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Out of Asia: Natricine Snakes Support the Cenozoic Beringian Dispersal Hypothesis

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Out of Asia: Natricine Snakes Support the Cenozoic Beringian Dispersal Hypothesis Molecular Phylogenetics and Evolution 63 (2012) 825–833 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Out of Asia: Natricine snakes support the Cenozoic Beringian Dispersal Hypothesis Peng Guo a,b,1, Qin Liu a,1, Yan Xu a,c, Ke Jiang d, Mian Hou e, Li Ding b, R. Alexander Pyron f, ⇑ Frank T. Burbrink g,h, a College of Life Sciences and Food Engineering, Yibin University, Yibin 644007, China b Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China c Chengdu University of Technology, Chengdu 610050, China d State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China e Sichuan Normal University, Chengdu 650068, China f Department of Biological Sciences, The George Washington University, 2023 G St. NW, Washington, DC 20052, USA g Department of Biology, The Graduate School and University Center, The City University of New York, 365 5th Ave., New York, NY 10016, USA h Department of Biology, The College of Staten Island, The City University of New York, 2800 Victory Blvd., Staten Island, NY 10314, USA article info abstract Article history: Based on a combination of six mitochondrial gene fragments (12S RNA, cyt b, ND1, ND2, ND4 and CO1) Received 30 September 2011 and one nuclear gene (c-mos) from 22 genera we infer phylogenetic relationships among natricine snakes Revised 16 February 2012 and examine the date and area of origin of these snakes. Our phylogenetic results indicate: (1) the sub- Accepted 22 February 2012 family Natricinae is strongly supported as monophyletic including a majority of extant genera, and a Available online 12 March 2012 poorly known and previously unassigned species Trachischium monticola, (2) two main clades are inferred within Natricinae, one containing solely taxa from the Old World (OW) and the other comprising taxa Keywords: from a monophyletic New World (NW) group with a small number of OW relatives. Within the first clade, Colubridea the genera Xenochrophis and Amphiesma are apparently not monophyletic. Divergence dating and ances- Amphiesma Trachischium tral area estimation indicate that the natricines originated in tropical Asia during the later Eocene or the Biogeography Oligocene. We recover two major dispersals events out of Asia, the first to Africa in the Oligocene (28 Ma) Phylogenetics and the second to the Western Palearctic and the New World at 27 Ma. This date is consistent with the Intercontinental dispersal dispersal of numerous other OW groups into the NW. Beringia Ó 2012 Elsevier Inc. All rights reserved. 1. Introduction many organisms, though, a basic understanding of their historical biogeography is unclear, and the commonality of various patterns A major goal of historical biogeography is to understand the and processes that have shaped their modern distribution is largely causes for common spatial and temporal patterns across taxa unknown. (Donoghue, 2001; Wiens and Donoghue, 2004; Lomolino et al., Globally distributed groups that are both diverse and ancient 2006). Using phylogenetic inference, divergence dating, and ances- provide a prime opportunity to examine comparative historical tral area estimation, the various biogeographic factors including biogeographic processes related to area of origin and inter-regional vicariance, dispersal, speciation, and extinction can be investigated dispersal. A common distributional pattern discovered among var- in an evolutionary context. Moreover, understanding the historical ious unrelated groups including insects, mammals, snakes, lizards biogeography of a group provides the structure for testing when and plants, is the tendency to have closely related taxa found and how adaptive radiations occur, how communities assemble throughout the Holarctic (Enghoff, 1995; Sanmartin et al., 2001; with respect to regional taxonomic pools, and how species richness Cook et al., 2005; Smith et al., 2005; Burbrink and Lawson, 2007; is controlled by areas of origin, rates of diversification, and niche Brandley et al., 2011). These groups may also include members conservatism (Blackburn and Gaston, 2004; Webb et al., 2006; that have distributions ranging well into the Neotropics or Paleo- Burbrink and Lawson, 2007; Mittelbach et al., 2007; Pyron and tropics. While timing and direction of colonization may be variable Burbrink, 2009a; Wiens et al., 2009; Kozak and Wiens, 2010). For across these groups, particularly given that dispersal across the Holarctic in endotherms was not limited by the onset of glaciers during the Pliocene and Pleistocene (Sanmartin et al., 2001), ⇑ Corresponding author at: Department of Biology, The College of Staten Island, remarkably, a number of taxa exhibit unidirectional dispersal The City University of New York, 2800 Victory Blvd., Staten Island, NY 10314, USA. across the Holarctic within a restricted timeframe. Fax: +1 718 9823961. Specifically, several squamate groups, including skinks (Plesti- E-mail address: [email protected] (F.T. Burbrink). odon), ratsnakes (NW Lampropeltini and OW Elaphe), and pitvipers 1 Equal contribution for this work. 1055-7903/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2012.02.021 826 P. Guo et al. / Molecular Phylogenetics and Evolution 63 (2012) 825–833 (Crotalinae), which are distributed throughout the Holarctic with in conjunction with the other groups likely indicates that entire adjacent tropical ranges, have shown similar patterns of dispersal squamate communities originated in the OW and existed across and diversification (Burbrink and Lawson, 2007; Wüster et al., Beringia and North America during the early Cenozoic. 2008; Pyron and Burbrink, 2009b; Brandley et al., 2011). From these studies, there are two common patterns that may be influ- 2. Methods and materials enced by similar processes: (1) all apparently originated in tropical or subtropical Asia from the late Eocene through the late Oligo- 2.1. Taxon sampling cene, and (2) all display a single unidirectional dispersal through Beringia into the New World (NW) during the late Oligocene or Here we follow Pyron et al.’s (2011) taxonomy for Colubridae. early Miocene, through the mixed mesophytic forests that domi- We obtained sequences for 80 individuals of 72 natricine species nated that area at the time. The collapse of these habitats by the from 21 genera and three outgroup species, for the nuclear pro- mid-Miocene severed connections among the OW and NW com- tein-coding genes oocyte maturation factor Mos (c-mos), the mito- munities, thus yielding disjunct Holarctic patterns seen today (San- chondrial protein-coding genes cytochrome b (cyt b), NADH martin et al., 2001). While distributional patterns and dispersal subunit 4 (ND4), NADH subunit 2 (ND2), cytochrome oxidase sub- within the OW ranges may differ among these groups, the single unit 1 (CO1) and 12S ribosomal RNA (12S RNA). Sequences for 62 area and timing of origin as well as dispersal to the New World individuals of the colubroid species were obtained from GenBank. is consistent in spite of the separate molecular trees each cali- We sequenced c-mos, ND2, ND4 and cyt b for 18 additional indi- brated with different fossils. viduals (15 species, 7 genera). To investigate the monophyly of Another large squamate group with a Holarctic distribution are Natricinae and to clarify the systematic position of Trachischium the watersnakes, Natricinae, which represent a diverse group of monticola, a poorly known putative colubrid, two representatives colubrid snakes composing 210 species in 29 genera found from the other subfamilies of Colubridae (Immantodes cenchoa throughout Asia, Europe, North Africa, Sub-Saharan West Africa, and Coluber constrictor) as well as one homalopsid (Enhydris plum- North America and Central America (The Reptile Database: bea), were chosen as outgroups based on previous studies (Lawson http://www.reptile-database.org). Although many of the species et al., 2005; Pyron et al., 2011). are associated with aquatic habitats and have diets consisting of amphibians or fish, many others are found in dry habitats and may consume invertebrates and mammals (Rossman et al., 1996; 2.2. DNA extraction, amplification and sequencing Gibbons and Dorcas, 2004; Vitt and Caldwell, 2009). Estimates using molecular phylogenies place the origin of the natricines from Total DNA was extracted from 85%-alcohol-preserved livers or other colubrids in the Eocene/Oligocene, indicating they are young muscle tissues by the standard method of proteinase K and phe- enough to have encountered the same environmental conditions as nol/chloroform (Sambrook and Russell, 2002). The entire gene se- the ratsnakes, skinks and crotaline snakes (Pyron and Burbrink, quences for the mitochondrial cytochrome b (cyt b) and NADH 2012). dehydrogenase subunit 2 (ND2), the partial gene sequences of Previous research using morphological and molecular data have NADH dehydrogenase subunit 4 (ND4) and one nuclear gene indicated that the New World natricines form a monophyletic c-mos were amplified by the polymerase chain reaction (PCR) using group (i.e., Thamnophiini) which might indicate that they origi- primers L14910/H16064 (Burbrink et al., 2000), L5238/H5382 (de nated as a single dispersal from OW groups (Rossman and Eberle, Queiroz et al., 2002), ND4/Leu (Arèvalo et al., 1994) and S77/S78 1977; Lawson, 1987; Alfaro and Arnold, 2001; de Queiroz et al., (Lawson
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