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Article
Published: 2020-06-19

A new species of Sphenomorphus (Squamata: Scincidae) from Phu Quoc Island, Vietnam with a discussion of biogeography and character state evolution in the S. stellatus group

Herpetology Laboratory, Department of Biology, La Sierra University, 4500 Riverwalk Parkway, Riverside, California 92515, USA.
Zoological Museum, Moscow State University, B. Nikitskaya ul. 2, Moscow 125009, Russia.
A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninsky Prospect, Moscow 119071, Russia.
Faculty of Biology, Department of Vertebrate Zoology, Moscow State University, Moscow, Russia. Laboratory of Tropical Ecology, Joint Russian-Vietnamese Tropical Research and Technological Center, Hanoi, Vietnam
Reptilia Phylogenetic systematics Indochina Cambodia Kien Giang Biosphere Reserve

Abstract

An integrative taxonomic analysis of the Sphenomorphus stellatus group recovered a newly discovered museum specimen from Phu Quoc Island, Kien Giang Province, Vietnam as a new species most closely related to S. preylangensis from Phnom Chi in central Cambodia, approximately 175 km to the northeast. Most notably, S. phuquocensis sp. nov. lacks the derived condition of having black dorsal stripes that diagnose S. annamiticus—the sister species to S. preylangensis plus S. phuquocensis sp. nov. A BioGeoBEARS analysis recovered the ancestor of the S. stellatus group to likely have ranged across forested regions on an exposed Sunda Shelf from southwestern Indochina to Peninsular Malaysia prior to diverging into northern and southern lineages separated by the Gulf of Thailand. Episodic fluctuations in sea levels and concomitant changes in the physiography of the Mekong Delta contributed to the fragmented distribution within and between species of the northern lineage. Sphenomorphus phuquocensis sp. nov. represents the second species of reptile endemic to Phu Quoc Island.

 

References

  1. Bain, R.H. & Hurley, M.M. (2011) A biogeographic synthesis of the amphibians and reptiles of Indochina. Bulletin of the American Museum of Natural History, 360, 1–138.

    https://doi.org/10.1206/360.1

    Barraclough, T.G., Birky, Jr., C.W. & Burt, A. (2003) Diversification in sexual and asexual organisms. Evolution, 57, 2166–2172.

    https://doi.org/10.1554/02-339

    Bobrov, V.V. (2011) Lizards of the Phu Quoc National Park. In: Kalyakin, M.V. (Ed.) Materialy zoologo-botanicheskikh issledovanii na ostrove Fu Kuok, Yuzhnyi Vietnam [Materials of zoological and botanical studies in Phu Quoc Island, South of Vietnam], Moscow, KMK Scientific Press, pp. 68–79. [in Russian]

    Bobrov, VV. (2013). Acanthosaura cardamomensis (Reptilia, Sauria, Agamidae) as a lizard species new for the Vietnam fauna. Modern Herpetology, 13(1-2), 64–66. [in Russian]

    Boettger, O. (1901) Aufzählung einer Liste von Reptilien und Batrachiern aus Annam. Berichte Senckenberg Ges, Senckenbergiana, 1901, 45–53

    Bollback, J P. (2006) SIMMAP: stochastic character mapping of discrete transition phylogenies. BMC Bioinformatics, 7, 88. https://doi.org/10.1186/1471-2105-7-88

    Boulenger, G.A. (1900) Descriptions of new batrachians and reptiles from Larut Hills, Perak. Annals of the Magazine of Natural History, series 7, vol. 6, 186–193.

    https://doi.org/10.1080/00222930008678356

    Chen, J.-M., Poyarkov, N.A. Jr., Suwannapoom, C., Lathrop, A., Wu, Y-H., Zhou, W-W., Yuan, Z-Y., Jin, J-Q., Chen, H-M., Liu, H.-Q., Nguyen, T.Q., Nguyen, S.N., Duong, T.V., Eto, K., Nishikawa, K., Matsui, M., Orlov, N.L., Stuart, B.L., Brown, R.M., Rowley, J.J.L., Murphy, R.W., Wang, Y.-Y. & Che, J. (2018) Large-scale phylogenetic analyses provide insights into unrecognized diversity and historical biogeography of Asian leaf-litter frogs, genus Leptolalax (Anura: Megophryidae). Molecular Phylogenetics and Evolution, 124, 162–171.

    https://doi.org/10.1016/j.ympev.2018.02.020

    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

    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

    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

    Freitas, E.S., Datta-Roy, A., Karanth, P., Grismer, L.L. & Siler, C.D. (2019) Multilocus phylogeny and a new classification for African, Asian and Indian supple and writhing skinks (Scincidae: Lygosominae). Zoological Journal of the Linnean Society, 186, 1067–1096.

    https://doi.org/10.1093/zoolinnean/zlz001

    Geissler, G., Poyarkov, N.A. Jr., Grismer, L.L., Nguyen, T.Q., An, H.T., Neang, T., Kupfer, A., Ziegler, T., Böhme, W. & Müller, H. (2015a) New Ichthyophis species from Indochina (Gymnophiona, Ichthyophiidae): 1. The unstriped forms with descriptions of three new species and the redescriptions of I. acuminatus Taylor, 1960, I. youngorum Taylor, 1960 and I. laosensis Taylor, 1969. Organisms Diversity & Evolution, 15, 143–174.

    https://doi.org/10.1007/s13127-014-0190-6

    Geissler, P., Hartmann, T., Ihlow, F., Rödder, D., Poyarkov, N.A. Jr., Nguyen, T.Q., Ziegler, T. & Böhme, W. (2015b) The Lower Mekong: an insurmountable barrier to amphibians in southern Indochina? Biological Journal of the Linnean Society, 114, 905–914.

    https://doi.org/10.1111/bij.12444

    Grismer, L.L. & Quah, E.S.H. (2015) The rediscovery of Sphenomorphus malayanus Doria, 1888 (Squamata: Scincidae) from the Titiwangsa Mountain Range of Peninsular Malaysia and its re-description as S. senja sp. nov. Zootaxa, 3931, 63–70. https://doi.org/10.11646/zootaxa.3931.1.4

    Grismer, L.L. & Grismer, J.L. (2017) A re-evaluation of the phylogenetic relationships of the Cyrtodactylus condorensis group (Squamata; Gekkonidae) and a suggestd protocol for the characterization of rock-dwelling ecomorphology in Cyrtodactylus. Zootaxa, 4300, 486–504.

    https://doi.org/10.11646/zootaxa.4300.4.2

    Grismer, L.L., Grismer, J.L., Wood, P.L., Jr., Ngo, V.T. & Chan, K.O. (2011) Herpetology on the fringes of the Sunda Shelf: a discussion of discovery, taxonomy, and biogeography. In: Schuchmann, K-L. (ed.) Tropical Vertebrates in a Changing World. Leibniz Gemeinschaft, Bonn, pp. 57–97.

    Grismer, L.L., Quah, E.S.H., Duzulkafly, Z. & Yambun, P. (2018b) On the taxonomy of Lygosoma bampfyldei Bartlett, 1895 (Squamata: Scincidae) with descriptions of new species from Borneo and Peninsular Malaysia and the resurrection of Lygosoma schneideri Werner, 1900. Zootaxa, 4438, 528–550.

    https://doi.org/10.11646/zootaxa.4438.3.6

    Grismer, L.L., Wood, Jr., P.L., Quah, E.S.H., Anuar, S., Ngadi, E. B., Nur, A.M. I. & Norhayati, A. (2018a) Systematics, ecomorphology, cryptic speciation and biogeography of the lizard genus Tytthoscincus Linkem, Diesmos & Brown (Squamata: Scincidae) from the sky-island archipelago of Peninsular Malaysia. Zoological Journal of the Linnean Society, 183, 635–671.

    https://doi.org/10.1093/zoolinnean/zlx067

    Grismer, L.L., Wood, Jr., P.L. Quah, E.S.H., Anuar, S., Poyarkov, N.A., Thy, N., Orlov, N.L., Thammachoti, P., Seiha, H. (2019a) Integrative taxonomy of the Asian skinks Sphenomorphus stellatus (Boulenger, 1900) and S. praesignis (Boulenger, 1900), with the resurrection of S. annamiticus (Boettger, 1901) and the description of a new species from Cambodia. Zootaxa, 4683(3), 381–411.

    https://doi.org/10.11646/zootaxa.4683.3.4

    Grismer, L.L., Dzukafly, Z., Muin, M.A., Quah, E.S.H., Karin, B.R., Shahrul, A. & Freitas, E.S. (2019b) A new skink of the genus Subdoluseps (Hardwicke & Gray, 1828) from Peninsular Malaysia. Zootaxa, 4609, 358–372.

    https://doi.org/10.11646/zootaxa.4609.2.10

    Hartmann, T., Geissler, P., Poyarkov, N.A. Jr., Ihlow, F., Galoyan, E.A., Rödder, D. & Böhme, W. (2013) A new species of the genus Calotes Cuvier, 1817 (Squamata: Agamidae) from southern Vietnam. Zootaxa, 3599 (3), 246–260.

    https://doi.org/10.11646/zootaxa.3599.3.3

    Hedges, S.B., Nussbaum, R.A. & Maxson, L.R. (1993). Caecilian phylogeny and biogeography inferred from mitochondrial DNA sequences of the 12S rRNA and 16S rRNA genes (Amphibia: Gymnophiona). Herpetological Monographs, 7, 64–76.

    Hillis, D.M. (2019) Species delimitation in herpetology. Journal of Herpetology, 53, 3–12.

    https://doi.org/10.1670/18-123

    Hillis, D.M., Moritz, C., Mable, B.K., & Graur, D. 1996. Molecular Systematics. Second Edition. Sinauer Associates, Inc., Sunderland (Massachusetts), 655 pp.

    Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q., & Vinh, L.S. (2018) Ufboot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35,513 518–522.

    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

    IUCN Standards and Petitions Subcommittee (2016) Guidelines for Using the IUCN Red List Categories and Criteria. Version 12. Prepared by the Standards and Petitions Subcommittee. Available from: http://www.iucnredlist.org/documents/RedListGuidelines.pdf (accessed 15 December 2019)

    Karin, B.R., Freitas, E.S., Shonleben, S., Grismer, S.S., Bauer, A.M. & Das, I. (2018) Unrealized diversity in an urban rainforest: a new species of Lygosoma (Squamata: Scincidae) from western Sarawak, Malaysia (Borneo). Zootaxa, 4370 (4), 345–362. https://doi.org/10.11646/zootaxa.4370.4.2

    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

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

    Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Pääbo, S., Villablanca, F.X. & Wilson, A.C. (1989). Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing of conserved primers. Proceedings of the National Academy of Sciences, USA, 86, 6196–6200.

    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

    Kuznetsov, A.N., & Kuznetsova, S.P. (2011) Forest vegetation of Phu Quoc Island. In: Kalyakin, M.V. (Ed.) Materialy zoologo-botanicheskikh issledovanii na ostrove Fu Kuok, Yuzhnyi Vietnam [Materials of zoological and botanical studies in Phu Quoc Island, South of Vietnam], Moscow, KMK Scientific Press, pp. 7–52. (in Russian)

    Landis, M., Matzke, N.J., Moore, B.R., & Huelsenbeck, J.P. (2013) Bayesian analysis of biogeography when the number of areas is large. Systematic Biology, 62, 789–804.

    https://doi.org/10.1093/sysbio/syt040

    Leaché, A.D., Koo, M.S., Spencer, C.S., 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, 106, 12418–12423.

    https://doi.org/10.1073/pnas.0906380106

    Linkem, C.W. (2013) Molecular Phylogenetics and Biogeography of Sphenomorphini (Squamata: Scincidae). Unpublished PhD Thesis, Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas.

    Matzke, N.J. (2013) Probabilistic historical biogeography: New models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing. Frontiers in Biogeography, 5, 242–248.

    https://doi.org/10.1093/sysbio/syu056

    Matzke, N.J. (2014) Model selection in historical biogeography reveals that founder-effect speciation is a crucial process in island clades. Systematic Biology, 63, 1–21.

    https://doi.org/10.1093/sysbio/syu056

    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

    Minh, Q., Nguyen, M.A.T. & von Haeseler, A. (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution, 30, 1188–1195.

    https://doi.org/10.1093/molbev/mst024

    Morice, A. (1875) Coup d’oeil sur la faune de la Cochinchine Francaise. Association Lyonnaise des Amis des Sciences Naturelles, Lyon, 121 pp. [in French]

    Murdoch, M.L., Grismer, L.L., Wood, Jr., P.L., Neang, T., Poyarkov, N.A., Ngo, V.T., Nazarov, R., Aowphol, A., Pauwels, O.S.G., Nguyen, H.N. & Grismer, J.L. (2019) Six new species of the Cyrtodactylus intermedius complex (Squamata: Gekkonidae) intermedius complex from the Cardamom Mountains and associated highlands of Southeast Asia. Zootaxa, 4554, 1–62.

    http://dx.doi.org/10.11646/zootaxa.4554.1.1

    Neang, T., Chan, S. & Poyarkov, N.A. Jr. (2018) A new species of smooth skink (Squamata: Scincidae: Scincella) from Cambodia. Zoological Research, 38 (3), 214–233.

    https://doi.org/10.24272/j.issn.2095-8137.2018.008

    Ngo, V.T., Grismer, L.L., & Grismer J.L. (2010) A new species of Cyrtodactylus Gray, 1827 (Squamata: Gekkonidae) in Phu Quoc National Park, Kien Giang Biosphere Reserve, Southwestern Vietnam. Zootaxa, 2604, 37–51.

    Nguyen V.S. & Ho T.C. (1979) Results of reptiles and frogs investigations in some areas of Southwest Vietnam and neighboring islands. Tạp chí Sinh học [Journal of Biology] (Hanoi), 1(1), 28–30. (in Vietnamese)

    Nguyen, H.N., Lu, C.-W., Chu, J.-H, Grismer, L.L., Hung, C.-M. & Lin, S.-M. (2018) Historical demography of four gecko species specializing in boulder cave habitat: Implications in the evolutionary dead end hypothesis and conservation. Molecular Ecology, 28, 772–784.

    https://doi.org/10.1111/mec.14985

    Nguyen S.N., Nguyen V.D.H., Nguyen L.T. & Murphy R.W. (2019) A new skink of the genus Scincella Mittleman, 1950 (Squamata: Scincidae) from Ba Den Mountain, Tay Ninh Province, southern Vietnam. Zootaxa, 4648, 273–286.

    Nguyen, H.N., Tran, B.V., Nguyen, L.H., Neang, T., Yushchenko, P.V. & Poyarkov, N.A. (2020) A new species of Oligodon Fitzinger, 1826 from Langbian Plateau, southern Vietnam, with additional information on Oligodon annamensis Leviton, 1953 (Squamata: Colubridae). PeerJ, 8, e8332.

    http://doi.org/10.7717/peerj.8332

    Nguyen, S.-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

    Nguyen, V.S., Ho. T.C. & Nguyen, T. Q. (2009) Herpetofauna of Vietnam. Frankfurt am Main: Edition Chimaira, 768 pp.

    Poyarkov, N.A. Jr., Duong, T.V., Orlov, N.L., Gogoleva, S.S., Vassilieva, A.B., Nguyen, L.T., Nguyen, V.H.D., Nguyen, S.N., Che, J. & Mahony S. (2017) Molecular, morphological and acoustic assessment of the genus Ophryophryne (Anura, Megophryidae) from Langbian Plateau, southern Vietnam, with description of a new species. ZooKeys, 672, 49–120.

    https://doi.org/10.3897/zookeys.672.10624

    Poyarkov, N.A., Jr., Geissler, P., Gorin, V.A., Dunayev, E.A., Hartmann, T. & Suwannapoom, C. (2019) Counting stripes: revision of the Lipinia vittigera complex (Reptilia, Squamata, Scincidae) with description of two new species from Indochina. Zoological Research, 40, 358–393.

    R Core Team. 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. [accessed 2016]. http://www.R-project.org

    Rambaut, A., & Drummond, A.J. (2013). TreeAnnotator v1. 7.0.

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

    Rambaut, A., Suchard, M.A., Xie, D., & Drummond, A.J. (2014). Tracer v1.6.

    https://doi.org/10.1093/sysbio/syy032

    Ree, R.H. & Sanmartín, I. (2018) Conceptual and statistical problems with the DEC+J model of founder-event speciation and its comparison with DEC via model selection. Journal of Biogeography, 2018, 1–9.

    https://doi.org/10.1111/jbi.13173

    Ree, R.H. & Smith, S.A. (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology, 57, 4–14.

    https://doi.org/10.1080/10635150701883881

    Revell, L.J. (2012) Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223.

    https://doi.org/10.1111/j.2041-210X.2011.00169.x

    Ripley, B., Venables, B., Bates, D.M., Hornik, K., Gebhardt, A. & Firth, D. (2018) Support functions and databases for Venables and Ripley’s MASS. [http://www.stats.ox.ac.uk/pub/MASS4/]

    Ronquist, F. (1997) Dispersal–vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology, 46, 195–203.

    https://doi.org/10.1093/sysbio/46.1.195

    Sheridan, J.A. & Stuart, B.L. (2018) Hidden species diversity in Sylvirana nigrovittata (Amphibia: Ranidae) highlight the importance of taxonomic revisions in biodiversity conservation. PLoS ONE 13: e0192766.

    https://doi.org/10.1371/journal.pone.0192766

    Siler, C.D., Heitz, B.B., Davis, D.R., Freitas, E.S., Aowphol, A., Termprayoon, K. & Grismer, L.L. (2018) New Supple Skink, Genus Lygosoma (Reptilia: Squamata: Scincidae), from Indochina and redescription of Lygosoma quadrupes (Linnaeus, 1766). Journal of Herpetology, 52, 332–347.

    https://doi.org/10.1670/16-064

    Sumarli, A., Grismer, L.L., Wood, P.L., Jr., Ahmad, A.B., Rizal, S., Ismail, L.H., Izam, N.A.M., Ahmad, M. & Linkem, C.W. (2016) The first riparian skink (Genus: Sphenomorphus Strauch, 1887) from Peninsular Malaysia and its relationship to other Indochinese and Sundaic species. Zootaxa, 4173, 029–044.

    https://doi.org/10.11646/zootaxa.4173.1.3

    Vassilieva, A.B., Galoyan, E.A., Poyarkov, N.A. & Geissler, P. (2016) A Photographic Field Guide to the Amphibians and Reptiles of the Lowland Monsoon Forests of Southern Vietnam. Chimaira Buchhandelsgesellschaft mbH, Frankfurt-am-Main, 319 pp.

    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

    Woodruff, D.S. (2010) Biogeography and conservation in Southeast Asia: how 2.7 million years of repeated environmental fluctuations affect today’s patterns and the future of the remaining refugial-phase biodiversity. Biodiversity Conservation, 19, 919–941.

    https://doi.org/10.1007/s10531-010-9783-3