Parapatric speciation

Speciation
Walter Salzburger:
Charles R. Darwin
(1809-1882)
What is a species?
Bombina bombina
Bombina variegata
What is a species?
‣ Species are fundamental (real) natural units
‣ Species are independent evolutionary units. Members of the
same species share a gene pool. Mutation, drift and selection
operate within species.
‣ Taxonomists define species by means of morphological or
phenetic characters
‣ Individuals within a species are variable. There is no “ideal” or
“typical” individual
What is a species?
‣ There is no agreement on how species should be defined...
frequency
Variation within/between Species:
trait
time
?
What is a species?
‣ There is no agreement on how species should be defined...
Ring Species:
Stebbins (1994)
Two species appear to be
present at one place, but those
two “species” are connected by
a series of forms that are
geographically arranged in a
ring. No phenetic character
could be used, except arbitrarily,
to divide the ring into two
species. A division would be
meaningless, as there really is a
continuum, not a number of
clear-cut, separate species.
What is a species?
‣ There is no agreement on how species should be defined...
P.
ca
Eu erul
rop eus
e
Salzburger et al. (2002)
For example, the Blue Tit (Parus
caeruleus) is a paraphyletic species.
The North African subspecies P. c.
degener and P. c. ultramarinus are the
sister group to the European Blue Tit
(P. c. caeruleus) plus the Eurasian
Azul Tit (P. cyanus) with four
subspecies (P. c. cyanus, flavipectus,
tianshanicus, and yaniseensis)
P.
c
Eu yanu
ras s
ia
The evolution of part of the original
species into a new one renders the
remaining populations paraphyletic.
P.
ca
N- erul
Af eus
ric
a
Paraphyletic Species:
Biological Species Concept (BSC)
‣ “Species are groups of interbreeding natural populations that are
reproductively isolated from other such groups” (Mayr 1963)
♥
♥
Biological Species Concept (BSC)
‣ “Species are groups of interbreeding natural populations that are
reproductively isolated from other such groups” (Mayr 1963)
‣ reproductive isolation: no interbreeding with members of other
species
‣ The BSC places the taxonomy of a species within the
framework of population genetics
‣ The BSC explains why members of a species resemble one
other, and differ from other species.
Biological Species Concept (BSC)
‣ problems:
‣ intermediate stages (“young species”, ring species)
‣ BSC fails to deal with low levels of gene flow between
taxa (e.g., introgression)
‣ asexual organisms or organisms with partially uniparental
reproduction
‣ using interbreeding and/or reproductive isolation alone
may distort evolutionary history
Ecological Species Concept (ESC)
‣ Species are defined ecologically by a shared ecological niche
‣ Members of a species occupy an adaptive zone that is different
from that of any other species (in its range)
‣ ESC is based on evolutionary cohesion
‣ main problem: how to a priori define the adaptive zone
characteristic for a species?
Phylogenetic Species Concept (PSC)
‣ A “phylogenetic species” is a basal cluster of organisms that
is diagnosably distinct from other such clusters (Cracraft 1989)
‣ A species is the smallest monophyletic group of common
ancestry (de Queiroz & Donoghue 1988)
‣ PSC is based on evolutionary history
‣ problems: the phylogeny of a gene might not reflect the entire
evolutionary history; paraphyly of species poses a problem,
too.
Reproductive Isolation
“speciation continuum”
species A
no
ancestral
species
time
partial
imperfect
reproductive
isolation
complete
reproductive
isolation
species B
Reproductive Isolation
‣ premating isolating barriers: mechanisms that prevent the
formation of hybrid zygotes by impeding gene flow before the
transfer of sperm or pollen
‣ postmating, prezygotic isolating barriers: mechanisms that
prevent the formation of hybrid zygotes after sperm or pollen
transfer but before fertilization
‣ postzygotic isolating barriers: mechanisms that reduce the
viability or fertility of hybrid zygotes
Premating isolating barriers
Behavioral
Mutual attraction between the sexes of different species is
weak or absent, preventing them from initiating courtship
Habitat isolation. The adaptation to different habitats in the
same general area prevents or limits gene exchange
Ecological
Temporal isolation. Gene flow between two taxa is impeded
on the basis of different breeding/flowering times
Pollinator isolation. Gene flow between angiosperm species
is reduced by differential interactions with pollinators.
Mechanical
Inhibition of normal copulation or pollination between two
species due to incompatibility of reproductive structures
Mating system
Evolution of partial or complete self-fertilization or asexual
reproduction can result in the creation of a new taxon
Premating isolating barriers
‣ Cichlid fishes of Lake Victoria, East Africa
+
0
-
P. nyererei
P. pundamilia
*no color vision
Preference of
P. nyererei female
monochromatic light*
Preference of
P. nyererei female
normal (white) light
+
P. nyererei x pundamilia
0
-
P. nyererei
Seehausen et al. (1997)
Seehausen & van Alphen (1998)
Premating isolating barriers
‣ Orchids of the genus Ophrys: pollinator isolation
www.grandsitesaintev
ictoire.com
P. pundamilia
Postmating, prezygotic isolating barriers
Copulatory
Behavior
Gametic
Isolation
Behavior of an individual during copulation is insufficient to
allow normal fertilization
Noncompetitive gametic isolation. Intrinsic problems with
transfer, storage, or fertilization of heterospecific gametes
in single fertilizations between members of different species
Competitive gametic isolation. Heterospecific gametes are not
properly transferred, stored, or used in fertilization when
competing with conspecific gametes (“conspecific sperm
or pollen preference”)
Postzygotic isolating barriers
Extrinsic
Ecological inviability. Hybrids develop normally but suffer
lower viability because they cannot find an appropriate
ecological niche
Behavioral sterility. Hybrids have normal gametogenesis but
are less fertile than parental species because they cannot
obtain mates
Hybrid inviability. Hybrids suffer developmental difficulties
causing full or partial lethality
Intrinsic
Hybrid sterility. Hybrids suffer problems in the development
of the reproductive system or gametes or suffer
neurological or physiological lesions that render them
incapable of successful courtship
fitness
Postzygotic isolating barriers
species A
aabb
species B
AABB
AA
bb
us
Bb
B
loc
loc
us
A
Aa
BB
aa
Reinforcement
‣ Reproductive isolation may be reinforced by natural selection
‣ Reinforcement is the evolution of divergent mate preferences
in response to selection against hybrids (if hybrids have low
fitness there is a high cost of mating with a wrong species)
‣ evidence: prezygotic isolation between sister-species
occurring in sympatry is greater than between pairs of species
that live in allopatry
Reinforcement
sister taxa
(in sympatry)
isolation index
sister taxa
(in allopatry)
genetic distance
Coyne & Orr (1997)
Biogeography of speciation
parapatric
speciation
allopatric
speciation
0
sympatric
speciation
m
1/2
migration rate
Gavrilets (2004)
Biogeography of speciation
‣ allopatric speciation is the origin of new species from
geographically isolated populations. There is no gene
exchange between the diverging populations
‣ parapatric speciation is the origin of new species when gene
flow between diverging populations is neither zero nor the
maximum possible
‣ sympatric speciation is the origin of new species without
geographic isolation. It is the emergence of new species from
a population where mating is random with respect to the
birthplace of the mating partners
Biogeography of speciation
parapatric speciation
sympatric speciation
time
allopatric speciation
Allopatric speciation
‣ In allopatric speciation, a gene pool is initially divided by an
external barrier to dispersal
‣ reproductive isolation evolves as byproduct of independent
evolution:
‣ Selection. Adaptation to different environments
‣ Mutation. Different mutations will arise in the populations
‣ Drift. Random change in gene frequencies
Allopatric speciation
Vicariance* speciation
...in Alpheus snapping shrimp from both sides of
the Isthmus of Panama
NASA
TW Doeppner
*is the splitting in the range of a taxon,
e.g., through continental drift, mountain formation, glaciation
Knowlton & Weight (1998)
snapping shrimp (Alpheus)
26
Kauai
Peripatric* speciation
12
Oahu
29
40
www.pacificislands.com
Maui complex
Drosophila
26
*a new species emerges from a small, isolated subpopulation on the periphery
e.g., colonization of an island (“founder effect speciation”)
Parapatric speciation
‣ Parapatric speciation involves the evolution of reproductive
isolation between two populations that exchange genes
‣ Clinal models require environmental gradients. Subpopulations
become adapted to their local habitats and speciate
‣ In ”stepping-stone” models only adjacent populations exchange
genes
‣ an intermediate step in parapatric speciation is a hybrid zone,
i.e. an area where hybridization occurs
NASA
Hawaii
Parapatric speciation
“Stepping-stone” models
Clinal models
colonization
wet
environmental gradient
dry
local adaptation
hybrid zone
hybrid
reproductive isolation
Parapatric speciation
“Stepping-stone” model: most realistic scenario?
dry
wet
colonization
0
time
population
expansion
local
adaptation
population
expansion
gene
flow
local
extinction
speciation!
river
re-colonization
Sympatric speciation
‣ “No aspect of speciation is as controversial as the view that
new species can begin to form sympatrically” (Coyne & Orr 2004)
‣ Mathematical models and computer simulations show that
sympatric speciation is theoretically plausible (under certain
conditions)
‣ However, evidence for sympatric speciation in nature is scarce...
‣ ...since - in many putative cases - alternative scenarios
(allopatric, parapatric) cannot be ruled out
Sympatric speciation
‣ two “fundamental” problems (Coyne & Orr 2004)
frequency
1. antagonism between selection
and recombination
2. development of sufficient ecological
differences to allow coexistence
reproductive isolation
and ability to coexist
must evolve simultaneously
trait
selection
interbreeding
“ecological speciation”
Sympatric speciation
‣ evidence
crater lake cichlids
palm trees on Lord Howe Island
Feder et al. (2000)
Savolainen et al. (2006)
www.organicgardenpests.com
apple maggot fly
Sympatric speciation
‣ apple maggot fly: sympatric host races
larvae of the original population of apple maggot
fly (Rhagoletis pomonella) feeds on hawthorn
www.wdr.de
host shift of one population to apple in the USA
in the mid-nineteenth century (Bush 1993)
within ca. 150 years, two ecologically distinct
species evolved
Feder et al. (2000)
www.gartenliebe.de
Sympatric speciation
Laguna de Apoyo
Arrow cichlid (A. zaliosus)
Midas cichlid (Amphilophus citrinellus)
Laguna de Apoyo
Sympatric speciation
Nicaraguan crater lake cichlids
✓sympatric occurrence
✓ecological difference
✓reproductive isolation
Barluenga et al. (2006)
✓monophyly
Ecological speciation
‣ ... is the evolution of barriers to gene flow resulting from
ecologically-based divergent selection
‣ (as opposed to ‘mutation-order speciation’, i.e. the evolution of
reproductive isolation by the chance occurrence and fixation
of different alleles between populations adapting to similar
selection pressures
‣ e.g. ‘ecomorphs’ of stickleback fish along environmental
gradients
Polyploidy and Hybrid Speciation
‣ New species may originate by polyploidization or as a
consequence of hybridization
‣ Polyploids arise naturally and are interfertile among
themselves, but reproductively isolated from parental species
‣ Hybrids may have a fitness advantage under certain conditions
‣ Polyploidy and hybrid speciation is common in plants, but
also animals appear to have originated in this way
Polyploidy and Hybrid Speciation
swamp
freshwater
marsh
I. fulva
hybrid
I. hexagona
Arnold & Bennett (1993); images: M. Arnold
Hybrid speciation in Louisiana irises
Polyploidy and Hybrid Speciation
Introgressive hybridization
back-crosses predominantly
with one parental species
(Rieseberg & Wendel 1993)
species 1
stabilized
introgressant
Polyploidy and Hybrid Speciation
“hybrid species”
Heliconius heurippa
Mavarez et al. (2006)
Xiphophorus clemenciae
Meyer et al. (2006)
species 2
Natural Selection...
images: www.idscaro.net, www.wikipedia.com
‣ ... “is the process by which the forms of organisms in a
population that are best adapted to the environment increase
in frequency relative to less well-adapted forms over a number
of generations” (Ridley 1996)
...Sexual Selection
images: www.crbs.umd.edu, www.smh.com.au
‣ ...“is the selection on mating behavior, either through
competition among members of one sex (usually males) for
access to members of the other sex or through
choice by members of one sex (usually females) for certain
members of the other sex” (Ridley 1996)
Natural Selection...
...Sexual Selection
fitness
competitors
sexual selection
individual fitness
other members of
the same sex
natural selection
fitness of the
genotype
other individuals in
the same
population
Natural Selection...
...Sexual Selection
‣ ...operates if the following conditions are met:
heredity
trait variation
variation in fitness
organisms must reproduce to form new
generations
offspring resemble parents
(“like must produce like”)
individuals in natural populations vary in
(adaptive) traits
individuals in natural populations vary in the
number of their offspring that survive to
reproduce (‘lifetime reproductive success’)
(Ridley 2004; Stearns & Hoekstra 2005)
reproduction
...Sexual Selection
‣ ...seems to play an important role in speciation (in allopatry,
parapatry, and sympatry)
‣ Traits involved in mate choice, courtship and mating evolve faster
than most other traits.
image: M. Schartl
‣ Sexual selection involves co-evolution of female preference
and male signals
Xiphophorus hellerii
...Sexual Selection
Sex
trait favored by sexual selection
traits that females find attractive
Male
traits that persuade females to mate
traits that discourage females from mating again (copulation
plugs, mating injuries, transmitted chemicals, etc.)
Female
choice of the best males (best genes, largest territory, least
parasites, etc.)
resistance to male persuasion
...Sexual Selection
‣ small ecological divergence
‣ large divergence in male ornaments
‣ low morphological divergence of females
www.smh.com.au
Birds of paradise
‣ large divergence of female preference
‣ low morphological divergence of females
‣ large divergence of female preference
images: E. Schraml
‣ large divergence in male nuptial coloration
image: E. Schraml
Cichlid fishes of Lakes Malawi & Victoria