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Molecular Phylogenetics of Sub-Saharan African Natricine Snakes, and the Biogeographic Origins of the Seychelles Endemic Lycognathophis Seychellensis

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Molecular Phylogenetics of Sub-Saharan African Natricine Snakes, and the Biogeographic Origins of the Seychelles Endemic Lycognathophis Seychellensis Molecular Phylogenetics and Evolution 161 (2021) 107152 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular phylogenetics of sub-Saharan African natricine snakes, and the biogeographic origins of the Seychelles endemic Lycognathophis seychellensis V. Deepak a,*, Simon T. Maddock a,b,c, Rhiannon Williams a,d, Zoltan´ T. Nagy e, Werner Conradie f,g, Sara Rocha h, D. James Harris i, Ana Perera i, Vaclav´ Gvoˇzdík j,k, Thomas M. Doherty-Bone a,l, Rachunliu G. Kamei a, Michele Menegon m,n, Jim Labisko c,o,p, Charles Morel q, Natalie Cooper a, Julia J. Day p, David J. Gower a,c a Department of Life Sciences, Natural History Museum, London SW7 5BD, UK b School of Biology, Chemistry and Forensic Science, Wolverhampton University, WV1 1LY, UK c Island Biodiversity and Conservation Centre, University of Seychelles, Mah´e, Seychelles d NRA Environmental Consultants, Cairns, Queensland 4870, Australia e Independent Researcher, Berlin, Germany f Port Elizabeth Museum (Bayworld), Humewood, Port Elizabeth 6013, South Africa g Department of Nature Conservation Management, Natural Resource Science and Management Cluster, Faculty of Science, George Campus, Nelson Mandela University, George, South Africa h Biomedical Research Center (CINBIO), University of Vigo & Galicia Sur Health Institute, Vigo, Spain i CIBIO-InBIO, Centro de Investigaçao~ em Biodiversidade e Recursos Gen´eticos, University of Porto, 4485-661 Vairao,~ Portugal j Institute of Vertebrate Biology of the Czech Academy of Sciences, Brno, Czech Republic k National Museum, Department of Zoology, Prague, Czech Republic l Conservation Programs, Royal Zoological Society of Scotland, Edinburgh EH12 6TL, UK m Division of Biology & Conservation Ecology, Manchester Metropolitan University, UK n PAMS Foundation, P.O. Box 16556, Arusha, Tanzania o Durrell Institute of Conservation and Ecology, School of Anthropology and Conservation, University of Kent, Canterbury CT2 7NR, UK p Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK q Natural History Museum, Victoria, Mah´e, Seychelles ARTICLE INFO ABSTRACT Keywords: Phylogenetic relationships of sub-Saharan African natricine snakes are understudied and poorly understood, Biogeography which in turn has precluded analyses of the historical biogeography of the Seychelles endemic Lycognathophis Gondwana seychellensis. We inferred the phylogenetic relationships of Seychelles and mainland sub-Saharan natricines by Natricinae analysing a multilocus DNA sequence dataset for three mitochondrial (mt) and four nuclear (nu) genes. The Natricidae mainland sub-Saharan natricines and L. seychellensis comprise a well-supported clade. Two maximally supported Overseas dispersal Systematics sets of relationships within this clade are (Limnophis,Natriciteres) and (Afronatrix,(Hydraethiops,Helophis)). The relationships of L. seychellensis with respect to these two lineages are not clearly resolved by analysing concat­ enated mt and nu data. Analysed separately, nu data best support a sister relationship of L. seychellensis with (Afronatrix,(Hydraethiops,Helophis)) and mt data best support a sister relationship with all mainland sub-Saharan natricines. Methods designed to cope with incomplete lineage sorting strongly favour the former hypothesis. Genetic variation among up to 33 L. seychellensis from fiveSeychelles islands is low. Fossil calibrated divergence time estimates support an overseas dispersal of the L. seychellensis lineage to the Seychelles from mainland Africa ca. 43–25 million years before present (Ma), rather than this taxon being a Gondwanan relic. 1. Introduction both a remote, oceanic setting and continental origins as a fragment of Gondwana. Thus, its extant biota is a mosaic of ancient, relictual line­ The Seychelles archipelago is an unusual island system in that it has ages and more recent overwater arrivals (Ali, 2017). This provides an * Corresponding author. E-mail address: [email protected] (V. Deepak). https://doi.org/10.1016/j.ympev.2021.107152 Received 14 April 2020; Received in revised form 8 March 2021; Accepted 8 March 2021 Available online 17 March 2021 1055-7903/© 2021 Elsevier Inc. All rights reserved. V. Deepak et al. Molecular Phylogenetics and Evolution 161 (2021) 107152 attractive system for studying evolutionary processes, though exploiting vertebral and hemipenial anatomy, and indicated a close relationship this system for evolutionary research depends on improved knowledge with (and possible membership of) a mainland sub-Saharan African of whether each resident lineage is ancient or relatively recent, as well as natricine radiation. However, those studies sampled only three of the six the status of populations on multiple Seychelles islands. Recently, some extant sub-Saharan African natricine genera (see Fig. 1 for distribution of this information has been generated for several lineages of Seychelles map) and only four of the 13 currently recognised species. Additionally, amphibians and reptiles (e.g., Brandley et al., 2005; Rocha et al., 2010, those previous studies disagreed as to whether L. seychellensis is more 2011, 2016a, b; Tolley et al., 2013; Maddock et al., 2014), but not yet for closely related to Afronatrix (Dubey et al., 2012; Pyron et al., 2013; any of the native snakes (see Williams et al., 2020 for the latest assess­ Zaher et al., 2019) or to Natriciteres (Guo et al., 2012). As far as we are ment of the non-native status of Seychelles Indotyphlops braminus). aware, there are no phylogenetic hypotheses that include all mainland The snake Lycognathophis seychellensis (Schlegel, 1837) is endemic to sub-Saharan African natricine genera such that, beyond the close the granitic islands of the Seychelles (Nussbaum, 1984). Several aspects inferred relationship of the only two previously sampled genera in of the systematics and historical biogeography of L. seychellensis remain molecular phylogenetic studies (Afronatrix and Natriciteres), there ap­ unclear. DNA sequence data (for two partial nuclear genes, cmos and pears to have been no previous consideration as to whether the main­ rag2) have been published for only one or two individuals of land sub-Saharan African natricines constitute a single radiation and L. seychellensis (Vidal et al., 2008). This species has been recorded from what their biogeographic origins might be. Finally, there are no pub­ six of the inner, granitic Seychelles islands (Fig. 1; Gerlach and Ineich, lished estimates of the age of the split between L. seychellensis and its 2006) and exhibits notable colour polymorphism (Nussbaum, 1984). closest extant relative. Having this temporal framework would allow a Other Seychelles reptile species have been found to display high levels of test of the hypothesis that the L. seychellensis lineage arrived in the variation within and among islands, with potential implications for Seychelles via overseas dispersal rather than being a Gondwanan relic. taxonomy and conservation management (Rocha et al., 2011, 2013, Here we present analyses of mitochondrial and nuclear DNA 2016; Valente et al., 2014; Harris et al., 2015). Thus, an inspection of sequence data in order to test the following hypotheses: (1) mainland possibly substantial intraspecific genetic variation in L. seychellensis is sub-Saharan African natricines are monophyletic, (2) L. seychellensis lies warranted. within the sub-Saharan African radiation, (3) intraspecific genetic Currently there are 252 recognised species in the colubrid subfamily variation within L. seychellensis is low across multiple Seychelles islands, Natricinae, with the majority of this diversity found in Asia (183 species and (4) the L. seychellensis lineage arrived in the Seychelles via oceanic ca. 72%), only 13 species (ca. 5%) in mainland sub-Saharan Africa, and dispersal rather than being an ancient, Gondwanan relic. none in Madagascar (Uetz et al., 2020). Previous molecular phylogenetic analyses (Vidal et al., 2008; Dubey et al., 2012; Guo et al., 2012; Pyron et al., 2013; Zaher et al., 2019) supported the natricine colubrid (natricid according to some classifications: e.g., Zaher et al., 2019) identity of L. seychellensis proposed by Dowling (1990) based on Fig. 1. Global distribution of sub-Saharan African (including Seychelles) natricine genera based on data from GBIF, Nagy et al. (2014), Chippaux & Jackson (2019), Conradie et al. (2020) and specimen vouchers from Port Elizabeth Museum (PEM). These genera comprise 14 currently recognised extant species as follows: Afronatrix (1 species), Helophis (1), Hydraethiops (2), Limnophis (3), Lycognathophis (1), and Natriciteres (6). Occurrence data for the one Seychelles and six of the mainland sub-Saharan African natricine genera (all except Helophis) were downloaded from the GBIF database (GBIF, 2019). Distribution data for Helophis were taken from Nagy et al. (2014). Spatial data were mapped using ArcGIS v. 10.5. (ESRI, The Redlands, CA). Sampling localities in mainland sub-Saharan Africa are labelled with numbers corresponding to those in Table 1. Precise locality information for L. seychellensis is presented in Table 1. 2 V. Deepak et al. Molecular Phylogenetics and Evolution 161 (2021) 107152 2. Materials and methods analysis using MrBayes v. 3.2.6 on XSEDE (Ronquist et al., 2012). Par­ titionFinder2 (Lanfear et al., 2016) was used to determine best-fit gene 2.1. DNA sequence data generation and alignment and codon partitioning
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