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Molecular Phylogenetics and Biogeography of the Neotropical Skink

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Molecular Phylogenetics and Biogeography of the Neotropical Skink YMPEV 5251 No. of Pages 24, Model 5G 3 August 2015 Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx 1 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev 6 7 3 Molecular phylogenetics and biogeography of the Neotropical skink 4 genus Mabuya Fitzinger (Squamata: Scincidae) with emphasis on q 5 Colombian populations a,⇑ b c a,d,e 8 Nelsy Rocío Pinto-Sánchez , Martha L. Calderón-Espinosa , Aurelien Miralles , Andrew J. Crawford , f 9 Martha Patricia Ramírez-Pinilla 10 a Departament of Biological Sciences, Universidad de los Andes, A.A. 4976 Bogotá, Colombia 11 b Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá, Colombia 12 c Centre d’Ecologie fonctionnelle and Evolutive, Montpellier, France 13 d Smithsonian Tropical Research Institute, Apartado 0843-03092, Panamá, Panama 14 e Círculo Herpetológico de Panamá, Apartado 0824-00122, Panamá, Panama 15 f Escuela de Biología, Universidad Industrial de Santander, Bucaramanga, Colombia 1617 18 article info abstract 3420 21 Article history: Understanding the phylogenetic and geographical history of Neotropical lineages requires having ade- 35 22 Received 18 February 2015 quate geographic and taxonomic sampling across the region. However, Colombia has remained a geo- 36 23 Revised 23 June 2015 graphical gap in many studies of Neotropical diversity. Here we present a study of Neotropical skinks 37 24 Accepted 24 July 2015 of the genus Mabuya, reptiles that are difficult to identify or delimit due to their conservative morphol- 38 25 Available online xxxx ogy. The goal of the present study is to propose phylogenetic and biogeographic hypotheses of Mabuya 39 including samples from the previously under-studied territory of Colombia, and address relevant biogeo- 40 26 Keywords: graphic and taxonomic issues. We combined molecular and morphological data sampled densely by us 41 27 Molecular phylogenetics within Colombia with published data representing broad sampling across the Neotropical realm, includ- 42 28 Species delimitation 29 Ancestral area reconstruction ing DNA sequence data from two mitochondrial (12S rRNA and cytochrome b) and three nuclear genes 43 30 Colombia (Rag2, NGFB and R35). 44 31 Mabuya To evaluate species boundaries we employed a general mixed Yule-coalescent (GMYC) model applied 45 32 Oceanic dispersal to the mitochondrial data set. Our results suggest that the diversity of Mabuya within Colombia is higher 46 33 than previously recognized, and includes lineages from Central America and from eastern and southern 47 South America. The genus appears to have originated in eastern South America in the Early Miocene, with 48 subsequent expansions into Central America and the Caribbean in the Late Miocene, including at least six 49 oceanic dispersal events to Caribbean Islands. 50 We identified at least four new candidate species for Colombia and two species that were not previ- 51 ously reported in Colombia. The populations of northeastern Colombia can be assigned to M. zuliae, while 52 specimens from Orinoquia and the eastern foothills of the Cordillera Oriental of Colombia correspond to 53 M. altamazonica. The validity of seven species of Mabuya sensu lato was not supported due to a combina- 54 tion of three factors: (1) non-monophyly, (2) <75% likelihood bootstrap support and <0.95 Bayesian pos- 55 terior probability, and (3) GMYC analysis collapsing named species. Finally, we suggest that Mabuya sensu 56 stricto may be regarded as a diverse monophyletic genus, widely distributed throughout the Neotropics. 57 Ó 2015 Elsevier Inc. All rights reserved. 58 59 60 61 1. Introduction 62 The Neotropical realm comprises one of the largest reservoirs of 63 q This paper was edited by the Associate Editor J.A. Schulte. terrestrial biodiversity (Maiti and Maiti, 2011; Santos et al., 2009). 64 ⇑ Corresponding author at: Biomics Laboratory, Edif. M1-301, Departamento de Much of the biological diversity in the Neotropics remains unde- 65 Ciencias Biológicas, Universidad de los Andes, Carrera 1E No. 18A – 10, A.A. 4976 Bogotá, Colombia. scribed, with large areas still lacking intensive sampling, especially 66 E-mail addresses: [email protected], [email protected] (N.R. in South America. This sampling gap is particularly evident in 67 Pinto-Sánchez), [email protected] (M.L. Calderón-Espinosa), miralles. Colombia, which remains a ‘black box’ regarding the systematics 68 [email protected] (A. Miralles), [email protected] (A.J. Crawford), [email protected]. of many groups, despite its key geographical position in the 69 co (M.P. Ramírez-Pinilla). http://dx.doi.org/10.1016/j.ympev.2015.07.016 1055-7903/Ó 2015 Elsevier Inc. All rights reserved. Please cite this article in press as: Pinto-Sánchez, N.R., et al. Molecular phylogenetics and biogeography of the Neotropical skink genus Mabuya Fitzinger (Squamata: Scincidae) with emphasis on Colombian populations. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.07.016 YMPEV 5251 No. of Pages 24, Model 5G 3 August 2015 2 N.R. Pinto-Sánchez et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx 70 historical exchange of faunas between North and South America delimitation within this group is somewhat complicated and con- 136 71 (Simpson, 1940; Cody et al., 2010; Pinto-Sánchez et al., 2012). troversial. In the present study, we employ a molecular phyloge- 137 72 Sampling Colombian populations may help to clarify the evolution- netic approach, combining samples from Colombia with 138 73 ary history, systematics, and biogeography of Neotropical lineages. previously published data to investigate species-level relationships 139 74 In this paper we present new morphological and DNA sequence and to infer the timing of diversification and biogeographical pat- 140 75 data from samples of the lizard genus Mabuya obtained from terns within Mabuya. We also used new and published morpholog- 141 76 Colombia and combine this information with previously published ical character data to compare Mabuya species from Colombia. We 142 77 data (Mausfeld, 2000; Carranza and Arnold, 2003; Miralles et al., addressed the following three main objectives: (1) to place popula- 143 78 2006, 2009; Whiting et al., 2006; Miralles and Carranza, 2010; tions of Mabuya from Colombia within a larger phylogenetic 144 79 Hedges and Conn, 2012) in order to provide the most complete framework, (2) to propose and implement a new interpretation 145 80 combined gene tree hypothesis of the genus. of the GYMC method to detect possible taxonomic alpha-error 146 81 Mabuya was first described by Fitzinger (1826) as a circumtrop- (type I error, or false positive concerning an hypothetical species 147 82 ical genus of skinks (Squamata: Scincidae). Subsequently, a com- boundary), and (3) to propose a biogeographic hypothesis of the 148 83 prehensive taxonomic and systematic revision of Mabuya from origin and spread of the genus Mabuya throughout South 149 84 the Americas was completed by Dunn (1935), who recognized nine America, Central America and the Caribbean islands. 150 85 Neotropical species, including M. mabouya, a species originally 86 thought to be widely distributed throughout Central America, 2. Materials and methods 151 87 South America and the Caribbean islands. The genus was subse- 88 quently divided into four genera based on congruence between 2.1. Sampling 152 89 molecular phylogenetic results and the continental distributions 90 of the inferred clades (Mausfeld et al., 2002), restricting Mabuya Molecular data included DNA sequences from 250 specimens of 153 91 to the Neotropics. The populations from the Antilles, Central Mabuya, of which 111 were collected for this study (Fig. 1, 154 92 America, and much of the South American mainland (aside from Appendix A), and 139 were downloaded from GenBank 155 93 Colombia) have been relatively well sampled and well-studied (Appendix A, Supplementary material Fig. S1). Five additional sam- 156 94 (Miralles et al., 2005a, 2006, 2009b; Vrcibradic et al., 2006; ples were included as outgroups: Pleistodon egregious, P. laticeps, 157 95 Whiting et al., 2006; Harvey et al., 2008; Miralles and Carranza, Trachylepis capensis, T. perrotetii and T. vittata. The two former spe- 158 96 2010; Hedges and Conn, 2012). Based on molecular evidence, cies were used as outgroup in Miralles and Carranza (2010) and 159 97 Miralles and Carranza (2010) recognized the existence of at least Hedges and Conn (2012), respectively, and in each case were cho- 160 98 28 species within Mabuya. More recently, Hedges and Conn sen based on a previous phylogenetic study of Scincidae that recov- 161 99 (2012) reviewed the systematics of Mabuya and proposed taxo- ered Mabuya as the sister genus of Trachylepis, which together 162 100 nomic changes involving the splitting of this Neotropical taxon into formed the sister clade to Pleistodon (Carranza and Arnold, 2003). 163 101 16 genera, describing 24 new species, along with a new phyloge- Information on the locality, voucher availability and GenBank 164 102 netic classification for Scincidae, elevating the genus Mabuya accession numbers for all sequences used in this study are pro- 165 103 (sensu Mausfeld et al., 2002) to family level (Mabuyidae). vided in Appendix A. 166 104 Nevertheless, this last point remains controversial (Pyron et al., We examined 13 morphological characters from 111 vouchered 167 105 2013; Lambert et al., 2015). Therefore, for present purposes, the individuals of Mabuya, and preliminarily assigned them to previ- 168 106 name Mabuya is used to refer to the whole Neotropical lineage ously described species when possible. Morphological characters 169 107 sensu Mausfeld et al. (2002). examined here were those routinely used in taxonomy of 170 108 Despite these recent molecular and taxonomic studies of Scincidae: (1) scale counts, (2) presence or absence of homologous 171 109 Mabuya, Colombian populations have not been well studied. The scale fusions, and (3) the variability in color patterns. Definition of 172 110 Colombian territory is geographically highly heterogeneous, with morphological characters followed Avila-Pires (1995).
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