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Type: Article
Published: 2018-12-04
Page range: 151–185
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A re-description of Cyrtodactylus chrysopylos Bauer (Squamata: Gekkonidae) with comments on the adaptive significance of orange coloration in hatchlings and descriptions of two new species from eastern Myanmar (Burma)

Herpetology Laboratory, Department of Biology, La Sierra University, 4500 Riverwalk Parkway, Riverside, California 92515, USA.
Department of Ecology and Evolutionary Biology and Biodiversity Institute, University of Kansas, Dyche Hall, 1345 Jayhawk Blvd, Lawrence, Kansas 66045-7561, USA.
Myanmar Environment Sustainable Conservation, Yangon, Myanmar.
Myanmar Environment Sustainable Conservation, Yangon, Myanmar.
Herpetology Laboratory, Department of Biology, La Sierra University, 4500 Riverwalk Parkway, Riverside, California 92515, USA.
Herpetology Laboratory, Department of Biology, La Sierra University, 4500 Riverwalk Parkway, Riverside, California 92515, USA.
School of Biological Sciences, Universiti Sains Malaysia, 11800 Minden, Penang, Malaysia.
Reptilia Burma phylogenetic taxonomy systematics color pattern Bent-toed Gecko gecko vision

Abstract

The karstic foothills and hilly western edge of the Shan Plateau of eastern Myanmar continue to be sources of discovery for new species of the gekkonid genus Cyrtodactylus. Two new karst-associated species within this unique landscape from Mandalay Region—C. aunglini sp. nov. from the Kyauk Nagar Cave and C. myaleiktaung sp. nov. from Mya Leik Taung Mountain—are described on the basis of color pattern, morphology, and genetics. A molecular phylogeny of the C. gansi group (defined herein) based on 1481 base pairs of the mitochondrial gene ND2 and its flanking tRNAs place C. aunglini sp. nov. as the sister species to C. gansi and C. myaleiktaung sp. nov. as the sister species of C. chrysopylos. A new population of C. chrysopylos from a boulder-strewn, karstic ridge near the village of Yane, Shan State at an elevation 951 m is reported here. Genetic and geographic variation as well as differences in natural history between it and the lowland cave population of C. chrysopylos from the type locality in the Panlaung-Pyadalin Cave Wildlife Sanctuary, Shan State at 303 m are discussed. Hatchlings of the new population from Yane are nearly uniformly bright-orange in color. We provide evidence in support of a hypothesis claiming this color functions as a mechanism for crypsis during low levels of illumination and is not involved in intraspecific communication.

 

References

  1. Acinas, S.G., Klepac-Ceraj, V., Hunt, D.E., Pharino, C., Ceraj, I., Distel, D.L. & Polz, M.F. (2004) Fine-scale phylogenetic architecture of a complex bacterial community. Nature, 430, 551–554.
    https://doi.org/10.1038/nature02649

    Agarwal, I, Bauer, A.M., Jackman, T.R. & Karanth, K.P. (2014) Insights into Himalayan biogeography from geckos: a molecular phylogeny of Cyrtodactylus (Squamata: Gekkonidae). Molecular Phylogenetics and Evolution, 80, 145–155.
    https://doi.org/10.1016/j.ympev.2014.07.018

    Barraclough, T.G., Birky, C.W. Jr. & Burt, A. (2003) Diversification in sexual and asexual organisms. Evolution, 57, 2166–2172.
    https://doi.org/10.1554/02-339

    Bauer, A.M. (2003) Descriptions of seven new Cyrtodactylus (Squamata: Gekkonidae) with a key to the species of Myanmar (Burma). Proceedings of the California Academy of Sciences, 54, 463–498.

    Brandley, M.C., Wang, Y., Guo, X., Nieto Montes de Oca, A., Feria-Ortiz, M., Hikida, T. & Ota, H. (2011) Accommodating heterogenous rates of evolution in molecular divergence dating methods: an example using intercontinental dispersal of Plestiodon (Eumeces) lizards. Systematic Biology, 60, 3–15.
    https://doi.org/10.1093/sysbio/syq045

    Cangelosi, R. & Goriely, A. (2007) Component retention in principal component analysis with application of cDNA microarray data. Biology Direct, 2, 2.
    https://doi.org/10.1186/1745-6150-2-2

    Carranza, S., Arnold, E.N., Mateo, J. & Lopez-Jurado, L. (2000) Long-distance colonization and radiation in gekkonid lizards, Tarentola (Reptilia: Gekkonidae), revealed by mitochondrial DNA sequences. Proceedings of the Royal Society B: Biological Sciences, 267, 637–649.
    https://doi.org/10.1098/rspb.2000.1050

    Clements, R., Sodhi, N.S., Schilthuizen, M. & Ng, P.K.L. (2006) Limestone karsts of Southeast Asia: imperiled arks of biodiversity. BioScience, 56, 733–742.
    https://doi.org/10.1641/0006-3568(2006)56[733:lkosai]2.0.co;2

    Coyne, J.A. & Orr, H.A. (1998) The evolutionary genetics of speciation. Philosophical Transactions of the Royal Society of London B, 353, 287–305.
    https://doi.org/0.1098/rstb.1998.0210

    Crescitelli, F., Dartnall, H.J. & Loew, E.R. (1977) The gecko visual pigments: A microspectrophotometric study. The Journal of Physiology, 268, 559–573.
    https://doi.org/10.1113/jphysiol.1977.sp011872

    Day, M.J. & Urich, P.B. (2000) An assessment of protected karst landscapes in Southeast Asia. Cave and Karst Science, 27, 61–70.

    Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415.
    https://doi.org/10.1111/j.1095-8312.2005.00503.x

    De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886.
    https://doi.org/10.1080/10635150701701083

    Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.
    https://doi.org/10.1093/molbev

    Fisher-Reid, M.C. & Wiens, J.J. (2011) What are the consequences of combining nuclear and mitochondrial data for phylogenetic analysis? Lessons from Plethodon salamanders and 13 other vertebrate clades. BMC Evolutionary Biology, 11, 1–20.
    https://doi.org/10.1186/1471-2148-11-300

    Fontaneto, D., Herniou, E.A., Boschetti, C., Caprioli, M., Melone, G., Ricci, C. & Barraclough, T.G. (2007) Independently evolving species in asexual bdelloid rotifers. PLoS Biology, 5, e87.
    https://doi.org/10.1371/journal.pbio.0050087

    Francis, C.M. (2008) A Field Guide to the Mammals of South-East Asia. New Holland Publishers, London, 392 pp.
    https://doi.org/10.1644/08-mamm-r-336.1

    Frost, D.R. & Kluge, A.G. (1994) A consideration of epistemology in systematic biology, with special reference to species. Cladistics, 10, 259–294.
    https://doi.org/10.1111/j.1096-0031.1994.tb00178.x

    Fujisawa, T. & Barraclough, T.G. (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology, 62, 707–724.
    https://doi.org/10.1093/sysbio/syt033

    Grismer, L.L. (2017a) Herpetofaunal survey of the Pyinyaung Limestone Mining Area. Unpublished report for Flora & Fauna International, Yangon, 12 pp.

    Grismer, L.L. (2017b) Herpetofunal survey of limestone habitats in the Salween Basin, Kayin and Mon States. Unpublished report for Flora & Fauna International, Yangon, 19 pp.

    Grismer, L.L. (2017c) Herpetofaunal survey of Mount Popa and limestone habitats in Kayah and Shan States. Unpublished report for Flora & Fauna International, Yangon, 29 pp.

    Grismer, L.L. (2018) Gecko Surveys of the Panlaung-Pyadalin Cave Wildlife Sanctuary and adjacent areas in Shan State and Mandalay Region. Unpublished report for Flora & Fauna International, Yangon, 17 pp.

    Grismer, L.L. & Norhayati, A. (2008) A new insular species of Cyrtodactylus

    (Squamata: Gekkonidae) from the Langkawi Archipelago, Kedah, Peninsular Malaysia. Zootaxa, 1924, 53–68.

    Grismer, L.L., Wood Junior, P.L., Anuar, S., Grismer, M.S., Muin, M.A., Davis, H.R., Aguilar, C., Klabacka, R., Cobos, A.J., Aowphol, A. & Sites Junior, J. (2016) Two new bent-toed geckos of the Cyrtodactylus pulchellus complex from Peninsular Malaysia and multiple instances of convergent adaptation to limestone forest ecosystems. Zootaxa, 4105, 401–429.
    https://doi.org/10.11646/zootaxa.4105.5.1

    Grismer, L.L., Wood Junior, P.L., Anuar, S., Muin, M.A., Quah, E.S.H., McGuire, J.A., Brown, R.A., Ngo, V.T. & Pham, H.T. (2013) Integrative taxonomy uncovers high levels of cryptic species diversity in Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) and the description of a new species from Peninsular Malaysia. Zoological Journal of the Linnean Society, 169, 849–880.
    https://doi.org/10.1111/zoj.12064

    Grismer, L.L., Wood Junior, P.L., Quah, E.S.H., Shahrul, A., Muin, M.A., Sumontha, M., Norhayati, A., Bauer, A.M., Wangkulangkul, S., Grismer, J.L. & Pauwels, O.S.G. (2012) A phylogeny and taxonomy of the Thai-Malay Peninsula bent-toed geckos of the Cyrtodactylus pulchellus complex (Squamata: Gekkonidae): combined morphological and molecular analyses with descriptions of seven new species. Zootaxa, 3520, 1–55.

    Grismer, L.L., Wood Junior, P.L., Quah, E.S.H., Thura, M.K., Murdoch, M.L., Grismer, M.S., Herr, M.W., Espinoza, R.E., Brown, R.M. & Lin, A. (2018b) Phylogenetic taxonomy of the Cyrtodactylus peguensis group (Reptilia: Squamata: Gekkonidae) with descriptions of two new species from Myanmar. PeerJ. [submitted]

    Grismer, L.L., Wood, Jr., P.L., Thura, M.K., Zin, T., Quah, E.S.H., Murdoch, M.L., Grismer, M.S., Herr, M.W., Lin, A. & Kyaw, H. (2018d) Three more new species of Cyrtodactylus (Squamata: Gekkonidae) from the Salween Basin of eastern Myanmar underscores the urgent need for the conservation of karst habitats. Journal of Natural History, 52, 1243–1294.
    https://doi.org/10.1080/00222933.2018.1449911

    Grismer, L.L., Wood Junior, P.L., Thura, M.K., Quah, E.S.H., Grismer, M.S., Murdoch, M.L., Espinoza, R.E. & Lin, A. (2018c) A new Cyrtodactylus Gray (Squamata, Gekkonidae) from the Shan Hills and the biogeography of bent-toed geckos from eastern Myanmar. Zootaxa, 4446 (4), 477–500.
    https://doi.org/10.11646/zootaxa.4446.4.4

    Grismer, L.L., Wood. Jr., P.L., Myint Kyaw Thura, Zin, T., Quah, E.S.H., Murdoch, M.L., Grismer, M.S., Lin, A., Kyaw, H. & Ngwe, L. (2018a) Twelve new species of Cyrtodactylus Gray (Squamata: Gekkonidae) from isolated limestone habitats in east-central and southern Myanmar demonstrate high localized diversity and unprecedented microendemism. Zoological Journal of the Linnean Society, 182, 862–959.
    https://doi.org/10.1093/zoolinnean/zlx057

    Heinicke, M.P., Greenbaum, E., Jackman, T.R. & Bauer, A.M. (2011) Phylogeny of a trans-Wallacean radiation (Squamata, Gekkonidae, Gehyra) supports a single early colonization of Australia. Zoologica Scripta, 40, 584–602.
    https://doi.org/10.1111/j.1463-6409.2011.00495.x

    Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Le, S.V. (2017) UFBoot2: Improving the Ultrafast Bootstrap Approximation. Molecular Biology and Evolution, 35, 518–522.
    https://doi.org/10.1093/molbev/msx281

    Huelsenbeck, J.P., Ronquist, F., Nielsen, R. & Bollback, J.P. (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310–2314.
    https://doi.org/10.1126/science.1065889

    Jackson, D.A. (1993) Stopping rules in principle component analysis: a comparison of heuristical and statistical approaches. Ecology, 74, 2204–2214.
    https://doi.org/10.2307/1939574

    Jombart, T., Devillard, S. & Balloux, F. (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics, 11, 94.
    https://doi.org/10.1186/1471-2156-11-94

    Katoh, M., & Kuma, M. (2002) MAFTT: a novel method for rapid sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066.
    https://doi.org/10.1093/nar/gkf436

    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.
    https://doi.org/10.1093/bioinformatics/bts199

    Kelber, A. & Lind, O. (2010) Limits of colour vision in dim light. Ophthalmic and Physiological Optics, 30, 454–459.
    https://doi.org/10.1111/j.1475-1313.2010.00721.x

    Kelber, A. & Roth, L.S.V. (2006) Nocturnal colour vision – not as rare as we might think. Journal of Experimental Biology, 209, 781–788.
    https://doi.org/10.1242/jeb.02060

    Knowles, L.L. & Carstens, B.C. (2007) Delimiting species without monophyletic gene trees. Systematic Biology, 56, 887–895.
    https://doi.org/10.1080/10635150701701091

    Kojima, D., Okano, T., Fukada, Y., Shichida, Y., Yoshizawa, T. & Ebrey, T. (1992) Cone visual pigments are present in gecko rod cells. Proceedings of the National Academy of Sciences, 89, 6841–6845.
    https://doi.org/10.1073/pnas.89.15.6841

    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870-–1874.
    https://doi.org/10.1093/molbev/msw054

    Leaché, A.D., Koo, M.S., Spencer, C.L., Papenfuss, T.J., Fisher, R.N. & McGuire, J.A. (2009) Quantifying ecological, morphological, and genetic variation to delimit species in the coast horned lizard species complex (Phrynosoma). Proceedings of the National Academy of Sciences of the United States, 106, 12418–12423.
    https://doi.org/10.1073/pnas.0906380106

    Lim, G.S., Balke, M. & Meier, R. (2012) Determining species boundaries in a world full of rarity: singletons, species delimitation methods. Systematic Biology, 61, 165–169.
    https://doi.org/10.1093/sysbio/syr030

    Loew, E.R., Govardovskii, V.I., Röhlich, P. & Szél, A. (1996) Microspectrophotometric and immunocytochemical identification of ultraviolet photoreceptors in geckos. Visual Neuroscience, 13, 247–256.
    https://doi.org/10.1017/s0952523800007483

    Macey, J.J., Larson, A., Ananjeva, N.B., Fang, Z. & Papenfuss, T.J. (1997) Two novel gene orders and the role of light-strand replication in rearrangement of the vertebrate mitochondrial genome. Molecular Biology and Evolution, 14, 91–104.
    https://doi.org/10.1093/oxfordjournals.molbev.a025706

    Maddison, W.P. & Maddison, D.R. (2015) Mesquite: a modular system for evolutionary analysis. Version 3.04. Available from: http://mesquiteproject.org (accessed 10 October 2018)

    Mahony, S. (2009) Taxonomic status of Cyrtodactylus khasiensis tamaiensis (Smith, 1940) and description of a new species allied to C. chrysopylos Bauer, 2003 from Myanmar (Reptilia: Gekkonidae). Hamadryad, 34, 62–74.

    Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, LA, pp. 1–8.
    https://doi.org/10.1109/GCE.2010.5676129

    Neitz, J. Geist, T. & Jacobs, G.H. (1989) Color vision in dogs. Visual Neuroscience, 3, 119–125.
    https://doi.org/10.1017/s0952523800004430

    Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274.
    https://doi.org/10.1093/molbev/msu300

    Pokorny, J., Lutze, M., Cao, D. & Zele, A.J. (2006) The color of night: surface color perception under dim light. Visual Neuroscience, 23, 525–530.
    https://doi.org/10.1017/s0952523806233492

    Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P, Hazell, S., Kamoun, S., Sumlin, W.D. & Vogler, A.P. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55, 595–609.
    https://doi.org/10.1080/10635150600852011

    R Core Team. (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. Available from: http://www.R-project.org (accessed 15 December 2016)

    Rambaut, A. & Drummond, A.J. (2013) TreeAnnotator. Version 1.8.0 MCMC Output Analysis.
    Institute of Evolutionary Biology, University of Edinburgh, Department of Computer Science, University of Auckland.

    Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer. Version 1.6. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed 10 October 2018)

    Röll, B. (2000) Gecko vision: visual cells, evolution, and ecological constraints. Journal of Neurocytology, 29, 471–484.
    https://doi.org/10.1023/A:1007293511912

    Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, B., Larget, L., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) Mr. Bayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.
    https://doi.org/10.1093/sysbio/sys029

    Roth, L.S. & Kelber, A. (2004) Nocturnal colour vision in geckos. Proceedings of the Royal Society of London B: Biological Sciences, 271, 485–487. [S485–S487]
    https://doi.org/10.1098/rsbl.2004.0227

    Roth, L.S.V., Lundström, L., Kelber, A., Kröger, R.H.H. & Unsbo, P. (2009) The pupils and optical systems of gecko eyes. Journal of Vision, 9, 1–11.
    https://doi.org/10.1167/9.3.27

    Sabaj, M.H. (2016) Standard symbolic codes for institutional resource collections in herpetology and ichthyology: an Online Reference. Version 6.5 (16 August 2016). American Society of Ichthyologists and Herpetologists, Washington, D.C. Electronically accessible. Available from: http://www.asih.org (accessed 10 October 2018)

    Schmitz, L. & Higham, T.E. (2018) Non-uniform evolutionary response to gecko eye size to changes in diel activity patterns. Biology Letters, 14, 21180064.
    https://doi.org/10.1098/rsbl.2018.0064

    Shaw, K.L. (2012) Conflict between nuclear and mitochondrial DND phylogenies of a recent species radiation: what DNA reveals and conceals about modes of speciation in Hawaiian crickets. Proceedings of the National Academy of Sciences of the United States, 99, 16122–16127.
    https://doi.org/10.1073/pnas.242585899

    Sukumaran, J. & Knowles, L.L. (2017) Multispecies coalescent delimits structure, not species. Proceedings of the National Academy of Sciences of the United States, 114, 1607–1612.
    https://doi.org/10.1073/pnas.1607921114

    Sumner, P. & Mollon, J.D. (2002) Colors of primate pelage and skin: objective assessment of conspicuousness. American Journal of Primatology, 59, 67–91.
    https://doi.org/10.1002/ajp.10066

    Toews, D.P.L.J. & Brelsford, A. (2012) The biogeography of nuclear discordance in animals. Molecular Ecology, 21, 3907–3930.
    https://doi.org/10.1111/j.1365-294x.2012.05664.x

    Uetz, P., Freed, P. & Hošek, J. (Eds.) (2018) The Reptile Database. Available from: http://www.reptile-database.org (accessed 5 April 2018)

    Warrant E.J. & Locket, N.A. (2004) Vision in deep sea. Biology Review, 79, 671–712.
    https://doi.org/10.1017/s1464793103006420

    Wilcox, T.P., Zwickl, D.J., Heath, T.A. & Hillis, D.M. (2002) Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Molecular Phylogenetics and Evolution, 25, 361–371.
    https://doi.org/10.1016/S1055-7903(02)00244-0

    Zamudio, K.R., Jones, K.B. & Ward, R.H. (1997) Molecular systematics of short-horned lizards: biogeography and taxonomy of a widespread species complex. Systematic Biology, 46, 284–305.
    https://doi.org/10.1093/sysbio/46.2.284