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Corallus Spp.) ⇑ Timothy J Molecular Phylogenetics and Evolution 66 (2013) 953–959 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular systematics and historical biogeography of tree boas (Corallus spp.) ⇑ Timothy J. Colston a,b, , Felipe G. Grazziotin c, Donald B. Shepard d, Laurie J. Vitt a,b, Guarino R. Colli e, Robert W. Henderson f, S. Blair Hedges g, Sandro Bonatto h, Hussam Zaher c, Brice P. Noonan i, Frank T. Burbrink j a Zoology Department, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019, USA b Sam Noble Oklahoma Museum of Natural History and Zoology Department, University of Oklahoma, 2401 Chautauqua Avenue, Norman, OK 73072, USA c Museu de Zoologia, Universidade de São Paulo, Caixa Postal 42.494, 04218-970, São Paulo, SP, Brazil d Bell Museum of Natural History and Department of Fisheries, Wildlife, and Conservation Biology, University of Minnesota, Saint Paul, MN 55108, USA e Departamento de Zoologia, Universidade de Brasília 70910-900 Brasília, DF, Brazil f Milwaukee Public Museum, 800 W. Wells St. Milwaukee, WI 53233, USA g Department of Biology, 208 Mueller Laboratory, Pennsylvania State University, University Park, PA 16802-5301, USA h Faculdade de Biociências, Pontifícia Universidade Católica do Rio Grande do Sul, Av Ipiranga 6681, 90619-900 Porto Alegre, RS, Brazil i Department of Biology, University of Mississippi, Box 1848, University, MS 38677, USA j Department of Biology, 6S-143, The College of Staten Island, 2800 Victory Blvd, Staten Island, NY 10314, USA article info abstract Article history: Inferring the evolutionary and biogeographic history of taxa occurring in a particular region is one way to Received 7 July 2012 determine the processes by which the biodiversity of that region originated. Tree boas of the genus Cor- Revised 19 November 2012 allus are an ancient clade and occur throughout Central and South America and the Lesser Antilles, mak- Accepted 30 November 2012 ing it an excellent group for investigating Neotropical biogeography. Using sequenced portions of two Available online 20 December 2012 mitochondrial and three nuclear loci for individuals of all recognized species of Corallus, we infer phylo- genetic relationships, present the first molecular analysis of the phylogenetic placement of the enigmatic Keywords: C. cropanii, develop a time-calibrated phylogeny, and explore the biogeographic history of the genus. We Neotropical diversity found that Corallus diversified within mainland South America, via over-water dispersals to the Lesser Bayesian analysis BEAST Antilles and Central America, and via the traditionally recognized Panamanian land bridge. Divergence Divergence dating time estimates reject the South American Caribbean-Track as a general biogeographic model for Corallus Ancestral area reconstruction and implicate a role for events during the Oligocene and Miocene in diversification such as marine incur- sions and the uplift of the Andes. Our findings also suggest that recognition of the island endemic species, C. grenadensis and C. cookii, is questionable as they are nested within the widely distributed species, C. hortulanus. Our results highlight the importance of using widespread taxa when forming and testing bio- geographic hypotheses in complex regions and further illustrate the difficulty of forming broadly appli- cable hypotheses regarding patterns of diversification in the Neotropical region. Ó 2012 Elsevier Inc. All rights reserved. 1. Introduction taxa (Castoe et al., 2009; Daza et al., 2009). Extreme geological and environmental complexity as well as areas of high richness, Inferring the evolutionary history of a group in a particular high endemism, and multiple major biogeographic provinces region is one way to elucidate the processes by which the fauna (Udvardy, 1975) make the Neotropical region particularly interest- of that region originated (Crisp et al., 2011; Riddle, 2009). In ing to biogeographers (Beheregaray, 2008; Graham, 1997). particular, comparing the evolutionary histories of multiple codis- However, complex interactions among multiple factors have also tributed lineages allows one to formulate general biogeographic precluded a consensus regarding the ecological and historical hypotheses that can be further tested and refined with additional processes that have generated observed patterns of diversity. Although several broad biogeographic hypotheses have been pro- ⇑ Corresponding author. Address: Department of Biology, University of Missis- posed, the evolutionary history of most Neotropical taxa remains sippi, P.O. Box 1848 University, MS 38677, USA. poorly understood and thus, the generality of these hypotheses E-mail addresses: [email protected] (T.J. Colston), [email protected] remains untested in many clades (Beheregaray, 2008). (F.G. Grazziotin), [email protected] (D.B. Shepard), [email protected] (L.J. Vitt), Multiple historical events have played a role in biological diver- [email protected] (G.R. Colli), [email protected] (R.W. Henderson), [email protected] sification in South America, but four major ones are of primary (S. Blair Hedges), [email protected] (S. Bonatto), [email protected] (H. Zaher), [email protected] (B.P. Noonan), [email protected] (F.T. Burbrink). importance and have received the most attention (Rull, 2011). 1055-7903/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2012.11.027 954 T.J. Colston et al. / Molecular Phylogenetics and Evolution 66 (2013) 953–959 First, marine incursions from the Pacific and Caribbean covered which could be used to test both spatial and temporal components large tracts of Amazonia with huge lakes and swamps during the of biogeographic hypotheses, is not presently available. Tertiary, isolating lineages in upland areas such as the Brazilian Here, we use DNA sequence data from two mitochondrial and and Guianan shields (Haffer, 2008; Webb, 1995). Second, the An- three nuclear genes of all species of Corallus to infer their phyloge- dean uplift during the Miocene created a major continental barrier netic relationships. We then reconstruct the biogeographic history to dispersal while also providing new montane habitat and oppor- of the group by integrating divergence times of species, as esti- tunities for colonization and diversification (Haffer, 2008; Rull, mated by relaxed-clock divergence dating methods, with ancestral 2011). Third, contraction of forests during Pleistocene climatic area analyses that account for dispersal and extinction to infer the fluctuations is thought to have isolated populations of forest- biogeographic history of the group. Finally, we use our results to adapted taxa in refugia, which subsequently led to speciation (Haf- evaluate the potential roles of major Neotropical biogeographic fer, 1969, 2008; Vanzolini, 1970). Finally, closure of the Panama- events (e.g., marine incursions, Andean uplift, Pleistocene refugia, nian Isthmus provided a dispersal route between North and and Panamanian Isthmus) in the diversification of Corallus. South America which has been coined the ‘‘Great American Biotic Interchange-GABI’’ (Lessa et al., 1997; Simpson, 1940). The GABI was first recognized by Wallace (1876) and has since been identi- 2. Materials and methods fied as important in structuring biogeographic patterns in multiple taxa including birds, mammals, and invertebrates (Johnson and 2.1. Taxon sampling Weckstein, 2011; Lessa et al., 1997; Zeh et al., 2003); however divergences in many squamate taxa that span both sides of the We used 20 specimens of Corallus including all species from 18 Panamanian Isthmus predate its formation (Castoe et al., 2009; localities across the distribution of the genus (Fig. 1, S1). We did Daza et al., 2009, 2010). Among these events, the formation of not have access to tissue samples from specimens positively Pleistocene refugia has received the most attention and debate, identified as C. batesii and available sequence data were restricted whereas the closure of the Panamanian Isthmus is the only event to cytochrome-b (cyt-b) from two individuals. Our Ecuadorian for which the timing is precisely dated (Rull, 2011). sample of C. annulatus could not be definitively classified as either The genus Corallus is a member of the subfamily Boinae, a group C. annulatus or C. blombergi, and as there is no question whether with clear Gondwanan origins (Noonan and Chippindale, 2006). these species are sister and we are not addressing the validity of Currently, eight species are recognized based on morphology or in C. blombergi, we treat C. annulatus herein as including both C. some cases morphology and molecular data: C. annulatus (sensu annulatus and C. blombergi. Tissue samples were collected by us, lato, but see taxon sampling in Materials and Methods), C. batesii, obtained through museum loans, or donated by private individuals C. caninus, C. cookii, C. cropanii, C. grenadensis, C. hortulanus, and C. from personal tissue collections. For phylogenetic analyses, we ruschenbergerii (Henderson et al., 2009). Four species are endemic included sequences from GenBank for additional boid taxa and to South America, including the rare and enigmatic C. cropanii, Cylindrophis for use as outgroups. These outgroup taxa were also which is only known from four specimens (three existing) and included in divergence dating analysis in order to provide external whose taxonomic placement has been of great interest (Kluge, nodes on which we could place prior
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