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Home , Aprasia inaurita, Bavayia, Carphodactylidae, Carphodactylus, Crenadactylus, Crenadactylus ocellatus

Journal of Biogeography (J. Biogeogr.) (2009) 36, 2044–2055

ORIGINAL Molecular evidence for Gondwanan ARTICLE origins of multiple lineages within a diverse Australasian radiation Paul M. Oliver1,2* and Kate L. Sanders1

1Centre for Evolutionary Biology and ABSTRACT , University of Adelaide and Aim Gondwanan lineages are a prominent component of the Australian 2Terrestrial Vertebrates, South Australian Museum, North Terrace, Adelaide, SA, terrestrial biota. However, most squamate ( and ) lineages in Australia appear to be derived from relatively recent dispersal from Asia (< 30 Ma) and in situ diversification, subsequent to the isolation of Australia from other Gondwanan landmasses. We test the hypothesis that the Australian radiation of diplodactyloid (families , and ), in contrast to other endemic squamate groups, has a Gondwanan origin and comprises multiple lineages that originated before the separation of Australia from Antarctica. Location Australasia. Methods Bayesian (beast) and penalized likelihood rate smoothing (PLRS) (r8s) molecular dating methods and two long nuclear DNA sequences (RAG-1 and c-mos) were used to estimate a timeframe for divergence events among 18 genera and 30 of Australian diplodactyloids. Results At least five lineages of Australian diplodactyloid geckos are estimated to have originated > 34 Ma (pre-) and basal splits among the Australian diplodactyloids occurred c. 70 Ma. However, most extant generic and intergeneric diversity within diplodactyloid lineages appears to post-date the late Oligocene (< 30 Ma). Main conclusions Basal divergences within the diplodactyloids significantly pre-date the final break-up of East Gondwana, indicating that the group is one of the most ancient extant endemic vertebrate radiations east of Wallace’s Line. At least five Australian lineages of diplodactyloid gecko are each as old or older than other well-dated Australian squamate radiations (e.g. elapid and agamids). The limbless Pygopodidae (morphologically the most aberrant living geckos) appears to have radiated before Australia was occupied by potential ecological analogues. However, in spite of the great age of the diplodactyloid radiation, most extant diversity appears to be of relatively recent origin, a pattern that is shared with other Australian squamate lineages. *Correspondence: Paul Oliver, Centre for Keywords Evolutionary Biology and Biodiversity, Australasia, Bayesian analysis, Carphodactylidae, Diplodactylidae, divergence University of Adelaide, Adelaide, 5005 SA, Australia. times, geckos, Gondwana, historical biogeography, Pygopodidae, relaxed-clock E-mail: [email protected] dating.

evolved in relative geographical isolation, originating from INTRODUCTION either of two sources: (1) an ancient Gondwanan biota that The Australian biota is dominated by diverse and largely became isolated in Australasia as the northward-drifting Indo- endemic radiations (Keast, 1981; Heatwole, 1987; Crisp et al., Australian tectonic plate detached from Antarctica c. 55– 2004). It has become widely accepted that these lineages 32 Ma; and (2) a modern fauna derived from over-water

2044 www.blackwellpublishing.com/jbi ª 2009 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2009.02149.x Gondwanan origins of Australasian geckos dispersals, usually from the north after the Australian and Asian not yet been assessed comprehensively and directly using plates came in close enough proximity to allow island-hopping, molecular data. In this paper we use two nuclear sequences to beginning c. 30 Ma and continuing through to the Pliocene examine generic relationships for the Australian diplo- (Heatwole, 1987; Hall, 2001; Metcalfe, 2001). For any endemic dactyloids and estimate a time-scale for major divergence Australasian radiation, these biogeographical scenarios have events within the group. distinct, testable predictions for divergence times and phylog- eny. A vicariant Gondwanan hypothesis is supported if diver- MATERIALS AND METHODS gence from sister lineages found outside the Australasian region on Gondwanan landmasses occurred at least 55 (vs. < 35) Ma. Sampling and gene sequencing Gondwanan elements are a prominent feature of most major groups of Australian terrestrial vertebrates, including mam- We sampled 64 taxa, comprising 32 diplodactyloids (c. 25% of mals (marsupials and monotremes; Archer et al., 1999; Beck, the Australian species), eight gekkotan outgroups (Table 1) 2008), birds (e.g. ratites, passerines, parrots; Cooper et al., and 24 other (lepidosaur and archosaur) taxa spanning robust 2001; Barker et al., 2004; Schodde, 2006), frogs (pelodryadid calibration nodes (see Table S1 in Supporting Information). treefrogs, myobatrachids and possibly microhylids; Roelants Sequence data were obtained from all recognized genera of et al., 2007) and chelid turtles (Georges & Thompson, 2006). Australian diplodactyloid geckos with the exception of , Whereas and snakes (squamates) are highly diverse in and multiple exemplars were obtained for species-rich and Australia (> 800 species: Wilson & Swan, 2008) and are among divergent genera in to test their and the most species-rich endemic Australasian radiations (Rabo- minimize long-branch artefacts. While we did not include sky et al., 2007), phylogenetic and recent dating studies of any genera, sequence data were obtained from most major extant Australian squamate lineages suggest these two genera of New Caledonian diplodactylids. Gekkonid are all Miocene immigrants that diverged from their nearest outgroups spanned three other gekkonoid families (Gekkon- extralimital (Old World) relatives within the last 10–35 Myr. idae, and ). This includes the venomous elapid snakes (Sanders & Lee, Whole genomic DNA was isolated from liver samples using 2008), pythons (Rawlings et al., 2008), agamid lizards (Hugall standard proteinase K protocols (Sambrook et al., 1989). et al., 2007), Sphenomorphus group (Rabosky et al., Standard polymerase chain reaction (PCR) protocols were 2007; Skinner et al., 2008) and varanid lizards (Ast, 2001). followed using 25 or 50 ml reactions and TAQgold (Applied Geckos are a conspicuous component of the Australian Biosystems, Carlsbad, CA, USA) and buffer at concentrations squamate fauna. Molecular phylogenetic studies of the global recommended by the manufacturer for 34 cycles. Concentra- gecko radiation have uncovered deep divergences that are tions of buffer were varied depending on the initial reaction consistent with ancient Gondwanan vicariance (Gamble et al., success. Optimal thermal cycling temperatures for different 2008). The Australian gecko fauna is dominated by diplo- primer combinations and taxa ranged from 48 to 62C. The PCR dactyloid geckos. This moderately diverse radiation consists of products were sequenced using the ABI PRISM BigDye Termi- three families: the Diplodactylidae, Carphodactylidae and nator Cycle Sequencing Ready Reaction Kit and an ABI 3700 Pygopodidae (Han et al., 2004), hereafter referred to jointly automated sequencer (Applied Biosystems). Two nuclear frag- as the Diplodactyloidea. The Carphodactylidae are entirely ments were selected: 1800 bp of RAG-1 (recombination reac- endemic to Australia, nearly all of the Pygopodidae are tivating gene 1) and 750 bp of c-mos (oocyte maturation factor). Australian endemics (two species occur in New Guinea) and These loci have been widely used in squamate studies; they are the Diplodactylidae comprise three relatively diverse radiations single copy, uninterrupted by introns and have a slow substi- in Australia, and New Zealand (Bauer, 1990; tution rate suitable for the time-scales of interest (e.g. Saint Wilson & Swan, 2008). Diplodactyloids include c. 15% of the et al., 1998; Townsend et al., 2004; Gamble et al., 2008). Primers Australasian squamate fauna and are the most ecologically and used are given in Table 2. Sequencing was outsourced to a morphologically diverse clade of gekkotan lizards in the world commercial firm (Macrogen, Seoul, South Korea) or the Insti- (Greer, 1989; Wilson & Swan, 2008). Notably aberrant are the tute of Medical and Veterinary Science (IMVS) in Adelaide. Pygopodidae, which are the world’s only limb-reduced geckos Sequence data were aligned by eye and then translated using and show a remarkable array of morphological and ecological MacClade (Maddison & Maddison, 2005) to check for adaptations to a limbless lifestyle within an only moderately mutations indicating the amplification of pseudogenes. species-rich clade (Greer, 1989; Webb & Shine, 1994). Previous phylogenetic studies that focused on the relation- Phylogenetic analyses ships within diplodactyloid clades (e.g. Kluge, 1987; Bauer, 1990; King, 1990; Couper et al., 2000; Jennings et al., 2003; Phylogenetic analysis using parsimony and likelihood methods Melville et al., 2004; Oliver et al., 2007a) or the higher-level was implemented in paup* version 4.0b10 (Swofford, 2002). phylogeny of gekkotans (King, 1987; Han et al., 2004; Gamble Bayesian inference was implemented in MrBayes version 3.1 et al., 2008) have all suggested that diplodactyloids have (Huelsenbeck & Ronquist, 2001). A maximum parsimony Gondwanan origins. However, divergence times and phylo- was estimated using unweighted heuristic searches with 50 genetic relationships across the diplodactyloid radiation have random step-wise sequence addition replicates and tree

Journal of Biogeography 36, 2044–2055 2045 ª 2009 Blackwell Publishing Ltd P. M. Oliver and K. L. Sanders

Table 1 Specimen numbers, GenBank accession numbers and localities for gekkonid lizards included in analyses, pre-existing GenBank accession numbers are indicated in bold.

Taxon Specimen Locality RAG-1 c-mos

Carphodactylids laevis QMJ 8944 Lake Barrine, Qld, Australia FJ855442 AF039467 Nephurus milii SAMA R38006 17 km SE Burra, FJ571622 FJ571637 Nephurus stellatus SAMA R36563 19.3 km NE Courtabie, South Australia FJ855446 FJ855466 SAMA R55649 10 km W Isaac River, Qld, Australia FJ855445 FJ855465 platurus ABTC 51012 Bents Basin, Sydney, Australia FJ855443 _ Phyllurus platurus NA NA __ AY172942 swaini SAMA R29204 Wiangaree, NSW, Australia FJ855444 FJ855464 Diplodactylids sauvagei AMS R125814 Mare Island, New Caledonia FJ855448 FJ855468 ocellatus horni SAMA R22245 10 km S Barrow Creek, NT, Australia AY662627 FJ571641 naso AMS R126186 Mitchell Plateau, FJ855458 FJ855479 Crenadactylus ocellatus ocellatus WAM R135495 False Entrance Well, Western Australia FJ855457 FJ855478 granariensis WAM R127572 Goongarrie, Western Australia FJ855452 FJ855473 Diplodactylus tessellatus SAMA R41130 Nr Stuart Hwy, South Australia FJ571624 FJ571639 byrnei SAMA R52296 Camel Yard Spring, South Australia FJ855453 FJ855474 Luscasium stenodactylum NTM R26116 Mann River, NT, Australia FJ855454 FJ855475 marmorata SAMA R34209 Lawn Hill NP, Qld, Australia FJ571623 FJ571638 Oedura reticulata SAMA R23035 73 km E. Norseman, Western Australia FJ855450 FJ855471 Oedura rhombifer SAMA R34513 Townsville area, Qld, Australia FJ855451 FJ855472 australis QMJ 57120 Heathlands, Qld, Australia FJ855449 FJ855470 Pseudothecadactylus lindneri AMS 90915 Liverpool River, NT, Australia AY662626 FJ855469 leachianus AMS R118009 Mt Gouemba, New Caledonia. FJ855447 FJ855467 Rhychoedura ornata SAMA R36873 Mern Merna Station, South Australia FJ855455 FJ855476 intermedius SAMA R28963 Gawler Ranges, South Australia FJ571625 FJ571640 SAMA R53984 11 km S. of Wycliffe Well, Qld FJ855456 FJ855477 Pygopodids inaurita SAMA R40729 2 km E of Burra, South Australia FJ571632 FJ571646 australis SAMA R22784 Mt Remarkable NP, South Australia FJ571633 FJ571647 SAMA R23137 Mt Remarkable NP, South Australia FJ571635 FJ571649 jicari TNHC 59426 NA AY662628 _ Lialis jicari NA Irian Jaya _ AY134564 Ophidiocephalus taeniatus SAMA R44653 Todmorden Stn, South Australia FJ571630 FJ571645 gracilis WAM R104374 Park, Western Australia FJ571631 _ Pletholax gracilis WBJ-2483 Lesueur NP, Western Australia _ AY134566 Paradelma orientalis QMJ 56089 20 km N Capella, Qld, Australia FJ571626 FJ571642 lepidopodus WAM R90378 Walpole-Nornalup NP, Western Australia FJ571627 FJ571643 Pygopus nigriceps SAM R23908 134 km ENE Laverton, Western Australia FJ571628 FJ571644 Other gekkonids marmoratus SAMA R42098 Wedge Is, South Australia FJ855440 FJ855461 marmoratus AMS R126129 Cibodas forest, Java, Indonesia FJ855438 FJ855459 variegata SAMA R54022 Brunette Downs, NT, Australia FJ855439 FJ855460 gekko MVZ 215314 NA AY662625 _ Gekko gekko FMNH 258696 NA _ AY444028 frenatus SAMA R34178 Daly Waters, NT, Australia FJ855441 FJ855462 przewalski CAS 171010 South Gobi Desert, Mongolia AY662624 AY662569 turkmenicus CAS 184771 NA AY662622 _ Eublepharis macularius ABTC 32296 Pet trade _ FJ855463 shreveri SBH 194572 Haiti AY662623 AY662547

Qld, ; NSW, ; NT, ; NP, national park; NA, not applicable. bisection–reconnection (TBR) branch swapping. Bootstrap and codon. Alternative partitioning strategies were run with support was calculated using 1000 bootstrap replicates. Bayes four incrementally heated chains for 3,000,000 generations factors (see Kelchner & Thomas, 2007) and average likelihoods (sampled every 1000th generation) using best-fit models of were used to assess the effect of partitioning data by gene nucleotide substitution for each partition identified using the

2046 Journal of Biogeography 36, 2044–2055 ª 2009 Blackwell Publishing Ltd Gondwanan origins of Australasian geckos

Table 2 Primer combinations used in this study (IUB redundancy codes are Y ¼ C, T: R ¼ A, G: M ¼ A, C: N ¼ A, T, G, C). [Correction added after online publication on 6 July 2009: values for N were corrected.]

Gene Primer References

RAG-1 G755 5¢-AAGTTTTCAGAATGGAAGTTYAAGCTNTT-3¢ Hugall et al. (2007) G756 5¢-TCTCCACCTTCTTCYTTNTCAGCAAA-3¢ Hugall et al. (2007) G1278 5¢-TGATGCAARAAYCCTTTCAGA-3¢ This study G1279 5¢-TCTCCACCTTCTTCTTTCTCAG-3¢ This study G889 5¢-AAAGGTGGACGCCCTAGGCARCA-3¢ Hugall et al. (2007) G883 5¢-TCATGGTCAGATTCATCAGCNARCAT-3¢ Hugall et al. (2007) c-mos G303 5¢-ATTATGCCATCMCCTMTTCC-3¢ Saint et al. (1998) G74 5¢-TGAGCATCCAAAGTCTCCAATC-3¢ Saint et al. (1998) G708 5¢-GCTACATCAGCTCTCCARCA-3¢ Hugall et al. (2008) G1092 5¢-CTTTTGTCCGATGGCTGAGTC-3¢ This study G1163 5¢-CTGCCTGCCAAAGTGGAAAG-3¢ This study

Table 3 beast prior probability distributions (Ma) for calibra- All other relationships were left free to vary so that topological tion nodes used in this study. The r8s analysis used the zero offset uncertainty was incorporated into posterior estimates of and upper 95% confidence intervals (CIs) of the lognormal priors divergence dates. A Yule branching process (appropriate for as minimum and maximum constraints. divergent, interspecific relationships) with a uniform prior was Prior distribution adopted. A relaxed clock was used with branch rate variation modelled using a lognormal distribution and initially assumed Lognormal: to be uncorrelated (Drummond et al., 2006; see below). These mode [zero offset, Normal: settings allow the pattern of rate variation to be quantified to Calibration node upper 95% CI] mode [95% CIs] ascertain whether more restricted models of rate variation (e.g. Pygopus–Paradelma 19 [16, 25] 20 [15, 25] strict clock, correlated lognormal) would be more appropriate. Scincomorphs vs. 168 [155, 200] 168 [135, 200] The combined loci were partitioned by codon position lacertoids + toxicoferans (1st + 2nd vs. 3rd) with unlinked parameter values. The final Bird– 240 [228, 271] 240 [207, 273] analysis consisted of two independent Markov chain Monte Root (mammal–bird) 255–310 (uniform) 255–310 (uniform) Carlo (MCMC) analyses; each chain was run for 15,000,000 generations with parameters sampled every 1000 steps. Inde- Akaike information criterion implemented in MrModeltest pendent runs converged on very similar posterior estimates (Nylander, 2004) and paup* (Swofford, 2002). A three- and were combined using LogCombiner version 1.4 (Drum- partition model with both genes combined and partitioned mond & Rambaut, 2006). Tracer 1.2 (Drummond & by codon position (1st + 2nd + 3rd) was selected as optimum Rambaut, 2006) was used to confirm adequate mixing of the based on a Bayesian information criterion approximation MCMC chain, appropriate burn-in (25%) and acceptable (Schwarz, 1978). The best-fit substitution model for each of effective sample sizes (> 200). these partitions was GTRig. This model was then run with four Most available gecko fossils calibrate shallow divergences chains for 5,000,000 generations, sampling every 1000 gener- (< 20 Myr) between taxa that are not included in the present ations. Values for all model parameters were unlinked, i.e. study (see Gamble et al., 2008). The fossil Pygopus hortulanus allowed to vary independently across partitions. The first is thought to be close to the origin of extant pygopodid genera 1,000,000 generations were discarded as burn-in. MrBayes Pygopus and Paradelma (available in this study) and is from a analyses were run in parallel across four nodes on a SGI Altix site dated as early–middle Miocene (c. 20 Ma; Hutchinson, XE1300 supercomputer (SGI Sunnyvale, CA, USA). 1998). Our phylogenetic analyses (see below) recovered Pygopus as paraphyletic with respect to Paradelma; the P. hortulanus calibration was therefore used conservatively to Molecular dating constrain the node containing all sampled Pygopus and Divergence times were estimated using Bayesian inference as Paradelma. Relaxed-clock dating benefits from multiple cali- implemented in beast version 1.4 (Drummond & Rambaut, brations spanning the divergences of interest (Drummond 2006) and penalized likelihood rate smoothing (PLRS) in r8s et al., 2006). We therefore used the P. hortulanus calibration in version 1.7 (Sanderson, 2002, 2003) and paup* version 4.0b10 combination with two well-corroborated external calibrations: (Swofford, 2002). Preliminary beast runs failed to resolve the Ornithodira (birds and relatives) vs. Crurotarsi ( and split between squamates (lizards and snakes) and rhyncho- relatives), and scincomorph lizards vs. lacertoid plus toxicof- cephalians (tuataras). However, because this relationship is eran lizards (Table 3; see Hugall et al., 2007; Sanders & Lee, well supported by previous molecular studies (e.g. Hugall 2007, 2008). All calibration priors were given a translated et al., 2007), it was constrained in all further beast analyses. lognormal distribution since this best reflects the asymmetrical

Journal of Biogeography 36, 2044–2055 2047 ª 2009 Blackwell Publishing Ltd P. M. Oliver and K. L. Sanders bias in the fossil record (the true divergence date is more likely RESULTS to be older than younger due to non-preservation). Additional analyses were performed assuming normally distributed Phylogenetic relationships (symmetrical) calibration priors; these returned very similar results (Table 4). In all beast analyses, a wide uniform The final data matrix consisted of 2367 sites (1740 RAG-1 and constraint of 255–310 Ma (e.g. Benton & Donoghue, 2006) 627 c-mos) of which 934 (689 RAG-1 and 245 c-mos) were was placed on the root of the tree (mammal–bird split) to variable within geckos and 553 (402 RAG-1 and 151 c-mos) prevent the chain from becoming fixed on unrealistic inflated were parsimony informative within geckos. All sequences values (Drummond et al., 2006). could be translated into amino acids with no evidence of An additional dating analysis was performed with the pseudogenes. Our c-mos sequence for the diplodactylid Oedura program r8s version 1.7 (Sanderson, 2002), using PLRS with marmorata contained a 12 bp indel. The model-based and the Truncated Newton (TN) algorithm and an additive penalty parsimony results were highly concordant, showing no con- function (Sanderson, 2002). Non-squamate taxa (archosaurs flicting node support; nodes that were strongly supported in and turtles) were removed from the final r8s analysis because the model-based methods were also strongly supported by the inclusion of these phylogenetically very distant taxa parsimony, and nodes with low support were collapsed in the appeared to hinder optimization of rate smoothing levels in parsimony consensus tree (Fig. 1). Relationships amongst preliminary r8s runs. The smoothing parameter was chosen squamate and gekkonid outgroup taxa were consistent with using cross-validation. The initial maximum-likelihood tree previously published studies (Townsend et al., 2004; Hugall was generated in paup* version 4.0b10 (Swofford, 2002) using et al., 2007; Gamble et al., 2008). The diplodactyloid geckos a GTRig substitution model (identified by MrModeltest); formed a strongly supported sister clade (node A) to all other parameters were optimized using an iterative process of sampled geckos (gekkonids, sphaerodactylids and Eublepharis) estimating parameter values, then performing new searches (node I). The monophyly of each of the three diplodactyloid using estimated values until the tree likelihood stabilized and families [Carphodactylidae (node B), Pygopodidae (node C) topology did not change significantly. To maximize similarity and Diplodactylidae (node D)] was strongly supported, with the beast analyses, we used zero offset and upper 95% although their interrelationships were unresolved. confidence interval (CI) values from the beast lognormal Within the diplodactyloids, multiple exemplars from single calibration priors (Table 3) as the upper and lower constraints genera formed strongly supported monophyletic groups with in the r8s analysis. two exceptions: Oedura may be paraphyletic with respect to

Table 4 Mean and range of divergence time estimates for selected gekkotan and calibration nodes obtained using outgroup (squamate and archosaur) calibrations alone, and outgroup calibrations combined with the Pygopus–Paradelma calibration. Values obtained for normal and lognormal priors are shown. All estimates are given in millions of years ago (Ma). Letters alongside major gecko splits correspond to node labels in Fig. 1.

beast posterior distributions: mean [95% highest posterior density] r8s

Lognormal calibration priors Normal priors Outgroup Node Outgroup only Outgroup + Pygopus Outgroup only Outgroup + Pygopus only

Gekkotans (A) Diplodactyloids 71.5 [53.2, 91.2] 79.1 [58.1, 101.7] 77.4 [56.1, 101.8] 83.5 [59.8, 110.1] 55.1 (B) Pygopodidae 31.3 [20.4, 44.9] 39.2 [27.0, 52.4] 33.7 [20.7, 48.6] 38.2 [25.4, 53.5] 23.7 (C) Carphodactylidae 33.4 [20.8, 46.1] 37.6 [22.3, 53.5] 36.4 [21.9, 52.8] 38.8 [23.4, 55.9] 25.7 (D) Diplodactylidae 56.9 [41.0, 73.2] 62.4 [44.6, 80.8] 61.4 [42.4, 81.4] 66.2 [46.6, 87.0] 45.8 (E) Most Australian Diplodactylidae 34.5 [25.1, 44.9] 37.7 [26.8, 49.5] 37.2 [25.7, 49.8] 39.7 [27.5, 53.2] 26.8 (F) Australian Diplodactylidae vs. New 51.2 [37.4, 66.2] 56.6 [40.1, 73.9] 55.9 [37.9, 74.3] 60.3 [41.5, 79.2] 42.9 Caledonia + Pseudothecadactylus (G) Australia vs. New Caledonia 42.8 [27.9, 58.7] 47.4 [29.8, 63.8] 47.5 [30.1, 66.6] 51.0 [32.2, 69.8] 38.5 (H) Diplodactyloids vs. other gekkonids 118.1 [88.9, 147.3] 125.4 [97.4, 155.8] 125.4 [91.3, 162.9] 134.7 [98.7, 172.2] 101.4 (I) Gekkonindae (sensu Han et al., 2004) 101.8 [74.6, 131.7] 108.6 [80.3, 140.4] 109.6 [75.4, 142.1] 116.9 [82.6, 152.7] 91.6 vs. Eublepharis Calibrations Pygopus–Paradelma 10.8 [5.5, 17.3] 20.0 [17.8, 22.7] 11.9 [5.9, 19.2] 17.0 [11.9, 22.3] 9.6 Scincomorphs vs. lacertoids + toxicoferans 172.5 [159.4, 188.2] 174.7 [160.2, 192.8] 183.8 [149.9, 217.5] 189.5 [156.7, 221.7] 170.5 Crown squamates 189.2 [169.3, 212.6] 192.5 [170.4, 216.5] 206.3 [163.1, 250.8] 215.4 [172.4, 260.6] 181.8 Bird–crocodile 239.6 [230.3, 252.8] 239.4 [230.1, 252.3] 221.9 [184.8, 259.4] 226.0 [189.9, 262.7] 271.2 Root 298.9 [281.7, 309.9] 300.8 [285.5, 310.0] 341.5 [268.8, 423.1] 359.3 [280.9, 444.3] NA

NA, not applicable.

2048 Journal of Biogeography 36, 2044–2055 ª 2009 Blackwell Publishing Ltd Gondwanan origins of Australasian geckos

Figure 1 Bayesian all compatible consensus of 40,000 sampled post-burn-in for the three families of Australian diplodactyloid geckos (shown in bold) and gekkotan outgroups. Support values > 0.98 for Bayesian and > 75% for parsimony analyses are shown. Letters at key nodes correspond to those in Table. 4.

Strophurus, and Pygopus is paraphyletic with respect to lengths, topology and clade posteriors), indicating adequate Paradelma. Within the Diplodactylidae, three highly divergent sampling of the posterior distribution. Levels of rate hetero- Australian lineages were recovered: (1) a monotypic Crena- geneity were moderate (coefficients of rate variation 0.53) and dactylus sister to all remaining diplodactylids (node D); (2) the rates were weakly correlated between adjacent branches northern Australian Pseudothecadactylus plus the New (branch rate covariance c. 0.06). The maximum credibility Caledonian radiation (Bavayia + Rhacodactylus) (node G); tree (Figs 2 & S1) retrieved from the combined analyses and (3) all other sampled diplodactylids separated by short (TreeAnnotator version 1.4; Drummond & Rambaut, 2006) internodes (node E). Within this third lineage the small is nearly identical to the MrBayes consensus tree (Fig. 1) in bodied, predominantly terrestrial forms Diplodactylus, Luca- topology and posterior support values. Bayesian and PLRS sium and formed a strongly supported clade and date estimates are presented in Table 4. Both methods yielded the hypothesis that Rhynchoedura is sister to Lucasium broadly similar date estimates, with PLRS giving consistently (Melville et al., 2004; Oliver et al., 2007b) was also supported. shallower dates for all nodes of interest. Among the remaining arboreal species in this third lineage, the monophyly of Strophurus was supported, but other inter- DISCUSSION and intra-generic relationships were unresolved (mainly involving the genus Oedura). Relationships between most Phylogeny genera within the Carphodactylidae and Pygopodidae were also relatively poorly resolved; however, there was strong The major gekkonid relationships recovered here are consis- support for a basal dichotomy between Delma and all other tent with previously published molecular studies (Donnellan pygopodid genera. et al., 1999; Han et al., 2004; Townsend et al., 2004; Gamble et al., 2008). In contrast to previous morphologically derived hypotheses (in which the Eublepharidae were regarded as the Divergence date estimates for the diplodactyloid basal lineage of gekkotans), these studies all indicate that the geckos diplodactyloids are sister to all other extant gekkotans. Our The two combined beast MCMC runs yielded high effective relatively complete sampling of genera provides strong support sample sizes (> 500) for all relevant parameters (e.g. branch for the monophyly of each of the three diplodactyloid families,

Journal of Biogeography 36, 2044–2055 2049 ª 2009 Blackwell Publishing Ltd P. M. Oliver and K. L. Sanders

Figure 2 beast maximum credibility ultra- metric tree for diplodactyloids and gekkotan outgroups. Nodes with posterior support below 0.98 are indicated with an asterisk (*). Australian diplodactyloid lineages are shown in bold. Letters at key nodes correspond to those in Table. 4. Node bars indicate 95% highest posterior age distributions for three strongly supported ingroup divergences that pre-date estimates of the last stages of the break-up of Australia and Antarctica (c. 50– 40 Ma; indicated by the light grey bar): (A) the crown diplodactyloid divergence; (D) the basal split in the Diplodactylidae; (F) the split between the New-Caledonian/ Pseudothecadactylus lineage and the main Australian radiation of diplodactyloids. Divergence date estimates for other major divergences are given in Table. 1. The time-scale is in millions of years ago (Ma). but like previous molecular studies (Han et al., 2004; Gamble variation shown by the clade containing the six remaining et al., 2008) failed to resolve their interrelationships. genera (Greer, 1989). In most other instances intergeneric This study has revealed the existence of the three highly relationships in all three families of diplodactyloid gecko are divergent Australian lineages within the family Diplodactyli- relatively poorly resolved. This is particularly striking within dae. Previous studies that sampled these taxa were based on the Carphodactylidae, the Pygopodidae exclusive of Delma and mitochondrial DNA (mtDNA) (e.g. Melville et al., 2004; the major Australian radiation of arboreal Diplodactylidae Oliver et al., 2007b); substitutional saturation at this rapidly (Oedura and Strophurus). In the two latter clades this poor evolving locus may have impeded resolution of these deep resolution and short internode branches have also been found divergences. Our data indicate that the monotypic genus in studies employing rapidly evolving mitochondrial markers Crenadactylus is the most basal lineage of the family Diplo- (Jennings et al., 2003; Oliver et al., 2007b). While additional dactylidae. Additional sampling of extralimital taxa and and larger datasets are required, these findings are suggestive of additional genes are required to test this hypothesis further. relatively rapid cladogenesis. Likewise Pseudothecadactylus was found to be highly divergent from all other Australian lineages and sister to the New Age and origin of the diplodactyloid geckos Caledonian radiation (as demonstrated by Bauer, 1990, using morphological data). We focus the following discussion on the results of our Jennings et al. (2003) were unable to robustly resolve Bayesian dating analyses because: (1) beast better incorporates generic relationships among pygopods but suggested that the uncertainty in calibration priors and rate smoothing (Drum- comparatively conservative genus Delma is sister to all other mond et al., 2006); and (2) PLRS performs best if rates are genera. Our data strongly support this hypothesis; a result that strongly autocorrelated across the tree (r8s documentation in underlines the high levels of ecological and morphological Sanderson, 2003), whereas our data show weak autocorrelation

2050 Journal of Biogeography 36, 2044–2055 ª 2009 Blackwell Publishing Ltd Gondwanan origins of Australasian geckos

(see branch rate covariance above). However, adopting the these landmasses separated considerably later than 80 Ma, as PLRS results would not change our overall interpretations of previously inferred from vicariance events and used to the biogeographical history of diplodactyloid geckos. calibrate dating studies of diplodactyloid geckos (e.g. Couper Analyses that did not enforce the Pygopus–Paradelma et al., 2000). Our mean estimate of c. 43 Ma (95% HPD 27.9– calibration dated this divergence at 10.8 Ma [95% highest 58.7) for the divergence between New Caledonian diplodacty- posterior density (HPD) 5.5, 17.3], almost half the minimum loids and their Australian sister lineage is not inconsistent with fossil-based age (based on P. hortulanus; Hutchinson, 1998). vicariance under newer models for the opening of the Tasman Recent morphological and phylogenetic reanalysis of this fossil Sea during the Palaeogene (see Gaina et al., 1998; Ladiges & suggests that there is considerable error associated with its Canttril, 2007). Neither does this relatively young date conflict phylogenetic placement (Lee et al., 2009). Enforcing the with an alternative scenario of at least limited dispersal Pygopus–Paradelma calibration only moderately inflated in- between Gondwanan fragments during the Oligocene. group age estimates (Table 4) and we focus our discussion on The Australasian diplodactyloid gecko radiation includes date estimates derived using only the better corroborated multiple lineages with Gondwanan origins that almost cer- external calibrations. tainly diversified before Australia became isolated from other For both external calibration nodes, mean posterior age Gondwanan continents (specifically Antarctica and South estimates were close to the priors: the scincomorphs vs. America). These ancient gecko lineages have persisted through lacertoids + toxicoferans split is dated at 172.5 Ma (95% HPD extreme changes in environment and climate (Byrne et al., 159.4–188.2), and the bird–crocodile split is dated at 239.6 Ma 2008) and are among the oldest radiations of vertebrates (95% HPD 230.3–252.8). The diplodactyloid–gekkonid diver- restricted to the Australasian region – contemporaneous with gence (node H) is dated at 125.4 Ma (95% HPD 97.4–155.8), marsupials (Beck, 2008) and passeriform birds (Barker et al., and is consistent with recent studies using relaxed-clock dating 2004), and significantly exceeded only by myobatrachid frogs and different combinations of data, taxa and fossil calibrations (Roelants et al., 2007). Many of these old Gondwanan clades to those applied in the present study (Hugall et al., 2007; are absent or ecologically depauperate outside the Australasian Gamble et al., 2008). Our date for the diplodactyloid crown region. Most famously, the marsupials and monotremes are group (node A), 71.5 Ma (95% HPD 53.2–91.2), is also highly widely regarded to have persisted and radiated in Australia congruent with the relaxed clock estimate of Gamble et al. through a combination of isolation and the absence of more (2008) and a study that used independent immunological data widespread and competitive groups of placental mammals (King, 1990). The proximity of our dates to those of previous, (Lillegraven et al., 1987). In parallel with this, other families of independently calibrated studies suggests that although our geckos (particularly ), whose ancestors diverged dating analyses are based on two distant external calibrations, from the diplodactyloids at least 100 Ma, dominate gecko the results have not been seriously affected by substantial rate faunas elsewhere in the world but are depauperate in the three variation between the calibration and ingroup taxa. Gondwanan fragments inhabited by diplodactyloids. The diplodactyloid lineage is estimated to have diverged from all other extant geckos before the mid- Comparison with other Australian squamate > 100 Ma (Table 4; see also Gamble et al., 2008). The radiations subsequent diversification of the crown diplodactyloid lineage is estimated to have occurred in the late Cretaceous, c. 70 Ma, The five main lineages of diplodactyloids are the only extant with five lineages diverging by at least 45 Ma. These dates squamate lineages that can convincingly be shown to have been strongly imply diversification in East Gondwana, with present at the time of Australia’s final rifting from Antarctica subsequent persistence of multiple diplodactyloid lineages on (c. 40–30 Ma) (Fig. 2). There are currently more than 800 the newly isolated Australian continent after the final split described species of Australian squamates and all available from Antarctica c. 32 Ma (Lawver & Gahagan, 2003; Wei, evidence (phylogeny, fossils, diversity distributions and molec- 2004). We date the divergence between the New Caledonian ular divergence dates) indicates that these largely stem from 10 diplodactyloids and their Australian sister lineage at c.43Ma to 15 over-water invasions of Australia (Table 5). Almost all of (95% HPD 27.9–58.7). Regardless of whether diplodactyloids these invasions have occurred since the Oligocene, in the last c. reached New Caledonia via dispersal or vicariance (see 30 Myr (including multiple post-Pliocene entries by colubroid Discussion below) this date provides further support for the snakes and gekkonid geckos). However, further data are long-term presence of diplodactyloids in East Gondwana. required for three additional squamate groups. Current data Thus, even in the absence of further biogeographical support do not rule out a Gondwanan origin for Australian Egernia and from the distribution of extralimital sister lineages, our date Eugongylus skinks, although low molecular distances (Austin & estimates for the basal diplodactyloid divergences both within Arnold, 2006; Smith et al., 2007) and the absence of fossils pre- Australia and between Australia and New Caledonia are highly dating the late Oligocene provide no indication of an ancient inconsistent with short-range dispersal from Asia in the last origin. The history and origin of the Australian Scolecophidian 30 Myr. (blindsnake) radiation is virtually unknown. Recent advances in our understanding of the geological The age and isolated history of the diplodactyloids may history of New Caledonia and Australia strongly suggest that explain their high morphological and ecological diversity

Journal of Biogeography 36, 2044–2055 2051 ª 2009 Blackwell Publishing Ltd P. M. Oliver and K. L. Sanders

Table 5 Summary of relaxed-clock age estimates and ancestral geographical origin (where available) for all major radiations of terrestrial Australian squamates. Asian biogeographical origin is inferred for endemic Australian radiations with basally positioned extralimital relatives distributed in Asia.

Time to most recent common Approx. number of Australian squamate clade ancestor (Ma) Biogeographical origin Australian species References

Elapid snakes (oxyuranines) 10 Asian 102 Sanders & Lee (2008) Booid snakes () 35 Asian 13 Rawlings et al. (2008) Agamid lizards 23 Asian 71 Hugall et al. (2008) Varanid lizards NA Asian 27 Ast (2001) Sphenomorphus group skinks 25–30 Asian 232 Rabosky et al. (2007) Skinner et al. (2008) Colubroid snakes Unknown Asian (multiple invasions) 10 Alfaro et al. (2008) Gekkonine geckos Unknown Asian/African (multiple 28 Wilson & Swan (2008), invasions) Greer (1989) Eugongylus group skinks Unknown Uncertain 120 Wilson & Swan (2008) Egernia group skinks Unknown Uncertain 45 Wilson & Swan (2008) Blindsnakes (scolecophidians) Unknown Uncertain 42 Wilson & Swan (2008) Diplodactyloid geckos 71 Gondwanan 121 This paper

relative to other gekkonids. Most notably, pygopods are the Doughty, Aaron Bauer, Steve Cooper and Adam Skinner world’s only limb-reduced geckos and probably evolved in the for advice and comments; Andrew Hugall also provided absence of almost all other extant Australian squamate unpublished sequence data. Bayesian analyses were performed lineages, including limb-reduced and ecologically equivalent using the supercomputer facilities at e-Research SA. We thank groups [Sphenomorphus group skinks (Skinner et al., 2008) Pauline Ladiges and two anonymous reviewers for their and elapid snakes (Sanders & Lee, 2008)]. constructive comments on the original manuscript. In contrast to the deep splits between the five major clades of Australian diplodactyloids, the majority of extant intergen- REFERENCES eric and generic diversity appears to have accumulated relatively recently. Mean crown group age estimates for the Alfaro, M.E., Karns, D.R., Voris, H.K., Brock, C.D. & Stuart, three most diverse Australian lineages (pygopodids, carpho- B.L. (2008) Phylogeny, evolutionary history, and biogeog- dactylids and the core Australian diplodactylids) are c. 30– raphy of the Oriental–Australia rear-fanged water snakes 35 Ma. All three groups differ in ecology, and their relatively (Colubroidea: Homolopsidae) inferred from mitochondrial contemporaneous diversification is suggestive of extrinsic and nuclear sequences. Molecular and Evolu- environmental change at this time. These divergence dates tion, 46, 576–593. are roughly coincident with age estimates for the formation of Archer, M., Arena, R., Bassarova, M., Black, K., Brammall, J., the Antarctic Circumpolar Current (Barker et al., 2007) and Cooke, B., Creaser, P., Crosby, K., Gillespie, A., Godthelp, associated onset of aridification in Australia. This process is H., Gott, M., Hand, S.J., Kear, B., Krikmann, A., Mackness, thought to have been the predominant abiotic driver of B., Muirhead, J., Musser, A., Myers, T., Pledge, N., Wang, Y. evolution and extinction in the Australian biota for the last & Wroe, S. (1999) The evolutionary history and diversity of 30 Myr (Heatwole, 1987; Jennings et al., 2003; Crisp et al., Australian mammals. Australian Journal of Mammalogy, 21, 2004; Rabosky et al., 2007; Byrne et al., 2008). Our observa- 1–45. tions support a picture of an extant Australian biota (and Ast, J.C. (2001) Mitochondrial DNA evidence and evolution in squamate fauna in particular) that is characterized by major (). Cladistics, 17, 211–226. radiations of both Gondwanan and Asian groups no older than Austin, J.J. & Arnold, E.N. (2006) Using ancient DNA to ex- the late Oligocene or early Miocene (e.g. Crisp et al., 2004; plore relationships of extinct and endangered Leiolopisma Beck, 2008; Table 5). skinks (Reptilia: Scincidae) in the Mascarene Islands. and Evolution, 39, 503–511. Barker, F.K., Cibois, A., Schikler, P., Feinstein, J. & Cracraft, J. ACKNOWLEDGEMENTS (2004) Phylogeny and diversification of the largest avian This work was supported by an Australia Pacific Science radiation. Proceedings of the National Academy of Sciences Foundation grant to Paul Doughty, Paul Oliver, Andrew USA, 111, 11040–11045. Hugall, Mark Adams and Mike Lee, and an Australian Barker, P.F., Filippelli, G.M., Florindo, F., Martin, E.E. & Research Council grant to Mike Lee and Mark Hutchinson. Scher, H.D. (2007) Onset and role of the Antarctic cir- We thank Andrew Hugall, Mike Lee, Mark Hutchinson, Paul cumpolar current. Deep Sea Research II, 54, 2388–2398.

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Saint, K.M., Austin, C.C., Donnellan, S.C. & Hutchinson, M.N. SUPPORTING INFORMATION (1998) C-mos, a nuclear marker useful for squamate phylogenetic analysis. Molecular Phylogenetics and Evolution, Additional Supporting Information may be found in the 10, 259–263. online version of this article: Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Figure S1 Maximum credibility beast chronogram of cloning: a laboratory manual, 2nd edn. Cold Spring Harbor relationships between diplodactyloids and both gekkotan and Laboratory Press, Cold Spring Harbor, NY. non-gekkotan outgroups showing (a) support values, (b) mean Sanders, K.L. & Lee, M.S.Y. (2007) Evaluating molecular clock node ages in millions of years, and (c) 95% confidence calibrations using Bayesian analyses with hard and soft intervals for age estimates. bounds. Biology Letters, 3, 275–279. Table S1 GenBank accession details for non-gekkotan Sanders, K.L. & Lee, M.S.Y. (2008) Molecular evidence for a outgroup sequences. rapid late-Miocene radiation of Australasian venomous snakes (, Colubroidea). Molecular Phylogenetics and Please note: Wiley-Blackwell is not responsible for the Evolution, 46, 1165–1173. content or functionality of any supporting materials supplied Sanderson, M.J. (2002) Estimating absolute rates of molecular by the authors. Any queries (other than missing material) evolution and divergence times: a penalized likelihood should be directed to the corresponding author for the approach. Molecular Biology and Evolution, 19, 101–109. article.

2054 Journal of Biogeography 36, 2044–2055 ª 2009 Blackwell Publishing Ltd Gondwanan origins of Australasian geckos

BIOSKETCHES

Paul Oliver is a postgraduate student at the University of Adelaide and South Australian Museum. His research is focused on the origin, evolution and systematics of the Australasian herpetofauna, especially gekkotan lizards and Melanesian frogs.

Kate Sanders is a postdoctoral researcher at the University of Adelaide. Her main research interests concern the evolutionary and conservation biology of squamate reptiles in and Australia.

Editor: Pauline Ladiges

Note added in press: The clade of geckos herein informally referred to as the diplodactyloids, has recently been formally named Pygopoidea, see Vidal & Hedges, 2009.

Journal of Biogeography 36, 2044–2055 2055 ª 2009 Blackwell Publishing Ltd