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Zoologica Scripta. 2022;00:1–13. wileyonlinelibrary.com/journal/zsc
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© 2022 Royal Swedish Academy of Sciences.
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INTRODUCTION
The Neotropical freshwater ichthyofauna is composed of
more than 6,000 described species, most of them inhabit-
ing river basins associated with the Amazon river (Fricke
et al., 2022; Jézéquel et al., 2020; Reis et al., 2003, 2016).
This diversity is probably even greater, and estimations in-
dicate that there may be more than 9000 freshwater fish
species in this region (Albert et al., 2020; Brosse et al.,
2013; Reis et al., 2016). Despite this vast diversity, there
is still little information about the biogeographical history
of most of those lineages. The first phylogenetic studies
analysing the biogeography of Neotropical fishes tried
to associate the current patterns of distribution of some
groups with paleogeographic events (e.g. Nelson, 1969;
Novacek & Marshall, 1976; Parenti, 1981; Rosen, 1975,
1979). However, due to methodological limitations and
the absence of analytical temporal approaches available
at that time, those chronological correlations presented
a low degree of precision (e.g. Hrbek & Larson, 1999;
Lovejoy et al., 2006; Lundberg, 1998; Murphy et al., 1999;
Murray, 2001; Schaefer, 1997). In the last few decades,
geological studies have brought new information about
South and Central American geographical evolution (e.g.
Received: 3 March 2022
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Revised: 19 March 2022
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Accepted: 22 March 2022
DOI: 10.1111/zsc.12539
ORIGINAL ARTICLE
Evolution and biogeography of Anablepsoides
killifishes shaped by Neotropical geological events
(Cyprinodontiformes, Aplocheilidae)
Pedro F.Amorim
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Wilson J. E. M.Costa
Laboratory of Systematics and
Evolution of Teleost Fishes, Institute
of Biology, Federal University of Rio de
Janeiro, Rio de Janeiro, Brazil
Correspondence
Pedro F. Amorim, Laboratory of
Systematics and Evolution of Teleost
Fishes, Institute of Biology, Federal
University of Rio de Janeiro, Av. Carlos
Chagas Filho, 373, A0- 120, Rio de
Janeiro 21.941- 902, Brazil.
Email: pedro_f_a@hotmail.com
Funding information
Coordenação de Aperfeiçoamento
de Pessoal de Nível Superior, Grant/
Award Number: 88887.466724/2019-
00; Fundação Carlos Chagas Filho de
Amparo à Pesquisa do Estado do Rio
de Janeiro, Grant/Award Number:
E- 26/201.213/2021; Conselho Nacional
de Desenvolvimento Científico e
Tecnológico, Grant/Award Number:
304755/2020- 6
Abstract
Anablepsoides is a widely distributed Neotropical killifish genus found in shallow
streams, in both dense forests and open areas, throughout northern and north-
eastern South America. The phylogenetic and biogeographic relationships of the
genus are here analysed, based on two nuclear and four mitochondrial genes of
26 species and six out- groups. The origin of Anablepsoides was recovered in Early
Miocene in an area corresponding to the Paleo- Amazon- Orinoco system. The
current analyses indicate that the initial diversification of the genus in two main
clades was associated with marine transgressions related to the formation of the
Pebas mega- wetland isolating each MRCA of those main clades in the upper
Amazon river basin and river basins of the Guiana Shield. The diversification
of the genus and the colonisation of new areas may be associated with Miocene
and Pliocene events such as changes in the sea level, formation and extinction of
wetlands, rupture of the Purus arch and Amazon river assuming the current flow
to the East. Also, the evolution of Anablepsoides could be associated with the di-
versification of several other Neotropical lineages, so that the present study leads
to a better understanding of the evolution of the Neotropical freshwater biota and
South American geological history.
KEYWORDS
Amazon river, ancestral area reconstruction, divergence- time estimation, Pebas mega- wetland,
Purus arch, sea- level variation
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AMORIM and COSTA
Behling et al., 2010; Figueiredo et al., 2009, 2010; Garzione
et al., 2008; Hoorn, 1994; Wesselingh & Salo, 2006) and
methodologies of temporal calibration analyses were de-
veloped, allowing to associate a temporal scale to phylo-
genetic analyses (e.g. Drummond et al., 2012; Gernhard,
2008; Heath, 2012). Such advances in these fields have
improved our temporal comprehension of the paleo-
geographic scenarios in which the diversification of the
Neotropical ichthyofauna has occurred and led to more
accurate hypotheses associating geological and biological
evolution.
During the Cenozoic period, several changes have oc-
curred in the Neotropical aquatic environments. Major
geological events, such as the Andean orogeny, associated
with the low topographic relief of the South American
platform have favoured the formation and extinction of
mega- wetlands, changes in river flow direction, connec-
tions and divisions between river basins (Cunha et al.,
1994; Garzione et al., 2008; Hoorn et al., 1995; Lundberg
et al., 1998; Wesselingh et al., 2006). In addition, peri-
ods of marine transgression (in which sea waters have
invaded continental areas) and regression (exposing the
continental shelf and expanding the range of the freshwa-
ter environments), also have affected the diversification
of Neotropical fishes, isolating populations or expanding
the geographical distribution of species (Haq et al., 1988;
Sosdian & Rosenthal, 2009; Woodburne, 2010). Despite
the recent progress in research focussing on the biogeog-
raphy of Neotropical species, there is still little informa-
tion on most of the Neotropical ichthyofauna lineages
(e.g. Amorim & Costa, 2018, 2019; Bloom & Lovejoy, 2017;
Costa et al., 2017; Friedman et al., 2013; Melo et al., 2021;
Thompson et al., 2014). Therefore, understanding the bio-
geography of these groups may also contribute to increase
the knowledge of the continental geological evolution.
The genus Anablepsoides Huber, 1992 is a widely dis-
tributed lineage inhabiting several basins associated with
the Amazon and Orinoco river systems, coastal basins in
northern and northeastern South America and even in the
Lesser Antilles (Costa, 2003, 2008a, 2011). Therefore, un-
derstanding the phylogeny and biogeography of this genus
may contribute to a better comprehension of the geologi-
cal evolution of South America. Anablepsoides comprises
more than 50 species that usually are found in shallow
streams in dense forests and open areas (Costa, 2006,
2008b, 2010; Costa et al., 2013; Costa & Lazzarotto, 2008;
Costa & De Luca, 2010; Fels & de Rham, 1981; Keith et al.,
2006). Among the members of this genus, the body size is
variable, with species ranging from 30mm to 120mm of
total length (Amorim & Bragança, 2018).
Anablepsoides was first proposed as a subgenus of
Rivulus Poey, 1860 (Huber, 1992), which until 2011 was
considered a widely distributed genus inhabiting South
and Central America, including Caribbean islands (Costa,
2011). After a phylogenetic analysis sampling morpholog-
ical and molecular data, Rivulus was not recovered as a
monophyletic group but as six independent lineages, and
consequently, five subgenera were elevated to the level of
genus (Costa, 2011). Despite the presence of species of
Anablepsoides in previous phylogenetic analyses focus-
sing on Neotropical Aplocheiloidei, only a few species
were included in those studies (e.g. Costa, 2011; Hrbek
& Larson, 1999; Murphy et al., 1999). Few information
is available for the relationships within the genus, three
informal species groups were proposed based on the co-
lour pattern and external morphology (Costa, 2010; Costa
et al., 2013); however, they were never evaluated under
a phylogenetic perspective. The A. limoncochae group
includes species from the western Amazon; the A.orna-
tus group is formed by species from the central Amazon
and Guiana shield; and the A.urophthalmus group com-
prises species from the Middle and Lower Amazon river
basin and coastal basins of the Guiana shield and Eastern
Venezuela, and coastal river systems from the mouth of
the Amazon to northeastern Brazil (Costa et al., 2013). In
addition to the few information about the evolution of the
genus, the biogeographical history of Anablepsoides was
also never explored. Thus, the aim of the present study
is to provide the first phylogenetic and time- calibrated
biogeographical analyses focussing on Anablepsoides to
understand the relationship among their species, how the
South American geological events have affected the evo-
lution and the distribution of their species, and which of
those biogeographical events have affected other members
of the Neotropical biota.
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MATERIALS AND METHODS
2.1
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Taxonomic sampling, DNA
extraction, PCR and sequencing
For the present study, 32 species were sampled, in which
26 represent the different lineages of Anablepsoides
and six Neotropical Aplocheiloidei species as out-
groups. The phylogenetic analyses were rooted with
Kryptolebias hermaphroditus Costa, 2011. Molecular
data were obtained from specimens euthanized just after
collection with a buffered solution of ethyl- 3- amino-
benzoate- methansulfonate (MS- 222) at a concentra-
tion of 250 mg/L, for a period of 10min or more, until
completely ceasing opercular movements, following the
methods for euthanasia approved by CEUA- CCS- UFRJ
(Ethics Committee for Animal Use of Federal University
of Rio de Janeiro; permit number: 01200.001568/2013- 87;
project number 065/18). The individuals were fixed and
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AMORIM and COSTA
preserved in absolute ethanol. Specimens analysed were
deposited in UFRJ (Coleção Ictiológica do Instituto de
Biologia da Universidade Federal do Rio de Janeiro) and
IEPA (Instituto de Pesquisas Científicas e Tecnológicas do
Estado do Amapá). The dataset was complemented with
sequences obtained from GenBank. A complete list of taxa
and specimen voucher used in the analyses is present in
the Supporting Information (File S1).
Genomic DNA was extracted from muscle tissue of the
right side of the caudal peduncle using the DNeasy Blood
and Tissue Kit (Qiagen), following the manufacturer's in-
structions. Two nuclear genes, ectodermal- neural cortex
(ENC1) and glycosyltransferase (GLYT), and four mito-
chondrial genes, 16S ribosomal RNA (16s), cytochrome
b (CytB), cytochrome c oxidase subunit 1 (COX1) and
NADH dehydrogenase subunit 2 (ND2) were sampled for
the analyses. Fragments of the DNA were amplified using
the primers listed in the Supporting Information (File
S2). Polymerase chain reactions (PCR) were performed
in 30 μl reaction mixtures containing 5× Green GoTaq
Reaction Buffer (Promega), 3.2mM MgCl2, 1μM of each
primer, 75 ng of total genomic DNA, 0.2 mM of each
dNTP and 1U of Taq polymerase. The thermocycling pro-
file was: (1) 1 cycle of 4min at 94°C; (2) 35 cycles of 1min
at 92°C, 1min at 50– 63°C and 1 min at 72°C; and (3) 1
cycle of 4min at 72°C. In all PCR reactions, negative con-
trols without DNA were used to check contaminations.
Amplified PCR products were purified using the Wizard
SV Gel and PCR Clean- Up System (Promega). Sequencing
reactions were made using the BigDye Terminator Cycle
Sequencing Mix (Applied Biosystems). Cycle sequenc-
ing reactions were performed in 10 μl reaction volumes
containing 1μl BigDye 2.5, 1.55μl 5× sequencing buffer
(Applied Biosystems), 2μl of the amplified products (10–
40ng) and 2μl primer. The thermocycling profile was: (1)
35 cycles of 10s at 96°C, 5s at 54°C and 4min at 60°C. The
sequencing reactions were purified and denatured and the
samples were analysed on an ABI 3130 Genetic Analyzer.
Sequences were edited using MEGA 7 (Kumar et al., 2016)
and aligned using ClustalW (Chenna et al., 2003). The
DNA sequences were translated into amino acids residues
to test for the absence of premature stop codons or in-
dels using the program MEGA 7. The GenBank accession
numbers of the analysed sequences are presented in the
Supporting Information (File S1).
2.2
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Phylogenetic analysis
A matrix with 6493bp was elaborated to perform phyloge-
netic and time- calibrated analyses. The dataset was ana-
lysed in the digital platform W- IQ- TREE (Trifinopoulos
et al., 2016) to determine the best nucleotide substitution
models; the optimal partition strategy is shown in the
Supporting Information (File S3). The phylogenetic
analyses were performed in the programs W- IQ- TREE
(Trifinopoulos et al., 2016), for Maximum Likelihood (ML)
and MrBayes 3.2.6 (Ronquist et al., 2012) for Bayesian in-
ference (BI). The support values of the ML analysis were
calculated by 2000 ultrafast bootstrap replications (Minh
et al., 2013). For BI analysis, four independent Markov
Chain Monte Carlo (MCMC) were performed with 1mil-
lion generations each, sampling one of every 1000 trees.
The support values of the BI analysis were calculated by
posterior probability. The quality of the MCMC chains
was evaluated in Tracer 1.6 (Rambaut et al., 2014), and a
25% burn- in was removed.
2.3
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Divergence- time estimation
The divergence- time analysis was performed in Beast
v.1.8 (Drummond et al., 2012; Heath, 2012), using the con-
catenated dataset with the same partitions as described
above, and a normal uncorrelated relaxed clock model,
which emphasises the minimum age. Bayesian inference
was performed with 50 million generations, a sampling
frequency of 1000. The value of parameters of the analy-
sis, convergence of the MCMC chains, sample size and
the stationary phase of the chains were evaluated using
Tracer v. 1.6 (Rambaut et al., 2014).
A Birth- Death speciation process was applied for the
tree prior (Gernhard, 2008). The calibration point was
placed at the stem comprising the root of the tree, corre-
sponding to the estimated age of the divergence between
Kryptolebias hermaphroditus and all other terminals (i.e.
mean age of 36.56 Mya, standard deviation 1.0). This esti-
mate was taken from a time- calibrated analysis involving
several lineages of Cyprinodontiformes and a wide sam-
pling of taxa of the Suborder Aplocheiloidei (Costa et al.,
2017), using as calibration points two fossil representa-
tives of the European clade comprising Aphaniidae and
Valenciidae, which includes the most rich and accurately
determined fossil record among cyprinodontiformes. This
analysis is chronologically compatible with the analysis
provided by Near et al. (2013) for acantomorph fishes
based on 37 calibration points, showing similar age for the
order Cyprinodontiformes and the main internal lineages.
2.4
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Ancestral area evolution analyses
The event- based analysis was performed using the ap-
proaches Statistical Dispersal- Vicariance Analysis (re-
ferred here as S- Diva) (Yu et al., 2010) and Lagrange
(Dispersal- Extinction- Cladogenesis model, referred
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AMORIM and COSTA
here as DEC) (Ree & Smith, 2008) to infer possible past
biogeographical scenarios of diversification of the genus
Anablepsoides without a priori assumptions about area
relationships (Ronquist, 1997). Reconstruction of ances-
tral states was conducted in the program RASP 3.02 (Yu
et al., 2015). The analysis was directed to historical bio-
geographical patterns, based on 13 areas of endemism de-
limited according to hydrographic basins inhabited by the
sampled Neotropical Aplocheiloidei species: (A) Lower
Amazon river basin; (B) Middle Amazon river basin; (C)
Upper Amazon river basin; (D) Negro river basin; (E)
Madeira river basin; (F) Xingú river basin; (G) Araguaia
river basin; (H) Parnaíba and Munim river basins; (I)
coastal basins of northeastern South America; (J) coastal
basins of Guiana shield; (K) Lesser Antilles.
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RESULTS
The analysed dataset included six genes, four mitochon-
drial and two nuclear, and 32 species comprising 6,493
base pairs. Both ML and BI analyses recovered very similar
topologies and high support for most of the nodes (Figure
1). In both analyses the monophyly of Anablepsoides
was recovered with high support and as sister group of
Cynodonichthys Meek, 1904. Species of Anablepsoides
have recovered clustering in two main groups, referred
to here as clades α (in which species are mostly associ-
ated with river systems related to the Lower Amazon river
basin, coastal rivers of northern and northeastern South
America, Guyana shield and Lesser Antilles) and β (com-
prising species that mostly inhabit areas related to Upper
and Middle Amazon river basin) (Figure 1).
The time- calibrated analysis (Figure 2) recovered
the origin of Anablepsoides (22.96 Ma, 95% HPD 28.7–
17.9Ma) and their diversification in the two main clades
(19.58Ma, 95% HPD 24.8– 14.9Ma) in the Early Miocene.
The diversification within both clades was recovered
as occurring in Middle Miocene (α- clade in 16.0 Ma,
95% HPD 18.7.6– 10.8 Ma; β- clade in 14.4Ma, 95% HPD
27.4– 17.9 Ma). The values of divergence- time estimation
mean and 95% highest posterior densities are presented in
Supporting Information (File S4).
S- Diva and DEC reconstruction of historical biogeo-
graphical analyses supported an ancestral origin of the
genus in an ancient area connecting the Upper Amazon
river basin and coastal basins of Guiana Shield (CJ)
(Figure 2). In both analyses, the most recent common
FIGURE Phylogenetic Bayesian inference. Values above the nodes are relative to the posterior probabilities. Values below the nodes
are relative to the Bootstrap of ML analysis. Illustrations representing: (a) A.xinguensis and (b) A.gamae
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AMORIM and COSTA
FIGURE Time- calibrated tree with the results of analyses of reconstruction of ancestral areas using the analytical approaches S- Diva
(Statistical Dispersal- Vicariance Analysis) and DEC (Lagrange- Dispersal- Extinction- Cladogenesis model). Black circle indicates the position
of the calibrations used. Bars represent the 95% highest posterior credibility intervals of divergence times. Map representing biogeographical
areas occupied by Anablepsoides: (A) Lower Amazon river basin; (B) Middle Amazon river basin; (C) Upper Amazon river basin; (D) Negro
river basin; (E) Madeira river basin; (F) Xingú river basin; (G) Araguaia river basin; (H) Parnaíba and Munim river basins; (I) coastal basins
of northeastern South America; (J) coastal basins of Guiana shield; (K) Lesser Antilles
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AMORIM and COSTA
ancestor (MRCA) of the clades α and β were recovered in-
habiting the Upper Amazon river basin (C) and the coastal
basins of Northern South America (J), respectively. The
complete results of DEC and S- Diva analyses are available
in Supporting Information (File S5).
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DISCUSSION
4.1
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Phylogenetic analysis
The genus Anablepsoides was recovered as the sister
group of Cynodonichthys tenuis Meek, 1904 with high
support in both analyses (Figure 1). In previous phylo-
genetic studies, the position of the genus was not clear,
as it was recovered in a polytomy with other Neotropical
Aplocheiloidei lineages (Hrbek & Larson, 1999; Murphy
et al., 1999) or as a sister group of Atlantirivulus Costa,
2008, but with low support values (Costa, 2011). In those
studies, few representatives of Anablepsoides were in-
cluded, and only mitochondrial information was ana-
lysed. So that, for the first time a wide sample of the
genus is analysed under a phylogenetic perspective and
with both mitochondrial and nuclear information. The
current phylogenetic analyses recovered Anablepsoides
as composed by two main clades (Figure 1), one of them
with species inhabiting river systems associated with the
Lower Amazon river basin; coastal basins of the Guiana
Shield and northeastern Brazil; and Lesser Antilles, re-
ferred to here as the α- clade (Figure 2). The species com-
prised in this clade are traditionally considered members
of the Anablepsoides urophthalmus species group (Costa,
2010; Costa et al., 2013). The second clade, referred here
as β- clade, is mainly composed of species inhabiting ba-
sins associated with the Upper and Middle Amazon river
basin (Figure 2). Both analyses recovered the species
usually included in the A. limoncochae and A. ornatus
species groups as the members of the β- clade (Figure 1).
The type species of the genus, A.atratus (Garman, 1895),
was recovered in the β- clade, related to other species of
the A.ornatus species group (Costa, 2010; Costa et al.,
2013).
4.2
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Initial diversification and the Paleo-
Amazon- Orinoco system
The time- calibrated analysis recovered the origin of
Anablepsoides between the Late Oligocene and Early
Miocene (22.96Ma, 95% HPD 28.7– 17.9Ma) and the di-
vergence between the two main clades of the genus ap-
proximately at the Early Miocene (19.58Ma, 95% HPD
24.8– 14.9Ma) (Figure 2). The analyses of ancestral area
reconstruction indicated that the MRCA of the genus
inhabited an area composed of the Upper Amazon river
basin and the coastal rivers of the Guiana Shield (CJ).
The division of this ancient area was coincident with
the diversification of the genus in clades α and β, so that
the MRCA of each clade remained restricted to coastal
rivers of the Guiana Shield (J) and the Upper Amazon
river basin (C), respectively (Figure 2). These results are
chronologically and geographically congruent with the
formation of the Pebas mega- wetland, a broad aquatic
environment connected to the Caribbean Sea. This eco-
system was initially formed by marine transgressions
and comprised different kinds of environments, mainly
with brackish water, but also presenting areas of salt and
freshwater (Wesseling et al., 2002, 2006). Before the for-
mation of the Pebas mega- wetland, the area was occu-
pied by the Paleo- Amazon- Orinoco system, which was
composed of river basins from the Guiana shield and
western Amazon areas, forming a system flowing north,
reaching the Caribbean sea (Hoorn et al., 1995; Lundberg
et al., 1998; Wesseling & Salo, 2006). The current analy-
ses corroborate that the MRCA of Anablepsoides was
probably distributed through the Paleo- Amazon- Orinoco
system, and the division of the lineages occurred due to
the marine transgressions associated with the formation
of the Pebas mega- wetland, isolating the MRCA of the
clades α and β in the Guiana Shield and Upper Amazon
basin, respectively. Only a few specialised Neotropical
Aplocheiloidei species may tolerate brackish waters, but
no species of Anablepsoides is known to occur in this
kind of environment. Therefore, this Cenozoic marine
transgression was probably the first geological event act-
ing over the distribution and diversification of the genus
Anablepsoides (Cooper et al., 2013; Costa, 2016). Despite
the advances in biogeographical knowledge regarding
Neotropical ichthyofauna, there is still few information
about how the formation of Pebas affected the distribu-
tion of Neotropical freshwater fishes; furthermore, the
geological conditions of such region make this area un-
suitable for fossil formation (Albert & Carvalho, 2011).
The diversity of environments found in Pebas had an im-
portant role in the transition of marine and brackish fish
lineages to colonise freshwater habitats (e.g. Amorim &
Costa, 2018; Bloom & Lovejoy, 2017; Fontenelle et al.,
2021; Sferco et al., 2017). For terrestrial vertebrates de-
pendent on freshwater environments, such as Anurans,
there is also evidence that those marine transgressions
related to Pebas have affected the distribution and di-
versification of the lineages, similarly as recovered here
for Anablepsoides (e.g. Jowers et al., 2021; Réjaud et al.,
2020).
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AMORIM and COSTA
4.3
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α- clade diversification and
Antillean colonisation
After the divergence between the clades α and β, the
MRCA of the α- clade was recovered as inhabiting the
coastal basins of the Guiana Shield (J) (Figure 2). The cur-
rent phylogenetic analyses recovered the most basal lin-
eages still occupying this same biogeographical area and
only two groups inhabiting new regions: one represented
by A.cryptocallus (Seegers, 1980), occurring in the Lesser
Antilles (K), and one composed of A. bahianus (Huber,
1990), A. vieirai Nielsen, 2016, A.xinguensis (Costa, 2010),
A.sp. and A.urophthalmus (Günther, 1866), in basins as-
sociated with the Lower Amazon river system and north-
eastern Brazil basins (A, F, G, H, I) (Figure 2). In this clade,
the first event of colonisation of new areas is coincident
with the diversification of the lineage composed of A.ba-
hianus, A.vieirai, A.xinguensis, A.sp, A.urophthalmus,
A.stagnatus, (Eigenmann, 1909) A.deltaphilus (Seegers,
1983) and A.cryptocallus at the Late Miocene (7.64Ma,
95% HPD 10.09– 5.43Ma) (Figure 2). The present analysis
of the reconstruction of ancestral areas indicates that this
event is related to the connection of the coastal basins of
the Guiana Shield (J) with new areas (Figure 2). The pe-
riod of this diversification is congruent with the Amazon
river assuming the current role of a transcontinental river,
flowing to the East and a global reduction in the sea level
(Figueiredo et al., 2009, 2010; Haq et al., 1988). Therefore,
changes in the sea level in association with this substan-
tial increase of freshwater in the area of the MRCA of this
group could have favoured the dispersion from coastal
basins of the Guiana Shield (J), making possible the colo-
nisation of new regions. Hence, the subsequent changes
in the sea level would have separated the lineage into two
groups: (i) one remaining in the ancestral area (J), repre-
sented here by A.stagnatus, A.deltaphilus and A.crypto-
callus, and (ii) the lineage colonising new areas associated
with the Lower Amazon river system and northeastern
South America basins (A, F, G, H, I), here represented by
A.bahianus, A.vieirai, A.xinguensis, A. sp and A.uroph-
thalmus (Figure 2). This biogeographical pattern was also
recovered for two independent lineages of the freshwa-
ter fish family Curimatidae (Melo et al., 2021). A recent
time- calibrated biogeographical analysis of this characi-
form group has recovered that species of Steindachnerina
Fowler, 1906 and Psectrogaster Eigenmann & Eigenmann,
1889 inhabiting river basins of northeastern Brazil are
phylogenetically related to lineages found in Amazon,
Orinoco and coastal Guiana Shield river basins, and the
divergence between those lineages, in both genera, were
recovered as occurring in the Late Miocene (Melo et al.,
2021). These results are congruent with the current analy-
ses for Anablepsoides (Figure 2), corroborating an ancient
connection between coastal basins of the Guiana Shield,
Lower Amazon river system and northeastern Brazil
basins.
During Pliocene, both events of colonisation of the
Lesser Antilles (K) and diversification in northeastern
Brazil and the Lower Amazon river systems (A, F, G, H,
I) were recovered in the α- clade (Figure 2). During this
geological period, several changes in the sea level were re-
corded, with marine regressions reaching 40m to 80m
and exposing the continental shelf (Lisiecki & Raymo,
2005; Sosdian & Rosenthal, 2009; Woodburne, 2010).
These variations in the oceanic level would have favoured
dispersal events between different coastal basins, such as
from Guiana Shield (J) to Lesser Antilles (K), allowing
the MRCA of A.cryptocallus and A.deltaphilus to expand
its distribution, colonising the Lesser Antilles and there-
after being isolated due to a subsequent rise of the sea,
separating the current lineages (3.04Ma, 95% HPD 4.47–
1.85Ma). Connections between northern South America
and Lesser Antilles along the Pliocene are also corrobo-
rated by analyses focussing on land Tetrapoda, such as
time- calibrated divergence of anurans, as recovered for
the families Centrolenidae and Microhylidae (Jowers
et al., 2014, 2021), and the fossil record of different orders
of mammalians (MacPhee et al., 2000).
The diversification of the lineage including A. bahi-
anus, A.vieirai, A.xinguensis, A. sp and A.urophthalmus
occurred in the Pliocene (3.73 Ma, 95% HPD 5.61–
2.17Ma), in a period close to the diversification of the lin-
eage composed of A.deltaphilus and A.cryptocallus. This
chronological proximity indicates that the diversification
and colonisation of new areas by this group are probably
also associated with Pliocene variations in the sea level,
as discussed above (Lisiecki & Raymo, 2005; Sosdian &
Rosenthal, 2009; Woodburne, 2010). The results of the cur-
rent analyses indicate that in periods of sea regression, the
MRCA of this group was inhabiting a broad coastal area,
from the Lower Amazon river (A) to northeastern Brazil
(I) (Figure 2). The subsequent episodes of sea- level rise
probably acted as vicariant events, splitting this lineage
into three main groups; first in coastal basins of northeast-
ern South America (I) (3.73Ma, 95% HPD 5.61– 2.17Ma);
second in Parnaíba River and Munim river basins (H)
(2.18Ma, 95% HPD 3.34– 1.29Ma); and a third group in
an area composed of Lower Amazon (A), Xingú (F) and
Araguaia (G) river basins. Such changes in the sea level
are indicated as a main factor acting over the distribution
of other lineages of freshwater fishes inhabiting coastal
basins in northern and northeastern South America, such
as the loricariid catfish genus Hypostomus Lacepède, 1803
(Montoya- Burgos, 2003).
For the lineage that includes A. urophthalmus,
A.xinguensis and A. sp, the diversification of those species
8
|
AMORIM and COSTA
occurred in the Early Pleistocene (1.68Ma, 95% HPD 2.46–
1.01Ma) (Figure 2). This period was marked by cycles of
climatic oscillations, with wide variations in temperature,
and reduction in humidity and precipitation rate (Behling
et al., 2010; Hammen & Hooghiemstra, 2000; Wesselingh
et al., 2010). Those prolonged dry seasons affected the vol-
ume of many rivers in the Amazon basin, which probably
contributed to the isolation of these lineages in the areas
currently inhabited by the group. This biogeographical
pattern is chronologically congruent with the diversifica-
tion found in the freshwater dolphins of the genus Inia
d'Orbigny, 1834 (Hrbek et al., 2014). The phylogenetic
event of diversification of these Cetaceans species inhab-
iting Amazon and Orinoco river basins [Inia geoffrensis
(de Blainville, 1817)], from the species found exclusively
in Araguaia- Tocantins river system (Inia araguaiaensis
Hrbek et al., 2014), was also recovered as occurring in
Early Pleistocene (Hrbek et al., 2014). This congruence
indicates that the same biogeographical events could have
affected the diversification of both groups.
4.4
|
β- clade diversification and the
Purus arch
After the formation of the Pebas Mega- Wetland, the
MRCA of the β- clade was recovered with a distribution re-
stricted to areas currently occupied by the Upper Amazon
river basin (Figure 2). During that period, those freshwater
environments in the western Amazon remained isolated
from other hydrographic basins not only due to the Pebas
mega- wetland but also by the conformation of the Purus
arch (Figueiredo et al., 2009). Stratigraphic evidence in-
dicates that the Pebas mega- wetland remained separated
from the eastern Amazonian river systems by the Purus
arch during the Early to Middle Miocene (Cunha et al.,
1994; Eiras et al., 1994; Figueiredo et al., 2009). In addition
to the MRCA of the β- clade, available evidence indicates
that several freshwater groups remained isolated in the
western Amazon region during the same period, such as
several lineages of Actinopterygii (e.g. Hubert & Renno,
2006), and freshwater stingrays (Fontenelle et al., 2021).
Only during the Late Miocene, a combination of events,
including the increase in the Andean uplift (Garzione
et al., 2008), climatic changes (Uba et al., 2007), rupture
of the Purus arch (Figueiredo et al., 2009) and decrease
in sea level (Haq et al., 1988), allowed the unification
between western and eastern Amazonian river systems
(Figueiredo et al., 2009, 2010). Therefore, the Amazon
river assumed the current flow to the east across the
continent, and the connection between the Pebas mega-
wetland and the Caribbean sea has ceased (Figueiredo
et al., 2009, 2010). After this great hydrographic change,
another wetland was formed in the area of the cur-
rent Upper Amazon river basin, the Acre mega- wetland
(Hovikoski et al., 2010; Wesselingh et al., 2010). This en-
vironment was composed of streams and shallow lakes,
similar to the modern Brazilian Pantanal (Cozzuol, 2006;
Latrubesse et al., 2007). The present analysis indicated that
few events of diversification have occurred in the β- clade
before the formation of the Acre mega- wetland (Figure 2).
Geological evidence supports that this environment has
suffered short sporadic events of influence of saltwater
along with its existence (from 11Ma to 7Ma); however,
the source of those marine transgressions is still uncertain
(Hulka et al., 2006; Hovikoski et al., 2007, 2010; Wesseling
et al., 2010). The Acre mega- wetland probably influenced
the early diversification of the genus in the current Upper
Amazon river area (C), first allowing the colonisation of
different systems associated with this mega- wetland and
thereafter isolating those systems due to the saltwater of
the marine transgressions. The formation of the Acre sys-
tem also influenced the diversification of other vertebrate
groups highly dependent on freshwater environments,
such as Anurans (Fouquet et al., 2021), and fossil lineages
of Crocodylomorpha (Cidade et al., 2019).
In the β- clade, most events in which new areas
were reached have occurred in the Pliocene (Figure 2).
However, the lineage represented by Anablepsoides be-
niensis (Myers, 1927), inhabiting the Madeira river basin
(E), indicates an earlier event of colonisation. The cur-
rent time- calibrated analysis recovered the origin of this
lineage occurring in the Late Miocene (7.95Ma 95% HPD
11.05– 5.21Ma) and the analyses of reconstruction of the
ancestral area support that there was an ancient area
composed of the Upper Amazon and the Madeira river
basins (CE) in this period (Figure 2). Such connection
is also corroborated by geological evidence, indicating a
connection persisting until the Late Miocene; the divi-
sion of those basins would have been caused by the uplift
of the Fitzcarrald Arch and the subduction of the Nazca
Ridge, therefore isolating the ancestor of the lineage rep-
resented by A.beniensis (Espurt et al., 2007; Westaway,
2006). A recent biogeographical analysis focussing on the
genus Fluviphylax Whitley, 1965, a miniature cyprino-
dontiform group, corroborates as well that these geo-
logical events are associated with the diversification of
species (Bragança & Costa, 2018). In this study, the diver-
sification between the F.pygmaeus (Myers & Carvalho,
1955), inhabiting the Madeira river basin, and F.simplex
Costa, 1996, found along floodplains of the Amazon river,
was also recovered as occurring in the Late Miocene, so
that these events would be the cause of the diversification
in both cyprinodontiform lineages.
In the Late Miocene, the present configuration of
the Amazon river was completely formed and there is
|
9
AMORIM and COSTA
no evidence of marine influence in this basin during
the last 7 Ma (Wesselingh & Hoorn, 2011). These condi-
tions made it possible for the members of the β- clade to
disperse to new areas of the Amazon river basin in inde-
pendent events along the Pliocene. This hydrological con-
figuration allowed the MRCA of the lineage composed of
Anablepsoides christinae (Huber, 1992) and A. urubuien-
sis Costa, 2013 to disperse, reaching the Middle Amazon
river basin (B) and Madeira river basin (E) (3.99Ma 95%
HPD 5.96– 2.42Ma) (Figure 2). Therefore, despite the pres-
ence of both A.beniensis (Myers, 1927) and A. christinae
in Madeira river basin (E), this distribution was the result
of two independent events at different periods. The age
of the diversification between A. urubuiensis, inhabiting
the Middle Amazon river basin (B), and A. christinae,
found in the Madeira river basin (E) (2.97Ma 95% HPD
4.61– 1.61 Ma) is also chronologically congruent with the
diversification of the freshwater dolphins Inia boliviensis
d'Orbigny, 1834, found in the Madeira river basin, and the
MRCA of the species I. geoffrensis and I. araguaiaensis
(Hrbek et al., 2014). This congruence may indicate that
those diversification events may be caused by the final
events associated with the uplift of the Fitzcarrald Arch
and the subduction of the Nazca Ridge (Espurt et al., 2007;
Westaway, 2006). Another process of colonisation of the
Middle Amazon river basin (B) has occurred in the MRCA
of the lineage composed of A.atratus, A.henschelae Costa
et al., 2013, A.amana (Costa & Lazzarotto, 2008), A.orna-
tus (Garman, 1895) and A.gamae Costa et al., 2013. For
this group, the environmental conditions made it possi-
ble to reach the Middle Amazon river basin (B) (Figure
2), and after that two probable events of dispersion were
recorded: one represented by A.henschelae, colonising the
Negro river basin (D) (2.85Ma 95% HPD 4.39– 1.58Ma)
and another by the lineage represented by A.gamae reach-
ing the Lower Amazon river basin (A) (0.85Ma 95% HPD
1.54– 0.29Ma) (Figure 2).
5
|
CONCLUSION
Considering the huge diversity of the Neotropical ich-
thyofauna, there are still few studies exploring how the
geological evolution of South America has influenced the
diversification of the freshwater fishes of this region. For
the first time, molecular data were applied in analyses fo-
cussing on the phylogenetic and biogeographical history
of Anablepsoides. Since this group has originated in the
Early Miocene, the current study represents important
steps not only to a better understanding on the evolu-
tion and relationships within the genus but also reflects
how the complex and dynamic geological history of South
America was able to shape the current distribution of the
Neotropical biota. The present results bring a higher reso-
lution for the Neotropical biogeography, corroborating
the importance of different geological and climatic events,
demonstrating how those events have acted, leading to the
diversification of not only Anablepsoides species but also
for different Neotropical lineages, such as other Teleostei
fishes, stingrays, anurans, crocodiles and both terrestrial
and aquatic mammals.
ACKNOWLEDGEMENTS
We are thankful to P.H.N. Bragança, F.P. Ottoni and E.
Henschel for collecting individuals that were used in this
study; to B.M. Camisão for assistance in analyses; and to
C. Gama for the loan of material. This study was funded
by Coordenação de Aperfeiçoamento de Pessoal de Nível
Superior (CAPES; grant 88887.466724/2019- 00 to PFA)
through Programa de Pós- Graduação em Genética/UFRJ,
by Conselho Nacional de Desenvolvimento Científico e
Tecnológico (CNPq; grant 304755/2020- 6 to WJEMC) and
Fundação Carlos Chagas Filho de Amparo a Pesquisa do
Estado do Rio de Janeiro (FAPERJ; E- 26/201.213/2021 to
WJEMC). Collections were made with permits provided
by IBAMA (Instituto Brasileiro de Meio Ambiente e dos
Recursos Naturais Renováveis) and ICMBio (Instituto
Chico Mendes de Conservação da Biodiversidade).
ORCID
Pedro F. Amorim https://orcid.
org/0000-0001-7029-0275
Wilson J. E. M. Costa https://orcid.
org/0000-0002-0428-638X
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How to cite this article: Amorim, P. F., &
Costa, W. J. E. M. (2022). Evolution and
biogeography of Anablepsoides killifishes shaped by
Neotropical geological events (Cyprinodontiformes,
Aplocheilidae). Zoologica Scripta, 00, 1– 13. https://
doi.org/10.1111/zsc.12539
