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Phylogeography and Species Limits in the Gymnodactylus Darwinii

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Phylogeography and Species Limits in the Gymnodactylus Darwinii Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Soci- ety of London, 2005? 2005 85? 1326 Original Article PHYLOGEOGRAPHY OF THE GYMNODACTYLUS DARWINII COMPLEX (GEKKONIDAE, SQUAMATA) K. C. M. PELLEGRINO Biological Journal of the Linnean Society, 2005, 85, 13–26. With 3 figures ET AL. Phylogeography and species limits in the Gymnodactylus darwinii complex (Gekkonidae, Squamata): genetic structure coincides with river systems in the Brazilian Atlantic Forest KATIA C. M. PELLEGRINO1,2*, MIGUEL T. RODRIGUES3, AARON N. WAITE4, MARIANA MORANDO5, YATIYO Y. YASSUDA2 and JACK W. SITES JR6 1Programa de Pós-Graduação em Ciências Ambientais e Saúde, Universidade Católica de Goiás. Rua 232 no. 128 Setor Universitário, 74.210–000, Goiânia, Goiás, Brazil Departamentos de 2Biologia e 3Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil 4University of Utah School of Medicine, Dean’s Office, 30 North 1900 East, Salt Lake City, Utah, US 84132–2101 5CENPAT U9120ACV Puerto Madryn, Chubut, Argentina 6Department of Integrative Biology and M. L. Bean Life Science Museum, Brigham Young University, Provo, Utah, US 84602 Received 4 December 2003; accepted for publication 28 June 2004 Phylogenetic analyses based on mtDNA cytochrome b were performed in 42 lizards of the Gymnodactylus darwinii complex from three regions within Brazil’s Atlantic Forest. Mainland regions and continental shelf islands in the south-eastern range and mainland areas from the north-east were sampled. The criteria of maximum parsimony (MP), maximum likelihood (ML) and Bayesian methods were explored, with the robustness for nodes assessed by bootstrapping (MP and ML) and posterior probabilities (Bayesian searches). By all methods, three distinctive phy- logroups were recovered: a south-eastern clade (SE) and two clades from northern regions (NE1 and NE2). The pat- tern of genetic structure of the major clades coincided with the presence of river systems in the Atlantic Forest, and based on corrected genetic distances between those clades, divergence times were tentatively estimated using mtDNA rates calibrated for squamate reptiles. The putative role of Atlantic Forest rivers in generating differenti- ation is discussed. We present a hypothesis of species limits for G. darwinii, based on concordant lines of evidence including cytogenetic and mtDNA analyses. Two chromosome races (cytotype A, 2n = 38; and cytotype B, 2n = 40) had distributions concordant with clades SE and NE1 + NE2, respectively. These races are interpreted to be full species on the basis of a number of empirical criteria. © 2005 The Linnean Society of London, Biological Journal of the Lin- nean Society, 2005, 85, 13–26. ADDITIONAL KEYWORDS: Ag-NORs – biogeography – Brazil – divergence times – karyotype – mtDNA – phylogroups – riverine barriers – species boundaries. INTRODUCTION est, G. g. geckoides in the Caatingas of north-eastern Brazil, and G. g. amarali from the central Brazilian The Brazilian lizard genus Gymnodactylus was first Cerrados. Although based on poor geographical cov- revised by Vanzolini (1953) who recognized a single erage of collections, this interpretation was widely species, G. geckoides, with three subspecies: adopted (Peters & Donoso-Barros, 1970). Later, the G. g. darwinii occurring throughout the Atlantic For- availability of larger samples and the absence of morphological intergrades between G. g. darwinii *Corresponding author. E-mail: [email protected] and the open formation races led Vanzolini (1982) to © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 13–26 13 14 K. C. M. PELLEGRINO ET AL. elevate darwinii to full species status. In this same species or evolutionary significant units), but these paper he described a new species, G. guttulatus, from should also receive supporting evidence from other the ‘campos rupestres’ of state of Minas Gerais, a sets of characters (Avise & Ball, 1990; Moritz, 1994; higher elevation rocky open habitat in the ‘Serra do Wiens & Penkrot, 2002), as recently demonstrated in a Espinhaço’, a large mountain range extending from phylogeographical study of Atlantic Forest pitvipers of the state of Minas Gerais to the state of Bahia. Pat- the genus Bothrops (Puorto et al., 2001). terns of geographical variation within, and phyloge- In addition to molecular data, chromosome data are netic relationships among these taxa, remain important in this case for two reasons. First, karyo- unresolved. types in geckos exhibit a high level of variation both in Geckos of the genus Gymnodactylus are small diploid number, which varies from 2n = 16 (Schmid (maximum snout–vent length = 48 mm), mostly noc- et al., 1994) to 2n = 48 (Ota et al., 1992), with most turnal, terrestrial, sit and wait, cryptically coloured karyotypes characterized by a series of acrocentrics lizards (Vanzolini, 1953, 1982). Additional natural gradually decreasing in size. Surprisingly, only a few history information is restricted largely to karyotypes have been reported for Neotropical species, G. g. geckoides (Vitt, 1995), which is insectivorous and which represent about 23% of the total number of rec- oviposits one egg. G. darwini occurs mostly in lowland ognized species. Until now, few data have been pub- forests near sea level, but it is occasionally found at lished on karyotypes of Gymnodactylus; intraspecific forest edges. variation due to the occurrence of a Robertsonian poly- At the time of the first revision, the known geo- morphism and supernumerary chromosomes has been graphical distribution of G. darwinii was restricted to detected in one well-sampled population of the Atlantic forests extending from the northern state G. g. amarali (2n = 38–41) from Serra da Mesa, on the of Bahia to the northern coastal regions of the south- central Brazilian Cerrados (Pellegrino, 1998). This eastern state of São Paulo (Vanzolini, 1953). Its range pattern suggests that additional chromosomal varia- has recently been expanded farther north into the tion may be present in these geckos. Second, issues of state of Rio Grande do Norte (Freire, 1998), and to sev- species boundaries remain unresolved in Gymnodac- eral continental-shelf islands off the coast of São tylus, and chromosomes may prove to be useful inde- Paulo. pendent characters to corroborate any well-supported Freire’s (1998) comprehensive study included clades recovered from mtDNA analyses. almost all specimens of G. darwinii in Brazilian col- The purposes of the present study were to: (1) lections from throughout the known range of the spe- describe patterns of genetic divergence and phylogeo- cies, and revealed conspicuous morphological graphical structure of mtDNA haplotypes across the differentiation among populations along the coast. geographical range of G. darwinii; (2) formulate a pre- However, this variation was clinal in all characters liminary biogeographical hypothesis about the Atlan- analysed, similar to a pattern previously described in tic Forest region, which is characterized by high the lizard Tropidurus torquatus, which is distributed species diversity and endemism, and is recognized glo- throughout the same general area (Rodrigues, 1987). bally for its conservation significance (Mittermeier This shared pattern of morphological variation sug- et al., 1999; Myers et al., 2000); (3) present a hypoth- gests that both species may have been influenced by esis of species limits in this group, based on concor- the same historical processes operating along broad dant lines of evidence. environmental gradients, but a precise hypothesis based on independent evidence to account for these patterns of morphological differentiation is lacking. A MATERIAL AND METHODS phylogeographical study based on molecular data (Avise, 2000) could provide sufficient resolution of TAXON SAMPLING AND OUTGROUPS population structure to formulate a more robust Forty-two specimens of G. darwinii were used to infer hypothesis for the evolution of this genus. a molecular phylogeny, and sampling included speci- Phylogeographical studies using Atlantic Forest mens from three major geographical areas across most taxa are relatively scarce, and most available data of the range within the Atlantic Forest of eastern Bra- come from studies of small-bodied mammals (e.g. Mus- zil. The south-eastern samples included specimens trangi & Patton, 1997; Lara & Patton, 2000; Costa, from the mainland regions of São Paulo and Espírito 2003). An exception is a recent study conducted on Santo, and some islands off the coast of São Paulo. four codistributed species of amphibian from Atlantic Further north, populations from the states of Bahia, Forest remnants in north-eastern Brazil (Carnaval, Alagoas and Rio Grande do Norte were also sampled 2002). Additionally, the establishment of DNA phylog- (Table 1). The congeneric G. geckoides, and two other enies is useful for suggesting hypotheses about the more distantly related genera (Hemidactylus and boundaries of genetically divergent groups (e.g. cryptic Phyllopezus), were used as outgroups. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 13–26 PHYLOGEOGRAPHY OF THE GYMNODACTYLUS DARWINII COMPLEX 15 Table 1. Samples of Gymnodactylus darwinii and outgroup taxa used in this study with respective field numbers and localities Specimen Field number Locality Coordinates Island South-east Brazil (SE) LG 872, 871, 883, 880 Ilhote do Sul, Ubatuba, SP (A) ᭹ 23∞34¢S, 45∞05¢W LG 870, *882 Ilhota
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