Open Access Open Access  Restricted Access Subscription or Fee Access

Lizards in pinstripes: morphological and genomic evidence for two new species of scincid lizards within Ctenotus piankai Storr and C. duricola Storr (Reptilia: Scincidae) in the Australian arid zone

DANIEL L. RABOSKY, PAUL DOUGHTY, HUATENG HUANG

Abstract


The scincid lizard genus Ctenotus is one of the most species-rich genera of squamate reptiles, but few molecular phylogenetic studies have been undertaken on the group. Here we assess molecular and morphological variation within C. piankai and C. duricola, an arid-adapted pair of nominate species characterized by a pattern of thin pale longitudinal lines on a dark background that occur primarily in the western deserts and Pilbara region of Australia. We sequenced mitochondrial DNA and genome-wide restriction-site associated DNA (RAD) from geographically widespread samples of these lizard taxa, with particularly dense sampling from the Pilbara region. Phylogenetic analyses of the mitochondrial cytochrome B gene and approximately 5,000 nuclear loci identified four highly divergent lineages within the two taxa. The four genetically-defined populations were concordant with geography and are distinguishable based on multiple morphological and color pattern characters, despite appearing superficially similar in appearance. Despite limited mtDNA exchange between two lineages in the Pilbara, we found no evidence for ongoing gene flow across the nuclear genome. For the western desert lineages, there was no evidence of introgression for either mtDNA or nDNA in our data. To resolve the taxonomy of the group, we redescribe C. piankai and C. duricola, and recognize the two divergent lineages as new species: C. rhabdotus sp. nov., from the south-eastern Kimberley, Ord, Victoria River and northern Tanami Desert regions of Western Australia and the Northern Territory, and C. pallasotus sp. nov., from the western Pilbara and North West Cape regions of Western Australia.

 


Keywords


Reptilia, Kimberley, morphology, North West Cape, Pilbara, RAD sequencing, skink, Sphenomorphinae, Tanami Desert

Full Text:

PDF (7MB)

References


Cogger, H.G. (1992) Reptiles and Amphibians of Australia. 5th Edition. Reed, Frenchs Forest, 704 pp.

Cogger, H.G. (2000) Reptiles and Amphibians of Australia. 6th Edition. Chelsea Green Publishing Co, Sydney, 808 pp.

Cogger, H.G. (2014) Reptiles and Amphibians of Australia. 7th Edition. CSIRO Publishing, Collingwood, xxx + 1033 pp.

Doughty, P., Oliver, P. & Adams, M. (2008) Systematics of stone geckos in the genus Diplodactylus (Reptilia: Diplodactylidae) from northwestern Australia, with a description of a new species from the Northwest Cape, Western Australia. Records of the Western Australian Museum, 24, 247–265.

https://doi.org/10.18195/issn.0312-3162.24(3).2008.247-265

Doughty, P., Pepper, M. & Keogh, J.S. (2010) Morphological and molecular assessment of the Diplodactylus savagei species complex in the Pilbara region, Western Australia, with a description of a new species. Zootaxa, 2393, 33–45.

Doughty, P., Kealley, L. & Melville, J. (2012) Taxonomic assessment of Diporiphora (Reptilia: Agamidae) dragon lizards from the western arid zone of Australia. Zootaxa, 3518, 1–24.

Doughty, P. & Oliver, P.M. (2011) A new species of Underwoodisaurus (Squamata: Gekkota: Carphodactylidae) from the Pilbara region of Western Australia. Zootaxa, 3010, 20–30.

Doughty, P., Kealley, L. & Donnellan, S.C. (2011a) Revision of the Pygmy Spiny-tailed Skinks (Egernia depressa species-group) from western Australia, with descriptions of three new species. Records of the Western Australian Museum, 26, 115–137.

https://doi.org/10.18195/issn.0312-3162.26(2).2011.115-137

Doughty, P., Rolfe, J.K., Burbidge, A.H., Pearson, D.J. & Kendrick, P.G. (2011b) Herpetologial assemblages of the Pilbara biogeographic region, Western Australia: ecological associations, biogeographic patterns and conservations. Records of the Western Australian Museum, 78 (Supplement), 315–341.

https://doi.org/10.18195/issn.0313-122x.78(2).2011.315-341

Doughty, P. & Oliver, P.M. (2011) A new species of Underwoodisaurus (Squamata: Gekkota: Carphodactylidae) from the Pilbara region of Western Australia. Zootaxa, 3010, 20–30.

Doughty, P., Kealley, L., Shoo, L.P. & Melville, J. (2015) Revision of the Australian Pebble-mimic Dragons (Tympanocryptis cephalus: Reptilia: Agamidae) species-group. Zootaxa, 4039 (1), 85–117.

https://doi.org/10.11646/zootaxa.4039.1.3

Drummond, A.J. & Rambaut, A. (2007a) BEAST: Bayesian Evolutionary Analysis Sampling Trees. BMC Evolutionary Biology, 7, 214.

https://doi.org/10.1186/1471-2148-7-214

Drummond, A.J. & Rambaut, A. (2007b) Tracer v1.4. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed 20 June 2017)

Eaton, D.A.R. & Ree, R.H. (2013) Inferring phylogeny and introgression using RADseq data: an example from flowering plants (Pedicularis: Orobanchaceae). Systematic Biology, 62, 689–706.

https://doi.org/10.1093/sysbio/syt032

Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 1–19.

https://doi.org/10.1186/1471-2105-5-113

Edgar, R.C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460–2461.

https://doi.org/10.1093/bioinformatics/btq461

Ehmann, H. (1992) Encyclopedia of Australian animals: reptiles. Angus & Robertson, Sydney, xv + 495.

Goodyear, S.E. & Pianka, E.R. (2011) Spatial and temporal variation in diets of sympatric lizards (Genus Ctenotus) in the Great Victoria Desert, Western Australia. Journal of Herpetology, 45, 265–271.

https://doi.org/10.1670/10-190.1

Gower, J.C. (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika, 53, 325–328.

https://doi.org/10.2307/2333639

Horner, P. (2009) Three new species of Ctenotus (Reptilia: Sauria: Scincidae) from the Kimberley region of Western Australia, with comments on the status of Ctenotus decaneurus yampiensis. Records of the Western Australian Museum, 25, 181–199.
https://doi.org/10.18195/issn.0312-3162.25(2).2009.181-199

Horner, P. & King, M. (1985) A new species of Ctenotus (Scincidae, Reptilia) from the Northern Territory. The Beagle, 2, 143–148.

Hutchinson, M.N., Adams, M. & Fricker, S. (2006) Genetic variation and taxonomy of the Ctenotus brooksi species complex (Squamata: Scincidae). Transactions of the Royal Society of South Australia, 130, 48–65.

https://doi.org/10.1080/3721426.2006.10887047

James, C.D. (1991) Temporal Variation in Diets and Trophic Partitioning by Coexisting Lizards (Ctenotus, Scincidae) in Central Australia. Oecologia, 85, 553–561.

https://doi.org/10.1007/BF00323768

James, C.D. & Shine, R. (2000) Why are there so many coexisting species of lizards in Australian deserts? Oecologia, 125, 127–141.

https://doi.org/10.1007/PL00008884

Kay, G.M. & Keogh, J.S. (2012) Molecular phylogeny and morphological revision of the Ctenotus labillardieri (Reptilia: Squamata: Scincidae) species group and a new species of immediate conservation concern in the southwestern Australian biodiversity hotspot. Zootaxa, 3390, 1–18.

Köhler, G. (2014) Characters of external morphology used in Anolis taxonomy—Definition of terms, advice on usage, and illustrated examples. Zootaxa, 3774 (3), 201–257.

https://doi.org/10.11646/zootaxa.3774.3.1

Maryan, B., Aplin, K.P. & Adams, M. (2007) Two new species of the Delma tincta group (Squamata: Pygopodidae) from northwestern Australia. Records of the Western Australian Museum, 23, 273–305.

https://doi.org/10.18195/issn.0312-3162.23(3).2007.273-305

Maryan, B., Oliver, P.M., Fitch, A.J. & O'Connell, M. (2014) Molecular and morphological assessment of Varanus pilbarensis (Squamata: Varanidae), with a description of a new species from the southern Pilbara, Western Australia. Zootaxa, 3768 (2), 139–158.

https://doi.org/10.11646/zootaxa.3768.2.3

Mecke, S., Doughty, P. & Donnellan, S.C. (2009) A new species of Eremiascincus (Reptilia: Squamata: Scincidae) from the Great Sandy Desert and Pilbara Coast, Western Australia and reassignment of eight species from Glaphyromorphus to Eremiascincus. Zootaxa, 2246, 1–20.

Mecke, S., Doughty, P. & Donnellan, S.C. (2013) Redescription of Eremiascincus fasciolatus (Günther, 1867) (Reptilia: Squamata: Scincidae) with clarification of its synonyms and the description of a new species. Zootaxa, 3701 (5), 473–517.

https://doi.org/10.11646/zootaxa.3701.5.1

Morton, S.R. & James, C.D. (1988) The diversity and abundance of lizards in arid Australia - a new hypothesis. American Naturalist, 132, 237–256.

https://doi.org/10.1086/284847

Oliver, P.M., Adams, M. & Doughty, P. (2010) Molecular evidence for ten species and Oligo-Miocene vicariance within a nominal Australian gecko species (Crenadactylus ocellatus, Diplodactylidae). BMC Evolutionary Biology, 10, 386.

https://doi.org/10.1186/1471-2148-10-386

Oliver, P.M., Adams, M., Lee, M.S.Y., Hutchinson, M.N. & Doughty, P. (2009) Cryptic diversity in vertebrates: molecular data double estimates of species diversity in a radiation of Australian lizards (Diplodactylus, Gekkota). Proceedings of the Royal Society B, Biological Sciences, 276, 2001–2007.

https://doi.org/10.1098/rspb.2008.1881

Oliver, P.M., Couper, P.J. & Pepper, M. (2014) Transitions between monsoonal and arid biomes revealed by systematic revision of a complex of Australian geckos (Diplodactylus: Diplodactylidae). PLOS ONE, 9, e111895.

https://doi.org/10.1371/journal.pone.0111895

Pepper, M., Doughty, P., Hutchinson, M.N. & Keogh, J.S. (2011) Ancient drainages divide cryptic species in Australia’s arid zone: Morphological and multi-gene evidence for four new species of Beaked Geckos (Rhynchoedura). Molecular Phylogenetics & Evolution, 61, 810–822.

https://doi.org/10.1016/j.ympev.2011.08.012

Pepper, M., Doughty, P. & Keogh, J.S. (2006) Molecular phylogeny and phylogeography of the Australian Diplodactylus stenodactylus (Gekkota; Reptilia) species-group based on mitochondrial and nuclear genes reveals an ancient split between Pilbara and non-Pilbara D. stenodactylus. Molecular Phylogenetics and Evolution, 41, 539–555.

https://doi.org/10.1016/j.ympev.2006.05.028

Pepper, M., Doughty, P. & Keogh, S.J. (2013) Synthesis: Geodiversity and endemism in the iconic Australian Pilbara region: a review of landscape evolution and biotic response in an ancient refugium. Journal of Biogeography, 40, 1225–1239.

https://doi.org/10.1111/jbi.12080

Peterson, B.K., Weber, J.N., Kay, E.H., Fisher, H.S. & Hoekstra, H.E. (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLOS ONE, 7, e37135.

https://doi.org/10.1371/journal.pone.0037135

Pianka, E.R. (1969) Sympatry of desert lizards (Ctenotus) in western Australia. Ecology, 50, 1012–1030.

https://doi.org/10.2307/1936893

Pianka, E.R. (1972) Zoogeography and speciation of Australian desert lizards: an ecological perspective. Copeia, 1972, 127–145.

https://doi.org/10.2307/1442789

Pianka, E.R. (1986) Ecology and Natural History of Desert Lizards. Princeton University Press, Princeton, 222 pp.

R Core Team. (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: https://www.R-project.org/ (accessed 20 June 2017)

Rabosky, D.L., Cowan, M.A., Talaba, A.L. & Lovette, I.J. (2011) Species interactions mediate phylogenetic community structure in a hyperdiverse lizard assemblage from arid Australia. American Naturalist, 178, 579–595.

https://doi.org/10.1086/662162

Rabosky, D.L., Donnellan, S.C., Grundler, M. & Lovette, I.J. (2014a) Analysis and visualization of complex macroevolutionary dynamics: an example from Australian scincid lizards. Systematic Biology, 63, 610–627.

https://doi.org/10.1093/sysbio/syu025

Rabosky, D.L., Hutchinson, M.N., Donnellan, S.C., Talaba, A.L. & Lovette, I.J. (2014b) Phylogenetic dissasembly of species boundaries in a widespread group of Australian skinks (Scincidae: Ctenotus). Molecular Phylogenetics and Evolution, 77, 71–82.

https://doi.org/10.1016/j.ympev.2014.03.026

Rabosky, D.L., Reid, J., Cowan, M.A. & Foulkes, J. (2007) Overdispersion of body size in Australian desert lizard communities at local scales only: no evidence for the Narcissus effect. Oecologia, 154, 561–570.

https://doi.org/10.1007/s00442-007-0849-1

Rabosky, D. L.,Talaba, A.L., Donnellan, S.C. & Lovette, I.J. (2009) Molecular evidence for hybridization between two Australian desert skinks, Ctenotus leonhardii and Ctenotus quattuordecimlineatus (Scincidae: Squamata). Molecular Phylogenetics and Evolution, 53, 368–377.

https://doi.org/10.1016/j.ympev.2009.06.020

Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.

https://doi.org/10.1093/bioinformatics/btl446

Storr, G.M. (1964) Ctenotus, a new generic name for a group of Australian skinks. Western Australian Naturalist, 9, 84–85.

Storr, G.M. (1969) The genus Ctenotus (Lacertilia: Scincidae) in the Eastern Division of Western Australia. Journal of the Royal Society of Western Australia, 51, 97–109.

Storr, G.M. (1975) The genus Ctenotus (Lacertilia: Scincidae) in the Kimberley and North-west Divisions of Western Australia. Records of the Western Australian Museum, 3, 209–243.

Storr, G.M., Smith, L.A. & Johnstone, R.E. (1981) Lizards of Western Australia: I. Skinks. Western Australian Museum, Perth, 200 pp.

Storr, G.M., Smith, L.A. & Johnstone, R.E. (1999) Lizards of Western Australia. I. Skinks: 2nd edition. Western Australian Museum, Perth, 291 pp.

Uetz, P. & Josek, J. (2016) The Reptile Database. Available from: http://www.reptile-database.org (accessed 20 June 2017)

Wagner, C.E., Keller, I., Wittwer, S., Selz, O.M., Mwaiko, S., Greuter, L., Sivasunder, A. & Seehausen, O. (2013) Genome-wide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Molecular Ecology, 22, 787–798.

https://doi.org/10.1111/mec.12023

Wilson, S. & Swan, G. (2003) A Complete Guide to Reptiles of Australia. Reed Natural History, Chatswood, 480 pp.

Wilson, S. & Swan, G. (2014) A Complete Guide to Reptiles of Australia. 3rd Edition. New Holland, Chatswood, 592 pp.

Wilson, S.K. & Knowles, D.G. (1988) Australia’s Reptiles: a Photographic Reference to the Terrestrial Reptiles of Australia. Williams Collins, Sydney, 447 pp.




DOI: http://dx.doi.org/10.11646/zootaxa.4303.1.1

Refbacks

  • There are currently no refbacks.


 
ISSN 1175-5326 (Print Edition) & ISSN 1175-5334 (Online Edition)
Published by Magnolia Press, Auckland, New Zealand