of C. canescens and separately by Northern and Southern Hemisphere
populations, as well as by populations of C. canescens from South America and
Australia. We partitioned all the locality data into training and testing data sets (75% vs.
25%, respectively) in order to build niche models and to evaluate the quality of the
model.
RESULTS
Carex section Glareosae was obtained as monophyletic in all the analyses with a strong
support (94% BS / 1 PP, Appendix S2). The monophyly of C. canescens was strongly
supported (97% BS / 1PP), with the single sampled population of C. canescens subsp.
disjuncta retrieved as sister to the remainder of C. canescens subsp. canescens. The
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internal phylogenetic resolution of the species was poor and populations from different
hemispheres or continents did not form clades. Most populations were embedded in a
polytomy, independently of their geographical origin, with the exception of two samples
from South America, which formed a weakly to moderately supported clade (61% BS /
0.84 PP, Appendix S2).
Haplotype network
The obtained ptDNA (5′trnK-rps16) haplotype network revealed five different
haplotypes (H1-H5) and one missing haplotype (Fig. 3). A probability of 95% that all
haplotypes have been sampled is given by Dixon’s (2006) method. Haplotype 1 (H1) is
shared by 34 samples from Australia, Eurasia and North America, while haplotype 2
(H2), separated by one mutation from H1, is shared by 11 samples from Eurasia, North
and South America. There are three haplotypes exclusive to single populations: one
from western North America (California; H3), one from South America (Argentina,
Santa Cruz; H4) and one from C. canescens subsp. disjuncta from north-eastern North
America (Massachusetts; H5). No more than one or two mutations are needed to
connect these singletons with H1 or H2 (Fig. 3). A loop connects H1, H2, H4 and the
missing haplotype that leads to H5, which reflects ambiguity about the evolutionary
history of these haplotypes due to homoplasy. Four of the five haplotypes (H1-H3, H5)
were found in North America, whereas two in Eurasia (H1, H2) and South America
(H2, H4) and only one in Australia (H1). Interestingly, populations from the Northern
Hemisphere shared haplotypes with those from the Southern Hemisphere (H1, H2),
whereas different haplotypes were found in Australia (H1) versus South America (H2,
H4).
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Divergence time estimation
The dating analyses produced a congruent topology with respect to the BI and ML
analyses presented above (Fig. 2 and Table 1). The divergence time of the clade
comprising section Glareosae was 6.55 Ma (95% highest posterior density, HPD, 2.56 –
10.99 Ma), which falls in the Late Miocene - Pliocene. Thus, the diversification of C.
canescens could have occurred during the Pleistocene (1.17 Ma; 95% HPD 0.34 – 2.17
Ma). The clade comprised by C. lachenalii and C. glareosa diverged during the same
Epoch (1.03 Ma, 95% HPD 0.18 – 2.14 Ma).
The PCA of the climatic data set showed that PC1 explained 48.1% of the variance,
whereas PC2 and PC3 explained 15.7 and 14.5% respectively (Appendix S1). The
variables with the highest loadings in PC1 were annual precipitation (bio12),
temperature seasonality (bio4) and precipitation of coldest quarter (bio19; Appendix
S1). The scatter plot of the three first components (Fig. 4) is coloured by geographic
groups corresponding to: C. canescens samples from North-East (Eurasia), North-West
(North America), South-East (Australasia) and South-West (South America) quadrants.
Separation between the Northern and Southern Hemisphere samples of C. canescens or
between different landmasses within the same hemisphere was not observed (Fig. 4).
Present distribution under climatic change scenarios
Current conditions
Our results show that the modelled ecological niche of C. canescens, including the
Northern and Southern Hemisphere samples, predicts suitable areas in both
hemispheres. The environmental variable that contributed most to explain the
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MAXENT models under WorldClim database layers and the most important
environmental variable when used alone, according to the jack-knife test, was annual
mean temperature (bio1). The modelled ecological niche of C. canescens including only
the Northern Hemisphere populations predicts suitable habitats also in the Southern
Hemisphere (Appendix S2). Values for the area under the curve (AUC) were all above
0.89, which indicate a good fit of the models. The average AUC for each group and the
most important environmental variables detected in each analysis are reported in
Appendix S1.
DISCUSSION
Our results show that C. canescens is a monophyletic species, which allows us to
strongly reject the convergent or parallel evolution hypotheses for the origin of the
bipolar disjunction (Hofsten, 1916; Scotland, 2011), since we would expect two or more
lineages of C. canescens with different common ancestors under these hypotheses.
Carex canescens diverged from its sister species in section Glareosae 1.17 Ma (95%
HPD: 0.34 – 2.17) and the clade formed by only two samples from South America is of
recent origin (Fig. 3). In addition, no clear genetic differentiation was found between the
other Northern and Southern Hemisphere populations, since they shared haplotypes
(H1, H2; Fig. 2), which also points to a rather recent origin of the bipolar disjunction.
Therefore, the remaining alternative hypotheses are mountain-hopping through the
American Cordillera and Malaysian mountains, direct long-distance dispersal, or a
combination of both.
Based on our haplotype network (Fig. 2), we cannot infer the direction of
dispersal (North-to-South or South-to-North). The haplotype with the highest number of
mutational connections (three), which is considered the ancestral haplotype under the
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coalescent theory (Posada & Crandall 2001), comprises populations from Eurasia,
North and South America (H2). Nevertheless, the haplotype H1 could also be ancestral,
as it is also widely distributed (Eurasia, North America and Australia) and has only one
connection less than H2. All 23-25 species of Carex section Glareosae (Maguilla et al.,
in press), with the exception of C. canescens and C. lachenalii, are exclusively
distributed in the Northern Hemisphere, which supports the hypothesis of a northern
origin of the species and a subsequent North-to-South direction of dispersal. The same
hypothesis is supported by the widespread distribution of C. canescens in the Northern
Hemisphere relative to its very restricted distribution in the Southern Hemisphere (Fig.
1). Other works on bipolar taxa (including two examples of bipolar Carex species) have
also shown a predominantly southwards colonization route (Gussarova et al., 2008;
Popp et al. 2011; Piñeiro et al., 2012; Villaverde et al., 2015a; 2015b). Therefore, we
suggest that C. canescens’ distribution is a result of long-distance dispersal from the
Northern Hemisphere to the Southern Hemisphere.
Not once but twice: the double colonization of the Southern Hemisphere by C.
canescens
While haplotype sharing was found between Northern and Southern Hemisphere
populations, genetic structure was detected between South America and Australia,
which did not share any of the sampled haplotypes (Fig. 2). Therefore, we can infer at
least two different colonization events of C. canescens from the Northern to the
Southern Hemisphere, one to each of these two southern landmasses. When taxa known
to have originated from the Northern Hemisphere are distributed in two landmasses
within the Southern Hemisphere, it can be either the result of a single colonization of
the Southern Hemisphere followed by subsequent dispersal to the other landmass (e.g.,
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Schuettpelz & Hoot, 2004; Inda et al., 2008; Gussarova et al., 2008; Nie et al., 2012) or
of multiple independent dispersals from the Northern Hemisphere (e.g., Yokoyama et
al., 2000; Escudero et al., 2009; Schaefer et al., 2009; Emadzade et al. 2011; Banasiak
et al., 2013).
Two different mountain ranges connect the Northern and Southern Hemispheres,
allowing migration of cold-adapted plant species by mountain-hopping. The mountain
uplift in Malaysia in the Miocene-Pliocene (10 Ma; Sanmartín & Ronquist, 2004) and
the gradually cooler climate in both hemispheres at that time (Scotese, 2002) could have
facilitated the dispersal of cold-adapted species into the Southern Hemisphere from
Eurasia (Smith, 1981). Similarly, the American cordillera has connected North and
South America since the Late Miocene (Smith, 1986) and it has acted as a corridor for
the dispersal of different organisms (e.g., Moreno et al., 1994; Antonelli & Sanmartín,
2011). The absence of genetic differentiation between the Southern and the Northern
Hemisphere and its diversification time suggest a very recent dispersal of C. canescens
to the Southern Hemisphere. The same pattern of genetic similarity between
Hemispheres was found in another bipolar Carex species (C. arctogena; Villaverde et
al., 2015b), for which direct long-distance dispersal best explains the bipolar
disjunction. A different genetic pattern was, however, found for C. maritima (Villaverde
et al., 2015a), whose populations from the Southern Hemisphere are genetically distinct
from the Northern populations. The obtained results for C. maritima did not allow us to
discern between direct long-distance dispersal or mountain hopping. Likewise, we
consider that the current study is not conclusive enough to be able to distinguish
between mountain-hopping or direct long-distance dispersal to explain C. canescens’
distribution.
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The high colonization capacity and competitiveness of C. canescens
None of the six bipolar species in the genus are known to occur in two landmasses
within the Southern Hemisphere, as well as the Falkland Islands, New Guinea and
Tasmania. The migration to such islands supports the high dispersal and colonization
ability of C. canescens, ranked as the bipolar Carex species with the greatest
distribution. With the exception of C. microglochin, none of the bipolar Carex species
displays standard morphological syndromes for long-distance dispersal (as described by
Higgins et al., 2003). Some dispersal agents might have been involved in the
distribution of C. canescens, such as birds, ocean or wind currents (Nathan et al., 2008;
Gillespie et al. 2012). Rare processes or unusual behaviour of vectors have been
inferred to have dispersed seeds over long distances (Higgins & Richardson, 1999;
Nathan et al., 2002; Higgins et al., 2003; Nathan et al., 2008). In fact, long-distance
dispersal is claimed as a widespread phenomenon in many plant species without
standard morphological syndromes for long-distance dispersal (Carlquist, 1967; Cain et
al., 2000; Higgins et al., 2003; Alsos et al., 2007; Dixon et al., 2009).
Establishment of plants following long-distance dispersal is determined by the
environment and biotic conditions of the host community, as well as by the colonization
capacity and competitiveness of the new hosted species. Our results show that in the
Southern Hemisphere C. canescens occupies a more restricted climatic niche than in the
Northern Hemisphere (Fig. 4 and Appendix S2), but falling within the general
ecological conditions tolerated by the species, which seem to be very wide (Fig. 4).
Furthermore, Carex species are generally highly self-pollinated (Whitkus, 1988;
Ohkawa et al., 2000; Arens et al., 2005; Friedman & Barrett, 2009; Escudero et al.,
2010b, 2013), which could also explain, at least in part, successful establishment after
dispersal (Carlquist, 1983; Baker, 1955). In addition, chromosome rearrangements have
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been shown to be correlated with phenotypic differences, as well as being thought to
enhance fitness in different habitats (Coghlan et al., 2005). Specifically, high
chromosome number evolution is a result of: (i) selection by climatic regime and
ecological strategies; and (ii) neutral processes such as phylogenetic inertia or migration
processes (Escudero et al., 2012, 2013). The high chromosome number variation in C.
canescens (2n = 52-54, 56-58, 60, 62; reviewed in Roalson et al., 2008) might also be a
result of the influence of the climatic environments at different latitudes and distant
regions.
CONCLUSIONS
Our results suggest that C. canescens originated during the Pleistocene and that its
disjunction could be explained by long-distance dispersal from the Northern to the
Southern Hemisphere. Carex canescens could have dispersed at least twice to the
Southern Hemisphere, once to Australia and once to South America, either by
mountain-hopping through the Andes cordillera and Malaysian mountains, by direct
jump or by a combination of both.
ACKNOWLEDGEMENTS
The authors thank to all staff from herbaria CAN, COLO, E, M, MSB, SI, UPOS and
WIN for granting us access to their collections and for providing plant material, E.
Maguilla (Universidad Pablo de Olavide, UPO) and F. Rodríguez-Sánchez (Estación
Biológica de Doñana, EBD-CSIC) for his help with MAXENT analyses, map editing
and valuable comments on the manuscript, M. Puscas (Babes-Bolyai University) for
plant material collections, L. P. Bruederle (University of Colorado, Denver) and P.
Vargas (Real Jardín Botánico de Madrid) for assistance in plant collections, and M.
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Míguez and F. J. Fernández (UPOS) for technical support. This research was supported
by the Spanish Ministry of Science and Technology through the project CGL201238744 and from the Regional Ministry of Economy, Innovation, Science and
Employment of Andalusia through the project RNM-2763.
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Additional Supporting Information may be found in the online version of this article:
Appendix S1 Studied material of Carex canesens, related species and outgroups;
molecular characteristics of the amplified regions; results from the principal
components analysis of 19 bioclimatic variables from the WorldClim database;
description of bioclimatic variables; and AUC values from MAXENT analyses.
Appendix S2 Distribution map of Carex canescens, phylogeny of C. canescens,
boxplots of the most important variables from bioclimatic principal component analyses
and ecological niche models of C. canescens.
254
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BIOSKETCH
Tamara Villaverde is a PhD student at Pablo de Olavide University, Seville (Spain).
Her research is focused on the evolution and phylogeography of angiosperms, with
special interest in the systematics and biogeography of the genus Carex
(Cyperaceae).
Author contributions: M.E. and M.L. conceived the idea; T.V., S.M-B and M.L.
collected the plant material; T.V., M.E. and S.M-B, carried out the lab work and
analysed the data; T.V., M.E. and S.M-B led the writing and drafted the
manuscript, although all authors contributed to its preparation.
255
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Table 1. Divergence dates of clades in Carex section Glareosae.
Divergence dates of clades in Carex section Glareosae presented as the posterior probability
followed by the mean time to the most recent common ancestor in million years ago (Ma) and
the 95% HPD interval obtained from the divergence time analysis of the combined nuclear
(ITS and ETS) and plastid (5’trnK intron and rps16) regions.
Clade
Section Glareosae
C. furva + C. lachenalii + C. glareosa +
C. canescens
C. lachenalii + C. glareosa
C. canescens
C. canescens from South America (2
populations)
256
Posterior
Probability
0.99
Mean
(Ma)
6.55
Min
(Ma)
2.56
Max
(Ma)
10.99
0.98
5.5
1.84
9.17
1
1
1.03
1.17
0.18
0.34
2.14
2.17
0.85
0.05
0
0.17
________________________________________________________________
________________________________________________________________
LISTS OF FIGURE LEGENDS
Figure 1. Distribution map of the sampled populations of C. canescens. The shaded
region denotes the distribution of C. canescens obtained from the World
Checklist of Cyperaceae (Govaerts et al., 2014).
Figure 2. Maximum credibility clade phylogeny of the Bayesian divergence time
analysis considering Carex canescens, other related species in sect. Glareosae
and outgroups using a combined matrix of nuclear (ITS and ETS) and plastid
(5’trnK and rps16) sequences. Node bars represent the 95% highest posterior
density intervals of the divergence time estimates linked to nodes with posterior
probabilities above 0.85 (values above branches) with mean ages inferred for
clades in million years (below branches). Light grey rectangle depicts C.
canescens populations from Northern and Southern Hemisphere; dark grey
rectangle depicts two populations of C. canescens from Argentina.
Figure 3. Haplotype network of concatenated cpDNA sequences of Carex canescens
and C. canescens subsp. disjuncta. Circles represent the five haplotypes found
(H1-H5), lines represent single mutational steps, and small black circles missing
haplotypes. Number of samples per haplotype are indicated in parentheses and
abbreviations after the names correspond to the geographical regions of the
world (Brummitt, 2001).
Figure 4. Scatter plots of the first three components of the Principal components
analysis depicting the position in a climate-niche space of the Carex canescens
sampled populations geographically grouped by Earth’s quadrants (North-East,
grey dots; North-West, pink; South-East, blue; South-West, red).
257
________________________________________________________________
________________________________________________________________
258
________________________________________________________________
________________________________________________________________
259
________________________________________________________________
________________________________________________________________
260
variables; and AUC values from MAXENT analyses.
261
results from the Principal Components Analysis of 19 bioclimatic variables from the WorldClim database; description of bioclimatic
Appendix S1. Studied material of Carex canesens, related species and outgroups; molecular characteristics of the amplified regions;
Tamara Villaverde, Marcial Escudero, Santiago Martín-Bravo and Modesto Luceño
of C. canescens (Cyperaceae)
Two independent dispersals to the Southern Hemisphere to become the most widespread Carex bipolar species: biogeography
Carex bipolar species:
________________________________________________________________
________________________________________________________________
262
Table S.1: List of material studied of species from sect. Glareosae (Carex canescens, C. canescens subsp. disjuncta, C. glareosa, C.
lachenalii, C. furva, C. arcta) and the outgroups (C. macloviana, C. paniculata subsp. paniculata, C. remota and C. maritima)
including population code, coordinates, voucher information and Genbank accessions for markers used for molecular studies.
Population codes correspond to geographical regions of the world (Brummitt, 2001) and population number.
Species
Population Latitude
Longitude
Voucher
Genbank Accesion
code
(ITS, ETS, 5’trnK
intron and rps16
intron)
C. canescens
AGS_1
-50.483197
-72.874399
Argentina: Santa Cruz, Los Glaciares
Forthcoming
National Park. 20-I-2010. J. Starr P14-4
10018 & T. Villaverde (UPOS3935)
C. canescens
AGS_2
-49.205715
-72.955547
Argentina: Santa Cruz, Los Glaciares
Forthcoming
National Park. 21-I-2010. J. Starr 10022/
P18-1 & T. Villaverde (UPOS3939)
C. canescens
AGS_3
-42.97121
-71.582108
Argentina: Chubut, Los Alerces National
Forthcoming
Park. 31-I-2010. J. Starr P24-1 10029 & T.
Villaverde (UPOS3946)
C. canescens
AGS_4
-54.8333333 -68.5
Argentina: Tierra del Fuego, Ushuaia, Tierra Forthcoming
del Fuego National Park. 08-I-2010. S.
Martín-Bravo 7SMB10, P. Vargas & M.
Luceño (UPOS4237)
C. canescens
AGS_5
-41.2579
-71.679915
Argentina: Río Negro, Nahuel Huapi
Forthcoming
National Park. 2-II-2010. J. Starr JS10032
P27-8 & T. Villaverde (UPOS3947)
C. canescens
AGS_6
-54.132279
-68.068818
Argentina: Tierra del Fuego, Río Grande,
Forthcoming
Ona River. 17-I-2010. S. Martín-Bravo
49SMB10, P. Vargas, M. González & M.
Luceño (UPOS4282)
C. canescens
AGS_7
-54.793811
-67.642027
Argentina: Tierra del Fuego, between
Forthcoming
Ushuaia and Tolhuin, Rancho Hambre. 9-I2010. S. Martín-Bravo 15SMB10, P. Vargas,
________________________________________________________________
________________________________________________________________
ASK_1
AUT_1
BEL_1
BUL_1
CAL_1
CHM_1
CLS_1
CLS_2
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
-54.140305
-53.395722
43.913021
38.8715
42.081017
50.253394
47.220106
62.322317
-68.845772
-71.126564
125.736503
-120.113116
23.903942
6.120001
11.629783
-150.094549
263
Chile: Region XII of Magallanes and
Chilean Antarctic, Brunswick Peninsula,
gate of Laguna Parrilar Forest Reserve. J.
Starr P13-7 10017 & T. Villaverde
(UPOS3934)
Chile: Region XII of Magallanes and
Chilean Antarctic, Big Island of Tierra del
Fuego. 27-XII-2005. M. Luceño 17905ML
USA: Alaska, Alaska Range District, Peters
Hills Mountains. 17-VII-1980. V.
Siplivinsky 666 (CAN453336)
Austria: Tirol, Ötztaler Alpen, Sölden. 11VII-1993. E. Vitek 33-11, A. Blab & G.
Dietrich (NSW815997)
Belgium: Hohes-Vann Park, between Eupen
and Mönschav. 29-VI-2008. S. MartínBravo 88SMB08 & M. Escudero
(UPOS3458)
Bulgary: Rhodopians, between Belovo and
Jakoruda. 9-VII-2010. P. Jiménez-Mejías
147PJM10, R. Jiménez Mejías & S. Jiménez
Mejías (UPOS4087)
USA: California, El Dorado Co, El Dorado
National Forest, Grass Lake. 23-VII-1987. J.
Pykälä, D. H. Norris & H. Toivoinen 2922
(BM s.n.)
China: Jilin. J. Jung 1007076 (AJOU)
M. González & M. Luceño (UPOS4245)
EU541865(ITS),
Forthcoming,
Forthcoming
JX644817
Forthcoming
Forthcoming
Forthcoming
Forthcoming
Forthcoming
________________________________________________________________
________________________________________________________________
FIN_1
GER_1
GNL_1
GNL_2
GNL_3
ICE_1
IRK_1
IRK_2
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
13.557863
24.486169
-46.613291
-44.336017
51.723501
57.16667
103.341859
104.55
65.02468333 -19.1181972
60.947449
60.003958
66.98333333 -52.3166667
51.764009
67.906062
GQ469855 (trnk),
EU541836 (rps16),
EU541867(ITS)
Forthcoming,
Forthcoming
Forthcoming
Forthcoming
Forthcoming
EU541833 (rps16),
Forthcoming,
EU541834 (rps16),
264
Russia: Siberia, Region of Lake Baikal,
Forthcoming
Valley of Korolok. 7-VII-1979. H. H. Iltis,
J. C. Coffey & M. F. Denton 504 (NYBG
s.n.)
Russia: Irkutskaya oblast, Valley of
Forthcoming
Bystraya River, west end of Lake Baikal. 14VII-1979. H. H. Iltis, J. C. Coffey & M. F.
Denton 833 (NYBG s.n.)
Finland: Pallas-Ounastunturi National Park.
4-VIII-2005. M. Luceño 2005ML & M.
Guzmán (UPOS314)
Germany: Brandenburg. VI-1903. R. Gross
s.n. (NSW816004)
Denmark: Greenland, Ikertoq, Maligiaq,
Itivneq. 26-27-VII-1978. C. Bay 78-1623, B.
Fredskild, S. Hanfgarn & P. F. Moller
(CAN488181)
Denmark: Greenland, Qassiarsuk,
Tassiussaq fjord. 4-VIII-2007. M. Luceño
3207ML & M. Guzmán (UPOS4471)
Denmark: Greenland, Qaleragdlit fjord. 5VIII-2007. M. Luceño 4407ML & M.
Guzmán (UPOS4481)
Iceland: between Storaborg and Mosfell. 6VIII-2006. M. Luceño 3206ML
(UPOS1941)
& R. Álvarez (UPOS0212)
________________________________________________________________
________________________________________________________________
KAM_1
KAM_2
KRA_1
LAB_1
MAS_1
NFL_1
NFL_2
NOR_1
NSW
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
159.116506
265
Russia: Kamchatka Peninsula, Pacific Ocean
coast, SE of Nalychevo. 29-VII-2003. A.
Farjon & G. Frisor 653 (E00270618)
55.913997
158.649107 Russia: Kamchatka Peninsula, Bristraya
River, Esso. 23-VII-2003. R. K. Brummitt &
G. Frisor 20883 (E00270610)
56.908423
96.518853
Russia: Krasnoyarsk Territory, Abansky
District. 27-VII-1960. Pavlova & T. Litvin
(NYBG s.n.)
53.06666667 -66.9666667 Canada: Newfoundland and Labrador, Carol
Lake, North end. 17-IX-1953. F. Harper
4031 (CAN226641)
41.678902
-70.489216
USA: Massachusetts, Sandwich, Boggy
swale. 8-VI-1932. C. A. Weatherby, U. F.
Weatherby, L. B. Smith & R. C. Smith s.n.
(NSW815995)
53.051214
-57.446935
Canada: Newfoundland and Labrador. Route
13 before Trans-Labrador (Hwy 510). 24VII-2008. R. Piñeiro 80RPP08 & M.
Escudero (UPOS s.n.)
51.421133
-55.616348
Canada: Newfoundland and Labrador, Strait
of Belle District, on road to Goose Cove. 19VIII-1992. A. Bouchard 92389, S. Hay & L.
Brouillet (CAN566828)
68.160421
13.749333
Norway: Lofoten Islands, Kallen, Kabelvag,
Svolvaer. 29-VII-2009. M. Escudero
61ME09, R. Piñeiro & M. Pimentel (UPOS
s.n.)
-36.3
148.3833333 Australia: New South Wales, Kosciuszko
National Park, Schlink Pass. 14-II-1985. K.
L. Wilson 6151 (NSW259564)
53.133376
-
Forthcoming
Forthcoming
Forthcoming
Forthcoming
Forthcoming
Forthcoming
Forthcoming
Forthcoming
________________________________________________________________
________________________________________________________________
NSW
NSW
NSW_1
NSW_2
NSW_3
NWT_1
NWT_2
QUE_1
ROM_1
SCO_1
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
56.366423
45.602362
-3.217611
24.61413
148.35
266
Romania: Carpathians, Fagaras Mountains,
Bâle Lake. 20-VII-2013. M. Puscas s.n. (CL
s.n.)
United Kingdom: Scotland, Perth. Glen
Girnaig. Altt na Core Lagain. 12-VII-1989.
A. C. Jermy 277960700 (BM18314)
Australia: New South Wales, Kosciuszko
National Park, near Spencer Creek. 23-I1975. G. Thompson 2260 (NSW656969)
-36.4163889 148.4027778 Australia: New South Wales, Kosciuszko
National Park, Blue Cow. 28-I-1977. G.
Thompson 2714. (NSW656966)
-36.432601
148.274963 Australia: New South Wales, Kosciusko,
Karlway Morraine Creek, Mount Northcott.
15-II-1970. C. Totterdell 73 (CANB343808)
-36.431037
148.33854
Australia: New South Wales, Kangaroo
Range, Charlotte. Pass to Kosciusko. 27-II1960. A. Gray 772 (CANB76959)
-36.501272
148.501272 Australia: New South Wales, Kosciusko,
Lower Twyneham Cirque. 11-II-1962.
Walker ANU-189 (CANB104756)
63.29613889 -129.831917 Canada: Northwest Territories, Canol Road
(Hwy 5), MacMillan Pass. 17-VII- 2004. P.
M. Peterson 18645, J. M. Saarela & S. F.
Smith. (CAN590896)
64.900522
-125.571633 Canada: Northwest Terriotories, Mackenzie
District, Fort Norman. 21-VII-1951. A. A.
Lindsey 365a (CAN216063)
46.15153889 -74.5848694 Canada, Quebec. 4-VIII-1997. A. Bond s.n.
(MTMG s.n.)
-36.4166667
Forthcoming
Forthcoming
AY757406 (ITS),
AY757384 (ETS)
Forthcoming
Forthcoming
Forthcoming
Forthcoming
Forthcoming
-
-
________________________________________________________________
________________________________________________________________
SCO_2
SPA_1
SPA_2
SPA_3
SWE_1
SWE_2
TCS_1
TCS_2
UTA_1
VIC
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
C. canescens
-36.851064
40.807997
39.680281
40.515209
58.67097
67.835408
42.242064
41.817486
42.323944
56.670389
147.343468
-109.511629
45.731723
44.184896
16.938393
67.835408
-6.795057
0.639162
-3.534748
-5.23363
267
United Kingdom: Scotland, Highlands
between Tynohumy and Glencoe. 25-VI2007. S. Martín-Bravo 140SMB07, P.
Jiménez-Mejías & M. Luceño (UPOS s.n.)
Spain: Burgos. Neila, Ducks Lagoon. 19VII-2000. M. Luceño 44000ML & J. Martín
(UPOS0087)
Spain: Lérida, Baños de Tredos. 2-VIII-2004
J. M. Marín 7604JMM, M. Luceño & L. E.
Bendrell (UPOS s.n.)
Spain: Zamora, Peña Trevinca, Laguna de
Cubillas. 28-VII-2007. S. Martín-Bravo
152SMB07, P. Jiménez-Mejías & I. Pulgar
(UPOS s.n.)
Sweden: Torne Lappmark, Jukkasjarvi. 22VII-1946. E. Nyholm s.n. (UPOS s.n.)
Sweden: Buskhyttan, Närke. 23-VI-1949. G.
Kjellmert s.n. (UPOS s.n.)
Armenia: Mt. Aragats, Aragatsotn, Aragats.
28-VI-2008. G. Fayuush et al. 08-1381
(NYBG s.n.)
Armenia: Sgunik Province, between Sisian
and Yerevan, Ughedzor Pass. 16-VI-2007.
Oganesian et al. 07-0725 (NYBG s.n.)
USA: Utah, Daggett County, Green Lake. 3VI-1986. V. E. McNeilus s.n. (NSW815990)
Australia: Victoria, Alpine National Park,
Mt Nelse. 13-I-1982. S. J. Forbes 783, R.
Adair & M. Gray. (NSW657404).
-
Forthcoming
Forthcoming
Forthcoming
Forthcoming
Forthcoming
Forthcoming
Forthcoming
EU541835 (rps16)
Forthcoming,
Forthcoming
________________________________________________________________
________________________________________________________________
-
-
-
C. lachenalli
C. furva
C. arcta
-
-
-
-
-
-135.790132
C. glareosa
MAS_1
63.805779
22.324799
-
YUK_1
C. canescens
42.709597
-
-
YUG_1
C. canescens
-
148.313587
-
WIN_1
C. canescens
-36.405835
146.273161
-
VIC_1
C. canescens
-37.846463
C. canescens
subsp.
disjuncta
C. glareosa
VIC
C. canescens
268
Australia: Victoria, Baw Baw Mount. 22-I1969. A. S. Johnson. (NSW143407)
Australia: Victoria, Snowfields, Bogong
High Plains. 18-I-1988. N. G. Walsh 1939,
P. S. Short & M. C. Looker (UPOS005029)
USA: Wisconsin. Hipp et al. 587 (WIS s.n.).
Unpublished.
Serbia: Rhodopians, Vlasina Lake,
Vlasinsko Jezero. 20-VI-2010. P. JiménezMejías 80PJM10, R. Jiménez & S. Jiménez
(UPOS4722)
Canada: Yukon, Vicinity of Halfway Lake,
North of Mayo. 29-VI-1967. R. T. Porsild
639 (CAN312366)
USA: Massachusetts, Berkshire County,
Thomas Pond. 9-VI-2001. T. M. Zebryk
7312 (NSW815989)
United States: Alaska, Bethel. Parker 17823
(MOR)
Iceland: Djúpivogur, Berufjördur. 9-VIII2006. M. Luceño & M. Guzman 7206ML
(UPOS1983)
Norway: Kvaenangsfjellet. 6-VIII-2005. M.
Luceño & M. Guzman, 5305ML
(UPOS354)
Spain: Granada, Capileira, Sierra Nevada
National Park. 08/VIII/2013. E. Maguilla &
J. M. G. Cobos 31EMS13(1) (UPOS5132)
USA: Minnesota, Clearwater County, along
County Route 39. 22-VI-1991. V. E.
McNeilus 91-565 (NSW815988)
Forthcoming
KP980522 (ITS),
KP980331 (ETS)
EU541869 (ITS)
EU541871 (ITS)
JN903115 (ETS)
Forthcoming
Forthcoming
Forthcoming
DQ460952 (ETS)
Forthcoming
-
________________________________________________________________
________________________________________________________________
-
-
-
C.maritima
-
-
-
C. paniculata
subsp.
paniculata
C. remota
-
-
C. macloviana
C. macloviana
269
Chile: between Punta Arenas and Puerto
Natales. 29-XII-2005. M. Luceño & R.
Alvarez 18605ML (UPOS1804)
Unitated States: Wyoming. A. L. Hipp, Hipp
1893 (WIS)
Greece, Épiro, Ioannina, Kambos Despoti.
23-VI-2008. M. Luceño 0808ML
(UPOS3419)
Montenegro, High Dinarics, Durmitor
National Park. 17-VII-2010. P. JiménezMejías 198PJM10 (UPOS4006)
Switzerland: Zermatt. 11-VIII-2012. M.
Luceño & M. Guzmán 25ML12 2/2
(UPOS4997)
Forthcoming
Forthcoming
KP980427 (ITS),
KP980240 (ETS)
DQ460993
EU541862
________________________________________________________________
________________________________________________________________
28
0
53.50%
613
505-610
45.3%
94.2%
55
39
0
58.40%
GRT+G / HKY / GTR + G
Aligned length (bp)
% Identical sites
% Pairwise identity
Variable characters
characters
Number of informative
indels
Mean % G+C content
Substitution model
270
HKY + I
69
98.3%
79.6%
214-557
560
41
56
Total number of sequences
in the alignment
Starr et al. (2003)
External transcribed spacer
of ribosomal RNA
Blattner (1999), White (1990)
Internal transcribed spacers 1 and 2
and 5.8S ribosomal RNA
ETS1f - 18S-R
References
Description
ITS1/ 5.8S/ ITS2
JC + I
21.70%
3
5
11
97.6%
61.5%
439-646
659
Escudero & Luceño
(2009)
47
Plastid intergenic
spacer
5'trnKCarexF5'trnkCarexR
GTR
25.30%
0
13
21
91.5%
91.5%
422-796
801
Oxelman et al.
(1997)
43
Plastid intergenic
spacer
rps16F-rpsR
Table S.2: Characteristics of the DNA regions sequenced for the complete datasets including Carex canescens, related species in section Glareosae
and outrgroups.
Complete dataset
________________________________________________________________
________________________________________________________________
%
BIO19
BIO18
BIO17
BIO16
BIO15
BIO14
BIO13
BIO12
BIO11
BIO10
BIO9
BIO8
BIO7
BIO6
BIO5
BIO4
BIO3
BIO2
BIO1
0.0
0.0
0.1
0.1
0.0
0.1
-0.3
-0.3
-0.2
-0.3
15.7%
0.1
-0.3
48.1%
0.0
0.0
-0.3
-0.2
-0.3
-0.3
-0.2
-0.5
0.0
-0.2
0.2
-0.3
-0.1
-0.1
0.3
-0.5
0.1
-0.3
-0.2
0.0
-0.3
0.2
0.3
-0.4
-0.2
-0.2
PC2
PC1
14.6%
0.2
0.3
0.2
0.3
0.2
0.2
0.3
0.3
-0.2
0.1
-0.1
0.0
0.3
-0.3
0.2
0.3
-0.1
0.2
-0.1
PC3
10.5%
-0.2
0.3
0.2
-0.1
-0.4
0.3
-0.1
0.0
0.0
0.2
-0.2
0.3
0.0
0.0
0.0
0.1
-0.4
-0.3
0.1
PC4
5.5%
0.0
-0.1
0.3
-0.2
-0.6
0.3
-0.2
0.0
-0.1
0.0
0.1
-0.4
0.2
-0.2
0.1
0.1
0.2
0.4
-0.1
PC5
3.0%
0.3
-0.4
0.0
0.0
0.0
0.0
0.0
0.0
-0.1
0.2
0.2
-0.4
0.1
0.0
0.1
0.2
-0.6
-0.3
0.0
PC6
1.2%
0.5
-0.5
0.0
0.1
-0.4
0.0
0.1
0.1
-0.1
-0.1
-0.3
0.5
0.0
0.0
0.0
0.0
0.1
0.0
-0.1
PC7
0.6%
0.0
0.1
-0.2
0.1
-0.2
-0.3
0.1
0.0
0.1
0.1
-0.7
-0.5
0.0
0.1
0.1
-0.1
0.1
-0.1
0.2
PC8
0.4%
0.0
-0.3
0.4
-0.2
0.4
0.4
-0.2
0.0
0.0
0.2
-0.4
-0.1
-0.1
0.0
-0.1
0.1
0.3
-0.2
0.1
PC9
271
0.2%
0.1
-0.1
0.2
-0.1
0.2
0.1
0.0
0.0
0.2
-0.3
-0.2
0.0
-0.1
0.1
0.1
-0.4
-0.5
0.5
0.0
PC10
0.1%
0.6
0.3
0.0
-0.2
0.1
-0.1
-0.6
0.1
-0.1
-0.1
0.0
0.0
-0.1
0.2
0.2
0.1
0.0
-0.1
-0.2
PC11
0.1%
0.2
0.1
0.0
0.0
0.0
-0.1
-0.2
0.0
0.1
0.1
0.0
0.0
0.1
-0.4
-0.6
0.0
-0.1
0.2
0.6
PC12
0.0%
-0.3
-0.1
0.6
0.0
0.0
-0.6
-0.1
0.4
0.0
0.0
0.0
0.0
0.0
0.1
0.0
0.1
0.0
0.0
0.0
PC13
0.0%
0.2
0.1
0.2
-0.5
0.0
-0.2
0.5
-0.4
0.0
0.2
0.0
0.0
-0.2
0.1
-0.2
0.1
0.0
0.2
-0.2
PC14
0.0%
0.1
0.1
0.2
-0.3
0.0
-0.1
0.2
-0.2
0.0
-0.3
0.0
0.0
0.4
-0.3
0.4
-0.4
0.1
-0.3
0.2
PC15
0.0%
0.0
0.0
-0.3
-0.5
0.0
0.1
0.1
0.6
0.2
0.2
0.0
0.0
0.1
-0.1
0.0
-0.2
0.0
0.0
-0.2
PC16
0.0%
0.0
0.0
-0.2
-0.3
0.0
0.1
0.2
0.2
-0.4
-0.4
0.0
0.0
-0.2
0.3
0.1
0.3
0.0
0.1
0.5
PC17
0.0%
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
-0.7
0.3
0.0
0.0
-0.1
0.1
0.0
-0.6
0.0
0.1
0.0
PC18
Table S.3: Loadings matrix obtained by the Principal Components Analysis of 19 bioclimatic variables on Carex canescens and the percentage of
variance explained by each principal component.
0.0%
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.7
0.6
-0.3
0.0
0.0
0.0
0.0
PC19
________________________________________________________________
________________________________________________________________
BIO 1
BIO 2
BIO 3
BIO 4
BIO 5
BIO 6
BIO 7
BIO 8
BIO 9
BIO 10
BIO 11
BIO 12
BIO 13
BIO 14
BIO 15
BIO 16
BIO 17
BIO 18
BIO 19
272
Description
mean diurnal temperature range [mean of monthly (maximum temperature - minimum temperature)]
isothermality (BIO2 / BIO7 x 100)
maximum temperature of the coldest month;
temperature range (BIO6 - BIO5)
Table S.4: Bioclimatic variables used. Units of bioclimatic variables are °C × 10 for temperature (excluding BIO 4 that was
calculated based on K × 10 to deal with negative temperatures) and mm for precipitation.
________________________________________________________________
________________________________________________________________
BIO6
BIO6
0.890 ± 0.001
0.891 ± 0.001
0.992 ± 0.002
0.996 ± 0.001
0.995 ± 0.002
All samples
Samples from the Northern
Hemisphere
Samples from the Southern
Hemisphere
Hemisphere – only South
American
Hemisphere – only
Australasian
BIO6
BIO1
AUC ± SD
C. canescens groups
Environmental
variables that
contributed most and
the most important
environmental
variable when used
alone
BIO1
Table S.5: Area under de curve (AUC) ± standard deviation (SD) and
the variables that contributed the most to explain MAXENT models
under WorldClim database layers and the most important when used
alone analyses, for each group of Carex canescens.
273
________________________________________________________________
________________________________________________________________
274
White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for
phylogenetics. PCR protocols: A guide to methods and applications (ed. by M. Innis, D. Gelfand, D. Sninsky, and T. White),
Academic Press, Orlando, Florida, pp. 315–322.
Starr, J.R., Harris, S.A. & Simpson, D.A. (2003) Potential of the 5 and 3 ends of intergenic spacer (IGS) of rDNA in the Cyperaceae:
new sequences for lower-level phylogenies in sedges with an example from Uncinia Pers. International Journal of Plant
Sciences, 164, 213–227.
Escudero, M. & Luceño, M. (2009) Systematics and evolution of Carex sects. Spirostachyae and Elatae (Cyperaceae). Plant
Brummitt R.K. (2001) World geographical scheme for recording plant distributions, 2nd ed. Hunt Institute for Botanical
Documentation, Pittsburgh, Pennsylvania, USA.
Blattner, F.R. (1999) Direct amplification of the entire ITS region from poorly preserved plant material using recombinant PCR.
Biotechniques, 27, 1180–1186.
References
________________________________________________________________
________________________________________________________________
Carex
bipolar species: biogeography of C. canescens
________________________________________________________________
________________________________________________________________
Two independent dispersals to the Southern Hemisphere to become the most widespread
Carex bipolar species: biogeography of C. canescens (Cyperaceae)
Tamara Villaverde, Marcial Escudero, Santiago Martín-Bravo and Modesto Luceño
Appendix S2. Distribution map of Carex canescens, phylogeny of C. canescens, boxplots
of the most important variables from the bioclimatic PCA and ecological niche models of
Carex canescens.
Figure S.1. Distribution map of the sampled populations of C. canescens obtained from
Global Biodiversity Information Facility data portal (http://www.gbif.org/, downloaded 12
February 2015; black dots). The grey region denotes the distribution of C. canescens
obtained from the World Checklist of Cyperaceae (Govaerts et al., 2014).
Figure S.2. Majority rule (50%) consensus tree derived from the Bayesian analysis of
Carex canescens and the related species in sect. Glareosae inferred from the combined
nuclear (ITS and ETS) and plastid (5’trnK and rps16) matrix. Carex macloviana, C.
remota, and C. paniculata were used as outgroups. Numbers above and below of the
branches represent the Bayesian posterior probability (>0.9 PP) and bootstrap (>60% BS)
values of the Maximum likelihood analysis, respectively. A grey rectangle highlights the C.
canescens samples of the Southern Hemisphere. Abbreviations after the names correspond
to the geographical regions of the world (Brummitt, 2001) and to the population number.
275
Carex
________________________________________________________________
________________________________________________________________
Figure S.3. Boxplots of the most important variables in principal components analysis
using populations from the Northern Hemisphere (NH), Australia (SH_AU) and South
America (SH_SA) obtained from Global Biodiversity Information Facility data portal
(http://www.gbif.org/, downloaded 12 February 2015).
Figure S.4. Ecological niche models of Carex canescens geographic groups. Projections of
the model to the current climatic conditions (~1950–2000). Colours correspond to habitat
suitability with values ranging from 0 to 1 (from white to red, respectively). (a) C.
canescens; (b) C. canescens populations from the Northern Hemisphere; (c) C. canescens
populations from the Southern Hemisphere.
276
________________________________________________________________
Carex
________________________________________________________________
277
Carex
________________________________________________________________
________________________________________________________________
278
Carex
________________________________________________________________
________________________________________________________________
279
Carex
________________________________________________________________
________________________________________________________________
280
Carex
________________________________________________________________
________________________________________________________________
281
Carex
________________________________________________________________
________________________________________________________________
References
Brummitt, R.K. (2001) World geographical scheme for recording plant distributions, 2nd
ed. Hunt Institute for Botanical Documentation, Pittsburgh, Pennsylvania, USA.
Govaerts, R., Koopman, J., Simpson, D., Goetghebeur, P., Wilson, K., Egorova, T. &
Bruhl, J. (2014) World Checklist of Cyperaceae. Facilitated by the Royal Botanic Gardens,
Kew. Published on the Internet; http://apps.kew.org/wcsp/ (Retrieved 2014-11-28).
282
Chapter 6
General discussion and conclusions
283
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Chapter 6. General discussion and conclusions
Carex arctogena is a bipolar species
Carex capitata and C. arcotgena are found to be morphologically different and populations
from South America correspond to C. arctogena. Therefore, Carex antarctogena should be
treated as a synonym of C. arctogena. Morphological variability, which also corresponds
with geographical distribution and ecological differentiation (Chapters 2 and 3), was found
within populations from western North America and we suggest the description of one
species and two subspecies: Carex cayouetteana, C. cayouetteana subsp. bajasierra and C.
cayouetteana subsp. altasierra. These three new taxa diverged during the Pleistocene [0.81
million years ago (Ma); 95% highest posterior density (HPD). 0.19- 1.66 Ma], a time of
climatic changes in the Northern Hemisphere that affected plant distributions in both North
America and Eurasia (e.g. Tremblay & Schoen, 1999; Abbott et al., 2000; Alsos et al.,
2005; Eidesen et al., 2007).
Contrary to what might have happened in Europe, where mountain chains are East-West
oriented, the advance and the retreat of the ice sheet during glacial periods could have had a
less severe effect shifting species distribution in latitude during climate changes, due to the
continuous mountains chains in a North-South direction (Albach et al., 2006) and to the
vast area available below the ice sheet in North America. Carex cayouetteana subsp.
bajasierra might have adapted to boreal habitats where it occurs now, whilst Carex
cayouetteana subsp. altasierra might have been isolated in tundra habitats in southern
California.
Population fragmentation during glacial periods may have led to the formation of new
species (Abbott & Brochmann, 2003) and their small population sizes could have led to the
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acquisition of morphological traits at a faster rate than in large populations (Vanderpoorten
& Shaw, 2010). A similar pattern appears to have occurred in the C. aquatilis Wahlenb. C. lenticularis Michx. group (section Phagocystis, Dragon & Barrington, (2009) where
species ecological specialization and the Quaternary geological history of North America,
split the group in different lineages
The lack of unique characters in chloroplast data set of the new taxa here described could
be due to insufficient phylogenetic signal or incomplete lineage sorting, as suggested for
other Carex species (e.g. Hipp et al., 2006; King & Roalson, 2008; Roalson & Friar, 2008).
Likewise, a multidisciplinary study of the C. backii complex (sect. Phyllostachyae),
revealed that it was composed by three different species (Saarela & Ford, 2001), C.
saximontana Mack., C. cordillerana Saarela & Ford and C. latebracteata Waterf. Although
all quantitative characters measured in the morphological study of C. saximontana, C.
cordillerana overlapped, anatomic, micromorphologic and phytogeographic characters
showed enough differences to recognize the three taxa at the species level which was later
supported by molecular studies (Ford et al., 2009). As the three new taxa here described are
not part of independent lineages, we suggest that studies at the population level could help
to reveal its genetic differentiation.
Long-distance dispersal as the main factor underlying bipolar disjunctions in Carex
Two hypotheses can be clearly rejected for all bipolar Carex species: vicariance and
convergent evolution. The vicariance hypothesis can be rejected because the fragmentation
of the trans-tropical highland bridges during the Mesozoic Era (from the early Jurassic, 195
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Ma; Scotese et al., 1988; Figure 3 in Chapter 1) is older than the time of divergence of the
Cyperaceae family (82.6 Ma, 95% highest posterior density, HPD: 75.9–85.6 Ma; Escudero
& Hipp, 2013). Therefore, bipolar disjunctions in Carex are not due to vicariance as the
result of area fragmentation. Moreover, the same reasoning may be applied for all the
remaining bipolar species, as the divergence time estimations for their respective families
are younger than the early Jurassic (see Table 1), except for Huperzia selago, which its
family (Lycopodiaceae) diverged during the late Devonian – early Carboniferous (329.1 –
372.9 Ma).
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Table 1. Divergence time estimated for the families including bipolar species and
corresponding reference.
Family
Lycopodiaceae
Epoch
Late Devonian – Early
Carboniferous (329,1 – 372,9 Ma)
Hymenophyllaceae Middle Jurassic (ca. 155,5 – 191,7
Ma)
Polygonaceae
Early to late Cretaceous (ca.
103,1– 125,0 Ma)
Caryophyllaceae
Early Cretaceous ( 111– 104 Ma)
Reference
Wikström & Kenrick (2001)
Ranunculaceae
Late Jurassic - Early Cretaceous
(131– 147 Ma)
Wikström et al. (2001); Zeng et al.
(2014)
Plantaginaceae
Miocene (7 – 11 Ma)
Li et al. (2014)
Plumbaginaceae
Lledó et al., 2005
Gentianaceae
Pliocene - Quaternary (5 - 2,5
Ma)
Late Cretaceous (83– 89 Ma)
Scrophulariaceae
Miocene (ca. 10 Ma)
Verboom et al. (2009)
Juncaginaceae
Miocene (ca. 10 Ma)
Janssen & Bremer (2004); von
Mering, (2013)
Poaceae
Early Cretaceous (113– 117 Ma)
Janssen & Bremer (2004)
Cyperaceae
Late Cretaceous (65.5–55.8 Ma)
Escudero & Hipp (2013)
Hennequin et al. (2008)
Schuster et al. (2013)
Winkstrom et al. (2001); Zeng et
al. (2014)
Wikström et al. (2001); Zeng et al.
(2014)
All Carex bipolar species share an immediate common ancestor for Northern and Southern
Hemispheres populations (Escudero et al., 2010a). Carex microglochin was retrieved as
polyphyletic in nuclear and plastid analyses (Escudero et al., 2010): two samples from
Chile appeared together with C. pulicaris and C. macrostyla in a strongly supported and
phylogenetically distant clade from the remaining five samples (Iceland, Norway,
Greenland), which grouped with Uncinia lechleriana, C. pauciflora, and C. curvula. Carex
microglochin samples from the Northern and Southern Hemisphere were also studied by
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Starr et al. (2008) and were retrieved as polyphyletic too, which leaded these authors to the
conclusion that it may be a consequence of hybridization, pseudogenes, or other factors.
Later on, it has been known that those populations from Chile were misidentified samples
of C. camptoglochin V. I. Krecz. (M. Luceño, personal communication). Carex
microglochin and C. camptoglochin differ both morphologically and ecologically, growing
sympatrically in both the northern and southern parts of South America, but C.
camptoglochin is restricted to South America and therefore is not a bipolar species
(Wheeler & Guaglianone, 2003). Therefore, we can reject the convergent evolution
hypothesis for all Carex bipolar species.
From the results of our work, the only hypothesis that cannot be rejected for any of the
bipolar Carex species is long-distance dispersal. Although long-distance dispersal
hypohtesis is not falsifiable for any taxon (i.e. distribution of all species could be explained
by dispersal), studies with phylogenetic reconstruction coupled with divergence time
estimation analyses have indicated that long-distance dispersal has played a major role in
shaping species distributions with respect to what previously thought (de Queiroz, 2005;
Michalak et al., 2010; Renner et al., 2010). Even traditional, paradigmatic examples of taxa
with a vicariant distribution, such as Araucaria or Nothofagus have been demonstrated
achieved part of its distribution by long-distance dispersal (Swenson et al., 2001; Cook &
Crisp, 2005). Therefore, although long-distance dispersal hypothesis is not rejectable,
vicariance hypothesis can be falsified and thus, dispersal would be support by default (de
Queiroz, 2005). Many studies comparing multiple taxa do not support vicariance
hypothesis for their disjunct distributions but dispersal [e.g. in South Africa (Galley &
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Linder, 2006); in New Zealand (Winkworth et al., 2005; Waters & Craw, 2006); in
Madagascar (Yoder and Nowak, 2006)].
Long-distance dispersal may have been either achieved by mountain-hopping (‘stepping
stones’) or by a direct event (a ‘giant leap’). This could have occurred during some of the
last cold periods at the end of the Pliocene (5.3 – 2.6 Ma) or in the Pleistocene (2.6 – 0.01
Ma), when the polar regions in both hemispheres recurrently expanded (Raven, 1963; Ball,
1990), or even at present times. Divergence times of the clades where the bipolar species
studied by us are found fall in the late Miocene to early Pleistocene in C. arctogena (5 Ma;
95% HPD: 2.01 – 8.03 Ma); middle–late Pliocene to early–middle Pleistocene in C.
maritima (0.23 Ma; 95% HPD: 0.03– 0.51 Ma); and during the Pleistocene in C. canescens
(1.17 Ma; 95% HPD: 0.34– 2.17 Ma; Figure 1). These ages are therefore embraced within
periods in which major climatic changes expanded polar regions in both hemispheres.
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Figure 1. Combined maximum-credibility-clade partial phylogenies from the Bayesian
divergence-time analysis of the studied Carex bipolar species (see Chapters 3, 4 and 5 for
details). Node bars represent the 95% highest posterior density intervals for the divergencetime estimates of nodes and vertical color bars highlight these intervals for species
divergence ages (C. arctogena, blue; C. canescens, green; and C. maritima, yellow).
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Geological and climatic changes since the Miocene that allowed Northern and Southern
Hemisphere connections for bipolar species
Since the late Cenozoic, and particularly since the Miocene (23 Ma) the climate has
suffered significant variations related to various causes such as continental displacement
due to plate tectonics, modification on the concentration of greenhouse gases in the lower
atmosphere and changes in astronomical parameters (e.g. eccentricity of the Earth orbit,
obliquity of the planetary axis and equinoctial precession; Rabassa et al., 2005). All these
changes led to climatic cycles of cold and warm periods and the development of planetary
ice ages since the Miocene (Rabassa et al., 2005; Rabassa & Coronato, 2009).
Geologically, different uplifts occurred since the Miocene. In Australasia, there is a system
of island arcs that goes from the eastern side of Australia to northern Australia and New
Guinea and links the southwestern Pacific region with Indonesia. These mountain belts are
the result of multiple collisions during the last 40 (million years) My, and particularly
during the last 25 My, and created a range of ca. 15.000 km with summits well above 4000
m (Figure. 2; Audley-Charles, 1991).
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Figure 2. Island-arc systems linked to New Guinea and associated basins. Abbreviation:
S.F.Z., Sorong fault zone. Figure taken from Audley-Charles (1991).
In South America, the uplift of the central Andes (Earth’s second largest mountain belt) is
the result of an oceanic lithosphere subducted beneath continental lithosphere that started
its uplift 70-50 Ma (McQuarrie et al., 2005). In this area, there is the drained Altiplano
basin flanked by the Western and Eastern Cordilleras, with peak elevations exceeding 6000
m. Since the beginning of the Miocene (23 Ma), the uplift of the Andes changed
dramatically the South American continent (e.g. it formed the only barrier to atmospheric
circulation in the Southern Hemisphere; Lenters et al., 1995). The central Andean plateau
probably started its elevation 20 Ma (McQuarrie et al., 2005), during the early Miocene, at
an age that coincides with the diversification of the first montane plant and animal genera
(reviewed in Hoorn et al., 2010). Sedimentology and carbon istoypes in the Altiplano and
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Eastern Cordillera suggest that the central Altiplano became more arid 10-6 Mya (middlelate Miocene, Quade et al., 2007), and it correspond to a time when the plateau experienced
other uplifts (Garzione et al., 2008; Hoorn et al., 2010; Figure 3-F). During this time, an
extensive migration occurred (known as the Great American Biotic Interchange, GABI) and
the new montane habitats in the Andes were colonized by taxa from North America (Hoorn
et al., 201). Therefore, since the divergence of the bipolar species studied, there have been
different mountain ranges allowing the connection between the Northern and Southern
Hemisphere.
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Figure 3. Paleogeographic maps from 65 to < 2.5 Mya (modified from Hoorn et al.,
2010). (A) Amazonia once extended over most of northern South America. Breakup of the
Pacific plates changed the geography and the Andes started uplifting. (B) The Andes
continued to rise with the main drainage toward the northwest. (C) Mountain building in
the Central and Northern Andes (ca. 12 Ma). (D) Uplifts of the Northern Andes. (E)
Closing of Panama Isthmus and start of GABI. (F) Quaternary.
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Direct long-distance dispersal vs. mountain-hopping
Since the Miocene, the Earth has been going through several ice ages that might have
affected plant distributions. Two different mountain ranges connect the Northern and
Southern Hemispheres, allowing migration of cold-adapted plant species by mountainhopping. First, a route connecting North and South America through the American
cordillera has been in place since the late Miocene (ca. 12 Ma; Smith, 1986). Then, a
gradual uplift of the cordillera during the late Pliocene created the high mountainous
environment with a much colder climate later on during the Pleistocene compared to that
incident today at the same latitudes and elevations (van der Hammen, 1974). This route has
acted as a corridor for the dispersal of different organisms (e.g. Moreno et al., 1994;
Antonelli & Sanmartín, 2011). Second, the mountain uplift in Malaysia in the MiocenePliocene (10 Ma; Sanmartín & Ronquist, 2004) and the gradually cooler climate in both
hemispheres at that time (Scotese, 2004) could have facilitated the dispersal of coldadapted species into the Southern Hemisphere (Smith, 1981).
For Carex species, no ecophysiological adaptations to cross the short-day conditions of the
tropical alpine environment seem to be necessary (Heide, 2002), but we are not aware of
any published fossil records or any other evidence for the occurrence of C. arctogena, C.
canescens or C. maritima in many vast areas between northern North America and southern
South America, or between Eurasia and Australia. If C. arctogena or C. canescens had
migrated to South America and/or Australia by the slow and gradual means predicted by
mountain-hopping, we would expect that such a process would have left a trace of genetic
differences in the plastid loci of populations from both hemispheres (Brochmann et al.,
2003; Scotland, 2011). Although we cannot completely reject the mountain-hopping
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hypothesis, the absence of genetic variability between populations of C. arctogena and C.
canescens from both hemispheres and their recent diversification times fit better with a
recent and direct long-distance dispersal. In congruence, direct long-distance dispersal has
been shown to be remarkably frequent in some other species of Cyperaceae (e.g. Viljoen et
al., 2013).
In the case of C. maritima, its genetic structure allows us to support both a direct longdistance dispersal or mountain-hopping. In the case of direct long-distance dispersal to the
Southern Hemisphere, it might be an older event of dispersal than in C. arctogena and C.
canescens due to the detected genetic differences between Hemispheres. It could have
arrived to South America and differentiated genetically with subsequent northward or
southward colonization along the Andes. In the case of mountain-hopping migration, it
might have occurred since the early Pleistocene, with a subsequent extinction of most of the
northern South American intermediate populations.
In conclusion, our results seem to suggest that C. arctogena and, maybe, C. canescens
could have achieved its current bipolar distribution through direct long-distance dispersal.
For the particular case of C. maritima, we conclude that the bipolar disjunction could have
been originated either by mountain-hopping along the American cordillera or through direct
long-distance dispersal.
North to South long-distance dispersal
The patterns of genetic diversity found in the three bipolar Carex species studied points to
North-to-South as the prevalent direction in bipolar long-distance dispersals between
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Hemispheres. The most widely distributed haplotypes were always found throughout the
Northern Hemisphere and comprised the highest number of haplotype connections, which
implies under the coalescent theory that they amount to the ancestral haplotypes (Posada &
Crandall, 2001; Figure 4). Moreover, the sections to which these bipolar species are
ascribed (sect. Capituligereae, C. arctogena; sect. Glareosae, C. canescens; sect. Foetidae,
C. maritima) have the majority of their species distributed in the Northern Hemisphere, a
fact that supports a northern origin and subsequent North-to-South long-distance dispersal.
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◄ Figure 4. Combined TCS haplotype networks of concatenated cpDNA sequences of the
studied bipolar Carex species and their sister species: (a) C. arctogena. Shaded and dashed
squares represent the geographical distributions of lineages; (b) C. maritima; and (c) C.
canescens; (see Chapters 3, 4 and 5 for details). Circles represent haplotypes, lines
represent single mutational steps and small black circles are missing haplotypes. Circle
shades indicate species, and numbers in parentheses indicate the number of samples per
haplotype.
Accordingly to our results, Northern to Southern Hemisphere long-distance dispersal is a
very frequent pattern of dispersal in plant species (e.g. Vargas et al., 1998; Vijverberg et al.,
1999; Yokoyama et al., 2000; Clayton et al., 2009; Escudero et al., 2009; Schaefer et al.,
2009; Wen & Ickert-Bond, 2009; Emadzade et al., 2011; Popp et al., 2011; Banasiak et al.,
2013; Lewis et al., 2014) and even in other bipolar species such as the lichen Cetraria
aculeata (Fernández-Mendoza & Printzen, 2013). However, other plant genera present the
opposite direction of dispersal. For example, the centre of origin of genus Larrea
(Zygophyllaceae) is located in South America and this genus was inferred to have migrated
to North America during the late Neogene by long-distance dispersal, using way stations in
Peru and Bolivia and probably mediated by birds (Lia et al., 2001). Likewise, the
Rubiaceae family was inferred to have migrated from South to North America during the
late Palaeocene–early Eocene using land bridges (Antonelli et al., 2009), as
Hoffmannseggia glauca (Fabaceae) via birds during the late Miocene or later (Simpson et
al., 2005).
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Means of dispersal
Wind and water dispersal
The utricle surrounding Carex fruit can show some features dispersal, as seen in the
inflated utricles of C. physodes for wind-dispersal (Egorova, 1999); in C. baccans, whose
red utricles are attractive to birds; or in C. paniculata, whose corky pericarp allows water
dispersal (reviewed in Allessio Leck & Schütz, 2005). One of the Carex bipolar species, C.
microglochin, has spikes with finely acute perigynia that reflex at maturity and are easily
detached, a characteristic that is suggested to facilitate animal dispersal (Savile, 1972). A
similar device has evolved independently in another bipolar species, Triglochin palustris
(Juncaginaceae; Savile, 1972).
However, with the exception of the above mentioned characteristics of the bladder-like
small utricles, Carex generally lack any obvious morphological features for dispersal by
abiotic or biotic forces. With the exception of C. microglochin, none of the bipolar Carex
species displays standard morphological syndromes for long-distance dispersal (as
described by Higgins et al., 2003). In fact, long-distance dispersal of seeds (> 100 km)
might not be necessarily driven by those vectors inferred from plant morphology; they are
usually associated with stochastic events (unusual behaviour of regular events or a
combination of vectors; Nathan et al., 2008).
Some dispersal agents are typically involved in long-distance dispersal, such as birds, ocean
or wind currents (Nathan et al., 2008; Gillespie et al., 2012). Considering the extreme
dispersal distance together with the shape and structure of the bipolar Carex propagules, we
consider that its dispersal was more likely to have been mediated by migratory animals than
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by wind or ocean currents, which seem insufficient for such enormous task. Besides, there
are no wind or oceans currents connecting Northern a Southern Hemispheres. Both wind
and ocean currents have opposite directions when approaching the Equator (Hyeong et al.,
2005); thus, if propagules have been transported by wind or ocean currents, they would
have to make a stop at low latitudes and then have been transported again into the other
hemisphere. Besides, successful oceanic dispersal is influenced by a complex interaction
between ocean dynamics and geomorphology at past and present times, together with the
ability of plants for survival during transportation (Gillespie et al., 2012). Although it
cannot be discarded, it seems an extremely unlikely event for bipolar plant dispersals.
Nonetheless, wind and ocean currents have been suggested to be responsible for plant
migration within hemispheres (e.g. Brooker et al., 2001; Brochmann et al., 2003; Renner,
2004; Alsos et al., 2009; Gillespie et al., 2012).
Bird dispersal
Some birds which migrate from North America to temperate zones of South America have
already been pointed out as the most likely dispersal agents of the several disjunct plant
groups (Cruden, 1966; and references therein; Popp et al., 2011; Lewis et al., 2014). Carex
seeds have been reported to be intact after transport by birds (Mueller & van der Valk,
2002), and arrivals of Carex species to newly formed islands have predominantly been
reported to happen when seeds were embedded in mud attached to birds’ feet or else when
eaten and carried inside by birds (Carlquist, 1967). Therefore, birds seem to be playing an
important role in Carex dispersal.
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Bird-mediated direct long-distance dispersal from North America to South America has
already been used to explain a bipolar disjunction in crowberries (Empetrum; Popp et al.,
2011). Most migratory birds that disperse seeds live in temperate and boreal regions
(Wheelwright, 1988). For birds to act as vectors for seed dispersal by endo- or
ectozoochory, the seeds must have morphological features for association with these
animals, and must be able to maintain their viability after intestinal transit to allow for
establishment in new environments (Gillespie et al., 2012). However, it has been proven
that Carex species are transported even in the lack of obvious morphological features for
zoochorous dispersal (Carlquist, 1967), as it happens to the three bipolar species studied
here.
Other structures or features that are not directly related with dispersal syndromes may be
involved, including anatomical features such as deposits of silica in the pericarp that harden
seeds (Graven et al., 1996; Prychid et al., 2004). These silica deposits could protect seeds
when passing through birds’ alimentary tracts (Graven et al., 1996) but could also make the
seeds as hard as pebbles and useful for grinding other organic material in bird gizzards.
Carex fruits could therefore be doubly preferred by birds – both as nourishment and as
gastroliths (Alexander et al., 1996). Some birds from North America, such as the pectoral
sandpiper, Calidris melanotos (Holmes & Pitelka, 1998), and the lesser yellowlegs, Tringa
flavipes (Tibbitts & Moskoff, 1999), are known to feed in sedge meadows before migrating
southwards to their wintering grounds in South America. Their breeding ranges closely
match the current distribution of Carex bipolar species in North and South America.
Although current bird migratory patterns do not necessarily coincide with past migrations,
these observations suggest that the bipolar disjunction in Carex species may have
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originated via bird-mediated long-distance dispersal. Additionally, dispersal may occur
through accidental displacement – vagrant birds or migrants, such as those flying to
Australia or New Zealand, deviating widely from their normal route (Battley et al., 2012).
With satellite telemetry, Gill et al. (2009) recorded transoceanic flights of bar-tailed
godwits (Limosa lapponica baueri) from Alaska to New Zealand and showed that they can
fly 10,153 km (± 1043 SD) non-stop in 7.8 days (± 1.3 SD). This extraordinary flight,
combined with species that can be preferentially chosen for fuel, could help species to
achieve a bipolar distribution by means of direct long-distance dispersal. Therefore, we
consider it plausible that bipolar Carex species could have acquired its bipolar distribution
by means of bird-mediated dispersal.
Human introductions
Six out of the 30 bipolar species are confirmed introductions or suspicious of being
introduced in the Southern Hemisphere (Table 1). Carex maritima is the only species
studied here that molecular data have been enough to prove a non-anthropochorus origin,
since Southern Hemisphere populations diverged during the early-middle Pleistocene. For
C. canescens, the weakly supported clade of two Argentinian samples, do not allow us to
reject that hypothesis; neither for C. arctogena, whose Southern Hemisphere populations
are genetically identical to the Northern Hemisphere ones. In these cases, species’
adaptation to local environmental conditions, biotic interactions and demographic processes
of these species would all have been established relatively quickly (Theoharides & Dukes,
2007). Populations of C. arctogena and C. canescens in Patagonia occur in well-conserved
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habitats and most are only accessible on foot. Specimens of C. arctogena from Patagonia
are few in the South American herbaria BA, BAA, BAB, BCRU, HIP and SI, with some
dating to the late 1880s, when the human influence in the southernmost parts of South
America was very limited. Although we cannot strongly rule out an anthropogenic
introduction of neither of these two species to South America, it seems very unlikely.
Unusual behaviour of vectors
A typical seed morphology has traditionally been associated to a particular dispersal vector,
(haplochory; i.e. dispersal mediated by a single standard dispersal vector; Nathan et al.,
2008); however, there is now more evidence of dispersal mediated by more than one vector
(i.e. polychory; reviewed in Nathan et al., 2008). One example of this shift is the dispersal
of Taraxacum officinale, a typical wind-dispersed species whose hairy seeds have a halftime buoyancy of 2.57 days in water (Boedeltje et al., 2003) and potential for ectozoochory
(Tackenberg et al., 2006). When dandelion seeds are wind dispersed, they go away from the
mother plant around 2.15 meters (Soons & Ozinga, 2005) whereas when they are waterdispersed or animal-dispersed, they can fairly increase that distance and hence, the potential
for long-distance dispersal by other vectors. In fact, species with small seeds such as those
of the dandelion and/or from water-influenced habitats are often highly dispersible taxa
(Mcglone et al., 2001). Therefore, species can be dispersed longer distances with
unpredicted or non-associated vectors than with vectors directly associated to its dispersal
syndromes. This could also be the case in arctic plant species, that have been demonstrated
to migrate enormous distances despite of the lack of specific syndromes (Abbott et al.,
2003). Thus, we suggest that relatively unspecialized structures for dispersal might play a
role in the distribution of these bipolar Carex species and we regard the hypothesis of non-
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standard vector-mediated dispersal, either by abiotic or biotic forces, as a possible
explanation of their bipolar disjunction.
Nonetheless, rare processes or unusual behaviour of vectors have been inferred to have
dispersed seeds over long distances (Higgins & Richardson, 1999; Nathan et al., 2002,
2008; Higgins et al., 2003). In fact, long-distance dispersal is claimed as a widespread
phenomenon in many plant species without standard morphological syndromes for longdistance dispersal (Carlquist, 1967; Cain et al., 2000; Higgins et al., 2003; Alsos et al.,
2007; Dixon et al., 2009).
Successful establishment after dispersal in Carex bipolar species
To produce a disjunct distribution, long-distance dispersal has to be followed by the
establishment of a permanent population in a new area. In many cases, establishment in a
new environment - which is determined by the environment and biotic conditions of the
host community (Mitchell et al., 2006) - may be more difficult to achieve that long-distance
dispersal per se. Therefore, it is not the chance of dispersal alone but the entire colonization
process, this is, dispersal followed by establishment, which is critical for a species to
expand its geographical range.
Our results show that in the Southern Hemisphere the three Carex bipolar species studied
occupy a more restricted climatic niche than in the Northern Hemisphere. It is more
differentiated in C. maritima and C. arctogena than in C. canescens, whose Southern
Hemisphere populations fall within the general ecological conditions tolerated by the
species, which seem to be very wide. This ecological plasticity of C. arctogena and C.
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maritima or the tolerance of harsher conditions in the Northern Hemisphere than in the
Southern Hemisphere could have been a key element in their establishment after dispersal.
If these species have been successful colonizing the Southern Hemisphere, why are not they
in the same ecological niche in the Northern Hemisphere? Are there any of the Southern
Hemisphere niches available in the Northern Hemisphere? If yes, why are not they found
there? One possible reason could be found in community assemblies or competitive
interaction of those areas (Waters, 2011), which could be easier to penetrate in the Southern
Hemisphere than in potential areas in the Northern Hemisphere. Such biotic differences
could have allowed them to shift into new habitats and climate zones (Broennimann et al.,
2007) in the Southern Hemisphere. Alternatively, establishment could have taken place at a
time when both areas had similar climatic conditions. More robust conclusions could be
obtained with principal component analysis methods by measuring climatic niche shifts
using Bayesian generalized linear models (e.g. González-Moreno et al., 2014).
Intrinsic conditions for long-distance dispersal and establishment
Self-fertilization is a reproductive characteristic displayed by many species with disjunct
populations in the temperate zones (Carlquist, 1983). This attribute could play in favour of
local survival and establishment after long-distance dispersal events, given that a single
propagule of self-compatible individuals could in principle be sufficient to start a sexuallyreproducing colony (Baker, 1955). In congruence, Carex species are predominantly
monoecious and in general highly self-pollinated (Friedman & Barrett, 2009), which has
been inferred from studies based on hand pollinations, isozyme work (e.g. Ohkawa et al.,
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2000; Friedman & Barrett, 2009) and microsatellite data (e.g. Escudero et al., 2010b, 2013).
This characteristic could explain, at least in part, the often successful colonization of Carex
species after a long-distance dispersal event (Moore et al., 1971; Ball, 1990; Escudero et
al., 2009).
In addition, chromosome rearrangements have been shown to be correlated with phenotypic
differences, as well as being thought to enhance fitness in different habitats (Coghlan et al.,
2005). Specifically, high chromosome number evolution is a result of: (i) selection by
climatic regime and ecological strategies; and (ii) neutral processes such as phylogenetic
inertia or migration processes (Escudero et al., 2012, 2013). The high chromosome number
variation in some bipolar Carex species [C. canescens, 2n = 52-54, 56-58, 60, 62; C.
macloviana, 2n= 82, 82-86, 86; C. magellanica, 2n= 58, ca. 60; reviewed in Roalson et al.,
2008) might also be a result of the influence of the climatic environments at different
latitudes and distant regions. Carex arctogena (2n=50) and C. maritima (2n=60) have not
been reported to display chromosome number variation (Roalson, 2008).
307
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________________________________________________________________
Conclusions
1. Carex capitata and C. arctogena are two different species; populations from South
America correspond to C. arctogena, and thus, Carex antarctogena is a synonym of
C. arctogena.
2. The morphological variation found in populations from Western North America
leads to the description of one new species C. cayouetteana, and two new
subspecies C. cayouetteana subsp. altasierra and C. cayouetteana subsp.
bajasierra.
3. The genus Carex is the genus with the largest number of bipolar species (six).
4. Two hypotheses can be rejected for all bipolar Carex species: vicariance and
convergent evolution. They only hypothesis that cannot be rejected is long-distance
dispersal.
5. The bipolar species studied have probably migrated from the Northern Hemisphere
to the Southern Hemisphere.
6. All bipolar Carex species studied originated from the late Miocene: C. arctogena
diverged in the late Miocene to early Pleistocene (5 Ma; 95% HPD: 2.01 – 8.03
Ma); C. maritima during middle–late Pliocene to early–middle Pleistocene (0.23
Ma; 95% HPD: 0.03– 0.51 Ma); and C. canescens during the Pleistocene (1.17 Ma;
95% HPD: 0.34– 2.17 Ma).
7. There are no genetic differences between Northern and Southern Hemispheres
populations of C. arctogena and C. canescens, which suggest a recent, direct longdistance dispersal, probably mediated by birds.
308
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________________________________________________________________
8. Carex maritima populations from the Southern Hemisphere were genetically and
ecologically differentiated from their northern counterparts.
9. Carex canescens have dispersed at least twice to the Southern Hemisphere, once to
Australia and once to South America.
309
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________________________________________________________________
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