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Anolis Chrysolepis Duméril and Bibron, 1837 (Squamata: Iguanidae), Revisited: Molecular Phylogeny and Taxonomy of the Anolis Chrysolepis Species Group

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Anolis Chrysolepis Duméril and Bibron, 1837 (Squamata: Iguanidae), Revisited: Molecular Phylogeny and Taxonomy of the Anolis Chrysolepis Species Group Marquette University e-Publications@Marquette Biological Sciences Faculty Research and Publications Biological Sciences, Department of 2011 Anolis chrysolepis Duméril and Bibron, 1837 (Squamata: Iguanidae), Revisited: Molecular Phylogeny and Taxonomy of the Anolis chrysolepis Species Group Annelise B. D'Angiolella Museu Paraense Enilio Goeldi Tony Gamble Marquette University, [email protected] Teresa C. S. Avila-Pires Museu Paraense Enilio Goeldi Guarino R. Colli Universidade de Brasília Brice P. Noonan University of Mississippi See next page for additional authors Follow this and additional works at: https://epublications.marquette.edu/bio_fac Part of the Biology Commons Recommended Citation D'Angiolella, Annelise B.; Gamble, Tony; Avila-Pires, Teresa C. S.; Colli, Guarino R.; Noonan, Brice P.; and Vitt, Laurie J., "Anolis chrysolepis Duméril and Bibron, 1837 (Squamata: Iguanidae), Revisited: Molecular Phylogeny and Taxonomy of the Anolis chrysolepis Species Group" (2011). Biological Sciences Faculty Research and Publications. 788. https://epublications.marquette.edu/bio_fac/788 Authors Annelise B. D'Angiolella, Tony Gamble, Teresa C. S. Avila-Pires, Guarino R. Colli, Brice P. Noonan, and Laurie J. Vitt This article is available at e-Publications@Marquette: https://epublications.marquette.edu/bio_fac/788 ANOLIS CHRYSOLEPIS DUME´ RIL AND BIBRON, 1837 (SQUAMATA: IGUANIDAE), REVISITED: MOLECULAR PHYLOGENY AND TAXONOMY OF THE ANOLIS CHRYSOLEPIS SPECIES GROUP ANNELISE B. D’ANGIOLELLA,1 TONY GAMBLE,2 TERESA C. S. AVILA-PIRES,3 GUARINO R. COLLI,4 BRICE P. NOONAN,5 AND LAURIE J. VITT6 ABSTRACT. The Anolis chrysolepis species group is cada subespe´cie de A. chrysolepis ao status de espe´cie. distributed across the entire Amazon basin and Fornecemos novas diagnoses morfolo´gicas e novos currently consists of A. bombiceps and five subspecies dados de distribuic,a˜o para cada espe´cie. of A. chrysolepis. These lizards are characterized by moderate size, relatively narrow digital pads, and a Palavras-chave: Anolis, Amazoˆnia, Iguanidae, filo- small dewlap that does not reach the axilla. We used genia molecular, taxonomia the mitochondrial gene ND2 to estimate phylogenetic relationships among putative subspecies of A. chryso- INTRODUCTION lepis and taxa previously hypothesized to be their close relatives. We also assessed the congruence between The Pleistocene Refuge Hypothesis pro- molecular and morphological datasets to evaluate the posed almost simultaneously by Haffer taxonomic status of group members. On the basis of the (1969) and Vanzolini and Williams (1970) two datasets, we present a new taxonomy, elevating each putative subspecies of A. chrysolepis to species posits that patches of lowland tropical forest status. We provide new morphological diagnoses and that existed during dry periods in the new distributional data for each species. Pleistocene served as core areas for speci- Key words: Anolis,Amazon,Iguanidae,mole- ation in birds and in the lizard complex cular phylogeny, taxonomy Anolis chrysolepis, respectively. Although the Pleistocene Refuge Hypothesis has been falsified for members of the A. chrysolepis RESUMO. O grupo de espe´cies Anolis chrysolepis atualmente consiste em A. bombiceps e cinco sub- species group because diversification oc- espe´cies de A. chrysolepis, ocupando toda a Bacia curred much earlier (15 mya) than the Amazoˆnica. Esses lagartos sa˜o caracterizados por Pleistocene (Glor et al., 2001), relationships tamanho moderado, lamelas digitais relativamente among all members of the group have not estreitas e um papo extensı´vel que na˜o chega a`s axilas. been worked out and related taxa (e.g., A. No´s utilizamos o gene mitocondrial ND2 para estimar as relac,o˜es filogene´ticas entre as subespe´cies de A. meridionalis and A. bombiceps) have not chrysolepis e ta´xons previamente considerados par- been properly placed with reference to the entes pro´ximos. No´s tambe´m determinamos a con- A. chrysolepis complex, and current names grueˆncia entre conjuntos de dados morfolo´gicos e do not accurately reflect the evolutionary moleculares, para avaliar o status taxonoˆmico dos history of the group (Glor et al., 2001; membros desse grupo. Com base nos dois conjuntos de dados, apresentamos uma nova taxonomia, elevando Nicholson et al., 2005). Because the A. chrysolepis species group has been and 1 Programa de Po´s-Graduac,a˜o em Zoologia UFPA- continues to be a model for evolutionary MPEG, Bele´m, PA, Brazil. Author for correspondence (Nicholson et al., 2006, 2007; Schaad and ([email protected]). Poe, 2010) and ecological (Vitt and Zani, 2 University of Minnesota, Minneapolis, Minnesota. 1996; Vitt et al., 2001, 2008) studies, it is 3 Museu Paraense Emı´lio Goeldi, Bele´m, PA, Brazil. 4 Universidade de Brası´lia, Brası´lia, DF, Brazil. critical that their relationships be properly 5 The University of Mississippi, University, Mississippi. understood. Here we present a phylogenetic 6 University of Oklahoma, Norman, Oklahoma. hypothesis for the A. chrysolepis species Bull. Mus. Comp. Zool., 160(2): 35–63, December, 2011 35 36 Bulletin of the Museum of Comparative Zoology, Vol. 160, No. 2 group using a much larger set of samples species of A. chrysolepis and a distinct than was available previously and provide species, A. bombiceps. Vanzolini and Wil- species names for taxa that can be identified liams (1970: 13) believed the level of as independent evolutionary lineages. Fol- differentiation between the subspecies were lowing de Queiroz (2007), we consider ‘‘closest to species difference, and indica- independent evolutionary lineages, here tive, perhaps, of past and future potential recognized on the basis of gene trees, species formation.’’ Anolis chrysolepis was analogous to species. Results of this study later examined by Avila-Pires (1995) under should be directly applicable to phylogeo- the name A. nitens. She described another graphic and phyloecological studies of the subspecies, A. n. tandai, and observed that A. chrysolepis species group. most specimens occurring in areas of The A. chrysolepis group comprises two intergradation according to Vanzolini and species: A. chrysolepis Dume´ril and Bibron, Williams (1970) could be assigned to one of 1837, and A. bombiceps Cope, 1876. Anolis the recognized subspecies. chrysolepis is currently composed of five Very little subsequent taxonomic research subspecies: A. chrysolepis chrysolepis, in has been conducted on the species of the A. eastern Guiana (Brazil, French Guiana, chrysolepis group. One molecular phyloge- Suriname, and southern Guyana); A. chry- netic study included three of the described solepis planiceps Troschel, 1848, in western A. chrysolepis subspecies and found they Guiana (Brazil, Suriname, northwestern formed a weakly supported clade (Glor et Guyana, Venezuela, and Trinidad); A. chry- al., 2001). Glor et al. (2001: 2664) concluded solepis scypheus Cope, 1864, in western that, ‘‘further study of geographical genetic Amazonia (Colombia, Ecuador, Peru, and interactions among these subspecies proba- northwestern Brazil); A. chrysolepis tandai bly will reveal that they are distinct species.’’ Avila-Pires, 1995, in southwestern Amazo- Additional molecular phylogenetic research, nia (Brazil and Peru); and A. chrysolepis with broad outgroup sampling, recovered brasiliensis Vanzolini and Williams, 1970, in a well-supported clade consisting of A. Brazil, from Maranha˜o and enclaves of open onca, A. annectans, A. lineatus, A. auratus, vegetation in southern Para´ south to Sa˜o A. meridionalis, and A. chrysolepis,al- Paulo (Vanzolini and Williams, 1970; Avila- though A. chrysolepis was represented by Pires, 1995; Icochea et al., 2001; Santos- just a single individual from Roraima, Brazil Jr et al., 2007). Anolis bombiceps occurs in (Nicholson et al., 2005). Members of this western Amazonia, in Peru, Colombia, and clade were included in another phylogenetic Brazil, at least in partial sympatry with A. c. analysis (Nicholson et al., 2006), using the scypheus and perhaps also with A. c. tandai same three A. chrysolepis subspecies of (Avila-Pires, 1995). Members of the A. Glor et al. (2001), which recovered a chrysolepis group are characterized by their paraphyletic A. chrysolepis. Nicholson et moderate size (up to 83 mm snout–vent al. (2006) found that A. c. tandai was more length); short heads; supraorbital semicir- closely related to A. meridionalis and the A. cles usually forming a pronounced ridge; onca + A. annectans clade, whereas A. c. relatively narrow digital pads, with distal scypheus and A. c. planiceps formed a clade lamellae under phalanx ii forming a slightly that was the sister group to the remaining prominent border; a dewlap that does not species + A. auratus. Like Glor et al. (2001), reach the axilla and is present in both sexes Nicholson et al. (2006) stressed the need for (but smaller in females); and keeled, imbri- additional research into the systematics of A. cate ventral scales that are distinctly larger chrysolepis and the possible existence of than dorsals. cryptic species. Anolis bombiceps has not The A. chrysolepis species group was been included in any molecular studies so far. examined morphologically by Vanzolini and The name A. chrysolepis has a long and Williams (1970), who recognized four sub- confusing history, with both A. nitens and A. ANOLIS CHRYSOLEPIS SPECIES GROUP N D’Angiolella et al. 37 chrysolepis considered valid names for the using SEQUENCHER ver. 4.2 (Gene species (Hoogmoed, 1973; Avila-Pires,
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