Molecular phylogeny of the highly diversified catfish subfamily

Transcription

Molecular Phylogenetics and Evolution 94 (2016) 492–517
Contents lists available at ScienceDirect
Molecular Phylogenetics and Evolution
journal homepage: www.elsevier.com/locate/ympev
Molecular phylogeny of the highly diversified catfish subfamily
Loricariinae (Siluriformes, Loricariidae) reveals incongruences with
morphological classification q
Raphaël Covain a,⇑, Sonia Fisch-Muller a, Claudio Oliveira b, Jan H. Mol c, Juan I. Montoya-Burgos d,
Stéphane Dray e,f
a
Muséum d’histoire naturelle, Département d’herpétologie et d’ichtyologie, route de Malagnou 1, case postale 6434, CH-1211 Genève 6, Switzerland
Departamento de Morfologia, Universidade Estadual Paulista Júlio de Mesquita Filho, Instituto de Biociências, Laboratório de Biologia e Genética de Peixes, Rubião Junior 18618-970,
Botucatu, SP, Brazil
c
University of Suriname, Center for Agricultural Research in Suriname, CELOS and Department of Biology, POB 9212, Paramaribo, Suriname
d
Université de Genève, Département de Génétique et Evolution, Sciences III, quai E. Ansermet 30, CH-1211 Genève 4, Switzerland
e
Université de Lyon, F-69000 Lyon, France
f
Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622 Villeurbanne, France
b
a r t i c l e
i n f o
Article history:
Received 24 February 2015
Revised 15 September 2015
Accepted 19 October 2015
Available online 26 October 2015
Keywords:
Systematics
Neotropics
Mitochondrial genes
Nuclear genes
Freshwaters
Amazon basin
a b s t r a c t
The Loricariinae belong to the Neotropical mailed catfish family Loricariidae, the most species-rich catfish
family. Among loricariids, members of the Loricariinae are united by a long and flattened caudal peduncle
and the absence of an adipose fin. Despite numerous studies of the Loricariidae, there is no comprehensive phylogeny of this morphologically highly diversified subfamily. To fill this gap, we present a molecular phylogeny of this group, including 350 representatives, based on the analysis of mitochondrial and
nuclear genes (8426 positions). The resulting phylogeny indicates that Loricariinae are distributed into
two sister tribes: Harttiini and Loricariini. The Harttiini tribe, as classically defined, constitutes a
paraphyletic assemblage and is here restricted to the three genera Harttia, Cteniloricaria, and Harttiella.
Two subtribes are distinguished within Loricariini: Farlowellina and Loricariina. Within Farlowellina,
the nominal genus formed a paraphyletic group, as did Sturisoma and Sturisomatichthys. Within
Loricariina, Loricaria, Crossoloricaria, and Apistoloricaria are also paraphyletic. To solve these issues, and
given the lack of clear morphological diagnostic features, we propose here to synonymize several genera
(Quiritixys with Harttia; East Andean members of Crossoloricaria, and Apistoloricaria with Rhadinoloricaria;
Ixinandria, Hemiloricaria, Fonchiiichthys, and Leliella with Rineloricaria), to restrict others (Crossoloricaria,
and Sturisomatichthys to the West Andean members, and Sturisoma to the East Andean species), and to
revalidate the genus Proloricaria.
Ó 2015 Elsevier Inc. All rights reserved.
1. Introduction
The Loricariinae represent a highly diversified subfamily among
the large Neotropical catfish family Loricariidae, or suckermouth
armored catfish. Loricariids have undergone an evolutionary radiation at a subcontinental scale, from Costa Rica to Argentina, which
has been compared to that of the Cichlidae of the Great Lakes of the
q
This paper was edited by the Associate Editor G. Orti.
⇑ Corresponding author.
E-mail addresses: [email protected] (R. Covain), sonia.fisch-muller@
ville-ge.ch (S. Fisch-Muller), [email protected] (C. Oliveira), [email protected]
(J.H. Mol), [email protected] (J.I. Montoya-Burgos), stephane.dray@
univ-lyon1.fr (S. Dray).
http://dx.doi.org/10.1016/j.ympev.2015.10.018
1055-7903/Ó 2015 Elsevier Inc. All rights reserved.
Rift Valley in Africa (Schaefer and Stewart, 1993). The species core
flock Loricariidae (sensu Lecointre et al., 2013), represents the most
species rich family of the Siluriformes with 898 valid species and
an estimated 300 undescribed species distributed in more than
100 genera (Reis et al., 2003; Ferraris, 2007; Eschmeyer and
Fong, 2015). Extremely variable color patterns and body shapes
among loricariid taxa reflect their high degree of ecological specialization, and because of their highly specialized morphology loricariids were recognized as a monophyletic assemblage in the
earliest classifications of the Siluriformes (de Pinna, 1998). The
Loricariidae are characterized by a depressed body covered by
bony plates, and above all, by the modification of the mouth into
a sucker disk. Within the Loricariidae, members of the subfamily
Loricariinae are diagnosed by a long and depressed caudal
R. Covain et al. / Molecular Phylogenetics and Evolution 94 (2016) 492–517
peduncle and by the absence of an adipose fin. They live stuck to
the substrate and show marked variations in body shape according
to the various habitats colonized, from lotic to lentic systems, on
mineral or organic substrates. For example, members of Farlowella
resemble a thin stick and blend remarkably among submerged
wood and leafs, whereas members of Pseudohemiodon are large
and flattened and bury themselves in sandy substrates like
flatfishes. Some groups have numerous teeth, pedunculated, and
organized in a comblike manner, while other groups have few
teeth or even no teeth on the premaxillae. Teeth are often strongly
differentiated, and can be bicuspid straight and thick, spoonshaped, reduced in size or very long. An important diversity in
lip characteristics, which can be strongly papillose, filamentous
or smooth, also characterizes this subfamily (Isbrücker, 1979;
Covain and Fisch-Muller, 2007).
Different hypotheses have been proposed to classify the Loricariinae (summarized in Table 1). The first attempt was performed
by Isbrücker (1979) who distributed them into four tribes and
eight subtribes on the basis of external morphology, but without
phylogenetic inferences. These included the Loricariini, comprising
six subtribes (Loricariina, Planiloricariina, Reganellina, Rineloricariina, Loricariichthyina, and Hemiodontichthyina), the Harttiini,
including two subtribes (Harttiina and Metaloricariina), the
493
Farlowellini, and the Acestridiini. The latter were subsequently
placed in the subfamily Hypoptopomatinae by Schaefer (1991).
In her PhD thesis, Rapp Py-Daniel (1997) proposed a phylogeny
of the Loricariinae based on a phylogenetic analysis of morphological characters. She confirmed the monophyly of the subfamily, and
split the Loricariinae into two tribes: Loricariini and Harttiini, the
latter comprising Farlowellini (sensu Isbrücker, 1979). In a
morphological phylogenetic analysis of the family Loricariidae,
Armbruster (2004) also obtained a similar splitting based on a
restricted sampling of the Loricariinae, with Harttiini (sensu Rapp
Py-Daniel, 1997, comprising Harttia, Lamontichthys, Sturisoma,
and Sturisomatichthys), forming the sister group of Loricariini
(sensu Rapp Py-Daniel, 1997, comprising Crossoloricaria, Loricaria,
Loricariichthys, Ixinandria, and Rineloricaria). Covain and FischMuller (2007), based on multivariate analyses of generic diagnostic
characters, also split the subfamily into two tribes, the Harttiini
and the Loricariini, and proposed four morphological groups within
the Loricariini: (1) the Pseudohemiodon group, (2) the Loricaria
group, (3) the Rineloricaria group, and (4) the Loricariichthys
group. Montoya-Burgos et al. (1998) proposed a first molecular
phylogeny of the family Loricariidae using mitochondrial genes.
Although, their analysis included only nine representatives of the
Loricariinae, they partially confirmed their subdivision into two
Table 1
Alternative classifications of the Loricariinae according to different authors.
The different colors provide limits of the different recognised tribes. These tribes can include different taxa according to the different authors. Salmon: Loricariini; blue:
Harttiini; green: Farlowellini; red: Acestridiini.
494
main groups, but with Harttia (nominal genus of Harttiini) forming
the sister genus of all other Loricariinae (comprising Farlowellini,
part of Harttiini, and Loricariini). Covain et al. (2008) using mitochondrial genes, and Rodriguez et al. (2011) using mitochondrial
and nuclear markers performed a molecular phylogeny on a small
sampling of the Loricariinae. Both studies restricted Harttiini to
Harttia, and included Farlowelliini as a subtribe of Loricariini.
Within the latter, the Loricariichthys and Loricaria–Pseudohemiodon
morphological groups (sensu Covain and Fisch-Muller, 2007) were
confirmed as natural groupings, whereas monophyly of the
Rineloricaria group was rejected. Similar results were also obtained
using different markers by Cramer et al. (2011) in a molecular
phylogeny of the Hypoptopomatinae (including four Loricariinae
in the outgroup), and by Lujan et al. (2015) in a molecular phylogeny of the Loricariidae (including 14 Loricariinae). In addition
to the conflicting results obtained using either morphological or
molecular data, the validity of several genera was regularly questioned by different authors rendering the taxonomy of the group
confused. Isbrücker and Isbrücker & Michels (in Isbrücker et al.,
2001) described four new genera: Fonchiiichthys, Leliella, Quiritixys
and Proloricaria, and revalidated the genus Hemiloricaria Bleeker,
1862 on the basis of a very restricted number of characters. Rapp
Py-Daniel and Oliveira (2001) considered Cteniloricaria a junior
synonym of Harttia. Ferraris (2003) maintained the validity of
Cteniloricaria, and considered junior synonyms of already described
genera all the genera described by Isbrücker and Isbrücker &
Michels (in Isbrücker et al., 2001). Covain and Fisch-Muller
(2007) followed Ferraris (2003) but maintained Cteniloricaria in
synonymy with Harttia. Ferraris (2007) modified his previous
statement and considered Fonchiiichthys, Proloricaria, and Hemiloricaria valid. Later on, Covain et al. (2012) revalidated Cteniloricaria.
There are currently 239 species of Loricariinae considered valid,
distributed in 32 genera (for a review see Covain and FischMuller, 2007; also Ghazzi, 2008; Ingenito et al., 2008; Fichberg
and Chamon, 2008; Rapp Py-Daniel and Fichberg, 2008;
Rodriguez and Miquelarena, 2008; Rodriguez and Reis, 2008;
Rodriguez et al., 2008, 2011, 2012; Thomas and Rapp Py-Daniel,
2008; de Carvalho Paixão and Toledo-Piza, 2009; Thomas and
Sabaj Pérez, 2010; Covain et al., 2012; Vera-Alcaraz et al., 2012;
Oyakawa et al., 2013; Thomas et al., 2013; Ballen and Mojica,
2014; Fichberg et al., 2014; Londoño-Burbano et al., 2014).
Given the confused systematics of the Loricariinae, we present a
comprehensive and robust molecular phylogeny of this group
based on mitochondrial and nuclear genes. The resulting phylogeny, in conjunction with morphological diagnostic characters,
will be subsequently used to (1) redefine the tribal and subtribal
ranks of the subfamily; (2) evaluate the validity and monophyly
of the different genera, and (3) test alternative hypotheses of classification proposed in the literature.
2. Material and methods
2.1. Taxonomic sampling
The molecular phylogeny was reconstructed using the taxonomic sampling given in Covain et al. (2008), and Rodriguez
et al. (2011) with the addition of 326 representatives of the Loricariinae and 16 outgroup species. The outgroup representatives
were chosen in other subfamilies of the Loricariidae. The list of
material used for this study is provided in Table 2. The analyzed
samples came from the tissue collection of the Muséum d’histoire
naturelle de la Ville de Genève (MHNG); Academy of Natural
Sciences of Drexel University in Philadelphia (ANSP); Smithsonian
Tropical Research Institute (STRI), Panama; Laboratório de Biologia
de Peixes, Departamento de Morfologia, Universidade Estadual
Paulista, Campus de Botucatu (LBP); Auburn University Museum,
Montgomery (AUM); and Museu de Ciências e Tecnologia of the
Pontifícia Universidade Católica do Rio Grande do Sul (MCP), Porto
Alegre. The sequences were deposited in GenBank.
2.2. DNA extraction, choice of markers, amplification, and sequencing
Tissue samples were preserved in 80% ethanol and stored at
20 °C. Total genomic DNA was extracted with the DNeasy Tissue
Kit (Qiagen) following the instructions of the manufacturer. The
choice of markers was governed by their ability to resolve inter
generic relationships at subfamilial ranks. We thus selected the
mitonchondrial genes 12S and 16S for the resolution of phylogenetic relationships between close ralatives (between species to
between genera relationships), and the nuclear Fish Reticulon-4
receptor (f-rtn4r) gene composed of two introns and three exons.
Exons of this marker are rather conserved and provide information
for deeper relationships (intra-familial to inter-ordinal relationships) whereas intronic regions are more variable and offer the
possibility to investigate phylogenetic relationships between closely related species. Thus, the selected molecular makers were
used to examine a range of taxomonic levels at subfamilial rank,
from intra-specific to inter-tribal relationshisps. The PCR amplifications of mitochondrial 12S and 16S, and the nuclear f-rtn4r genes
were carried out using the Taq PCR Core Kit (Qiagen). The methodology for PCR amplifications followed Chiachio et al. (2008) for
f-rtn4r using the set of primers Freticul4-D, Freticul4-R, Freticul4
D2, and Freticul4 R2 (Roxo et al., 2014). For the complete sequencing of f-rtn4r, three internal primers were designed additionally to
Freticul4-iR (Roxo et al., 2014): Freticul4-iD2 50 -CAA CAT CAC YTG
GAT TGA GG-30 , Freticul4-LiD 50 -ATG ACC GTG AGC TGC CAG GC-30 ,
and Freticul4-LiR 50 -GCT CAG TAA TAC GGT TGT TCT GCA-30 . To
amplify the almost complete 12S, tRNAval and 16S mitochondrial
genes in a single 2500 bp long fragment, a Nested PCR protocol
was used. The external round of PCR was performed using the pair
of primers Phe-L941 (Roxo et al., 2014) and H3059 (Alves-Gomes
et al., 1995). The external amplifications were performed in a total
volume of 50 ll, containing 5 ll of 10 reaction buffer, 1 ll of
dNTP mix at 10 mM each, 1 ll of each primer at 10 lM, 0.2 ll of
Taq DNA Polymerase equivalent to 1 unit of Polymerase per tube,
and 1–4 ll of DNA. Cycles of amplification were programmed with
the following profile: (1) 3 min. at 94 °C (initial denaturing), (2)
35 s. at 94 °C, (3) 30 s. at 51 °C, (4) 150 s. at 72 °C, and (5) 5 min
at 72 °C (final elongation). Steps 2–4 were repeated 35–39 times
according to the quality and concentration of DNA. The internal
round of PCR was performed using 1 ll of DNA template sampled
from external round PCR product, the pair of primers: An12S-1D:
50 -GTA TGA CAC TGA AGA TGT TAA G-30 and iH3059: 50 -GAA CTC
AGA TCA CGT AGG-30 , and the same protocol as above except for
the annealing temperature that was set to 54 °C. PCR products
were sent to Macrogen Inc. (Seoul, Korea) for sequencing. For the
complete sequencing of the 2500 bp long mitochondrial fragment,
two internal primers were used: Lor1D-1D: 50 -AGG AGC CTG TTC
TAG AAC CG-30 and Lor12S-3D (Covain et al., 2008) for a walking
sequencing procedure with around 700 bp between each step.
2.3. Sequence alignment, phylogenetic reconstruction, and topological
tests
The DNA sequences were edited and assembled using BioEdit
7.0.1 (Hall, 1999), aligned using ClustalW (Thompson et al.,
1994) and final alignment optimized by eye. Regions with ambiguous alignments in loop regions of mitochondrial ribosomal genes
were excluded from the analyses. The fragment of the f-rtn4r gene
analyzed here contained relatively long introns, ranging from
489 bp in Rineloricaria altipinnis to 1385 bp in R. cf. latirostris for
the first intron, and from 373 bp in R. pentamaculata to 656 bp in
495
Table 2
Taxa list, specimen and sequence data for the 350 Loricariinae and 18 outgroup representatives analyzed in this study. The acronyms of institutions follow Fricke and Eschmeyer
(2015).
Species
Catalog number
Field number
Locality
mt 12S + 16S bases
+ GenBank No.
Ref.
F-RTN4 bases
+ GenBank No.
Ref.
Harttia guianensis
MHNG 2643.016
GF00-351
2440 EU310447
2092 FJ013232
Loricaria parnahybae
MHNG 2602.067
BR98-274
French Guiana,
Marouini River
Brazil, Rio Parnahyba
Crossoloricaria
venezuelae
Dasyloricaria
tuyrensis
Farlowella aff.
oxyrrynchac
Farlowella
platorynchus
Hemiodontichthys
acipenserinus
Lamontichthys
stibaros
Limatulichthys
punctatusc
Loricaria clavipinna
INHS 35467
VZ 049
2419 EU310444
MHNG 2674.052
PA00-012
Venezuela, Rio Santa
Rosa
Panama, Rio Ipeti
MHNG 2588.064
PE96-022
Peru, Rio Tambopata
2433 EU310443
MHNG 2588.093
PE96-071
Peru, Rio Ucayali
2432 EU310446
MHNG 2651.012
GY04-015
2422 EU310448
MHNG 2677.039
MUS 208
MHNG 2651.013
GY04-018
MHNG 2640.044
PE98-002
Guyana, Rupununi
River
Peru, aquarium trade,
Rio Itayab
Guyana, Rupununi
River
Peru, Rio Putumayo
MHNG 2621.042
SU01-056
2428 EU310453
MHNG 2650.054
GY04-012
MHNG 2677.086
GF00-083
2438 EU310455
MHNG 2677.038
MUS 211
MHNG 2588.059
PE96-011
Surinam, Sarramacca
River
Guyana, Rupununi
River
French Guiana,
Marouini River
Rio Itayab
Peru, Rio Tambopata
UFRJ 6-EF4
BR 1114
Brazil, Rio Maranhão
2427 EU310459
MHNG 2651.009
GY04-083
2423 EU310458
1981 KR478422
Chiachio et al.
(2008)
Chiachio et al.
(2008)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
Rodriguez et al.
(2011)
This study
MHNG 2651.033
GY04-187
Guyana, Rupununi
River
Guyana, Sawarab River
c
Sturisoma robustum
MHNG 2588.055
PE96-001
Peru, Rio de las Piedras
2440 EU310460
Sturisomatichthys
citurensis
Fonchiiloricaria
nanodon
Fonchiiloricaria
nanodon
Spatuloricaria aff.
caquetaec
Spatuloricaria sp.
Nanay
Apistoloricaria
ommation
Apistoloricaria
ommation
Aposturisoma
myriodon
Aposturisoma
myriodon
Brochiloricaria
macrodon
Brochiloricaria sp.
Uruguay
Crossoloricaria aff.
bahuaja
Crossoloricaria
bahuaja
Crossoloricaria
cephalaspis
Crossoloricaria
cephalaspis
Crossoloricaria rhami
Crossoloricaria
variegata
Cteniloricaria napova
MHNG 2676.004
PA97-032
Panama, Rio Tuyra
2438 EU310462
MHNG 2710.048
PE08-199
Peru, Rio Monzon
2432 HM592626
MHNG 2710.060
PE08-336
Peru, Rio Aucayacu
2432 HM592627
MHNG 2710.050
PE08-230
Peru, Rio Huallaga
2421 HM592624
MHNG 2677.071
PE05-014
2422 HM592625
ANSP 182331
P6265
Rio Nanayb
Peru, Rio Amazonas
2417 KR478088
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Covain et al.
(2008)
Rodriguez et
(2011)
Rodriguez et
(2011)
Rodriguez et
(2011)
Rodriguez et
(2011)
This study
MHNG 2708.086
MUS 437
2423 KR478089
This study
1982 KR478423
This study
MHNG 2710.035
PE08-004
Rio Amazonasb
Peru, Rio Huacamayo
2435 KR477910
This study
2289 KR478244
This study
MHNG 2710.043
PE08-131
Peru, Rio Huyhuantal
2435 KR477911
This study
2287 KR478245
This study
LBP 5048
LBPN 24033
Brazil, Rio Paraguay
2425 KR478052
This study
1972 KR478386
This study
MCP 28414
MCP 28414
Brazil, Rio Ibicui-Mirim
2426 KR478053
This study
1986 KR478387
This study
MHNG 2710.072
PE08-714
Peru, Rio Cushabatai
2415 KR478091
This study
1983 KR478425
This study
ANSP 180793
P4078
Peru, Rio Madre de Dios 2417 KR478092
This study
1967 KR478426
This study
Stri-1449
53
Colombia, Rio San Juan
2421 KR478077
This study
2001 KR478411
This study
Stri-1577
22
Colombia, Rio Atrato
2421 KR478076
This study
1997 KR478410
This study
MHNG 2710.041
Stri-6781
PE08-120
36
Peru, Rio Aguaytia
Panama, Rio Tuira
2416 KR478083
2422 KR478075
This study
This study
1984 KR478417
1986 KR478409
This study
This study
MHNG 2704.030
SU07-650
Brazil, Paru de Oeste
River
2440 KR477882
This study
2086 KR478216
This study
Loricariichthys
maculatus
Loricariichthys
microdon
Metaloricaria
paucidens
Planiloricaria
cryptodon
Rineloricaria
lanceolata
Rineloricaria
osvaldoic
Rineloricaria
platyura
Sturisoma monopelte
2423 EU310452
2419 EU310445
2433 EU310449
2426 EU310450
2427 EU310451
2427 EU310454
2418 EU310456
2423 EU310457
2439 EU310461
1967 FJ013231
1994 HM623647
1996 HM623639
2228 HM623650
2292 HM623649
2231 HM623645
2029 HM623648
1950 HM623644
1964 HM623653
2212 HM623642
1934 HM623643
2064 HM623637
1991 HM623646
2211 HM623640
2008 HM623652
2204 HM623641
1965 HM623651
2547 HM623636
2259 HM623635
al.
2006 HM623656
al.
2006 HM623657
al.
1971 HM623654
al.
1980 HM623655
(continued on next page)
496
Table 2 (continued)
Species
Catalog number
Field number
Locality
mt 12S + 16S bases
+ GenBank No.
Ref.
F-RTN4 bases
+ GenBank No.
Ref.
Cteniloricaria
platystoma
Cteniloricaria
platystoma
Cteniloricaria
platystoma
Cteniloricaria
platystoma
Cteniloricaria
platystoma
Dasyloricaria latiura
Dasyloricaria
tuyrensis
Farlowella
schreitmuelleri
Farlowella acus
MHNG 2672.067
SU05-340
2439 KR477888
This study
2091 KR478222
This study
MHNG 2674.003
SU05-039
2441 KR477889
This study
2090 KR478223
This study
MHNG 2650.082
GY04-336
2437 KR477881
This study
2090 KR478215
This study
MHNG 2700.054
GF07-265
2437 KR477902
This study
2089 KR478236
This study
MHNG 2643.015
GF00-352
2439 KR477887
This study
2089 KR478221
This study
Stri-1559
Stri-4140
20
51
Suriname, Corantijn
River
Suriname, Suriname
River
Guyana, Essequibo
River
French Guiana, Mana
River
French Guiana,
Marouini River
Panama, Rio Atrato
Panama, Rio Tuira
2424 KR477966
2424 KR477965
This study
This study
2017 KR478300
2018 KR478299
This study
This study
MHNG 2601.087
BR98-106
Brazil, Rio Guamá
2437 KR477943
This study
2241 KR478277
This study
MER95T-22
42
2440 KR477936
This study
2311 KR477936
This study
Farlowella aff. rugosa
Farlowella amazona
Farlowella curtirostra
Farlowella hahni
Farlowella knerii
Farlowella
mariaelenae
Farlowella martini
Farlowella nattereri
ANSP 179 768
MHNG 2601.065
MER95T-13
MHNG 2678.022
MHNG 2710.052
VZ-59
T2200
BR98-052
43
PR-029
PE08-259
45
Venezuela, Valencia
Lake
Guyana, Simoni River
Brazil, Rio Acara
Venezuela, Rio Motatan
Argentina, Santa Fé
Peru, Rio Aspuzana
Venezuela, Rio Caipe
2435
2432
2435
2437
2437
2439
This
This
This
This
This
This
2298
2299
2301
2235
2234
2309
This
This
This
This
This
This
VZ-126
MHNG 2650.099
49
GY04-291
2436 KR477940
2439 KR477952
This study
This study
2307 KR478274
2305 KR478286
This study
This study
Farlowella nattereri
MHNG 2654.067
GY04-306
2438 KR477944
This study
2306 KR478278
This study
Farlowella
oxyrryncha
Farlowella
oxyrryncha
Farlowella
oxyrryncha
Farlowella
oxyrryncha
Farlowella
oxyrryncha
Farlowella
oxyrryncha
Farlowella
oxyrryncha
Farlowella
paraguayensis
Farlowella
paraguayensis
Farlowella
platorynchus
Farlowella
platorynchus
Farlowella
platorynchus
Farlowella reticulata
MHNG 2710.034
PE08-051
Venezuela, Rio Aroa
Guyana, Kurupukari
cross
Guyana, Kurupukari
cross
Peru, Rio Huacamayo
2437 KR477953
This study
2239 KR478287
This study
MHNG 2613.035
CA 21
Peru, Rio Ucayali
2437 KR477960
This study
2241 KR478294
This study
MHNG 2601.095
BR98-118
Brazil, Rio Guamá
2440 KR477958
This study
2240 KR477958
This study
LBP 2441
LBPN 16200
Brazil, Rio Araguiaia
2436 KR477956
This study
2183 KR478290
This study
MHNG 2710.069
PE08-698
Peru, Rio Neshua
2437 KR477955
This study
2242 KR478289
This study
MHNG 2710.081
PE08-823
2437 KR477957
This study
2242 KR478291
This study
LBP4043
LBPN 22907
Brazil, Rio Jurua
2437 KR477959
This study
2228 KR478293
This study
Stri-2205
25
2437 KR477961
This study
2236 KR478295
This study
LBP 5217
LBPN 26396
Paraguay, Arroyo
Curuguati
Brazil, Rio Paraná
2434 KR477962
This study
2238 KR478296
This study
MHNG 2650.096
GY04-290
2435 KR477949
This study
2296 KR478283
This study
MHNG 2602.021
BR98-163
Guyana, Kurupukari
cross
Brazil, Rio Peritoro
2435 KR477950
This study
2302 KR478284
This study
MHNG 2710.094
PE08-906
Peru, Rio Ucayali
2432 KR477951
This study
2301 KR478285
This study
MHNG 2683.081
GF06-637
2439 KR477963
This study
2243 KR478297
This study
MHNG 2683.070
GF06-588
2438 KR477942
This study
2242 KR478276
This study
MHNG 2681.060
GF06-118
2437 KR477964
This study
2242 KR478298
This study
Farlowella smithi
Farlowella taphorni
Farlowella vittata
Harttia aff. punctata
Harttia carvalhoi
ANSP 180541
VZ-89
VZ-63
LBP 5839
MHNG 2587.027
P4099
48
46
LBP 28353
BR 1236
2436
2433
2438
2433
2432
This
This
This
This
This
2236
2168
2303
2084
2046
This
This
This
This
This
Harttia carvalhoi
LBP 2115
LBP 21352
Harttia
Harttia
Harttia
Harttia
LBP 5859
LBP 5863
LBP 7505
MHNG 2690.013
LBP 28331
LBP 28339
LBP 34804
SU01-445
MHNG 2643.022
GF99-202
French Guiana, Maroni
River
French Guiana, Mana
River
French Guiana, Oyapock
River
Peru, Rio Manuripe
Venezuela, Rio Mayupa
Venezuela, Rio Caipe
Brazil, Rio Tocantins
Brazil, Rio Paraíba do
Sul
Sul
Brazil, Rio Tapajós
Suriname, Coppename
River
River
dissidens
dissidens
duriventris
fluminensis
Harttia fowleri
KR477948
KR477937
KR477938
KR477941
KR477954
KR477939
KR477945
KR477946
KR477947
KR477898
KR477891
study
study
study
study
study
study
study
study
study
study
study
KR478282
KR478271
KR478272
KR478275
KR478288
KR478273
KR478279
KR478280
KR478281
KR478232
KR478225
study
study
study
study
study
study
study
study
study
study
study
2433 KR477890
This study
2046 KR478224
This study
2435
2435
2432
2435
This
This
This
This
1955
1954
1951
2092
This
This
This
This
KR477892
KR477914
KR477915
KR477884
2442 KR477880
study
study
study
study
This study
KR478226
KR478248
KR478249
KR478218
2086 KR478214
study
study
study
study
This study
497
Table 2 (continued)
Species
Catalog number
Field number
Locality
mt 12S + 16S bases
+ GenBank No.
Ref.
F-RTN4 bases
+ GenBank No.
Ref.
Harttia gracilis
Harttia guianensis
LBP 6331
MHNG 2662.091
LBP 29819
GF03-160
2433 KR477916
2438 KR477885
This study
This study
2041 KR478250
2092 KR478219
This study
This study
Harttia guianensis
MHNG 2680.053
RV-21
2443 KR477886
This study
2092 KR478220
This study
Harttia kronei
MHNG 2586.058
BR 1166
2424 KR477900
This study
2081 KR478234
This study
Harttia kronei
LBP 2661
LBP 17427
2426 KR477894
This study
2083 KR478228
This study
Harttia kronei
LBP 2883
LBP 18609
2425 KR477895
This study
2080 KR478229
This study
Harttia kronei
LBP 1269
LBP 11215
2426 KR477899
This study
2080 KR478233
This study
Harttia
Harttia
Harttia
Harttia
LBP 6847
LBP 6492
DZSJRP 2819
LBP 2121
LBP 31528
LBP 31545
BR98-747
LBP 21362
2435
2436
2429
2435
KR477918
KR477917
KR477903
KR477896
This
This
This
This
study
study
study
study
2068
2068
2072
2041
KR478252
KR478251
KR478237
KR478230
This
This
This
This
study
study
study
study
LBP 5836
MHNG 2645.059
MHNG 2645.053
LBP 5845
LBP 5860
LBP 5861
LBP 5838
LBP 28348
BR 995
BR 1051
LBP 28327
LBP 28333
LBP 28335
LBP 28352
Brazil, Rio Paraná
French Guiana,
Approuague River
French Guiana,
Sinnamary River
Brazil, Rio Ribeira de
Iguape
Iguape
Iguape
Iguape
Brazil, Rio São Francisco
Sul
Brazil, Rio Xingu
Brazil, Rio Xingu
Brazil, Rio Xingu
2429
2431
2430
2433
2432
2436
2429
KR477897
KR477893
KR477905
KR477907
KR478245
KR477908
KR477904
This
This
This
This
This
This
This
study
study
study
study
study
study
study
2060
2084
2084
1971
1973
1973
2061
KR478231
KR478227
KR478239
KR478241
KR478246
KR478242
KR478238
This
This
This
This
This
This
This
study
study
study
study
study
study
study
LBP 6528
LBP 31652
Brazil, Rio São Francisco 2431 KR477919
This study
2061 KR477919
This study
LBP 5857
LBP 5850
LBP 5838
LBP 28329
LBP 28367
LBP 28351
2436 KR477906
2433 KR477901
Brazil, Rio São Francisco 2429 KR477920
This study
This study
This study
1968 KR478240
2085 KR478235
2061 KR478254
This study
This study
This study
MHNG 2674.042
SU05-001
2438 KR477883
This study
2092 KR478217
This study
LBP 5835
MHNG 2704.029
LBP 28346
SU07-644
Suriname, Suriname
River
Brazil, Paru de Oeste
River
Suriname, Nassau
Mountains
Suriname, Nassau
Mountains
Suriname, Nassau
Mountains
French Guiana, Trinité
Mountains
Mountains
Mountains
French Guiana,
Balenfois Mountains
French Guiana,
Balenfois Mountains
French Guiana,
Balenfois Mountains
Mountains
Mountains
Mountains
French Guiana, Lucifer
Mountains
Mountains
Mountains
Mountains
Mountains
Mountains
French Guiana, Crique
Limonade
2433 KR477913
2437 KR477909
This study
This study
2054 KR478247
2092 KR478243
This study
This study
2418 KR478145
This study
2026 KR478474
This study
2417 KR478146
This study
2026 KR478475
This study
2418 KR478131
This study
2026 KR478460
This study
2418 KR478164
This study
2021 KR478490
This study
2418 KR478165
This study
2022 KR478491
This study
2418 KR478135
This study
2022 KR478464
This study
2418 KR478136
This study
2005 KR478465
This study
2419 KR478159
This study
2005 KR478485
This study
2418 KR478133
This study
2005 KR478462
This study
2418 KR478144
This study
2022 KR478473
This study
2422 KR478134
This study
2022 KR478463
This study
2418 KR478139
This study
2022 KR478468
This study
2414 KR478153
This study
2152 KR478479
This study
2414 KR478154
This study
2149 KR478480
This study
2414 KR478155
This study
2152 KR478481
This study
2414 KR478156
This study
2152 KR478482
This study
2414 KR478158
This study
2152 KR478484
This study
2414 KR478157
This study
2148 KR478483
This study
2414 KR478478
This study
NA
–
leiopleura
leiopleura
longipinna
loricariformis
Harttia novalimensis
Harttia punctata
Harttia punctata
Harttia sp. 1 Xingu
Harttia sp. 2 Xingu
Harttia sp. 3 Xingu
Harttia sp. Rio São
Francisco
Harttia sp. Serra do
Cipó
Harttia sp. Tapajos
Harttia sp. Tocantins
Harttia sp. Três
Marias
Harttia surinamensis
Harttia torrenticola
Harttia tuna
Harttiella crassicauda MHNG 2679.098
MUS 306
MUS 221
MUS 231
Harttiella intermedia
MHNG 2713.087
MUS 650
MHNG 2713.087
MUS 651
MHNG 2713.087
MUS 652
Harttiella longicauda
MHNG 2723.094
MUS 470
MHNG 2723.094
MUS 463
MHNG 2723.094
MUS 456
MHNG 2699.070
GF07-026
MHNG 2699.070
GF07-082
MHNG 2699.070
GF07-111
Harttiella lucifer
MHNG 2721.088
GF10-034
Harttiella lucifer
MHNG 2721.088
GF10-043
Harttiella lucifer
MHNG 2721.088
GF10-037
Harttiella lucifer
MHNG 2721.091
GF10-051
Harttiella lucifer
MHNG 2721.091
GF10-053
Harttiella lucifer
MHNG 2721.091
GF10-055
Harttiella lucifer
MHNG 2712.085
MUS 592
498
Table 2 (continued)
Species
Catalog number
Field number
Locality
mt 12S + 16S bases
+ GenBank No.
Ref.
F-RTN4 bases
+ GenBank No.
Ref.
Harttiella lucifer
MHNG 2712.085
MUS 593
2414 KR478151
This study
NA
–
Harttiella lucifer
MHNG 2712.085
MUS 594
2413 KR478152
This study
NA
–
Harttiella parva
MHNG 2723.093
MUS 606
2416 KR478147
This study
2026 KR478476
This study
Harttiella parva
MHNG 2723.093
MUS 607
2416 KR478148
This study
2026 KR478477
This study
Harttiella parva
MHNG 2723.093
MUS 611
2416 KR478477
This study
2026 KR478478
This study
Harttiella pilosa
MHNG 2682.055
GF06-344
2417 KR478132
This study
2026 KR478461
This study
Harttiella pilosa
MHNG 2682.055
GF06-343
2417 KR478137
This study
2026 KR478466
This study
Harttiella pilosa
MHNG 2724.002
GF03-033
2419 KR478138
This study
2026 KR478467
This study
Hemiodontichthys
acipenserinus
Hemiodontichthys
acipenserinus
Hemiodontichthys
acipenserinus
Hemiodontichthys
acipenserinus
Ixinandria steinbachi
Lamontichthys
filamentosus
Lamontichthys
filamentosus
Lamontichthys
llanero
Lamontichthys
stibaros
Limatulichthys
punctatus
Limatulichthys
punctatus
Limatulichthys
punctatus
Limatulichthys
punctatus
Limatulichthys
punctatus
Limatulichthys
punctatus
Limatulichthys
punctatus
Loricaria sp. Guyana
Loricaria sp. Guyana
Loricaria aff.
nickeriensis
Loricaria aff.
parnahybae
Loricaria apeltogaster
Loricaria cataphracta
MHNG 2588.057
PE96-005
Limonade
Limonade
French Guiana, Atachi
Bakka Mountains
Bakka Mountains
Bakka Mountains
French Guiana, Tortue
Mountains
Mountains
Mountains
Peru, Madre de Dios
2425 KR478140
This study
2259 KR478469
This study
MHNG 2602.007
BR98-138
Brazil, Rio Guamá
2421 KR478141
This study
2217 KR478470
This study
MCP 28819
MCP 28819
Brazil, Rio Purus
2424 KR478142
This study
2238 KR478471
This study
LBP 5524
LBPN 26640
Brazil, Rio Jari
2422 KR478143
This study
2283 KR478472
This study
NA
MHNG 2680.009
IXS2
MUS 310
Argentina, Salta
Peru, aquarium trade
2427 KR477986
2434 KR478262
This study
This study
2513 KR478320
2116 KR478263
This study
This study
LBP 162
LBPN 4038
Brazil, Rio Branco
2433 KR477930
This study
2115 KR478264
This study
MHNG 2749.019
MUS 356
2434 KR477928
This study
2089 KR478262
This study
MHNG 2710.049
PE08-224
Colombia, aquarium
trade
Peru, Rio Huallaga
2433 KR477931
This study
2040 KR478265
This study
ANSP 182707
P6232
Peru, Rio Itaya
2424 KR478095
This study
1957 KR478429
This study
MHNG 2602.009
BR98-140
Brazil, Rio Guamá
2424 KR478094
This study
1963 KR478428
This study
AUM 42223
V5319
Venezuela, Rio Orinoco
2425 KR478097
This study
1960 KR478431
This study
LBP 5055
LBPN 23618
Brazil, Rio Jurua
2422 KR478096
This study
1959 KR478430
This study
MHNG 2710.037
PE08-112
Peru, Rio Agaytia
2427 KR478093
This study
1959 KR478427
This study
LBP 5285
LBPN 26769
Brazil, Rio Jari
2427 KR478183
This study
1956 KR478508
This study
LBP 5249
LBPN 26472
Brazil, Rio Jari
2426 KR478182
This study
1958 KR478507
This study
MHNG 2650.057
MHNG 2651.031
MHNG 2681.009
GY04-110
GY04-191
GF06-044
2424 KR478068
2424 KR478069
2424 KR478061
This study
This study
This study
1979 KR478402
1983 KR478403
1944 KR478395
This study
This study
This study
LBP 1615
LBPN 11690
Guyana, Pirara River
Guyana, Sawarab bridge
River
Brazil, Rio Araguaia
2434 KR478059
This study
1977 KR478393
This study
NA
MHNG 2749.022
NA
GF98-044
2427 KR478056
2428 KR478057
This study
This study
1973 KR478390
1943 KR478391
This study
This study
Loricaria cataphracta MHNG 2683.061
GF06-570
2425 KR478062
This study
1933 KR478396
This study
SU08-042
2424 KR478054
This study
1932 KR478388
This study
SU08-943
2424 KR478055
This study
1932 KR478389
This study
Loricaria cf. lata
Loricaria nickeriensis
LBP 5053
MHNG 2672.080
LBPN 16148
SU05-334
2423 KR478058
2424 KR478060
This study
This study
1961 KR478392
1932 KR478394
This study
This study
Loricaria prolixa
Loricaria prolixa
Loricaria simillima
LBP 7511
LBP 7511
MHNG 2677.075
LBPN 34925
LBPN 34924
PE05-030
2429 KR478063
2428 KR478064
2424 KR478065
This study
This study
This study
1975 KR478397
1975 KR478398
1950 KR478399
This study
This study
This study
Loricaria sp.
Araguaia
Loricaria sp. Branco
Loricaria sp. Branco
Loricaria sp. Mato
Grosso
LBP 5049
LBPN 11506
Argentina, Entre Rios
French Guiana, Kourou
River
French Guiana, Mana
River
Suriname, Suriname
River
Suriname, Commewijne
River
Suriname, Corantijn
River
Brazil, Rio Paraná
Brazil, Rio Paraná
Rio Amazonasb
2429 KR478066
This study
2006 KR478400
This study
LBP 169
LBP 223
MCP 36566
LBPN 4032
LBPN 4101
MCP 36566
Brazil, Rio Branco
Brazil, Rio Branco
Paraguay, Mato Grosso
2424 KR478067
2424 KR478090
2429 KR478070
This study
This study
This study
1969 KR478401
1967 KR478424
1949 KR478404
This study
This study
This study
499
Table 2 (continued)
Species
Catalog number
Field number
Locality
mt 12S + 16S bases
+ GenBank No.
Ref.
F-RTN4 bases
+ GenBank No.
Ref.
Loricaria sp. Orinoco
Loricaria sp.
Paraguay
Loricaria sp.
Rupununi
Loricaria
tucumanensis
Loricariichthys anus
AUM 42224
MHNG 2677.003
V5315
PY9093
Paraguay, Rio Paraguay
2426 KR478071
2427 KR478072
This study
This study
1961 KR478071
1930 KR478406
This study
This study
MHNG 2651.036
GY04-129
2427 KR478074
This study
1967 KR478408
This study
NA
AG06-018
Guyana, Rupununi
River
Argentina, Ita-Ibate
2423 KR478073
This study
1976 KR478407
This study
MCP 28415
MCP 28415
2430 KR478175
This study
2280 KR478500
This study
MCP 21317
MCP 21317
2430 KR478174
This study
2276 KR478499
This study
Loricariichthys
castaneus
Loricariichthys
castaneus
Loricariichthys
castaneus
Loricariichthys cf.
ucayalensis
Loricariichthys derbyi
Loricariichthys derbyi
Loricariichthys
labialis
Loricariichthys
melanocheilus
Loricariichthys
platymetopon
Loricariichthys sp.
Amazonas
Loricariichthys sp.
Jari
Loricariichthys sp.
Jari
Loricariichthys sp.
Orinoco
Loricariichthys sp.
Rio Baia
Metaloricaria nijsseni
LBP 578
MHNG 2583.068
LBPN 7309
BR 162
2429 KR478176
2430 KR478114
This study
This study
2272 KR478501
2230 KR478444
This study
This study
LBP 7489
LBPN 35548
Brazil, Rio Grande do
Sul
Sul
Brazil, Rio Guiaba
Brazil, surroundings of
Rio de Janeiro
Brazil
2429 KR478115
This study
2275 KR478445
This study
LBP 7490
LBPN 35549
Brazil
2429 KR478116
This study
2279 KR478446
This study
ANSP 182668
P6046
Peru, Rio Nanay
2424 KR478117
This study
2197 KR478447
This study
MHNG 2602.061
LBP 5531
MHNG 2677.001
BR98-250
LBPN 27214
PY9094
2428 KR478119
2425 KR478171
2429 KR478178
This study
This study
This study
2240 KR478449
2243 KR478497
1956 KR478503
This study
This study
This study
MCP 28915
MCP 28915
Brazil, Rio Ibicui-Mirim
2426 KR478120
This study
2271 KR478450
This study
MHNG 2677.004
PY9098
2427 KR478118
This study
2232 KR478448
This study
Stri-531
28
Peru, Rio Amazonas
2426 KR478173
This study
2231 KR478498
This study
LBP 5517
LBPN 26622
Brazil, Rio Jari
2428 KR478112
This study
2228 KR478442
This study
LBP 5420
LBPN 27135
Brazil, Rio Jari
2427 KR478121
This study
2232 KR478451
This study
AUM 42225
V5310
2426 KR478109
This study
NA
–
LBP 3094
LBPN 19263
Brazil, Rio Baia
2429 KR478113
This study
2226 KR478443
This study
MHNG 2674.025
SU05-012
2435 KR477934
This study
2089 KR478268
This study
Metaloricaria nijsseni MHNG 2672.053
SU05-359
2437 KR477967
This study
2089 KR478301
This study
Metaloricaria nijsseni MHNG 2690.016
SU01-459
2441 KR477933
This study
2089 KR478267
This study
Metaloricaria
paucidens
Paraloricaria agastor
Paraloricaria agastor
Paraloricaria vetula
Pseudohemiodon aff.
apithanos
Pseudohemiodon aff.
apithanos
Pseudohemiodon aff.
apithanos
Pseudohemiodon
apithanos
Pseudohemiodon
apithanos
Pseudohemiodon
laminus
Pseudohemiodon
laticeps
Pseudohemiodon
laticeps
Pseudohemiodon sp.
MHNG 2681.042
GF06-108
2439 KR477932
This study
2073 KR478266
This study
NA
NA
NA
MHNG 2677.070
AG06-017
AG06-019
YC-008
PE05-009
2427
2426
2425
2416
This
This
This
This
1984
1984
1984
2003
This
This
This
This
ANSP 178115
P1759
MHNG 2710.086
PE08-852
Suriname, Suriname
River
Suriname, Corantijn
River
Suriname, Coppename
River
River
Argentina, Ita-Ibate
Argentina, Puerto Abra
Argentina, Entre Rios
Rio Amazonasb
Rio Itayab
MHNG 2677.073
PE05-020
MHNG 2677.074
PE05-026
MHNG 2677.077
PE05-035
LBP 4332
Pseudoloricaria
laeviuscula
Pseudoloricaria
laeviuscula
Pseudoloricaria
laeviuscula
Pseudoloricaria
laeviuscula
KR478167
KR478168
KR478166
KR478080
study
study
study
study
KR478493
KR478494
KR478492
KR478414
study
study
study
study
2418 KR478078
This study
2003 KR478412
This study
2411 KR478079
This study
2004 KR478413
This study
2414 KR478110
This study
2012 KR478440
This study
2414 KR478081
This study
2012 KR478415
This study
2426 KR478082
This study
2009 KR478416
This study
LBPN 24034
Rio Itayab
Rio Nanayb
Rio Amazonasb
2424 KR478169
This study
2003 KR478495
This study
NA
NA
Argentina, Corrientes
2424 KR478170
This study
2004 KR478496
This study
MHNG 2677.076
PE05-034
2406 KR478111
This study
1980 KR478441
This study
AUM 44646
G5231
Rio Amazonasb
Guyana, Takutu River
2427 KR478099
This study
1990 KR478433
This study
AUM 44646
G5232
2427 KR478100
This study
1990 KR478434
This study
AUM 44646
G5233
2427 KR478103
This study
1990 KR478436
This study
INPA 28991
MUS 517
Brazil, Rio Madeira
2430 KR478098
This study
1990 KR478432
This study
500
Table 2 (continued)
Species
Catalog number
Field number
Locality
mt 12S + 16S bases
+ GenBank No.
Ref.
F-RTN4 bases
+ GenBank No.
Ref.
Pterosturisoma
microps
Rhadinoloricaria aff.
macromystax
Rhadinoloricaria sp.
Orinoco
Orinoco
Orinoco
Rineloricaria
aequalicuspis
Rineloricaria aff.
cadeae
Rineloricaria aff.
cadeae
Rineloricaria aff.
fallax
Rineloricaria aff.
langei
Rineloricaria aff.
latirostris
Rineloricaria aff.
phoxocephala
Rineloricaria aff.
phoxocephala
Rineloricaria aff.
phoxocephala
Rineloricaria aff.
phoxocephala
Rineloricaria aff.
phoxocephala
Rineloricaria aff.
phoxocephala
Rineloricaria aff.
stewarti
Rineloricaria aff.
stewarti
Rineloricaria aff.
stewarti
Rineloricaria aff.
stewarti
Rineloricaria aff.
stewarti
Rineloricaria aff.
stewarti
Rineloricaria aff.
stewarti
Rineloricaria aff.
strigilata
Rineloricaria
altipinnis
Rineloricaria
altipinnis
Rineloricaria cadeae
MHNG 2677.072
PE05-016
Peru, aquarium trade
2439 KR477921
This study
2075 KR478255
This study
ANSP 182349
T2364
2414 KR478084
This study
1967 KR478418
This study
ANSP 185044
T4029
Guyana, Rupununi
River
2415 KR478085
This study
1979 KR478419
This study
AUM 42094
V5507
2414 KR478086
This study
1980 KR478420
This study
AUM 42094
V5508
2415 KR478087
This study
1979 KR478421
This study
MCP 29282
MCP 29282
2427 KR478213
This study
2499 KR478534
This study
LBP 901
LBPN 7359
Brazil, Arroio Molha
Coco
Brazil, Eldorado do Sul
2424 KR477987
This study
2492 KR478321
This study
LBP4772
LBPN 25580
Brazil, Rio Guiaba
2424 KR477976
This study
2533 KR478310
This study
LBP 4085
LBPN 23512
Brazil, Rio Japim
2420 KR477979
This study
1984 KR478313
This study
LBP 1189
LBPN 10585
Brazil, Rio Iguaçu
2425 KR478323
This study
2501 KR478324
This study
MHNG 2749.014
MUS 491
Brazil, aquarium trade
2425 KR478185
This study
2507 KR478510
This study
MCP 28832
495
Brazil, Rio Purus
2427 KR478104
This study
2243 KR478437
This study
MCP 28832
496
Brazil, Rio Purus
2426 KR478126
This study
2246 KR478455
This study
MCP 28832
NA
Brazil, Rio Purus
2427 KR478125
This study
2243 KR478454
This study
LBP 4123
LBPN 23617
Brazil, Rio Jurua
2431 KR478127
This study
2242 KR478456
This study
MHNG 2749.013
PI 720
Peru, Rio Momon
2431 KR478128
This study
2241 KR478457
This study
ANSP 182368
T2101
2431 KR478038
This study
2244 KR478372
This study
MHNG 2663.003
GF03-196
2425 KR478023
This study
2209 KR478357
This study
MHNG 2681.019
GF06-077
2422 KR478028
This study
2214 KR478362
This study
MHNG 2682.091
GF06-428
2425 KR478025
This study
2209 KR478359
This study
MHNG 2683.049
GF06-538
2425 KR478024
This study
2209 KR478358
This study
MHNG 2617.015
MUS
2425 KR478029
This study
2209 KR478363
This study
MHNG 2704.040
SUJM-064
2429 KR478035
This study
2210 KR478369
This study
MHNG 2749.011
SU08-945
2426 KR478037
This study
2210 KR478371
This study
LBP 2949
LBPN 19534
2417 KR477992
This study
2258 KR478326
This study
Stri-3589
40
2425 KR478026
This study
1866 KR478360
This study
MHNG 2709.086
PA97-045
2423 KR478027
This study
1866 KR478361
This study
MCP 21217
MCP 21217
2427 KR477991
This study
2479 KR478325
This study
NA
RC
Guyana, Essequibo
River
French Guiana,
Approuague River
River
River
French Guiana, Mana
River
French Guiana,
Sinnamary River
Suriname, Suriname
River
Suriname, Commewijne
River
Brazil, Córrego da
batata
Panama, Rio
Chucunaque
Panama, Rio
Chucunaque
Sul
Argentina, Salta
2429 KR477989
This study
2511 KR478323
This study
MHNG 2680.033
NA
Argentina, Rio Sali
2426 KR477988
This study
2511 KR478322
This study
LBP 1248
LBPN 11175
2429 KR478108
This study
2498 KR478439
This study
LBP 771
LBPN 8534
Brazil, Rio Ribeira do
Iguape
Brazil, Rio Marumbi
2429 KR478347
This study
2802 KR478348
This study
Colombia, aquarium
trade
Suriname, Corantijn
River
Guyana, Rupununi
River
Guyana, Berbice River
Guyana, Demerara
River
2428 KR477984
This study
2206 KR478318
This study
2429 KR477980
2427 KR477975
This study
This study
2284 KR478314
2280 KR478309
This study
This study
2427 KR477978
This study
2281 KR478312
This study
2427 KR477973
2427 KR477977
This study
This study
2281 KR478307
2280 KR478311
This study
This study
Rineloricaria
catamarcensis
Rineloricaria
catamarcensis
Rineloricaria cf.
kronei
Rineloricaria cf.
latirostris
Rineloricaria
eigenmanni
Rineloricaria fallax
NA
MUS 494
MHNG 2651.054
MHNG 2672.015
GY04-146
SU05-412
MHNG 2650.072
GY04-009
MHNG 2651.034
MHNG 2650.067
GY04-396
GY04-384
501
Table 2 (continued)
Species
Catalog number
Field number
Locality
mt 12S + 16S bases
+ GenBank No.
Ref.
Rineloricaria formosa
Rineloricaria formosa
Rineloricaria
heteroptera
Rineloricaria
heteroptera
Rineloricaria
heteroptera
Rineloricaria
heteroptera
Rineloricaria hoehnei
LBP 4343
ANSP 185291
AUM 43885
AUM 43886
LBPN 24075
V5405
V5531
V5530
Brazil, Boa Vista
2429
2429
2429
2429
This
This
This
This
AUM 43886
V5534
2429 KR477969
This study
2219 KR478303
This study
AUM 43886
V5529
2429 KR477970
This study
2219 KR478304
This study
AUM 43928
V5562
2428 KR477971
This study
2220 KR478305
This study
MHNG 2678.018
PR-018
2424 KR477972
This study
2221 KR478306
This study
LBP 729
LBPN 8268
2426 KR477985
This study
2208 KR478319
This study
MHNG 2613.029
CA-01
Paraguay, Paraguay
River
Brazil, Jaragua do Sul,
Rio Itapocu
Peru, Rio Ucayali
2423 KR478203
This study
2232 KR478528
This study
MHNG 2651.029
GY04-172
2424 KR477996
This study
2231 KR478330
This study
MHNG 2651.059
GY04-252
2424 KR477995
This study
2232 KR478329
This study
MHNG 2680.008
MUS 244
Guyana, Mauishparu
River
Brazil, Purus River
2424 KR477997
This study
2232 KR478331
This study
Stri-2422
26
2425 KR478326
This study
2219 KR478327
This study
LBP 1557
LBPN 11505
Argentine Rio
Corrientes
2424 KR477994
This study
2198 KR478328
This study
MHNG 2710.033
PE08-053
Peru, Rio Huacamayo
2423 KR478202
This study
2230 KR478527
This study
MCP 38347
MCP 38347
2426 KR478018
This study
2804 KR478352
This study
LBP 4409
LBPN 24247
2427 KR477983
This study
2204 KR478317
This study
MHNG 2680.011
MCP 21263
MUS 312
MCP 21263
2427 KR478013
2426 KR478212
This study
This study
2203 KR478347
2504 KR478533
This study
This study
MHNG 2680.034
MUS
2421 KR477999
This study
2214 KR478333
This study
MHNG 2749.015
PI 719
Sul
Brazil, Rio Negro,
Barcelos
Sul
Argentina, Rio CunaPiru
Peru, Rio Momon
2425 GBxxxxx
This study
2280 KR478334
This study
MHNG 2678.014
LBP 5
LBP 1319
PR-009
LBPN 3656
LBPN 11000
Argentina, Santa Fé
Brazil, Rio Tibagi
2433 KR478012
2433 KR478190
2432 KR478040
This study
This study
This study
2522 KR478346
2506 KR478515
2021 KR478375
This study
This study
This study
LBP 1731
LBPN 12864
Brazil, Rio Amazonas
2421 KR478036
This study
2220 KR478370
This study
MHNG 2601.081
BR98-088
Brazil, Rio Guamá
2428 KR478123
This study
NA
–
MHNG 2663.004
GF03-193
2427 KR478102
This study
953 KR478435
This study
NA
MUS 334
French Guiana,
Approuague River
Brazil, Rio Purus
2426 KR478129
This study
2229 KR478458
This study
MHNG 2650.074
GY04-197
2424 KR478122
This study
2220 KR478452
This study
MHNG 2749.012
GF99-009
French Guiana, Kaw
2427 KR478101
This study
NA
–
MHNG 2601.063
BR98-049
Brazil, Rio Acara
2428 KR478124
This study
949 KR478453
This study
MCP 28832
497
Brazil, Rio Purus
2426 KR478130
This study
931 KR478459
This study
MCP 21195
MCP 21195
Brazil, Lagoa Fortaleza
2427 KR478106
This study
2504 KR478438
This study
Stri-1399
52
Colombia, Rio Baudo
2426 KR478001
This study
2244 KR478335
This study
MHNG 2587.054
BR1253
2426 KR478194
This study
2790 KR478519
This study
MHNG 2587.015
BR1215
2424 KR478191
This study
2507 KR478516
This study
LBP 1750
LBPN 11818
Sul
Sul
2428 KR478040
This study
2034 KR478040
This study
MHNG 2586.083
BR1190
Brazil, Rio Betari
2429 KR478192
This study
2515 KR478517
This study
MHNG 2586.072
BR1184
Brazil, Rio Betari
2429 KR478172
This study
NA
–
LBP 2654
LBPN 17410
Brazil, Rio Carombé
2427 KR478034
This study
2208 KR478368
This study
Rineloricaria
jaraguensis
Rineloricaria
lanceolata
Rineloricaria
lanceolata
Rineloricaria
lanceolata
Rineloricaria
lanceolata
Rineloricaria
lanceolata
Rineloricaria
lanceolata
Rineloricaria
lanceolata
Rineloricaria
longicauda
Rineloricaria melini
Rineloricaria melini
Rineloricaria
microlepidogaster
Rineloricaria
misionera
Rineloricaria
morrowi
Rineloricaria parva
Rineloricaria parva
Rineloricaria
pentamaculata
Rineloricaria
platyura
Rineloricaria
platyura
Rineloricaria
platyura
Rineloricaria
platyura
Rineloricaria
platyura
Rineloricaria
platyura
Rineloricaria
platyura
Rineloricaria
platyura
Rineloricaria
quadrensis
Rineloricaria
sneiderni
Rineloricaria sp.
Agua Santa
Rineloricaria sp. Ao
Itai
Rineloricaria sp.
Araguaia
Rineloricaria sp.
Betari
Rineloricaria sp.
Betari
Rineloricaria sp.
Carombé
KR477974
KR477981
KR477982
KR477968
study
study
study
study
F-RTN4 bases
+ GenBank No.
Ref.
2285
2253
2253
2219
This
This
This
This
KR477974
KR478315
KR478316
KR478302
study
study
study
study
502
Table 2 (continued)
Species
Catalog number
Field number
Locality
mt 12S + 16S bases
+ GenBank No.
Ref.
F-RTN4 bases
+ GenBank No.
Ref.
Rineloricaria sp.
Corantijn
Rineloricaria sp.
Corantijn
Rineloricaria sp.
Corantijn
Rineloricaria sp.
Corrego Seco
Rineloricaria sp.
Guama 4
Rineloricaria sp.
Guama 5
Rineloricaria sp.
Guama 5
Rineloricaria sp.
Guama 5
Rineloricaria sp.
Guama 6
Rineloricaria sp.
Huacamayo
Rineloricaria sp.
Huacamayo
Rineloricaria sp.
Macacu
Rineloricaria sp.
Maroni 2
Rineloricaria sp.
Maroni 2
Rineloricaria sp.
Martinso
Rineloricaria sp.
Mongaguá
Rineloricaria sp.
Orinoco
Rineloricaria sp.
Orinoco
Rineloricaria sp.
Panama
Rineloricaria sp.
Paraiba do Sul
Rineloricaria sp.
Parguaza
Rineloricaria sp.
Piedade
Rineloricaria sp.
Previsto
Rineloricaria sp.
Puerto Ayacucho
Rineloricaria sp.
Ribeira
Rineloricaria sp. Rio
da Toca
Rineloricaria sp. São
João
João 2
João 2
Rineloricaria sp.
Ucayali
Rineloricaria sp.
Ucayali 2
Rineloricaria sp.
Uruguay
Rineloricaria sp. Von
Humbolt
Rineloricaria stewarti
MHNG 2671.085
SU05-450
MHNG 2704.035
SU07-017
MHNG 2722.048
SU01-417
MHNG 2586.065
BR1176
MHNG 2601.091
BR98-112
Suriname,
River
Suriname,
River
Suriname,
River
Brazil, Rio
Iguape
Brazil, Rio
Corantijn
2431 KR478005
This study
2188 KR478339
This study
Sipaliwini
2430 KR478002
This study
2188 KR478336
This study
Nickerie
2433 KR478006
This study
2194 KR478340
This study
Ribeira do
2429 KR478184
This study
2716 KR478509
This study
Guamá
2426 KR478199
This study
2474 KR478524
This study
MHNG 2601.044
BR98-010
Brazil, Rio Gurupi
2425 KR478200
This study
2508 KR478525
This study
MHNG 2601.042
BR98-008
Brazil, Rio Gurupi
2425 KR478201
This study
2510 KR478526
This study
MHNG 2602.025
BR98-167
Brazil, Rio Piria
2417 KR478198
This study
2508 KR478523
This study
MHNG 2601.063
BR98-047
Brazil, Rio Acara
2427 KR478501
This study
2285 KR478502
This study
MHNG 2613.032
CA-33
Peru, Rio Pisqui
2431 KR478015
This study
2453 KR478349
This study
MHNG 2710.032
PE08-057
Peru, Rio Huacamayo
2431 KR478016
This study
2528 KR478350
This study
MHNG 2587.082
BR1273
Brazil, Rio da Toca
2425 KR478017
This study
2506 KR478351
This study
MHNG 2749.018
SU08-441
2430 KR478003
This study
2249 KR478337
This study
MHNG 2749.018
SU08-442
2430 KR478004
This study
2249 KR478338
This study
MHNG 2586.089
BR1196
Suriname, Paloemeu
River
Suriname, Paloemeu
River
Brazil, Rio Martinso
2429 KR478020
This study
2802 KR478354
This study
LBP 2128
LBPN 21378
2429 KR478019
This study
2786 KR478353
This study
AUM 44067
V5435
Brazil, Riacho Sitio do
Meio
2428 KR478030
This study
2197 KR478364
This study
AUM 44067
V5437
2428 KR478031
This study
2197 KR478365
This study
MHNG 2749.016
PA00-011
Panama, Rio Ipeti
2427 KR478181
This study
989 KR478506
This study
MHNG 2583.065
BR 156
2427 KR478107
This study
NA
–
LBP 2308
LBPN 15846
2427 KR478032
This study
2217 KR478366
This study
MHNG 2586.055
BR1163
Sul
Venezuela, Rio
Parguaza
Brazil, Rio Piedade
2429 KR478039
This study
2226 KR478373
This study
MHNG 2710.047
PE08-186
Peru, Rio Previsto
2433 KR478195
This study
2528 KR478520
This study
MHNG 2749.017
MUS 489
2427 KR478033
This study
2279 KR478367
This study
MHNG 2586.088
BR1195
2429 KR478193
This study
2493 KR478518
This study
MHNG 2587.078
BR1269
Venezuela, aquarium
trade
Brazil, Rio Ribeira do
Iguape
Brazil, Rio Macacu
2423 KR478022
This study
2573 KR478356
This study
LBP 802
LBPN 7954
Brazil, Rio São João
2429 KR478188
This study
2793 KR478513
This study
MHNG 2586.052
BR1155
Brazil, Rio Araraguara
2428 KR478187
This study
2505 KR478512
This study
MHNG 2586.052
BR1156
Brazil, Rio Araraguara
2425 KR478186
This study
2501 KR478511
This study
MHNG 2710.095
PE08-905
Peru, Rio Ucayali
2426 KR478520
This study
2481 KR478521
This study
LBP 3273
LBPN 20081
Peru, Rio Huancabamba 2433 KR478021
This study
2536 KR478355
This study
MCP 21616
MCP 21616
2432 KR478189
This study
2506 KR478514
This study
MHNG 2710.068
PE08-697
2430 KR478197
This study
2532 KR478522
This study
MHNG 2651.057
GY04-257
2424 KR478009
This study
2289 KR478343
This study
Rineloricaria stewarti MHNG 2651.027
GY04-183
SU05-592
2429 KR478010
2427 KR478007
This study
This study
2286 KR478344
2289 KR478341
This study
This study
SU05-457
Sul
Peru, bosque Von
Humbolt
Guyana, Mauishparu
River
Suriname, Coppename
River
Suriname, Corantijn
River
2426 KR478008
This study
2270 KR478342
This study
503
Table 2 (continued)
Species
Catalog number
Field number
Locality
mt 12S + 16S bases
+ GenBank No.
Ref.
F-RTN4 bases
+ GenBank No.
Ref.
Rineloricaria
strigilata
Rineloricaria teffeana
Rineloricaria
uracantha
Rineloricaria
uracantha
Rineloricaria wolfei
Spatuloricaria cf.
evansii
Spatuloricaria
puganensis
Spatuloricaria
puganensis
Spatuloricaria sp.
Araguaia
Spatuloricaria sp.
Ireng
Spatuloricaria sp.
Magdalena 1
Spatuloricaria sp.
Magdalena 2
Spatuloricaria sp.
Magdalena 2
Spatuloricaria sp.
Magdalena 2
Spatuloricaria sp.
Orinoco
Sturisoma aureum
MCP 23751
MCP 23751
2426 KR477998
This study
2780 KR478332
This study
NA
Stri-1662
NA
23
Sul
SR, aquarium specimen
Panama, Rio Mandinga
2427 KR478011
2426 KR478180
This study
This study
2281 KR478345
2245 KR478505
This study
This study
LBP 2762
LBPN 18551
2424 KR478179
This study
2230 KR478504
This study
ANSP 182695
LBP 2385
P6236
LBPN 16145
Panama, Santa Rita
Arriba
Peru, Rio Itaya
2424 KR478105
2427 KR478042
This study
This study
NA
1958 KR478376
–
This study
ANSP 180486
P4743
Peru, Rio Yanatili
2421 KR478043
This study
1957 KR478377
This study
ANSP 180789
P4747
Peru, Rio Urubamba
2421 KR478044
This study
1958 KR478378
This study
LBP 1556
LBPN 11507
2427 KR478046
This study
1960 KR478380
This study
ANSP 182372
T2361
Guyana, Ireng River
2423 KR478047
This study
1978 KR478381
This study
MHNG 2722.096
MUS 353
2426 KR478045
This study
1981 KR478379
This study
IAvHP
6635
2418 KR478048
This study
1960 KR478382
This study
IAvHP
6637
2418 KR478049
This study
1961 KR478383
This study
IAvHP
6638
2419 KR478050
This study
1961 KR478384
This study
ANSP 185303
P4006
Colombia, aquarium
trade
Colombia, Rio
Magdalena, Honda
Colombia, Rio
Magdalena, Honda
Colombia, Rio
Magdalena, Honda
2427 KR478051
This study
1958 KR478385
This study
NA
MUS 286
2438 KR477925
This study
2287 KR478259
This study
Sturisoma aureum
MHNG 2684.019
MUS 357
2442 KR478160
This study
2287 KR478486
This study
Sturisoma cf.
guentheri
Sturisoma dariense
Sturisoma festivum
ANSP 182587
P6330
2446 KR477926
This study
1977 KR478260
This study
MHNG 2674.059
MER95T-20
PA97-019
44
2440 KR477922
2443 KR477923
This study
This study
2302 KR478256
2295 KR478257
This study
This study
Sturisoma frenatum
Sturisoma
nigrirostrum
Sturisoma
panamense
Sturisoma robustum
Sturisoma sp. Rio
Branco
Sturisomatichthys
leightoni
Ancistrus cirrhosusa
Stri-872
ANSP 178322
47
P1593
Panama, Darien
Venezuela, Maracaibo
Lake
Colombia, Rio San Juan
Peru, Rio Amazonas
2440 KR477924
2444 KR478162
This study
This study
2304 KR478258
2589 KR478488
This study
This study
MHNG 2674.058
PA00-013
Panama, Rio Ipeti
2443 KR478163
This study
2302 KR478489
This study
MHNG 2677.002
LBP 1615
PY9091
LBPN 4044
Brazil, Rio Branco
2443 KR478161
2442 KR477935
This study
This study
2540 KR478487
2583 KR478269
This study
This study
NA
MUS 327
2440 KR477927
This study
2307 KR478261
This study
MHNG 2645.037
MUS 202
Colombia, aquarium
specimen
Argentina, Rio Uruguay
2425 EU310442
Pseudorinelepis
genibarbisa
Guyanancistrus
brevispinisa
Guyanancistrus
longispinisa
Guyanancistrus
nigera
Hypostomus
gymnorhynchusa
Lasiancistrus
heteracanthusa
Lithoxus lithoidesa
MHNG 2588.079
PE96-040
Peru, Rio Ucayali
2436 HM592623
MHNG 2725.099
GF00-103
2439 JN855735
MHNG 2725.100
GF99-204
MHNG 2722.089
GF99-185
MHNG 2621.098
SU01-160
MHNG 2613.037
CA 13
River
River
River
French Guiana,
Approuague River
Peru, Rio Pauya
MHNG 2651.087
GY04-136
2428 JN855740
Pseudancistrus
barbatusa
Hemiancistrus
mediansa
Peckoltia oligospilaa
MHNG 2653.059
GF00-074
MHNG 2664.078
GF00-084
MHNG 2602.017
BR98-154
Guyana, Essequibo
River
River
Suriname, Tapanahony
River
Brazil, Rio Guamá
2439 KR478207
Covain et al.
(2008)
Rodriguez et al.
(2011)
Covain and FischMuller (2012)
This study
Peckoltia sabajia
MHNG 2651.016
GY04-029
2437 KR478206
This study
MHNG 2651.020
GY04-030
2441 KR478205
This study
MNHN 2011-0013
GF00-115
Guyana, Rupununi
River
Guyana, Rupununi
River
River
2435 KR478204
This study
1809 HM623638 Rodriguez et al.
(2011)
1925 HM623634 Rodriguez et al.
(2011)
1807 JN855772
1808 JN855757
1809 JN855759
1818 JN855789
1790 JN855787
1715 JN855777
1809 JN855761
1820 JF747011
Fisch-Muller et al.
(2012)
1814 JF747020
Fisch-Muller et al.
(2012)
1815 JF747019
Fisch-Muller et al.
(2012)
1808 JF747017
Fisch-Muller et al.
(2012)
1814 JF747016
Fisch-Muller et al.
(2012)
Peckoltia cavatica
Panaqolus koko
a
a
Colombia, aquarium
trade
Colombia, aquarium
trade
Peru, Rio Nanay
2439 JN855720
2438 JN855722
2442 JN855752
2432 JN855750
2442 JN855724
2437 JN855719
504
Table 2 (continued)
a
b
c
Species
Catalog number
Field number
Locality
mt 12S + 16S bases
+ GenBank No.
Ref.
F-RTN4 bases
+ GenBank No.
Ref.
Scobinancistrus
aureatusa
Hypancistrus zebraa
MHNG 2684.020
MUS 358
2442 KR478210
This study
1816 KR478531
This study
MHNG 2708.072
MUS 420
2435 KR478209
This study
1790 KR478530
This study
Megalancistrus cf.
parananusa
Neoplecostomus
micropsa
MHNG 2711.048
MUS 332
Brazil, aquarium trade,
Rio Xingub
Brazil, aquarium trade,
Rio Xingub
2442 KR478208
This study
1816 KR478529
This study
MHNG 2588.002
BR 1283
Brazil, Rio dos Frades
2442 KR478211
This study
1816 KR478532
This study
Outgroup.
According to the exporter.
Specimen reidentified after publication.
Harttiella lucifer for the second, with several species dependent
indels that locally challenged the alignment process. To reduce
the misleading effects of misaligned regions, we used the model
alignment for this marker given by Rodriguez et al. (2011) that
produced good assessment statistics according to SOAP 1.2a4
(Löytynoja and Milinkovitch, 2001), better than automatic alignments produced by CLUSTAL-X 1.83 under various parameter
values (i.e. increase in mean nodal support, model adequacy, and
tree balance). Moreover, and despite the presence of indels in its
intronic regions, this same marker has proven to be efficient in
solving the phylogenetic relationships among other catfish subfamilies (Chiachio et al., 2008; Cardoso and Montoya-Burgos,
2009; Alexandrou et al., 2011; Cramer et al., 2011; Covain and
Fisch-Muller, 2012; Roxo et al., 2012, 2014; Costa e Silva et al.,
2014). Additionally, Fisch-Muller et al. (2012) demonstrated that
in Ancistrinae, the two introns of f-rtn4r were rather conserved,
and displayed less variation than coding mitochondrial genes,
making easier detection of homologous regions. Gaps were considered as missing data, and regions impossible to amplify or to
sequence were coded as ambiguities (N). The final alignment of
f-rtn4r marker is accessible on Dryad (http://datadryad.org/) using
accession number XXXX. Since mitochondrial DNA is presumably
transmitted through maternal lineage as a single non recombining
genetic unit (Meyer, 1993), a first partition corresponding to the
mitochondrial genes was created. With the mutational patterns
in intronic and exonic regions of f-rtn4r being rather characterized
by insertions/deletions and transitions/transversions respectively,
two other partitions were created for introns and exons. Congruence in phylogenetic signals contained in mitochondrial and
nuclear markers was secondarily assessed using the Congruence
Among Distance Matrices (CADM) test (Legendre and Lapointe,
2004) as implemented in ape 2.6.2 (Paradis et al., 2004; Paradis,
2006) in R 2.12.1 (R Development Core Team, 2009). Patristic pairwise maximum likelihood (ML) (Felsenstein, 1981) distances were
computed as estimates of tree topologies with Treefinder (Jobb
et al., 2004) version of October 2008 for each partition using a likelihood model under which the distances are optimized. Appropriate substitution models corresponding to each potential partition
were accordingly determined with the Akaike Information Criterion (Akaike, 1974) as implemented in Treefinder. The CADM test
was computed using 9999 permutations of the three ML distances
matrices. Two phylogenetic reconstruction methods allowing the
analysis of partitioned data were used. First, a ML reconstruction
was performed with Treefinder, and robustness of the results
was estimated by resampling the data set with the nonparametric
bootstrap (Efron, 1979) following Felsenstein’s (1985) methodology with 2,000 pseudoreplicates. Second, a Bayesian inference
analysis was conducted in MrBayes 3.1.2 (Huelsenbeck and
Ronquist, 2001; Ronquist and Huelsenbeck, 2003). Two runs of
eight chains (one cold, seven heated) were conducted simultane-
ously for 2 107 generations, with the tree space sampled each
1000th generation. Convergence between chains occurred after
2 106 generations (average standard deviation of split frequencies <0.01). After a visual representation of the evolution of the
likelihood scores, and checking for the stationarity of all model
parameters using Tracer 1.5 (Rambaut and Drummond, 2007)
(i.e.: potential scale reduction factor (PSRF), uncorrected roughly
approached 1 as runs converged (Gelman and Rubin, 1992), and
Effective Sample Size (ESS) of all parameters above 200), the
2 106 first generations were discarded as burn-in. The remaining
trees were used to compute the consensus tree. Alternative
hypotheses (i.e. topologies) were tested against the null hypothesis
that all hypotheses provided equally good explanations of the data
using the Approximately Unbiased (AU) (Shimodaira, 2002), the
Bootstrap Probability (BP), and the Expected-Likelihood Weights
(ELW) of the alternative hypothesis (Strimmer and Rambaut,
2002) tests as implemented in Treefinder using 1 106 RELL
replicates (Kishino et al., 1990). All alternative topologies were
constructed in order to reflect, as much as possible given our taxonomic sampling, already proposed hypotheses (Isbrücker, 1979;
Rapp Py-Daniel, 1997; Armbruster, 2004), or the monophyly of
different groups.
3. Results
3.1. Phylogenetic analysis of the subfamily Loricariinae
We sequenced the almost complete 12S and 16S mitochondrial
genes, and the partial nuclear gene f-rtn4r for 326 specimens of
217 species of Loricariinae and 8 Loricariidae belonging to Hypostominae (7 species) and Neoplecostominae (1 species) as outgroup
(Table 1). Other sequences for 24 representatives of Loricariinae,
and ten Loricariidae belonging to Rhinelepinae (1 species), and
Hypostominae (9 species) were obtained from GenBank using the
accession numbers provided in Covain et al. (2008), Chiachio et al.
(2008), Rodriguez et al. (2011), Covain and Fisch-Muller (2012),
and Fisch-Muller et al. (2012). The sequence alignment initially
including 8503 positions was restricted to 8426 positions after
removal of regions with ambiguous alignment. A subset of 2545
positions corresponded to the mitochondrial genes (962 positions
for the 12S rRNA gene, 74 for the tRNA Val gene, and 1509 for the
16S rRNA gene), and 5881 to the nuclear f-rtn4r gene (894 positions
for the exonic regions, and 4987 for the intronic regions). No significant conflicting phylogenetic signal was detected in the data set, as
the global CADM test displayed a high coefficient of concordance
between matrices and rejected the null hypothesis of incongruence
between them (CADM: W = 0.7964, v2ref = 163976.6, p(v2refPv2⁄) =
0.0001). The CADM a posteriori tests did not detect any conflicting
matrix with the global phylogenetic signal (rS mitochondrion =
0.6295, pðrS refPr Þ ¼ 0:0003Þ ; r S exons = 0.7239, pðrS refPr Þ ¼ 0:0003;
S
S
r S introns = 0.7304, pðrS refPr Þ ¼ 0:0003). Thus, despite the presence of
S
indels in the intronic regions, and of a lower contribution of the
mitochondrial genes to the global phylogenetic signal, there was no
indication to discard these regions from the phylogenetic analyses.
The sequences were consequently concatenated, and three partitions
corresponding to mitochondrial genes, exonic parts of f-rtn4r, and
intronic parts of f-rtn4r were used to reconstruct the tree. The models
GTR + G (Tavaré, 1986) for mitochondrial genes and intronic regions
of f-rtn4r, and HKY + G (Hasegawa et al., 1985) for exonic regions of
f-rtn4r displayed the smallest AIC and accordingly fitted our data
the best as calculated with Treefinder. Maximun Likelihood and
Bayesian phylogenetic reconstructions lead to equivalent tree topologies (Appendices A and B respectively), both comparable in broad outline to the one obtained by Covain et al. (2008), and Rodriguez et al.
(2011). The ML tree (Fig. 1 and Appendix A; ln L = 116343.2) and
Bayesian tree (Appendix B) both show a basal split within the Loricariinae [100 Bootstrap Probability (BP) and 1 Posterior Probability (PP)]
resulting in two highly supported lineages: the Harttiini (clade 1;
95.65 BP and 1 PP) and the Loricariini (clade 2; 85.68 BP and 1 PP).
The Loricariini was divided, in turn, into two strongly supported
clades: the Farlowellina (clade A; 100 BP and 1 PP); and the Loricariina
(clade B; 78.85 BP and 1 PP). Within the Loricariina, three main groups
were resolved with high supports, one forming the Loricariichthys
group (sensu Covain and Fisch-Muller, 2007; 85.95 BP and 1 PP), a second comprising Spatuloricaria in a sister position to the Loricaria plus
Pseudohemiodon groups (sensu Covain and Fisch-Muller, 2007; 99.95
505
BP and 1 PP), and a third comprising all Rineloricaria representatives
(99.6 BP and 1 PP). Metaloricaria, Dasyloricaria, and Fonchiiloricaria
were not included in these morphological groups.
3.1.1. Harttiini
The Harttiini tribe formed a monophyletic group (Fig. 1, clade 1)
and included the genera Harttia, Cteniloricaria, and Harttiella
(Fig. 2). Cteniloricaria and Harttiella were resolved as monophyletic
with high statistical supports (both with 100 BP and 1 PP; Appendices A and B). Cteniloricaria included two species, C. napova and
C. platystoma (type species). Harttiella comprised six species,
H. crassicauda (type species), H. parva, H. pilosa, H. longicauda,
H. intermedia, and H. lucifer. Harttiella intermedia was nested within
H. longicauda. Relationships among other Harttiini belonging to
Harttia were partly unresolved. Guianese Harttia comprising
H. guianensis, H. surinamensis, H. fluminensis, and H. tuna formed a
highly supported monophyletic group (100 BP and 1 PP) but were
weakly supported as members of Harttia (BP below 50). In the
Bayesian inference they formed the sister group of Cteniloricaria
with very low posterior probabilities (0.53). The only relationship
better supported in Harttia was the clade including Amazonian
representatives (H. punctata, H. duriventris, H. dissidens, H. sp.
Xingu1, H. sp. Xingu2, H. sp. Xingu3, H. sp. Tapajos, H. sp. Tocantins,
and H. aff. punctata) plus the Guianese H. fowleri in a sister
position to representatives from South East Brazil (including
H. loricariformis, type species of the genus and H. leiopleura type
Fig. 1. Maximum likelihood tree of the Loricariinae (ln L = 116343.2) inferred from the combined analysis of sequences of partial 12S and 16S mitochondrial genes, and
partial f-rtn4r nuclear gene. The models GTR + G for mitochondrial genes and intronic regions of f-rtn4r, and HKY + G for exonic regions of f-rtn4r were applied for both ML and
Bayesian reconstructions. Blackened branches in the ingroup indicate nodes with both bootstrap supports and posterior probabilities below 50 and 0.70 respectively. Stars
indicate incongruence between ML and Bayesian reconstructions. 1: Harttiini; 2: Loricariini; A: Farlowellina, B: Loricariina. Circled numbers refer to subtrees figured in the
text. Scale indicates the number of substitutions per site as expected by the model.
506
species of Quiritixys) with a low bootstrap probability of 54.5 but a
posterior probability of 1 (Appendices A and B respectively). Deeper relationships among genera were not statistically supported.
3.1.2. Loricariini, Farlowellina
The Loricariini tribe was resolved as monophyletic (Fig. 1, clade
2). Within Loricariini, the subtribe Farlowellina also constituted a
monophyletic assemblage (Fig. 1, clade A), and comprised Lamon-
tichthys, Pterosturisoma, Sturisoma, Farlowella, Aposturisoma, and
Sturisomatichthys (Fig. 3). Interspecific relationships were congruent between both phylogenetic analyses. Lamontichthys (including
L. filamentosus, type species) was monophyletic and formed, with
high support (100 BP and 1 PP), the sister group of all other representatives of the subtribe. The second diverging genus was the
monotypic Pterosturisoma microps that formed the sister group of
the remaining Farlowellina. Then all cis-Andean (East of the Andes
Fig. 2. Maximum likelihood tree, labeled subtree of the Harttiini tribe. Numbers above branches indicate bootstrap supports above 50 followed by posterior probabilities
above 0.70. Within species supports are provided in Appendices A and B. Dash (–) represent low supports. Blackened branches indicate nodes with both bootstrap supports
and posterior probabilities below 50 and 0.70 respectively. Stars indicate incongruence between ML and Bayesian reconstructions and NAs indicate nodes absent in
topologies of Appendices A and B. Bold type refers to type species of different genera. Scale indicates the number of substitutions per site as expected by the model.
507
Fig. 3. Maximum likelihood tree, labeled subtree of the Loricariini tribe: Farlowellina subtribe. Numbers above branches indicate bootstrap supports above 50 followed by
posterior probabilities above 0.70. Within species supports are provided in Appendices A and B. Dash (–) represent low supports. Blackened branches indicate nodes with
both bootstrap supports and posterior probabilities below 50 and 0.70 respectively. Stars indicate incongruence between ML and Bayesian reconstructions and NAs indicate
nodes absent in topologies of Appendices A and B. Bold type refers to type species of different genera. Scale indicates the number of substitutions per site as expected by the
model.
508
following the definition of Haffer, 1967; and Albert et al., 2006)
representatives of Sturisoma included in this study, branched with
high statistical support (100 BP and 1 PP) in a sister position to all
other representatives of Sturisoma, Sturisomatichthys, Farlowella
and Aposturisoma. The subsequent, also highly supported, group
comprised a mix of representatives of Sturisomatichthys (including
S. leightoni, type species) and of the trans-Andean (West of the
Andes) Sturisoma rendering both genera paraphyletic. Within the
last group of Farlowellina, a first group of Farlowella consisted of
the stockiest forms of the genus (including F. platorynchus, F. amazona, F. aff. rugosa, F. taphorni and F. curtirostra) branched in a sister
position to Aposturisoma myriodon forming in turn and with high
support (99.96 BP and 1 PP) the sister genus of a second group of
Farlowella (including F. acus, type species) rendering Farlowella
paraphyletic.
3.1.3. Loricariini, Loricariina
The subtribe Loricariina (Fig. 1, clade B) was also monophyletic
and formed the sister group of Farlowellina (Fig. 1, clade A). The
basal split (Fig. 4) gave rise to two strongly supported lineages,
one comprising the representatives of Metaloricaria (including
Metaloricaria paucidens, type species; 99.9 BP and 1 PP) and the
second including all other Loricariina (Fig. 4; 99.8 BP and 1 PP).
Then a second diverging group comprising Dasyloricaria representatives in a sister position to the monotypic Fonchiiloricaria nanodon, formed in turn the sister group of the remaining
Loricariina. The sister relationship between Dasyloricaria and
Fonchiiloricaria was however not supported by bootstrap values
(BP < 50) but displayed relatively high posterior probability
(0.83). The sister group of these two genera split into two groups
with on one side representatives of Rineloricaria and Ixinandria,
and on the other side members of the Loricaria–Pseudohemiodon
and Loricariichthys groups.
3.1.3.1. Loricariini, Loricariina, Rineloricaria. The genus Rineloricaria
formed the most species rich group of the subfamily and constituted a monophyletic assemblage comprising members of Fonchiiichthys, Hemiloricaria, Leliella, and Ixinandria steinbachi, type
species of Ixinandria, with high statistical support (Fig. 5; 99.6 BP
and 1 PP). The first diverging group of Rineloricaria comprised the
trans-Andean R. altipinnis in a sister relationship to the
cis-Andean R. stewarti, R. fallax, R. formosa, R. melini, R. teffeana,
R. morrowi, and several undescribed species (88.5 BP and 0.98
PP). The second diverging group comprised different populations
of R. lanceolata and R. hoehnei. The latter species was nested within
R. lanceolata and all internal relationships were fully resolved and
highly supported (82.4 < BP < 100 and 1 PP). These two species
formed the sister group of all remaining Rineloricaria representatives. Concerning the sister group of the R. lanceolata clade,
the two phylogenetic methods provided alternative hypotheses. The
Bayesian inference (Appendix B) resolved the monophyly of
the Southeastern species of Rineloricaria plus Ixinandria steinbachi
(nested within Rineloricaria as sister species of R. misionera) which
formed the sister group of a second monophyletic group comprising the representatives of Rineloricaria from the Amazon, Orinoco,
and trans-Andean region (except R. altipinnis), whereas the ML
Fig. 4. Maximum likelihood tree, labeled subtree of the Loricariini tribe: Loricariina subtribe. Numbers above branches indicate bootstrap supports above 50 followed by
posterior probabilities above 0.70. Within species supports are provided in Appendices A and B. Dash (–) represent low supports. Bold type refers to type species of different
genera. Scale indicates the number of substitutions per site as expected by the model.
reconstruction (Appendix A) resolved the species R. osvaldoi and
relatives as sister group of all the remaining Rineloricaria plus
Ixinandria. Then the species from the Amazon, Orinoco, and the
trans-Andean region diverged and formed the sister group of
509
Amazonian species including R. wolfei in a sister position to the
Southeastern clade (including I. steinbachi, type species of Ixinandria). However, the Bayesian inference lead to a better resolution
of the phylogeny with all posterior probabilities greater than 0.6,
Fig. 5. Maximum likelihood tree, labeled subtree of the Loricariini tribe: Loricariina subtribe, Rineloricaria group. Numbers above branches indicate bootstrap supports above
50 followed by posterior probabilities above 0.70. Within species supports are provided in Appendices A and B. Dash (–) represent low supports. Blackened branches indicate
nodes with both bootstrap supports and posterior probabilities below 50 and 0.70 respectively. Stars indicate incongruence between ML and Bayesian reconstructions and
NAs indicate nodes absent in topologies of Appendices A and B. Bold type refers to type species of different genera. Scale indicates the number of substitutions per site as
expected by the model.
510
whereas bootstrap values only supported the monophyly of the
Southeastern clade (98.7 BP). In both reconstructions, the type species of Ixinandria was nested within Southeastern Rineloricaria. The
species R. uracantha (type species of Fonchiiichthys), R. heteroptera
(type species of Leliella), and R. eigenmanni and relatives from
Orinoco basin (potentially close relatives of R. caracasensis, type
species of Hemiloricaria) were all resolved in a nested position
within Rineloricaria, in positions strongly supported by bootstrap
Fig. 6. Maximum likelihood tree, labeled subtree of the Loricariini tribe: Loricariina subtribe, Loricariichthys group. Numbers above branches indicate bootstrap supports
above 50 followed by posterior probabilities above 0.70. Within species supports are provided in Appendices A and B. Bold type refers to type species of different genera. Scale
indicates the number of substitutions per site as expected by the model.
values and posterior probabilities (81.85 < BP < 100 and
0.98 < PP < 1). The genus Rineloricaria sensu lato constituted the sister
group of the Loricariichthys and Loricaria–Pseudohemiodon groups.
3.1.3.2. Loricariini, Loricariina, Loricariichthys group. Within Loricariina, members of the Loricariichthys group formed a strongly
supported natural group (85.95 BP and 1 PP) comprising Pseudoloricaria, Limatulichthys, Loricariichthys, and Hemiodontichthys
(Fig. 6) and formed the sister clade of the Loricaria–Pseudo-
511
hemiodon group. Loricariichthys (including L. maculatus, type species) was monophyletic and constituted the sister genus of all
other members of its groups. The second diverging genus was
the monotypic Hemiodontichthys acipenserinus with its different
populations, and was the sister group of the genera Pseudoloricaria and Limatulichthys. All internal relationships within the
Loricariichthys group were congruent in both reconstructions
and fully resolved with high statistical supports (Appendices A
and B).
Fig. 7. Maximum likelihood tree, labeled subtree of the Loricariini tribe: Loricariina subtribe, Loricaria–Pseudohemiodon group. Numbers above branches indicate bootstrap
supports above 50 followed by posterior probabilities above 0.70. Within species supports are provided in Appendices A and B. Dash (–) represent low supports. Blackened
branches indicate nodes with both bootstrap supports and posterior probabilities below 50 and 0.70 respectively. Stars indicate incongruence between ML and Bayesian
reconstructions and NAs indicate nodes absent in topologies of Appendices A and B. Bold type refers to type species of different genera. Scale indicates the number of
substitutions per site as expected by the model.
512
3.1.3.3. Loricariini, Loricariina, Loricaria–Pseudohemiodon group.
The Loricaria–Pseudohemiodon group formed a strongly supported
clade (99.95 BP and 1 PP) comprising the genera Spatuloricaria,
Loricaria (including Proloricaria), Brochiloricaria, Paraloricaria,
Planiloricaria, Crossoloricaria, Pseudohemiodon, Apistoloricaria, and
Rhadinoloricaria, and formed the most genera rich group (Fig. 7).
Interspecific relationships were congruent between both reconstructions except for the species and populations closely related
to L. cataphracta. Spatuloricaria was resolved as monophyletic and
formed the sister genus of all other genera of the group. The
remaining members of the Loricaria–Pseudohemidon group split
into two strongly supported clades corresponding to the Loricaria
group (sensu Covain and Fisch-Muller, 2007) on one side and the
Pseudohemiodon group (sensu Covain and Fisch-Muller, 2007) on
the other side. The Loricaria group was strongly supported (100
BP and 1 PP) and comprised Loricaria (including L. cataphracta type
species), Brochiloricaria, and Paraloricaria. At the exclusion of L. prolixa (type species of Proloricaria) and L. apeltogaster, the remaining
Loricaria species formed a statistically highly supported monophyletic group (100 BP and 1 PP). Loricaria formed the sister genus
of all other representatives of its group. The sister group of Loricaria
comprised Loricaria prolixa in a sister position to Brochiloricaria
representatives, both in turn forming the sister group of L. apeltogater as sister species of representatives of Paraloricaria. However,
the positions of L. prolixa and L. apeltogaster were not statistically
supported (50 < BP and 0.66 < PP < 0.68), with the exception of
their exclusion of the group containing all other Loricaria representatives (100 BP and 1 PP). The Pseudohemiodon group was also
strongly supported (86.2 BP and 1 PP). The trans-Andean representatives of Crossoloricaria (including C. variegata, type species) was
the first diverging group, and formed the sister group of all other
Pseudohemiodon group members. The second diverging group comprised the monotypic Planiloricaria cryptodon in a sister position to
the remaining genera of the group. The third diverging group comprised the representatives of Pseudohemiodon which were resolved
as monophyletic with high statistical support (99.95 BP and 1 PP).
The sister group of Pseudohemiodon was also strongly supported
(98.95 BP and 1 PP) and comprised a mix of representatives of
Rhadinoloricaria, Apistoloricaria and the cis-Andean Crossoloricaria,
where Rhadinoloricaria was obtained paraphyletic. All internal relationships were however fully resolved with strong support
(Appendices A and B).
3.2. Evaluation of alternative phylogenetic hypotheses
Alternative hypotheses were evaluated using topological tests
and results are summarized in Table 3. The hypothesis proposed
by Isbrücker (1979) classifying the Loricariinae into three tribes:
Harttiini, Loricariini, and Farlowellini without phylogenetic relationships between them (coded as a polytomy at origin of the three
lineages) was significantly rejected by all testing procedures
(Table 3, H1). The hypothesis of Rapp Py-Daniel (1997), partly
confirmed by Armbruster (2004), and consisting in splitting the
Loricariinae into two sister tribes: Harttiini on one side (including
Harttia, Cteniloricaria, Harttiella, Lamontichthys, and Pterosturisoma
forming the subtribe Harttiina in a sister position to Farlowella,
Aposturisoma, Sturisoma, and Sturisomatichthys forming the subtribe Farlowelliina), and Loricariini on the other side (comprising
all other genera) was also significantly rejected (Table 3, H2). The
hypothesis proposing, within Farlowellina (as defined by Covain
et al., 2008, 2010), the monophyly of Farlowella as sister genus of
Aposturisoma on one side, and of Surisoma as sister genus of Sturisomatichthys on the other side was also significantly rejected by all
tests (Table 3, H3). The enforced monophyly of Crossoloricaria as
sister genus of Apistoloricaria and Rhadinoloricaria (Table 3, H4),
as well as the monophyly of Loricaria, comprising L. prolixa, and
L. apeltogaster (Table 3, H5), were both significantly rejected.
Within the Rineloricaria clade (Fig. 5), the validity of Ixinandria,
Hemiloricaria, Rineloricaria, Leliella, and Fonchiiichthys was evaluated by assigning each species to the corresponding genus (as
listed in Isbrücker, 2001) but without providing phylogenetic
hypothesis of relationships between these five genera (coded as a
polytomy at origin of all lineages). This hypothesis was also
rejected (Table 3, H6). In the same way, the validity of Quiritixys
was assessed by creating a polytomy at origin of Cteniloricaria,
Harttia, Harttiella, and Quritixys lineages. This hypothesis was
rejected by all testing procedures (Table 3, H7).
4. Discussion
The phylogenetic results confirmed the monophyly of the subfamily Loricariinae, and its splitting into two tribe-level clades,
namely the Harttiini, and the Loricariini. Two subtribe-level clades
were obtained for Loricariini, the Farlowellina and the Loricariina,
the latter being the most diversified and further divided in three
main clades. A reappraisal of these tribes, subtribes, and their
respective genera is here proposed (summarized in Table 4). The
taxonomic status of some species will also be revised, with new
synonymisations and generic reassignations.
4.1. Harttiini
Corroborating previous results (Montoya-Burgos et al., 1998;
Covain et al., 2008; Rodriguez et al., 2011; Lujan et al., 2015), the
Harttiini are restricted to Harttia (type genus), Harttiella and
Cteniloricaria. Moreover, the enlarged definition of Harttiini comprising Farlowellina (Rapp Py-Daniel, 1997; Armbruster, 2004) is
here significantly rejected (Table 2). Harttiini were primarily
diagnosed by 14 caudal-fin rays, no postorbital notches, no predorsal keels, a circular mouth with papillose lips, and numerous
Table 3
Alternative phylogenetic relationships evaluated using the Approximately Unbiased (AU), Bootstrap Probability (BP), and the Expected-Likelihood Weights (ELW) of the
alternative hypothesis tests using 1 106 RELL replicates. ln L: likelihood of the hypothesis; Dln L: difference in likelihood between the alternative hypothesis and the Maximum
Likelihood (ML) tree as best explanation of the data. Reported results correspond to p-values.
Hypothesis
Ref
ln L
Dln L
AU
BP
ELW
H0
H1
H2
Best ML tree
Three tribes: Farlowellini, Loricariini, Harttiini
Two tribes: Harttiini (incl. Harttiina and Farlowellina) and Loricariini
116343.2
116579.5
116968.6
–
236.3
625.4
–
0
0
–
0
0
–
0
0
H3
H4
H5
H6
Monophyly
Monophyly
Monophyly
Monophyly
and Leliella
Monophyly
This study
Isbrücker (1979)
Rapp Py-Daniel (1997) and Armbruster
(2004)
This study
This study
This study
As defined by Isbrücker (2001)
116723.6
116461.5
116424.1
117873.3
380.4
118.3
80.9
1530.1
0
0
0
0
0
0
0
0
0
0
8.38 107
0
As defined by Isbrücker (2001)
116532.8
189.6
0
0
0
H7
of
of
of
of
Sturisoma, Sturisomatichthys, and Farlowella
Crossoloricaria, Apistoloricaria, and Rhadinoloricaria
Loricaria
Ixinandria, Rineloricaria, Hemiloricaria, Fonchiiichthys,
of Harttia, Cteniloricaria, Harttiella, and Quiritixys
Table 4
Loricariinae classification with list of valid genera following this study.
Loricariidae
Loricariinae
Harttiini
Harttia (synonym: Quiritixys)
Harttiella
Cteniloricaria
Loricariini
Farlowellina
Lamontichthys
Pterosturisoma
Farlowella
Aposturisoma (possibly a synonym of Farlowella)
Sturisoma (restricted to cis-Andean region)
Sturisomatichthys (including all trans-Andean Sturisoma)
Loricariina
Metaloricaria
Dasyloricaria
Fonchiiloricaria
Rineloricaria group
Rineloricaria (synonyms: Fonchiiichthys, Hemiloricaria, Leliella,
and Ixinandria)
Loricariichthys group
Pseudoloricaria
Limatulichthys
Loricariichthys
Hemiodontichthys
Furcodontichthys (not available for this study; group assignment
based on morphology)
Loricaria–Pseudohemiodon group
Spatuloricaria
Loricaria
Proloricaria (revalidated)
Brochiloricaria
Paraloricaria
Crossoloricaria (restricted to trans-Andean region)
Planiloricaria
Pseudohemiodon
Rhadinoloricaria (including all cis-Andean Crossoloricaria; synonym:
Apistoloricaria)
Dentectus (not available for this study; group assignment based on
morphology)
Reganella (not available for this study; group assignment based on
morphology)
Pyxiloricaria (not available for this study; group assignment based
on morphology)
Ricola (not available for this study; group assignment based on
morphology)
pedunculated teeth organized in a comblike manner (Isbrücker,
1979; Covain and Fisch-Muller, 2007). However, these features
are shared by Harttiini, Farlowellina and partly by Fonchiiloricaria
nanodon within Loricariini, rendering the definition of Harttiini
sensu stricto invalid. We nevertheless note that in Harttiini, the
abdominal cover made of small rhombic platelets can be present
or absent, and when it is present, the abdominal cover never
extends to the lower lip margin. The latter condition is, on the contrary, always observed in Farlowellina. If this criterion applies, then
the recently described Harttia absaberi (Oyakawa et al., 2013)
should be regarded as a putative member of Farlowellina. Deeper
relationships within Harttiini are not resolved due to very short
internal branches suggesting explosive radiation of the main
lineages. The nested position of H. leiopleura, type species of
Quiritixys, within the Southeastern species of Harttia which also
included H. loricariformis, the type species of the genus, renders
Harttia paraphyletic with the necessity to describe several new
genera (considering our sampling, a total of four would be needed
to render each lineage monophyletic). To prevent this taxonomic
issue, a conservative approach consists in placing Quiritixys into
synonymy with Harttia. This conclusion is reinforced by the significant rejection of the hypothesis evaluating its validity (Table 2). A
513
second problem concerns the position of Harttiella intermedia
nested within H. longicauda. A rapid overview of this situation
would probably lead to the placement of H. intermedia into the
synonymy of H. longicauda. However, based on morphometric
analyses, Covain et al. (2012) demonstrated that the former was
perfectly distinct from the latter, and even belonged to another
morphological group (the crassicauda group comprising all stockier
species while H. longicauda belonged to the longicauda group comprising all slender species). In that study the barcode COI sequence
of H. intermedia was also identical to that of H. longicauda, and the
authors hypothesized introgressive hybridization or a recent founder effect in an isolated population to explain this phenomenon,
both species being present in the same basin. The use of the
nuclear f-rtn4r gene in the present study, and the topological result
identical to that obtained using barcode sequences, invalidate the
hypothesis of introgressive hybridization. Since the establishment
of reciprocal monophyly between two sister taxa is a function of
time (Hubert et al., 2008), when not enough time passed to accumulate mutations able to differentiate sister species, a paraphyletic
grouping may be observed with one species nested within a second
one [i.e. the coalescent of the first species is contained within the
coalescent of the second (Meyer and Paulay, 2005)]. Harttiella
intermedia thus represents a rather recent vicariant form of H. longicauda isolated in the Trinité Massif in French Guiana, and corroborates the alternative hypothesis of Covain et al. (2012) of a
morphologically fast evolving species not yet genetically distinguishable from its ancestor following the example of the East African lacustrine cichlid species flock (e.g. Won et al., 2005).
4.2. Loricariini, Farlowellina
Within Loricariini, the phylogeny of Farlowellina revealed unexpected results. All genera except Lamontichthys and Pterosturisoma
appeared paraphyletic, and their enforced monophyly was significantly rejected (Table 2). The nested position of Aposturisoma
within Farlowella renders the latter polyphyletic. If one considers
Aposturisoma a valid genus, based on its particular body shape, ecological habits and restricted distribution to the HuacamayoAguaytia drainage, members of the F. amazona species group (sensu
Retzer and Page, 1997) should be placed in a new genus. However,
the lack of significant distinctive features between the F. amazona
group and other Farlowella, and the close relatedness of Aposturisoma and Farlowella, may imply that Aposturisoma corresponds to
a local form of Farlowella adapted to rheophilic habits. This corroborates the hypothesis of Covain and Fisch-Muller (2007) who interpreted the morphological characteristics of Aposturisoma as
adaptations to stream habitat rather than an intermediary shape
between Farlowella and Sturisoma as supposed by Isbrücker et al.
(1983). If this hypothesis is applied, Aposturisoma should be considered a junior synonym of Farlowella. Nevertheless, this question
still deserves further investigation. The taxonomy of Farlowella is
also confused and the group needs further revision. In the last revision of the genus, Retzer and Page (1997) described F. platorynchus
without examining the holotype of F. amazona. However, examination of the holotypes of both species strongly suggests that
F. platorynchus is a junior synonym of F. amazona. In addition,
F. gladiolus was placed in synonymy with F. amazona, but should
be regarded as a valid species. Moreover, identification at specific
level remains difficult due to the very divergent morphology of
the genus and the great similarity of its members. Consequently,
species with a large geographic distribution may comprise species
complexes (see e.g. F. oxyrryncha in Fig. 3). The second paraphyly
highlighted here concerns the genera Sturisoma and Sturisomatichthys. Contrary to the preceding case, a strong geographical
structure is represented in this result with one group of Sturisoma
comprising all cis-Andean species, and a second group comprising
514
all trans-Andean members of Sturisoma and Sturisomatichthys.
Moreover, the type species of Sturisoma, S. rostrata, is described
from Brazilian rivers, whereas the type species of Sturisomatichthys,
S. leightoni, is described from the Magdalena River in Colombia. For
these reasons, Sturisoma is here restricted to the species occurring
in the cis-Andean region (including S. barbatum, S. brevirostre, S.
guentheri, S. lyra, S. monopelte, S. nigrirostrum, S. caquetae, S. robustum, S. rostratum, and S. tenuirostre) whereas Sturisomatichthys
comprises all former trans-Andean species of Sturisoma and
Sturisomatichthys (i.e. S. aureum, S. citurensis, S. dariense, S. festivum,
S. frenatum, S. kneri, S. leightoni, S. panamense, and S. tamanae). The
diagnostic feature provided by Isbrücker and Nijssen (in Isbrücker,
1979) to distinguish Sturisomatichthys from Sturisoma, i.e. the
absence of a rostrum in Sturisomaticthys, is not phylogenetically
informative (Covain et al., 2008), as it can be absent or present
according to the species, and thus is not a valid criterion to
diagnose the genus.
4.3. Loricariini, Loricariina
The Loricariina comprises some particular forms that can be
seen as relictual species due to their particular morphological characteristics, restricted distributions, and long branches, rendering
the phylogenetic signal noisy. Metaloricaria is indeed the first
diverging group of the subtribe and it possesses a very particular
morphology reminiscent to that of Harttia with which it shares
the same habitat (stream waters in riffles). This resemblance probably resulted in the initial description of M. nijsseni as a member of
Harttia (Boeseman, 1976), despite clear autapomorphic features
such as a horse-shoe like mouth shape, teeth pedunculated yet
reduced in size and number, and 13 caudal-fin rays, that indicate
the future trends of the Loricariina (strong modifications in mouth,
lips, and teeth characteristics, decrease of the number of caudal-fin
rays, etc.). Metaloricaria is restricted to the Guiana Shield in rivers
flowing through Suriname and French Guiana. In the same way,
Dasyloricaria which is restricted to the Pacific slope of the Andes
(a unique pattern of distribution within the subfamily), shares a
mosaic of morphological characteristics with representatives of
other Loricariina mainly distributed on the Atlantic slope. Along
with members of Rineloricaria, it shares papillose lips and hypertrophied odontodes along the sides of the head in breeding males.
With some representatives of the Loricariichthys group (sensu
Covain and Fisch-Muller, 2007), it shares deep postorbital notches,
a strongly structured abdominal cover, and a similar mouth shape,
including the hypertrophied lower lip of breeding males
(Steindachner, 1878). Finally, with some representatives of the
Loricaria group, it shares a triangular head, strong predorsal keels,
and the upper caudal fin ray produced into a long whip. Finally,
Fonchiiloricaria is restricted to the Upper Huallaga River in Peru.
It possesses 14 caudal-fin rays, and no postorbital notches, two features characteristic for Harttiini and Farlowellina. In addition it
also possesses autapomorphic features such as an extreme reduction in size and number of premaxillary teeth (when not missing)
relative to dentary teeth (Rodriguez et al., 2011). All these relictual
species exhibit features that will be successively lost or maintained
in other Loricariina lineages. In this case the observed autapomorphic features would correspond to the retention of ancestral
characters.
Rineloricaria constitutes by far the most species rich genus of
the Loricariinae, including 66 valid species and numerous undescribed ones. Several attempts have been made to split this genus.
Isbrücker and Nijssen (1976) proposed the revalidation of
Hemiloricaria Bleecker, 1862 (type species: Hemiloricaria caracasensis), but they finally left it in the synonymy of Rineloricaria because
of the lack of obvious characters to split these two genera. Later on,
in an aquarist hobbyist journal, Isbrücker (in Isbrücker et al., 2001)
changed his mind and revalidated Hemiloricaria based on the disposition of breeding odontodes in males, and assigned 24 species
to this genus (R. altipinnis, R. beni, R. cacerensis, R. caracasensis,
R. castroi, R. eigenmanni, R. fallax, R. formosa, R. hasemani, R. hoehnei,
R. jubata, R. konopickyi, R. lanceolata, R. magdalenae, R. melini,
R. morrowi, R. nigricauda, R. parva, R. phoxocephala, R. platyura,
R. sneiderni, R. stewarti, R. teffeana, and R. wolfei), most of them
belonging to different lineages according to the present results.
Moreover, the breeding odontodes on the predorsal area of males
are not always present in the species assigned to this group (e.g.
R. platyura). In the same publication, Isbrücker and Michel
described Fonchiiichthys (type species: Loricaria uracantha), and
Isbrücker described Leliella (type species: Rineloricaria heteroptera)
on the basis of subtle differences in sexual dimorphism. However,
in our phylogenetic reconstruction R. uracantha, R. heteroptera and
R. eigenmanni (a very close relative of R. caracasensis following the
examination of type specimens) were nested within the same
clade, and their enforced monophyly was significantly rejected
(Table 3). For these reasons, Hemiloricaria, Fonchiiichthys, and
Leliella are here placed in synonymy with Rineloricaria. In addition,
the nested position of Ixinandria steinbachi in a sister position to
R. misionera within Southeastern representatives of Rineloricaria,
renders Rineloricaria paraphyletic. We therefore place Ixinandria
in synonymy with Rineloricaria. The diagnostic feature given by
Isbrücker and Nijssen (in Isbrücker, 1979) for Ixinandria, a naked
belly and particular sexual dimorphism, should be considered as
specific characters. This is reinforced by the appearance, in close
relatives of R. steinbachi from Southeast Brazil or Argentina, of a
gradual increase in the abdominal plating, rendering thus the belly
partly covered (e.g. R. maquinensis, R. aequalicuspis or R. misionera).
Finally, the nested position of R. hoehnei within R. lanceolata
renders the latter paraphyletic. We confirm here results of VeraAlcaraz et al. (2012) and also place R. hoehnei (Miranda Ribeiro,
1912) in synonymy with R. lanceolata (Günther, 1868). However,
considering the branch lengths of the phylogenetic tree compared
to other species of Rineloricaria, R. lanceolata may prove to host a
species complex.
The Loricariichthys group appears more structured, with all genera resolved as monophyletic and strongly supported. With the
exception of the nominal genus, this group surprisingly comprises
mostly monotypic or poorly diversified genera (Limatulichthys,
Pseudoloricaria, and Hemiodontichthys, with the addition of
Furcodontichthys following results of Covain and Fisch-Muller,
2007). However, given their broad geographic range, and long
branches among populations, Hemiodontichthys acipenserinus and
Pseudoloricaria laeviuscula could comprise species complexes.
Indeed, Isbrücker and Nijssen (1974) reported variations in
morphometric features of H. acipenserinus, with populations from
the Amazonian region tending to be more slender than those from
the Paraguay and Guaporé Rivers.
Within the Loricaria group, the nominal genus is resolved as
paraphyletic, and its enforced monophyly is statistically rejected
(Table 3). Loricaria prolixa connected in a sister position to representatives of Brochiloricaria, and L. apeltogater in a sister position
to Paraloricaria. Loricaria prolixa was designated by Isbrücker (in
Isbrücker et al., 2001) as type species of a new genus Proloricaria,
based on a flattened and anteriorly broad body. The weakness of
these supposed diagnostic features that are also present in other
genera (e.g. Pyxiloricaria, Pseudohemiodon) lead several authors to
consider Proloricaria as a junior synonym of Loricaria (Ferraris in
Reis et al., 2003; Covain and Fisch-Muller, 2007). However, our
results sustain the validity of Proloricaria which is here revalidated.
The sister position of L. apeltogater to Paraloricaria needs further
investigation. The specimen included in the present study was
not preserved, and we can not be certain that it belonged to the
species. However, in the description of P. agastor, Isbrücker
(1979) had already noticed the close resemblance of both species
(the smallest syntype of L. apeltogaster was even subsequently
identified as P. agastor), distinguishing them on the basis of the
dentition. Paraloricaria possesses small teeth on both jaws whereas
L. apeltogater possesses the typical dentition for Loricaria with premaxillary teeth two times longer than dentary ones.
Within the Pseudohemiodon group, the trans-Andean Crossoloricaria which includes C. variegata, type species, branches in a sister
position to all other genera, whereas the cis-Andean Crossoloricaria,
are nested within the remaining members of the Pseudohemiodon
group, rendering Crossoloricaria paraphyletic. Crossoloricaria is
poorly diagnosed, its only distinctive character (incomplete
abdominal cover consisting of a double median row of plates)
being shared by Apistoloricaria and Rhadinoloricaria. Moreover,
Crossoloricaria rhami possesses a complete abdominal plate development (Isbrücker and Nijssen, 1983), thus rendering the diagnostic feature of Crossoloricaria invalid. Apistoloricaria is also not well
diagnosed and is distinguished from Rhadinoloricaria primarily by
the presence or absence of the iris operculum (absent or vestigial
in Apistoloricaria versus present in Rhadinoloricaria), a more conspicuous rostrum in Rhadinoloricaria, and by the number of fringed
barbels (14 in Apistoloricaria versus 12 in Rhadinoloricaria). Based
on the present phylogenetic results, the rejection of the enforced
monophyly of Crossoloricaria, Apistoloricaria, and Rhadinoloricaria
(Table 3), and the weakness of these diagnostic features, Crossoloricaria is here restricted to the trans-Andean region (including C. variegata, C. venezuelae, and C. cephalaspis), whereas the cis-Andean
species of Crossoloricaria (C. rhami, C. bahuaja) are transferred to
Rhadinoloricaria. Apistoloricaria is also placed in synonymy with
Rhadinoloricaria.
515
(Conservación de Recursos Naturales); P. de Rham, Lausanne,
P. Gaucher, CNRS Guyane; R. Vigouroux and P. Cerdan, Hydreco
Guyane; C. Weber, and A. Merguin, MHNG; M. Dewynter, ONF
Guyane; F. Melki, Biotope France; K. Wan Tong You and P. Ouboter,
NZCS; C. Bernard, CSBD; the North Rupununi District Development
Board; and the Iwokrama organization for their field and logistic
assistance; the G. and A. Claraz Foundation for their financial support for the missions in Suriname in 2001, 2005, 2007 and 2008,
and in French Guiana in 2006; the Académie Suisse des Sciences
Naturelles (ScNat) for their financial support for the missions in
Guyana 2004 and French Guiana 2006; The C. Topali Fund for their
financial contribution to the acquisition of field material for the
mission Suriname 2007, and lab material in 2009; the All Catfish
Species Inventory (NSF-DEB 0315963) for the financing of collection consultancies to RC (NMW and ANSP in 09/2007 and
12/2007), and open access in Zootaxa to Covain and Fisch-Muller
(2007); and the A. Lombard Fund for data acquisition in 2010.
We are also grateful to A. Huser, Sallmann-Fehr AG for the gift of
gill nets for the mission in Suriname in 2005 and 2007; the Guyana
Environmental Protection Agency, and Ministry of Amerindian
affairs; the French Guiana Diren, and Préfecture; and the Surinamese Ministry of Agriculture, Animal Husbandry and Fisheries
for the different necessary authorizations and collecting permits.
Part of this project was supported by the Fond National Suisse de
la Recherche Scientifique (JIMB 31003-141233). CO researches
are supported by CNPq and FAPESP in Brazil. The figures were
finalized by Florence Marteau, MHNG. John Hollier, MHNG,
improved language usage and style. Jan Pawlowski and José Fahrni,
University of Geneva, are acknowledged for laboratory facilities.
Appendix A. Supplementary material
5. Conclusions
This work represents the first comprehensive phylogeny of the
Loricariinae and provides considerable additional data to the evolutionary tree of one of the most diversified vertebrate families.
The Loricariinae, the second species-rich subfamily of the Loricariidae, and hitherto phylogenetically underinvestigated, is analyzed
with 368 OTUs (350 Loricariinae). An important gap in the evolutionary tree of the Loricariidae is thus filled, and the present results
complement other molecular works at familial and subfamilial
ranks such as Lujan et al. (2015) on the family Loricariidae with
focus on Hypostominae (203 OTUs), Roxo et al. (2014) on Hypoptopomatinae, Neoplecostominae, and Otothyrinae (155 OTUs),
Cramer et al. (2011) on the Loricariidae with focus on Neoplecostominae and Hypoptopomatinae (146 OTUs), Chiachio et al.
(2008) on Hypoptopomatinae and Neoplecostominae (53 OTUs),
and Montoya-Burgos et al. (1998) on the family Loricariidae with
emphasis on Hypostominae (58 OTUs), providing thereby a more
comprehensive view of the dramatic diversification of the Loricariidae in South America.
Acknowledgments
We are grateful to M. Sabaj Perez, and J.G. Lundberg, ANSP; E.
Bermingham, and G.R. Reina, STRI; M. Lucena, MCP; J. Armbruster,
AUM; O.T. Oyakawa, MZUSP; J. Casciota, and A. Almirón, MLP; Y.P.
Cardoso, AUGM-UNLP; M.S. Rodriguez, LIRP; G. Costa Silva, LBP; P.
Keith, R. Causse, and P. Pruvost, MNHN; M. van Oijen and K. van
Egmond, RMNH; R. Vonk and H. Praagman, ZMA; J. Maclaine,
BMNH; H. Wellendorf, NMW; S. Schaefer, AMNH; M.A. Rogers,
FMNH; D. Catania, CAS; G.M. Gonzo, UNSA; L. Rapp Py-Daniel
and M. Rocha, INPA; C. Dhlouy, San Lorenzo; and S. Rubin and L.
Moissonier, France; for the loan of specimens and/or tissue samples. We acknowledge H. Ortega, M. Hidalgo and V. Meza Vargas,
MUSM; T. Pequeño and collaborators from CIMA; L. Rodriguez
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.ympev.2015.10.
018.
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Molecular phylogeny of the highly diversified catfish subfamily

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