Systematics, biogeography, and evolution of Hemidactylus geckos (Reptilia: Gekkonidae) elucidated using mitochondrial DNA sequences

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Abstract

With more than 80 species inhabiting all warm continental land masses and hundreds of intervening continental and oceanic islands, Hemidactylus geckos are one of the most species-rich and widely distributed of all reptile genera. They consequently represent an excellent model for biogeographic, ecological, and evolutionary studies. A molecular phylogeny for Hemidactylus is presented here, based on 702 bp of mtDNA (303 bp cytochrome b and 399 bp 12S rRNA) from 166 individuals of 30 species of Hemidactylus plus Briba brasiliana, Cosymbotus platyurus, and several outgroups. The phylogeny indicates that Hemidactylus may have initially undergone rapid radiation, and long-distance dispersal is more extensive than in any other reptilian genus. In the last 15 My, African lineages have naturally crossed the Atlantic Ocean at least twice. They also colonized the Gulf of Guinea, Cape Verde and Socotra islands, again sometimes on more than one occasion. Many extensive range extensions have occurred much more recently, sometimes with devastating consequences for other geckos. These colonizations are likely to be largely anthropogenic, involving the ‘weedy’ commensal species, H. brookii s. lat, H. mabouia, H. turcicus, H. garnotii, and H. frenatus. These species collectively have colonized the Mediterranean region, tropical Africa, much of the Americas and hundreds of islands in the Pacific, Indian, and Atlantic oceans. Five well-supported clades are discernable in Hemidactylus, with the African H. fasciatus unallocated. 1. Tropical Asian clade: (Cosymbotus platyurus (H. bowringii, H. karenorum, H. garnotii)) (H. flaviviridis (Asian H. brookii, H. frenatus)). 2. African H. angulatus and Caribbean H. haitianus. 3. Arid clade, of NE Africa, SW Asia, etc.: (H. modestus (H. citernii, H. foudai)) (H. pumilio (H. granti, H. dracaenacolus) (H. persicus, H. macropholis, H. robustus, H. turcicus (H. oxyrhinus (H. homoeolepis, H. forbesii))). 4. H. mabouia clade (H. yerburii, H. mabouia). 5. African–Atlantic clade: H. platycephalus ((H. agrius, H. palaichthus) (H. longicephalus, H. greeffi, H. bouvieri, Briba brasiliana))). Cosymbotus and Briba are synonymized with Hemidactylus, and African populations of H. brookii separated as H. angulatus, with which H. haitianus may be conspecific. Some comparatively well-sampled widespread species show high genetic variability (10–15% divergence) and need revision, including Cosymbotus platyurus, H. bowringii, Asian H. brookii, H. frenatus, H. angulatus, and H. macropholis. In contrast, most populations of H. mabouia and H. turcicus are very uniform (1–2% divergence). Plasticity of some of the morphological features of Hemidactylus is confirmed, although retention of primitive morphologies also occurs.

Introduction

Hemidactylus Gray, 1845 is one of the most species-rich genera of the family Gekkonidae and comprises about 80 recognized species. Most are listed, together with their synonymies, by Wermuth (1965), Kluge (1991), and Bauer and Henle (1994), but some have been described only recently (Baha el Din, 2003, Baha el Din, 2005, Bauer and Pauwels, 2002, Henle and Böhme, 2003, Rösler and Wranik, 1999). Hemidactylus geckos are mainly nocturnal and often climb. They occur naturally through much of tropical Asia and Africa and in the intervening more arid areas of Northeast Africa and Southwest Asia, and also extend into the Mediterranean region, and have reached South America apparently by natural transmarine colonization (Kluge, 1969). More recent introductions of Old World species have also been made into other areas of the Americas and the West Indies, and into Australia and the islands of the Indian, Pacific, and Atlantic Oceans. Hemidactylus has more apparent cases of such large range extensions than any other reptilian group.

The great majority of Hemidactylus species have relatively small distributions confined to southern Asia and Africa, and just eight species are responsible for most of the huge geographical area covered by the genus, namely H. mabouia, H. turcicus, H. brookii, H. frenatus, H. garnotii, H. persicus, H. flaviviridis, and H. bowringii. The first five of these are especially widespread and are present in both the Old and New Worlds, with H. mabouia also occurring on islands in the Atlantic and H. frenatus and H. garnotii being widespread in the Pacific. These forms are sometimes called ‘weedy’ species (Kluge, 1969). They are very frequently commensal with people, often occurring in and around human habitations and in anthropogenically modified habitats and in ecotones. It is therefore possible that much of their range is the result of human introduction, but some very long transmarine journeys may have been natural (Kluge, 1969). Recent molecular studies have included some populations of some ‘weedy’ Hemidactylus species, in the Cape Verde (Jesus et al., 2001), Gulf of Guinea (Jesus et al., 2005), Comoro islands (Rocha et al., 2005) and in Madagascar (Vences et al., 2004), and results have been interpreted as indicating both natural and human-mediated colonizations. On occasion, the recent spread of Hemidactylus has had devastating consequences for endemic species. The arrival of H. frenatus in the Mascarene islands decimated a radiation of six species of Nactus geckos, three now being entirely extinct and the remainder limited to relict populations on the offshore islets of Mauritius (Arnold, 2000, Cole et al., 2005).

The species of Hemidactylus share a unique combination of derived features in toe morphology. These include the unusual form and interrelationships of the antepenultimate phalanx of digits III–V of the pes (Russell, 1977), the distal extent of the dorsal interossei muscles along the digit, and the means of tendinous insertion of these muscles onto the scansors (Bauer and Russell, 1995, Russell, 1976, Russell, 1977). These features also occur in the monotypic South American Briba, in southeast Asian Cosymbotus, and in the two Indian species of Teratolepis (Bauer and Russell, 1995). Toe structure strongly suggests that all these geckos form a clade (Bauer and Russell, 1995). The monotypic Indian Dravidogecko, which has similar digits has already been placed in the synonymy of Hemidactylus (Bauer and Russell, 1995), and it may be appropriate to treat the other three genera similarly.

Hemidactylus is morphologically conservative in many features, such as skull structure and number of presacral vertebrae (usually 26, a primitive trait in gekkonids). There is however considerable variation in a range of external features including the following: body size; proportions of the head, body and limbs, and of the unregenerated tail which may be laterally expanded or swollen; number of internasal granules; size of dorsal scales and their degree of posterior imbrication; presence or absence of enlarged dorsal tubercles and, when they are present, their number, size, detailed shape, and extent on body head and limbs; number and extent of femoral pores in males or their complete absence; size of adhesive pads on digits and the number of expanded subdigital lamellae that constitute them externally (especially on toes 1 and 4), and whether or not the lamellae extend proximally onto the sole of the foot; presence or absence of the distal section of digit I of manus and pes including the claw; presence or absence of webbing on the toes; presence or absence of enlarged tubercles on the tail and whether these are spinose; whether subcaudal scales are enlarged and laterally expanded or small; dorsal and ventral colouring and pattern. Conditions in the apparent close relatives of the Hemidactylus group and in other gekkonids suggest that the following features are derived: unregenerated tail laterally expanded or swollen; enlargement and posterior imbrication of dorsal scales; absence or reduction of dorsal tubercles; reduction or loss of femoral pores; loss of distal section of digit I; presence of webbing on toes; and enlarged tubercles on tail spinose or absent.

Hemidactylus is taxonomically difficult. Many of its external features appear quite plastic, often varying within species or between otherwise similar ones. Some species are quite variable geographically, and these and others may be easily confused. This variation makes it hard to construct unambiguous identification keys for them, especially as some are known from few specimens. The last extensive revision of Hemidactylus was of the African species nearly sixty years ago (Loveridge, 1947). It has not been possible to produce even a tentative phylogeny for the genus using morphology, and studies of DNA sequence to date have focused instead on relatively small assemblages of species, often on islands (Jesus et al., 2001, Jesus et al., 2005, Rocha et al., 2005, Vences et al., 2004).

In lizard groups like Hemidactylus where there are many systematic problems, DNA sequences are often very illuminating, as they have been in the other gekkonid genera Tarentola (Carranza et al., 2000, Carranza et al., 2002), Phelsuma (Austin et al., 2004), and Pachydactylus (Lamb and Bauer, 2001, Lamb and Bauer, 2002). In the present study, we use fragments of two mitochondrial genes, cytochrome b and 12S rRNA, from 30 species of Hemidactylus to explore the phylogeny, evolution, and biogeography of the genus. The phylogenetic positions of Briba and Cosymbotus are investigated and a systematic framework produced to facilitate further studies. The validity of several species is tested in terms of their genetic homogeneity and separation from other taxa. Finally, long-distance colonizations are identified, and ancient ones that are certainly natural differentiated from more recent ones that may be anthropogenic, with special attention being paid to some of the ‘weedy’ species.

Section snippets

Samples, DNA extraction, and amplification

In total 183 specimens were used for this study, 166 Hemidactylus, 4 specimens of Cosymbotus platyurus, 4 Briba brasilianus, and 8 Tarentola and 1 Pachydactylus employed as outgroups. Specimens used in the present study, their localities, specimen codes, and GenBank accession numbers for the two genes analyzed are listed in Table 1. Partial sequences of the mitochondrial genes encoding cytochrome b (cytb) and the mitochondrial ribosomal 12S rRNA (12S) were amplified and sequenced following

Results

A total of 702 characters (303 bp of the cytb and 399 of the 12S) were used in the phylogenetic analyses. Of these, 457 were variable and 423 parsimony-informative. Results are presented in Fig. 1. All three methods of analysis (ML, MP, and BI) gave very similar results and showed only minor differences, mainly at the base of the tree where relationships have little support. The phylogeny comprised five well-supported clades consisting of 2–13 species, with H. fasciatus occupying an isolated

Status of Briba and Cosymbotus

The molecular data clearly place members of the small genera, Briba and Cosymbotus, within specific groups of Hemidactylus, respectively, the Asian and African–Atlantic clades. It is therefore appropriate to transfer them to Hemidactylus. Briba brasiliana becomes Hemidactylus brasilianus comb. nov., while Cosymbotus playturus becomes Hemidactylus platyurus comb. nov. (which is not the same as H. platurus Bleeker, 1858 = Gehyra mutilata, fide M.A. Smith, 1935). A second species assigned to

Acknowledgments

We thank J. Roca for technical help in the later part of this investigation, and the following colleagues for providing tissue samples for DNA extraction. J. Vindum, California Academy of Sciences, San Francisco (extensive material from Southeast Asia, East and West Africa), S. Baha el Din (Egypt), W. Wranik and H. Rösler (Socotra), J.M. Padial (Mauritania), the late J. Gasperetti (Arabia), T. Papenfuss (Oman, Somaliland), Jonathan Baillie (São Tomé), P. Eggleton (Cameroun), M. Wilkinson and D.

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