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A Molecular Perspective on the Evolution of Microteiid Lizards (Squamata, Gymnophthalmidae), and a New Classification for the Family

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A Molecular Perspective on the Evolution of Microteiid Lizards (Squamata, Gymnophthalmidae), and a New Classification for the Family Biological Journal of the Linnean Society (2001), 74: 315–338. With 5 figures doi:10.1006/bijl.2001.0580, available online at http://www.idealibrary.com on A molecular perspective on the evolution of microteiid lizards (Squamata, Gymnophthalmidae), and a new classification for the family KATIA C. M. PELLEGRINO1,3, MIGUEL T. RODRIGUES2, Y. YONENAGA-YASSUDA1 and JACK W. SITES, JR3∗ 1 Departamento de Biologia, Instituto de Biocieˆncias, Universidade de Sa˜o Paulo. C.P. 11.461 CEP: 05422-970, Sa˜o Paulo, Brasil 2 Departamento de Zoologia, Instituto de Biocieˆncias, e Museu de Zoologia, Universidade de Sa˜o Paulo, Sa˜o Paulo, Brasil 3 Department of Zoology and M. L. Bean Life Science Museum, Brigham Young University, Provo, Utah, 84602, USA Received 26 March 2001; accepted for publication 22 June 2001 A molecular phylogeny was reconstructed for 26 recognized genera of the Gymnophthalmidae using a total of 2379 bp of mitochondrial (12S, 16S and ND4) and nuclear (18S and c-mos) DNA sequences. We performed maximum parsimony (MP) and maximum likelihood (ML) analyses, and data partitions were analysed separately and in combination under MP. ML analyses were carried out only on the combined sequences for computational simplicity. Robustness for the recovered nodes was assessed with bootstrap and partitioned Bremer support (PBS) analyses. The total molecular evidence provided a better-resolved hypothesis than did separate analysis of individual partitions, and the PBS analysis indicates congruence among independent partitions for support of some internal nodes. Based on this hypothesis, a new classification for the family is proposed. Alopoglossus, the sister group of all the other Gymnophthalmidae was allocated to a new subfamily Alopoglossinae, and Rhachisaurus (a new genus for Anotosaura brachylepis) to the new Rhachisaurinae. Two tribes are recognized within the subfamily Gymnophthalminae: Heterodactylini and Gymnophthalmini, and two others within Cercosaurinae (Ecpleopini and Cercosaurini). Some ecological and evolutionary implications of the phylogenetic hypothesis are considered, including the independent occurrence of limb reduction, body elongation, and other characters associated with fossoriality. 2001 The Linnean Society of London ADDITIONAL KEY WORDS: phylogeny – DNA sequences – mitochondrial – nuclear – fossoriality – limb reduction – maximum parsimony – maximum likelihood – combined analysis – karyotypes. INTRODUCTION Two subfamilies are presently recognized: the Tu- pinambinae, comprised of genera Callopistes, Dra- The Teiioidea is an assemblage of exclusively Neo- caena, Tupinambis and Crocodilurus, and the Teiinae, tropical lizards comprised of the families Teiidae and including Teius, Dicrodon, Ameiva, Cnemidophorus Gymnophthalmidae (Estes, de Queiroz & Gauthier, and Kentropyx (Presch, 1974; Denton & O’Neill, 1995; 1988), informally referred to as macroteiids and Sullivan & Estes, 1997). microteiids, respectively, due to marked difference in In contrast to macroteiids, the small to medium- body size (some macroteiids grow to a metre in length, sized Gymnophthalmidae (about 4–15 cm snout–vent Ruibal, 1952). Although much work is still needed to length) are much more diversified and far from taxo- understand intrageneric affinities, relationships nomically well known at specific, generic or supra- among macroteiid genera are relatively well known. generic levels. They occur from Southern Mexico to Argentina, in the Caribbean, and on some islands of the continental shelves of South and Central America. Presently, 178 species, 10 of them polytypic and in- ∗ Corresponding author. E-mail: jack–[email protected] cluding a total of 26 subspecies, have been assigned 315 0024–4066/01/110315+24 $35.00/0 2001 The Linnean Society of London 316 K. C. M. PELLEGRINO ET AL. to 36 genera, most of them exclusive to South America into four groups based upon characters of external (Table 1). The complex taxonomy of Gymnophthal- morphology. Species later known as macroteiids (Tei- midae derives not only from the rarity of many taxa idae) were included in his first group, and the mi- in collections, but also from the presence of convergent croteiids (Gymnophthalmidae) in the other three morphological adaptations to specialized habitats. groups. Several studies followed Boulenger’s proposal Limb reduction, body elongation, loss of eyelids and/ in attempting to subdivide his groups into smaller or of external ear openings, or presence/absence of monophyletic clades (Presch, 1980), or to raise the some head scales, are some of the characters that status of microteiids to an independent subfamily or contribute to the present difficulty of resolving re- family distinct from Teiidae (MacLean, 1974; Presch, lationships among microteiids at all hierarchical levels. 1983; Estes, 1983; Presch, 1988; Estes et al., 1988). Gymnophthalmids occur in habitats ranging from Although important revisions and descriptions of new open areas in the high Andes to lowland tropical rain- genera of microteiids have been made since Boulenger, forests. Most species are terrestrial and lizard-like in there is as yet no phylogenetic proposal based on general appearance, but some are semi-aquatic, as are a large number of taxa and characters. Therefore, those in the genus Neusticurus, and others show limb Boulenger’s work remains a basic reference due to the reduction to various degrees. Limb reduction has ap- lack of a more complete study of the family (Harris, parently occurred many times within microteiids, and 1985). it is accompanied by body elongation. Bachia and Furthermore, evidence for monophyly of Gym- Calyptommatus are good examples of these processes nophthalmidae is still ambiguous. Harris (1985) ana- (Rodrigues, 1991a, 1995) but, in species of Bachia, lysed the infralingual plicae of 30 microteiid genera, reduction is more pronounced in the hindlimbs than and suggested that they be retained in the Teiidae, as in the forelimbs, while in Calyptommatus, forelimbs proposed by Boulenger. Harris’ data confirmed that are entirely lacking and hindlimbs are vestigial. Notho- Teiidae and Gymnophthalmidae are monophyletic only bachia and Psilophthalmus are examples of the Calyp- because they are unique in sharing infralingual plicae; tommatus-like process of forelimb reduction, his work does not provide evidence to contradict the whereas Heterodactylus, Anotosaura, Colobosaura and hypothesis of monophyly for microteiids. Hoyos (1998) Colobodactylus have been referred to as examples of concluded that there is not enough data to support the Bachia-like hindlimb reduction (Rodrigues, 1991a; monophyly of Gymnophthalmidae, but his study was Kizirian & McDiarmid, 1998). These lizards are often based on limited character and taxonomic sampling secretive or burrowing species in tropical forests or (15 osteological and myological characters from 11 open areas (Bachia), or occupy specialized sand dune genera, assigned to 16 species). habitats in the semiarid Brazilian Caatinga (as Calyp- More recently, a group of eight genera previously tommatus, Rodrigues, 1991a, 1995). The wide geo- proposed as monophyletic by one of us (Rodrigues, graphic distribution of many taxa, coupled with 1991b), was studied on the basis of analysis of different degrees of limb reduction and body elong- 71 characters of osteology, external morphology and ation, loss of eyelids or external ear openings, con- hemipenial anatomy (Rodrigues, 1995). The sug- siderable variation in head squamation, the presence gested relationships for this group are: (Tretioscincus of parthenogenesis in species of Gymnophthalmus and (Micrablepharus (Gymnophthalmus ((Procellosaurinus, Leposoma, conspicuous chromosome variation (Cole et Vanzosaura)(Psilophthalmus (Calyptommatus and al., 1990; Cole, Dessauer & Markezich, 1993; Yonen- Nothobachia)))))). Some genera of this radiation show aga-Yassuda et al., 1995, 1996a; Pellegrino, 1998; the most striking characteristics associated with psa- Yonenaga-Yassuda & Rodrigues, 1999; Pellegrino, Ro- mophily and fossorial habitat so far reported for lizards, drigues & Yonenaga-Yassuda, 1999a, b), and un- including forelimb reduction, body elongation, and loss resolved relationships among most genera, make this of eyelids accompanied by the differentiation of an an ideal group for phylogenetic studies. ocular scale covering the eye. The early history of herpetology is marked by several Allozymes, mitochondrial DNA restriction-site and attempts to allocate gymnophthalmids in suprageneric chromosome data have also been collected for this ra- groups but, due to the characters related to limb- diation (Martins, 1997; Benozzati & Rodrigues, sub- lessness or the presence of quincuncial scales in some mitted; Yonenaga-Yassuda et al., 1995, 1996a; Yonenaga- taxa, several genera were originally placed close to the Yassuda, Pellegrino & Rodrigues, 1996b; Yonenaga-Yas- presently recognized lizards of the families Teiidae, suda & Rodrigues, 1999; Pellegrino et al., 1999a). The Lacertidae or Scincidae (Gray, 1827, 1845, 1838, 1839; phylogenetic analyses based on allozymes and re- Merrem, 1820; Wagler, 1830). striction-site data also supported the monophyly of this The first robust taxonomic proposal for Gym- group, and the topologies show some degree of con- nophthalmidae was presented by Boulenger (1885), gruence with morphological data. The only published who recognized only one family (Teiidae), and split it nucleotide sequences for Gymnophthalmidae are those Table 1. List of recognized genera of Gymnophthalmidae
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