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A Molecular Phylogenetic Study of Ecological Diversification in the Australian Lizard Genus Ctenophorus

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A Molecular Phylogenetic Study of Ecological Diversification in the Australian Lizard Genus Ctenophorus JEZ Mde 2035 JOURNAL OF EXPERIMENTAL ZOOLOGY (MOL DEV EVOL) 291:339–353 (2001) A Molecular Phylogenetic Study of Ecological Diversification in the Australian Lizard Genus Ctenophorus JANE MELVILLE,* JAMES A. SCHULTE II, AND ALLAN LARSON Department of Biology, Washington University, St. Louis, Missouri 63130 ABSTRACT We present phylogenetic analyses of the lizard genus Ctenophorus using 1,639 aligned positions of mitochondrial DNA sequences containing 799 parsimony-informative charac- ters for samples of 22 species of Ctenophorus and 12 additional Australian agamid genera. Se- quences from three protein-coding genes (ND1, ND2, and COI) and eight intervening tRNA genes are examined using both parsimony and maximum-likelihood analyses. Species of Ctenophorus form a monophyletic group with Rankinia adelaidensis, which we suggest placing in Ctenophorus. Ecological differentiation among species of Ctenophorus is most evident in the kinds of habitats used for shelter. Phylogenetic analyses suggest that the ancestral condition is to use burrows for shelter, and that habits of sheltering in rocks and shrubs/hummock grasses represent separately derived conditions. Ctenophorus appears to have undergone extensive cladogenesis approximately 10–12 million years ago, with all three major ecological modes being established at that time. J. Exp. Zool. (Mol. Dev. Evol.) 291:339–353, 2001. © 2001 Wiley-Liss, Inc. The agamid lizard genus Ctenophorus provides ecological categories based on whether species abundant opportunity for a molecular phylogenetic shelter in rocks, burrows, or vegetation. Eight spe- study of speciation and ecological diversification. cies of Ctenophorus are associated with rocks: C. Agamid lizards show a marked radiation in Aus- caudicinctus, C. decresii, C. fionni, C. ornatus, C. tralia, where there are 64 recognized species in rufescens, C. tjantjalka, C. vadnappa, and C. 13 genera (Cogger, 2000). Within this group, the yinnietharra. Eight species spend much of their large endemic genus Ctenophorus contains 23 active time on open ground of sand plains or sand largely terrestrial species, and is widespread dunes covered with shrubs or hummock grasses throughout the continent, particularly in semi-arid and flee to these shrubs and grass hummocks: C. to arid areas. Monophyly of Ctenophorus has not cristatus, C. femoralis, C. fordi, C. isolepis, C. been established with certainty, and phylogenetic maculatus, C. mckenziei, C. rubens, and C. scut- relationships among species within this genus are ulatus. Pianka (’71, personal communication) de- largely unknown. Microcomplement fixation of al- scribes C. cristatus and C. scutulatus as moving bumin (Baverstock and Donnellan, ’90), chromo- and foraging in open spaces between plants, and somal and immunogenetic data (King, ’90), and in a 15-month study by Pianka (’71), they were mitochondrial DNA sequences (Honda et al., 2000; never observed to use burrows during their daily Macey et al., 2000) have been used to evaluate activity. Ctenophorus mckenziei is very similar to higher-level phylogenetic relationships within C. scutulatus in habitat and morphology, differ- Agamidae and have included single species of ing only in adult size and subtle color modifica- Ctenophorus, but no previous molecular study has tions (Storr et al., ’83; Peterson et al., ’94). examined relationships within this genus. Previous Consequently, we have included C. cristatus, C. studies have divided Ctenophorus into species scutulatus, and C. mckenziei in the shrub/grass groups based primarily on ecological and morpho- logical data (Moody, ’80; Wilson and Knowles, ’88; Grant sponsor: National Science Foundation; Grant number: DEB- Greer, ’89), but the phylogenetic significance of 9318642; Grant sponsor: National Science Foundation; Grant num- these groupings is uncertain. ber: DEB-9726064; Grant sponsor: National Science Foundation; Grant number: DEB-9982736; Grant sponsor: Australian Research Ecological differentiation among species of Council; Grant number: ARC00104045. Ctenophorus is most evident in the kinds of habi- *Correspondence to: Jane Melville, School of Biological Sciences (A08), University of Sydney, Sydney NSW 2006, Australia. tats that lizards use for shelter. Greer (’89) sug- E-mail: [email protected] gested that Ctenophorus falls into three distinct Received 7 February 2001; Accepted 11 June 2001 © 2001 WILEY-LISS, INC. 340 J. MELVILLE ET AL. dwelling group. The final group includes species species Physignathus cocincinus and Papua New that dig burrows in which they shelter from Guinean species Hypsilurus dilophus are also in- weather and predators: C. clayi, C. gibba, C. cluded as outgroups based on results of Macey et maculosus, C. nuchalis, C. pictus, C. reticulatus, al. (2000); other species of Hypsilurus (not sampled) and C. salinarum. Extensive work on C. macu- occur in Australia (Cogger, 2000). losus by Mitchell (’73) indicates that this is a bur- rowing species, sheltering below the crusty salt- MATERIALS AND METHODS layer of Lake Eyre, South Australia. Specimen information A major evolutionary question is whether these ecological categories represent stable characteris- Museum numbers and localities of voucher tics of ancient clades, or labile features that evolved specimens from which DNA was extracted and repeatedly in parallel among different communi- GenBank accession numbers are provided below. ties. Recent phylogenetic studies of the lizard ge- Acronyms are SAM for the South Australian Mu- nus Anolis in the Caribbean demonstrate the latter seum, Adelaide, Australia and ANWC for the Aus- situation, in which habitat specialists that share tralian National Wildlife Collection, CSIRO, characteristic morphological features appear to Canberra, Australia. Ctenophorus caudicinctus: have evolved in parallel on different islands (Losos SAMAR42752, GenBank# AF375623, Winton, et al., ’98; Jackman et al., ’99). The evolutionary Queensland. Ctenophorus clayi: SAMAR48593, history of anoles demonstrates ancient evolution- GenBank# AF375620, 12.2 km northwest of Mt. ary radiations, in which numerous lineages split Cheesman, South Australia. Ctenophorus crist- from a common ancestral population in a time in- atus: SAMAR31851, GenBank# AF375622, 17 km terval that was short relative to the subsequent east southeast of Mt. Christie Siding, South Aus- evolutionary history of the group (Jackman et al., tralia. Ctenophorus femoralis: SAMAR22803, ’99). Rapid radiation of evolutionary lineages com- GenBank# AF375627, 12 km south of Barradale, bined with highly labile morphological characters Western Australia. Ctenophorus fionni: SAMAR- makes phylogenetic reconstruction particularly dif- 38263, GenBank# AF375638, South Pearson, ficult. We suspect that this same combination of South Australia. Ctenophorus fordi: SAMAR- factors may be evident in the evolutionary diver- 31886, GenBank# AF375626, Mt. Finke, South sification of Ctenophorus, which is still in an early Australia. Ctenophorus gibba: SAMAR45990, phase of ecomorphological study. GenBank# AF375625, William Creek Rd., 20 km We present a molecular phylogenetic study of east of Coober Pedy, South Australia. Ctenophorus 22 of the 23 recognized species of Ctenophorus (all isolepis: SAMAR26194, GenBank# AF375629, 25 species except C. yinnietharra) to test the hypoth- km southwest of Mabel Creek homestead, South esis that ecological categories constitute phyloge- Australia. Ctenophorus maculatus: SAMAR29397, netic groups, and to estimate ages of diversification GenBank# AF375628, 34 km south of Denham, among species of Ctenophorus. Sequences re- Western Australia. Ctenophorus maculosus: SAM- ported here include a 1,799 base-pair segment of AR25909, GenBank# AF375621, Lake Eyre, South the mitochondrial genome extending from the pro- Australia. Ctenophorus mckenziei: SAMAR32266, tein-coding gene ND1 (subunit one of NADH de- GenBank# AF375631, Mitcherie Rockhole, South hydrogenase), through the genes encoding tRNAGln, Australia. Ctenophorus nuchalis: SAMAR42726, tRNAIle, tRNAMet, ND2 (NADH dehydrogenase sub- GenBank# AF375633, 18 km north of Muttaburra, unit two), tRNATrp, tRNAAla, tRNAAsn, tRNACys, Queensland. Ctenophorus ornatus: SAMAR29487, tRNATyr, to the protein-coding gene, COI (subunit GenBank# AF375624, Lort R., Western Austra- I of cytochrome c oxidase). These sequences are lia. Ctenophorus pictus: SAMAR28208, GenBank# homologous to those used in earlier phylogenetic AF375635, 73 km north of Oodnadatta, South Aus- studies of acrodont lizards (Macey et al., 2000; tralia. Ctenophorus reticulatus: SAMAR29373, McGuire and Heang, 2001), permitting phyloge- GenBank# AF375634, Nanga Rubbish Dump, netic comparisons of Ctenophorus species to other Western Australia. Ctenophorus rubens: SAMAR- Australian agamid genera, including Lophogn- 22844, GenBank# AF375630, 12 km south of athus, Amphibolurus, Chlamydosaurus, Caim- Barradale, Western Australia. Ctenophorus rufe- anops, Diporiphora, Pogona, Tympanocryptis, scens: SAMAR28276, GenBank# AF375636, Near Rankinia, Arua, Chelosonia, Physignathus, and Victory Well, South Australia. Ctenophorus salin- Moloch. This sampling allows an effective test of arum: SAMAR18178, GenBank# AF375640, north monophyly for Ctenophorus. The southeast Asian of Serpentine Lakes, South Australia. Ctenophorus EVOLUTION AND DIVERSIFICATION IN CTENOPHORUS 341 scutulatus: SAMAR29402, GenBank# AF375632, cations. Amplified products were purified on 2.5% 1 km south of Wanoo, Western Australia. Cteno- Nusieve GTG agarose gels
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