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      Fossil snakes (Squamata, Serpentes) from the tar pits of Venezuela: taxonomic, palaeoenvironmental, and palaeobiogeographical implications for the North of South America during the Cenozoic/Quaternary boundary

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          Abstract

          Background

          Tar seep deposits in South America historically are well-known for their rich record of fossil mammals, contrasting with only a few formal reports of reptile remains. Here we report a new snake fauna recovered from two tar pits from Venezuela. The fossil remains come from two localities: (a) El Breal de Orocual, which comprises an inactive tar seep estimated to be Plio/Pleistocene in age; and (b) Mene de Inciarte, an active surface asphalt deposit with an absolute age dating to the late Pleistocene.

          Methods

          The taxonomic identity of all specimens was assessed via consultation of the relevant literature and comparison with extant specimens. The taxonomic assignments are supported by detailed anatomical description.

          Results

          The Mene de Inciarte snake fauna comprises vertebral remains identified as the genus Epicrates sp. (Boidae), indeterminate viperids, and several isolated vertebrae attributable to “Colubridae” (Colubroidea, sensu Zaher et al., 2009). Amongst the vertebral assemblage at El Breal de Orocual, one specimen is assigned to the genus Corallus sp. (Boidae), another to cf. Micrurus (Elapidae), and several others to “Colubrids” (Colubroides, sensu Zaher et al., 2009) and the Viperidae family.

          Conclusions

          These new records provide valuable insight into the diversity of snakes in the north of South America during the Neogene/Quaternary boundary. The snake fauna of El Breal de Orocual and Mene de Inciarte demonstrates the presence of Boidae, Viperidae, “colubrids”, and the oldest South American record of Elapidae. The presence of Corallus, Epicrates, and viperids corroborates the mosaic palaeoenvironmental conditions of El Breal de Orocual. The presence of Colubroides within both deposits sheds light on the palaeobiogeographical pattern of caenophidians snake colonization of South America and is consistent with the hypothesis of two episodes of dispersion of Colubroides to the continent.

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          Most cited references76

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          Tracing an invasion: landbridges, refugia, and the phylogeography of the Neotropical rattlesnake (Serpentes: Viperidae: Crotalus durissus).

          Abstract Pleistocene fragmentation of the Amazonian rainforest has been hypothesized to be a major cause of Neotropical speciation and diversity. However, the role and even the reality of Pleistocene forest refugia have attracted much scepticism. In Amazonia, previous phylogeographical studies have focused mostly on organisms found in the forests themselves, and generally found speciation events to have predated the Pleistocene. However, molecular studies of open-formation taxa found both north and south of the Amazonian forests, probably because of vicariance resulting from expansion of the rainforests, may provide novel insights into the age of continuous forest cover across the Amazon basin. Here, we analyse three mitochondrial genes to infer the phylogeography of one such trans-Amazonian vicariant, the Neotropical rattlesnake (Crotalus durissus), which occupies primarily seasonal formations from Mexico to Argentina, but avoids the rainforests of Central and tropical South America. The phylogeographical pattern is consistent with gradual dispersal along the Central American Isthmus, followed by more rapid dispersal into and across South America after the uplift of the Isthmus of Panama. Low sequence divergence between populations from north and south of the Amazon rainforest is consistent with mid-Pleistocene divergence, approximately 1.1 million years ago (Ma). This suggests that the Amazonian rainforests must have become fragmented or at least shrunk considerably during that period, lending support to the Pleistocene refugia theory as an important cause of distribution patterns, if not necessarily speciation, in Amazonian forest organisms. These results highlight the potential of nonforest species to contribute to an understanding of the history of the Amazonian rainforests themselves.
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            Snake phylogeny based on osteology, soft anatomy and ecology.

            Relationships between the major lineages of snakes are assessed based on a phylogenetic analysis of the most extensive phenotypic data set to date (212 osteological, 48 soft anatomical, and three ecological characters). The marine, limbed Cretaceous snakes Pachyrhachis and Haasiophis emerge as the most primitive snakes: characters proposed to unite them with advanced snakes (macrostomatans) are based on unlikely interpretations of contentious elements or are highly variable within snakes. Other basal snakes include madtsoiids and Dinilysia--both large, presumably non-burrowing forms. The inferred relationships within extant snakes are broadly similar to currently accepted views, with scolecophidians (blindsnakes) being the most basal living forms, followed by anilioids (pipesnakes), booids and booid-like groups, acrochordids (filesnakes), and finally colubroids. Important new conclusions include strong support for the monophyly of large constricting snakes (erycines, boines. pythonines), and moderate support for the non-monophyly of the trophidophiids' (dwarf boas). These phylogenetic results are obtained whether varanoid lizards, or amphisbaenians and dibamids, are assumed to be the nearest relatives (outgroups) of snakes, and whether multistate characters are treated as ordered or unordered. Identification of large marine forms, and large surface-active terrestrial forms, as the most primitive snakes contradicts with the widespread view that snakes arose via minute, burrowing ancestors. Furthermore, these basal fossil snakes all have long flexible jaw elements adapted for ingesting large prey ('macrostomy'), suggesting that large gape was primitive for snakes and secondarily reduced in the most basal living foms (scolecophidians and anilioids) in connection with burrowing. This challenges the widespread view that snake evolution has involved progressive, directional elaboration of the jaw apparatus to feed on larger prey.
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              Diversification rates and phenotypic evolution in venomous snakes (Elapidae)

              The relationship between rates of diversification and of body size change (a common proxy for phenotypic evolution) was investigated across Elapidae, the largest radiation of highly venomous snakes. Time-calibrated phylogenetic trees for 175 species of elapids (more than 50% of known taxa) were constructed using seven mitochondrial and nuclear genes. Analyses using these trees revealed no evidence for a link between speciation rates and changes in body size. Two clades (Hydrophis, Micrurus) show anomalously high rates of diversification within Elapidae, yet exhibit rates of body size evolution almost identical to the general elapid ‘background’ rate. Although correlations between speciation rates and rates of body size change exist in certain groups (e.g. ray-finned fishes, passerine birds), the two processes appear to be uncoupled in elapid snakes. There is also no detectable shift in diversification dynamics associated with the colonization of Australasia, which is surprising given that elapids appear to be the first clade of venomous snakes to reach the continent.
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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                peerj
                peerj
                PeerJ
                PeerJ Inc. (San Francisco, USA )
                2167-8359
                14 August 2018
                2018
                : 6
                : e5402
                Affiliations
                [1 ]Departamento de Biologia, Laboratório de Paleontologia de Ribeirão Preto, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto, Universidade de São Paulo , Ribeirão Preto, São Paulo, Brazil
                [2 ]Centro de Ecología, Laboratório de Paleontología, Instituto Venezolano de Investigaciones Científicas , Caracas, Venezuela
                Article
                5402
                10.7717/peerj.5402
                6097493
                50306438-8dcb-4165-81cc-fc01795388d3
                ©2018 Onary et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                History
                : 22 February 2018
                : 18 July 2018
                Funding
                Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)
                Funded by: Richard Gilder Graduate School of American Museum of Natural History (AMNH)
                Funded by: Collection Study Grants
                Funded by: Conselho Nacional de Desenvolvimento Científico e Tecnológico
                Award ID: 309434/2015-7
                Funded by: Fundação de Amparo à Pesquisa do Estado de São Paulo
                Award ID: 2011/14080-0
                Award ID: 2017/00845-1
                Funded by: Venezuelan Education University, Science, and Technology Ministry
                Award ID: IVIC-1096
                Funded by: Instituto de Patrimonio Cultural, Venezuela
                This research was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES); Richard Gilder Graduate School of American Museum of Natural History (AMNH), Collection Study Grants (grant to Silvio Onary), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Proc. n. 309434/2015-7 for Annie S. Hsiou), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Process n. 2011/14080-0 for Annie S. Hsiou and Process n. 2017/00845-1 for Silvio Onary), the Venezuelan Education University, Science, and Technology Ministry (grant to Ascanio D. Rincón IVIC-1096, Venezuelan PaleoMapas); the Petróleos de Venezuela S.A. (PDVSA), and Instituto de Patrimonio Cultural, Venezuela. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Biogeography
                Evolutionary Studies
                Paleontology
                Taxonomy
                Zoology

                boidae,colubroidea,elapidae,micrurus,palaebiogeography,fossils snakes,venezuela,south america,panama isthmus

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