Phylogeography of the arid-adapted Malagasy bullfrog, Laliostoma labrosum, influenced by past connectivity and habitat stability

Pabijan, Maciej; Brown, Jason L.; Chan, Lauren M.; Rakotondravony, Hery A.; Raselimanana, Achille P.; Yoder, Anne D.; Glaw, Frank; Vences, Miguel

doi:10.1016/j.ympev.2015.05.018

Cited by 14 publications

(10 citation statements)

References 92 publications

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“…In southern Europe it was often a result of speciation by isolation in consequence of severe alterations and fragmentations of habitats during Pleistocene climatic oscillations ( Hewitt, 2004 ; Salicini, Ibanez & Juste, 2013 ; Goncalves et al, 2015 ). However, the presence of pre-Pleistocene lineages within conventionally recognised morphospecies was reported for several terrestrial and fewer freshwater taxa, including: reptiles; amphibians; and fish, but also insects and molluscs (e.g., Albrecht et al, 2007 ; Marková et al, 2010 ; Falniowski et al, 2012 ; Garcia Munoz et al, 2014 ; Previšić et al, 2014 ; Pabijan et al, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

Neogene paleogeography provides context for understanding the origin and spatial distribution of cryptic diversity in a widespread Balkan freshwater amphipod

Grabowski

Mamos

Bącela-Spychalska

et al. 2017

PeerJ

101

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BackgroundThe Balkans are a major worldwide biodiversity and endemism hotspot. Among the freshwater biota, amphipods are known for their high cryptic diversity. However, little is known about the temporal and paleogeographic aspects of their evolutionary history. We used paleogeography as a framework for understanding the onset of diversification in Gammarus roeselii: (1) we hypothesised that, given the high number of isolated waterbodies in the Balkans, the species is characterised by high level of cryptic diversity, even on a local scale; (2) the long geological history of the region might promote pre-Pleistocene divergence between lineages; (3) given that G. roeselii thrives both in lakes and rivers, its evolutionary history could be linked to the Balkan Neogene paleolake system; (4) we inspected whether the Pleistocene decline of hydrological networks could have any impact on the diversification of G. roeselii.Material and MethodsDNA was extracted from 177 individuals collected from 26 sites all over Balkans. All individuals were amplified for ca. 650 bp long fragment of the mtDNA cytochrome oxidase subunit I (COI). After defining molecular operational taxonomic units (MOTU) based on COI, 50 individuals were amplified for ca. 900 bp long fragment of the nuclear 28S rDNA. Molecular diversity, divergence, differentiation and historical demography based on COI sequences were estimated for each MOTU. The relative frequency, geographic distribution and molecular divergence between COI haplotypes were presented as a median-joining network. COI was used also to reconstruct time-calibrated phylogeny with Bayesian inference. Probabilities of ancestors’ occurrence in riverine or lacustrine habitats, as well their possible geographic locations, were estimated with the Bayesian method. A Neighbour Joining tree was constructed to illustrate the phylogenetic relationships between 28S rDNA haplotypes.ResultsWe revealed that G. roeselii includes at least 13 cryptic species or molecular operational taxonomic units (MOTUs), mostly of Miocene origin. A substantial Pleistocene diversification within-MOTUs was observed in several cases. We evidenced secondary contacts between very divergent MOTUs and introgression of nDNA. The Miocene ancestors could live in either lacustrine or riverine habitats yet their presumed geographic localisations overlapped with those of the Neogene lakes. Several extant riverine populations had Pleistocene lacustrine ancestors.DiscussionNeogene divergence of lineages resulting in substantial cryptic diversity may be a common phenomenon in extant freshwater benthic crustaceans occupying areas that were not glaciated during the Pleistocene. Evolution of G. roeselii could be associated with gradual deterioration of the paleolakes. The within-MOTU diversification might be driven by fragmentation of river systems during the Pleistocene. Extant ancient lakes could serve as local microrefugia during that time.

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Section: Discussionmentioning

confidence: 99%

Neogene paleogeography provides context for understanding the origin and spatial distribution of cryptic diversity in a widespread Balkan freshwater amphipod

Grabowski

Mamos

Bącela-Spychalska

et al. 2017

PeerJ

101

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“…However, the presence of pre-Pleistocene lineages within conventionally recognised morphospecies was reported for several terrestrial and fewer freshwater taxa, including: reptiles; amphibians; and fish, but also insects and molluscs (e.g. Albrecht et al, 2007;Marková et al, 2010;Falniowski et al, 2012;Garcia Munoz et al, 2014;Previšić et al, 2014;Pabijan et al, 2015). (Verovnik et al, 2005;Sworobowicz et al, 2015), which is similar to the spatial distribution pattern we have obtained for G. roeselii.…”

Section: High Level and Pre-pleistocene Onset Of Cryptic Diversitysupporting

confidence: 86%

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Supplemental Information 1: Detailed Information for All Analysed Individuals

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Background. The Balkans are a major biodiversity and endemism hotspot, worldwide. Among the freshwater biota, amphipods are known for their high cryptic diversity. However, little is known about the temporal and paleogeographic aspects of their evolutionary history. We used paleogeography as a framework for understanding the onset of diversification in Gammarus roeselii: 1) we hypothesised that, given the high number of isolated waterbodies in the Balkans, the species is characterised by high level of cryptic diversity, even on a local scale; 2) the long geological history of the region might promote pre-Pleistocene divergence between lineages; 3) given that G. roeselii thrives both in lakes and rivers, its evolutionary history could be linked to the Balkan Neogene paleolake system; 4) we inspected whether the Pleistocene decline of hydrological networks could have any impact on the diversification of G. roeselii. Material and Methods. DNA was extracted from 136 individuals collected from 26 sites all over Balkans. All individuals were amplified for ca. 650 bp long fragment of the mtDNA cytochrome oxidase subunit I (COI). After defining molecular operational taxonomic units (MOTU) based on COI, 50 individuals were amplified for ca. 900 bp long fragment of the nuclear 28S rDNA. Molecular diversity, divergence, differentiation and historical demography based on COI sequences were estimated for each MOTU. The relative frequency, geographic distribution and molecular divergence between COI haplotypes were presented as a median-joining network. COI was used also to reconstruct time-calibrated phylogeny with Bayesian inference. Probabilities of ancestors' occurrence in riverine or lacustrine habitats, as well their possible geographic locations, were estimated with the Bayesian method. A Neighbour Joining tree was constructed to illustrate the phylogenetic relationships between 28S rDNA haplotypes. Results. We revealed that G. roeselii includes at least 13 cryptic species or molecular operational taxonomic units (MOTUs), mostly of Miocene origin. A substantial Pleistocene diversification within-MOTUs was observed in several cases. We evidenced secondary contacts between very divergent MOTUs and introgression of nDNA. The Miocene ancestors could live in either lacustrine or riverine habitats yet their presumed geographic localisations overlapped with those of the Neogene lakes. Several extant riverine populations had Pleistocene lacustrine ancestors. Discussion. Neogene divergence of lineages resulting in substantial cryptic diversity may be a common phenomenon in extant freshwater benthic crustaceans occupying areas that were not glaciated during

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“…On the other hand, large body size is part of a dispersal-prone phenotype and is linked to diversification in toads (Van Bocxlaer et al, 2010). In general, body size is positively correlated with range size as recently shown in a comprehensive study of Malagasy amphibians and reptiles (Brown et al, 2015), reflecting higher dispersal capacity of large-sized animals, but this association has not yet been analyzed in a large-scale macroecological study in amphibians. Likewise, no large-scale test of habitat associations and body size is available, even though many large-bodied temperate species (anurans and salamanders) seem to be associated with aquatic habitat, many large-bodied tropical species seem to be arboreal, whereas small species from both high and low latitudes seem to be more terrestrial (Wells, 2007).…”

Section: Iie Body Size In Mantellid and Other Frogs: Traits And Specimentioning

confidence: 95%

“…Aquatic breeders with free-swimming larvae (and usually large clutch sizes) may be more mobile because of periodic migrations of adults to breeding habitats. Mobility may be particularly high in species adapted to dry climates in which breeding habitat is ephemeral and unstable, as suggested by elevated levels of gene flow across landscapes (Chan and Zamudio, 2009;Pabijan et al, 2015). Moreover, dispersal may be facilitated in species that deposit eggs or larvae in rivers, streams or periodically flooded pools, due to occasional long distance transport in lotic waters.…”

Section: Iie Body Size In Mantellid and Other Frogs: Traits And Specimentioning

confidence: 99%

Mechanisms of speciation in reptiles and amphibians: a synopsis

Marshall

Bastiaans

Caccone

et al. 2018

Preprint

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Speciation processes have long been inferred from phylogenetic, phylogeographic, and biogeographic pattern-driven perspectives. Now much current speciation research is attempting to more directly describe the underlying processes and mechanisms of divergence leading to speciation. Ideally, researchers should integrate both process- and pattern-based approaches for a more comprehensive understanding of speciation. To this end, a symposium was organized during the 7th World Congress of Herpetology in Canada with the goal of bringing leading experts together to share successful examples of these perspectives and to promote a more cohesive understanding of reptile and amphibian speciation. Here we present a joint paper of short and updated summaries of each of these contributions with the aim of providing a reference source and launching pad for students and researchers interested in speciation in amphibians and reptiles.

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Phylogeography of the arid-adapted Malagasy bullfrog, Laliostoma labrosum, influenced by past connectivity and habitat stability

Cited by 14 publications

References 92 publications

Neogene paleogeography provides context for understanding the origin and spatial distribution of cryptic diversity in a widespread Balkan freshwater amphipod

Neogene paleogeography provides context for understanding the origin and spatial distribution of cryptic diversity in a widespread Balkan freshwater amphipod

Untitled

Mechanisms of speciation in reptiles and amphibians: a synopsis

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