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A Molecular Study of Phylogenetic Relationships and Evolution of Antipredator Strategies in Australian Diplodactylus Geckos, Subgenus Strophurus

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A Molecular Study of Phylogenetic Relationships and Evolution of Antipredator Strategies in Australian Diplodactylus Geckos, Subgenus Strophurus Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2004? 2004 821 123138 Original Article ANTIPREDATOR STRATEGIES IN STROPHURUS J. MELVILLE ET AL. Biological Journal of the Linnean Society, 2004, 82, 123–138. With 5 figures A molecular study of phylogenetic relationships and evolution of antipredator strategies in Australian Diplodactylus geckos, subgenus Strophurus JANE MELVILLE1,2*, JAMES A. SCHULTE, II2 and ALLAN LARSON2 1Department of Sciences, GPO Box 666E, Museum Victoria, Melbourne, VIC 3000, Australia 2Department of Biology, Washington University, St Louis, MO 63130, USA Received 26 February 2003; accepted for publication 17 December 2003 We present phylogenetic analyses of the lizard genus Diplodactylus subgenus Strophurus using 1646 aligned posi- tions of mitochondrial DNA sequences containing 893 parsimony-informative characters for samples of 12 species of Strophurus and 19 additional Australian gecko species. Sequences from three protein-coding genes (ND1, ND2 and COI) and eight intervening transfer RNA genes were examined using parsimony, maximum-likelihood and Bayesian analyses. Species of Strophurus appeared to form a monophyletic group with the possible exception of S. taenicauda. Strophurus has evolved two distinct defence/display characteristics: caudal glands, which expel an unpalatable sub- stance, and striking mouth colours. Caudal glands appeared to have arisen once in a common ancestor of Strophurus, with dermal augmentation of caudal glands characterizing a subclade within the subgenus. Evolution of yellow and dark-blue mouth colours in Strophurus occurred in the context of diurnal activity and may be interpreted as an aug- mentation of defensive behavioural displays. Molecular divergence suggests that arboreality evolved in a common ancestor of Oedura and Strophurus approximately 29 Mya and that the caudal glands of Strophurus arose approx- imately 25 Mya. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 123– 138. ADDITIONAL KEYWORDS: Australia – defensive display – Gekkonidae – Gekkota – molecular systematics – Pygopodidae – mitochondrial DNA – Reptilia – Sauria. INTRODUCTION est genus within Diplodactylini, but prior phylogenetic hypotheses suggest that it is not a monophyletic group We examined phylogenetic relationships among diplo- (Greer, 1989). dactyline geckos in Australia with emphasis on Diplo- The 16 species placed in subgenus Strophurus pos- dactylus subgenus Strophurus, a group distinguished sess caudal glands that eject a sticky noxious sub- from its closest relatives by arboreality and diurnal stance through skin ruptures on the mid-dorsal line of activity. Diplodactylus and related genera (Crenadac- the tail to repel predators (Rosenburg & Russell, tylus, Oedura, Rhynchoedura) belong to the taxon 1980). Strophurus is diagnosed also by fleshy cloacal Diplodactylini, one of two major subgroups of the spurs, inscriptional ribs approaching the ventral line, gekkonid subfamily Diplodactylinae (Fig. 1) recog- and absence of the lateral pair of postcloacal bones nized by Kluge (1967a, b, 1987) and Bauer (1990). Mol- (Böhme & Sering, 1997). Russell & Rosenburg (1981) ecular phylogenetic work by Donnellan, Hutchinson & initially placed D. ciliaris, D. elderi, D. michaelseni, Saint (1999) supports monophyly of Diplodactylini but D. spinigerus, D. strophurus, D. taenicauda and provides no strong support for monophyly of the other D. williamsi in the subgenus Strophurus. Rosenburg, subgroup, Carphodactylini. Diplodactylus is the larg- Russell & Kapoor (1984) later discovered caudal glands in D. rankini and added this species to Stro- phurus, while also suggesting that D. wilsoni should *Corresponding author. E-mail: [email protected] be included in this subgenus. Since then, D. assimilis, © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 123–138 123 124 J. MELVILLE ET AL. Carphodactylini Diplodactylini Australia New Caledonia New Zealand Hoplodactylus Naultinus Bavayia Rhacodactylus Eurydactylodes Pseudothecadactylus Phyllurus Nephrurus Underwoodisaurus Carphodactylus Diplodactylus Lucasium Rhynchoedura Crenadactylus Oedura Strophurus Diplodactylinae Figure 1. Schematic diagram of hypothetical relationships within Diplodactylinae as proposed by Greer (1989), based primarily on Kluge (1967b). Lucasium has been synonymized with Diplodactylus, and Phyllurus was split into three genera (Orraya, Phyllurus and Saltuarius) in subsequent studies (Kluge, 2001; Hoskin, Couper & Schneider, 2003). D. intermedius, D. jeanae, D. mcmillani, D. robinsoni, Another striking defence/display feature of most D. taeniatus, D. wellingtonae and D. wilsoni have been Strophurus is a conspicuous mouth colour, either added to Strophurus (Greer, 1989; Cogger, 2000; dark blue or yellow (Greer, 1989). Geckos have a Kluge, 2001), which is given generic status by some characteristic defensive posture that usually involves authors. Although we regard these species tentatively lifting and arching the body, extending the throat, as being part of Diplodactylus, we refer to them in the and slowly waving the raised tail from side to side. remainder of this manuscript using Strophurus in Within Diplodactylinae, this behaviour has been place of the genus name to distinguish them from documented in Nephrurus spp. (Galliford, 1978), other Diplodactylus. Oedura tryoni, Phyllurus platurus, and S. taeniatus Geckos of the subgenus Strophurus can fire from the (Schmida, 1973). Many species open their mouths dorsal surface of their tail thin streams of viscous tail- during these displays, exposing the mouth colour gland secretions aimed by curving the tail (Rosenburg (Bustard, 1964). A blue mouth occurs in S. assimilis, & Russell, 1980; Greer, 1989). Preliminary biochemi- S. ciliaris, S. intermedius, S. rankini, S. spinigerus, cal characterization shows that the substance con- S. strophurus, S. wellingtonae and S. williamsi; a tains protein and glycoprotein and is similar among yellow/orange mouth colour occurs in S. ciliaris and species (Rosenburg et al., 1984). Previous studies sug- S. taeniatus, whereas S. elderi has the pink mouth gest that the caudal glands are evolutionary modifica- characteristic of most Diplodactylini (Greer, 1989). tions of fat bodies that occupy a similar position in We present a molecular phylogenetic study of 12 of many other lizards, including other Diplodactylini the 16 recognized species of Strophurus (excepting (Rosenburg et al., 1984; Greer, 1989). Most Strophurus S. jeanae, S. michaelseni, S. robinsoni and S. wilsoni) lack caudal fat bodies, their place being filled by cau- to examine evolutionary patterns of caudal glands and dal glands (Rosenburg & Russell, 1980). Caudal mouth colours. Sequences reported include a 1853-bp glands have evolved separately in the diplodactyline segment of the mitochondrial genome extending from genus Eurydactylodes from New Caledonia (Böhme & the protein-coding gene ND1 (subunit one of NADH Sering, 1997). dehydrogenase), through the genes encoding tRNAIle, © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 123–138 ANTIPREDATOR STRATEGIES IN STROPHURUS 125 tRNAGln, tRNAMet, ND2 (NADH dehydrogenase sub- loops (dihydrouridine (D), TYC (T) and variable Trp Ala Asn unit two), tRNA , tRNA , tRNA , OL (origin of loops) of some tRNA genes, and some intergenic light-strand synthesis), tRNACys and tRNATyr, to the sequences, were excluded from the phylogenetic protein-coding gene, COI (subunit I of cytochrome c analyses. oxidase). In addition, we sampled eight other species within Diplodactylini, including representatives of three previously recognized species groups of Diplo- PHYLOGENETIC ANALYSIS dactylus, and eight species in Carphodactylini. We also Phylogenetic trees were estimated using PAUP* beta included in our analysis a pygopodid lizard, Lialis version 4.0b10a (Swofford, 2002) with 100 heuristic jicari, because prior studies suggest a phylogenetic searches using random addition of sequences under affinity between pygopodids and diplodactyline geckos the parsimony criterion. Bootstrap resampling was (Donnellan et al., 1999). Two Australian gekkonine applied to assess support for individual nodes using taxa, Heteronotia binoei and Gehyra variegata, and a 500 bootstrap replicates with ten heuristic searches previously published sequence of the south-east Asian featuring random addition of sequences. Decay indices species, Gekko gecko (Macey et al., 1999), were (= ‘branch support’ of Bremer, 1994) were calculated included as outgroups. for all internal branches of the tree using TREEROT version 2a (Sorenson, 1999). We refer to bootstrap per- centages and decay indices as heuristic measures of MATERIAL AND METHODS branch support because they provide useful informa- tion regarding the amount of character support for SPECIMEN INFORMATION individual branches but they do not constitute statis- Details of the voucher specimens from which DNA was tical tests of hypotheses. extracted are given in Table 1. Maximum likelihood was used to estimate a phy- logenetic tree that maximized the probability of the observed data. ModelTest version 3.06 (Posada & LABORATORY PROTOCOLS AND ALIGNMENT OF Crandall, 1998) was used to compare the goodness- DNA SEQUENCES of-fit of different models of sequence evolution to the Genomic DNA was extracted from liver, muscle or data, and to generate optimal likelihood settings.
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