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(Sphaerodactylinae, Gekkota) Revisited: a Molecular Phylogenetic Perspective

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(Sphaerodactylinae, Gekkota) Revisited: a Molecular Phylogenetic Perspective Molecular Phylogenetics and Evolution 49 (2008) 92–101 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev The genus Coleodactylus (Sphaerodactylinae, Gekkota) revisited: A molecular phylogenetic perspective Silvia Rodrigues Geurgas a,*, Miguel Trefaut Rodrigues a, Craig Moritz b a Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo, SP, Brazil b Museum of Vertebrate Zoology, 3101 Valley Life Sciences Building #3160, UC Berkeley, CA 94720, USA article info abstract Article history: Nucleotide sequence data from a mitochondrial gene (16S) and two nuclear genes (c-mos, RAG-1) were Received 31 January 2008 used to evaluate the monophyly of the genus Coleodactylus, to provide the first phylogenetic hypothesis Revised 28 May 2008 of relationships among its species in a cladistic framework, and to estimate the relative timing of species Accepted 30 May 2008 divergences. Maximum Parsimony, Maximum Likelihood and Bayesian analyses of the combined data Available online 7 June 2008 sets retrieved Coleodactylus as a monophyletic genus, although weakly supported. Species were recovered as two genetically and morphological distinct clades, with C. amazonicus populations forming the sister Keywords: taxon to the meridionalis group (C. brachystoma, C. meridionalis, C. natalensis, and C. septentrionalis). Within Coleodactylus this group, C. septentrionalis was placed as the sister taxon to a clade comprising the rest of the species, Sphaerodactylinae Phylogeny C. meridionalis was recovered as the sister species to C. brachystoma, and C. natalensis was found nested Pleistocene refuges within C. meridionalis. Divergence time estimates based on penalized likelihood and Bayesian dating 16S methods do not support the previous hypothesis based on the Quaternary rain forest fragmentation RAG-1 model proposed to explain the diversification of the genus. The basal cladogenic event between major c-mos lineages of Coleodactylus was estimated to have occurred in the late Cretaceous (72.6 ± 1.77 Mya), approximately at the same point in time than the other genera of Sphaerodactylinae diverged from each other. Within the meridionalis group, the split between C. septentrionalis and C. brachystoma + C. meridio- nalis was placed in the Eocene (46.4 ± 4.22 Mya), and the divergence between C. brachystoma and C. meridionalis was estimated to have occurred in the Oligocene (29.3 ± 4.33 Mya). Most intraspecific cladogenesis occurred through Miocene to Pliocene, and only for two conspecific samples and for C. natalensis could a Quaternary differentiation be assumed (1.9 ± 1.3 Mya). Ó 2008 Elsevier Inc. All rights reserved. 1. Introduction tral Amazonian Forest, and through southern Venezuela to south- ern Guyana (Ávila-Pires, 1995); C. meridionalis is associated The New World Sphaerodactylinae includes five genera of diur- mainly with the Atlantic Forest, but also occurs in fragments of for- nal geckos found in forested areas in West Indies, Central and ests in Caatinga and Cerrado (Vanzolini, 1980; Freire, 1999; Colli northern South America: Coleodactylus, Gonatodes, Lepidobepharis, et al., 2002), and C. brachystoma occurs in forested enclaves in Pseudogonatodes, and Sphaerodactylus (Underwood, 1954; Kluge, the Cerrado of Central Brazil (Vanzolini, 1968a,b, 1970; Colli 1967, 1987, 1995; Gamble et al., 2008a). Monophyly of sphaero- et al., 2002). The other two species have a more restricted distribu- dactyls is well supported by both morphological (Noble, 1921; tion: C. septentrionalis occurs from eastern Venezuela to western Kluge, 1987, 1995) and molecular data (Gamble et al., 2008a). Ex- Suriname and northern Roraima, (Ávila-Pires, 1995) and C. natalen- cept for Gonatodes, genera present claws enclosed in an ungual sis is confined to forested areas between dunes at the Parque Nac- sheath, one of the characters long recognized as diagnostic as diag- ional das Dunas, Rio Grande do Norte (Freire, 1999). Although all nostic of the family (Noble, 1921; Kluge, 1967, 1995). Accounting species are restricted to the leaf litter (Vanzolini, 1980; Ávila-Pires, for only five of the about 150 species described for the subfamily, 1995), C. amazonicus is basically found in shaded forest environ- Coleodactylus is the most widespread genus in Brazil, extending ments (Vitt et al., 2005), whereas the other species can occur in its distribution from eastern Amazonian Forest, through Cerrado habitats ranging from closed-canopy wet forests to more mesic and Caatinga in central Brazil to the Atlantic Forest. Three species open formations (Vanzolini, 1980; Ávila-Pires, 1995; Freire, 1999; are widely distributed: C. amazonicus is found in eastern and cen- Vitt et al., 2005). The most remarkable biogeographic characteristic of * Corresponding author. Fax: +55 11 3091 7553. Coleodactylus is the broad disjunct distribution of C. meridionalis E-mail address: [email protected] (S.R. Geurgas). and C. septentrionalis. These species are inferred to be closely 1055-7903/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2008.05.043 S.R. Geurgas et al. / Molecular Phylogenetics and Evolution 49 (2008) 92–101 93 related (Vanzolini, 1980), but are separated by the Amazon ba- provide the first phylogenetic hypothesis of relationships among sin, which is occupied by the congener, C. amazonicus. The at- its species in a cladistic framework, and (3) estimate the relative tempt to explain this pattern of distribution was fundamental timing of species divergences. The results were compared with for the development of the diversification model of South Amer- the previous hypothesis based on the Quaternary rain forest frag- ican biota based on recent and rapid cycles of forest expansion mentation model proposed to explain the diversification of the and retraction caused by climatic alterations proposed by Vanz- genus. olini and Williams (1970) for the Anolis nitens (formely Anolis chrysolepis; Ávila-Pires, 1995) species group (Vanzolini, 1980). 1.1. Systematic background Considering the Amazon basin as the putative center of Coleo- dactylus diversification and the limited dispersal capacity of Barbour (1921), in his review of the genus Sphaerodactylus, these leaf litter geckos, the disjunct distribution was interpreted noticed that the species described as S. meridionalis Boulenger, as evidence of speciation by geographical isolation caused by 1888, collected on the northeastern region of the Atlantic successive disruptions of a formerly continuous forest (Vanzolini, coast, and S. amazonicus Andersson, 1918, collected in the 1957, 1968b, 1970, 1980; Vanzolini and Williams, 1970). Accord- Amazon Basin near Manaus, although having an asymmetrical ing to Vanzolini’s (1957, 1968b, 1970, 1980) hypothesis, a first ungual sheath, did not present the supraciliary spine character- episode of forest fragmentation would have led to the differenti- istic of all species of Sphaerodactylus, and suggested that they ation of the widespread ancestral stock in C. brachystoma in a should not belong to the genus. Parker (1926) erected the southern refuge and C. meridionalis in a northern refuge. The lat- genus Coleodactylus for S. meridionalis, based on the lack of ter species expanded its range through a continuous forest the supraciliary spine, clavicle not perforated and differences across the Amazon basin and Atlantic Forest during the subse- in composition and asymmetry of the five scales enclosing quent wetter period. A second fragmentation episode would the claws. Subsequently, Wettstein (1928) described a new have separated eastern and western populations of C. meridional- species, C. zernyi, from the lower Tapajós River in Amazon ba- is, giving rise to C. septentrionalis and promoting the speciation sin, which was distinguishable from C. meridionalis by having of C. amazonicus in a non-specified refuge. Competitive exclusion keeled dorsal scales and one post-nasal, and from S. amazoni- with C. amazonicus (Vanzolini, 1968b, 1970) or ecological adapta- cus by the number of post-nasals and absence of a pattern tions of C. meridionalis and C. septentrionalis to drier formations of longitudinal bands on the head. The differences in number, could have precluded these species from recolonizing the Ama- shape, and asymmetry of the ungual sheath scales in relation zon Basin (Vanzolini, 1980). to that of C. meridionalis were described. Despite of the lack Despite studies focused on intraspecific morphological varia- of the supraciliary spine, the justification for incorporing the tion (Vanzolini, 1957; Ávila-Pires, 1995; Freire, 1999), ecology new species into the genus Coleodactylus instead of in Sphaero- (Ramos, 1981; Vitt et al., 2005), and karyotype description (San- dactylus was the absence of a second outer scale on the ungual tos et al., 2003), the knowledge about Coleodactylus is extremely sheath. limited, and even the monophyly of the genus has yet to be In the only review of the genus Coleodactylus, Vanzolini established. Since the species were intuitively grouped based on (1957) synonymized S. amazonicus and C. zernyi within C. the overall conservative morphology and structure and asymme- amazonicus and placed Homonota brachystoma Amaral, 1935, try of the ungual sheath (Vanzolini, 1957), the monophyly of and S. pfrimeri Miranda-Ribeiro, 1937, in the synonymy of C. Coleodactylus have been accepted, yet so far not rigorously tested. brachystoma. A new species, C. guimaraesi,
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