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Issue: Vol. 5352 No. 1: 2 Oct. 2023
Type: Article
Published: 2023-10-02
DOI: 10.11646/zootaxa.5352.1.4
Page range: 109-136
Abstract views: 715
PDF downloaded: 25

A new species of Cyrtodactylus Gray, 1827 (Squamata: Gekkonidae) from the Thai-Malay Peninsula and the independent evolution of cave ecomorphology on opposite sides of the Gulf of Thailand

Herpetology Laboratory; Department of Biology; La Sierra University; 4500 Riverwalk Parkway; Riverside; California 92505; USA; Department of Herpetology; San Diego Natural History Museum; PO Box 121390; San Diego; California; 92112; USA; Institute for Tropical Biology and Conservation; Universiti Malaysia Sabah; Kota Kinabalu; Malaysia
Division of Fishery; School of Agriculture and Natural Resources; University of Phayao; Phayao; Thailand
Department of Vertebrate Zoology; Lomonosov Moscow State University; Leninskiye Gory; GSP–1; Moscow 119991; Russia
Department of Vertebrate Zoology; Lomonosov Moscow State University; Leninskiye Gory; GSP–1; Moscow 119991; Russia
Zoological Museum; Moscow State University; Moscow; 2 Bolshaya Nikitskaya St.; Moscow 125009; Russia
Division of Fishery; School of Agriculture and Natural Resources; University of Phayao; Phayao; Thailand
Zoological Museum; Moscow State University; Moscow; 2 Bolshaya Nikitskaya St.; Moscow 125009; Russia; Joint Vietnam - Russia Tropical Science and Technology Research Centre; 63 Nguyen Van Huyen Road; Nghia Do; Cau Giay; Hanoi; Vietnam
Reptilia Gecko Indochina Southeast Asia karst integrative taxonomy habitat preference

Abstract

An integrative taxonomic analysis recovers a distinctive new species of the gekkonid genus Cyrtodactylus Gray, 1827 from Satun Province in extreme southern Thailand as the sister species to the Cyrtodactylus intermedius group of southern Indochina, approximately 600 km to the northeast across the Gulf of Thailand. Based on 1449 base pairs of the mitochondrial gene NADH dehydrogenase subunit 2 (ND2) and its flanking tRNAs, the new species, C. disjunctus sp. nov., bears a pairwise sequence divergence from the mean divergences of the intermedius group species ranging from 17.9–23.6%. Three different principal component analyses (PCA) and a multiple factor analysis (MFA) recover C. disjunctus sp. nov. as a highly distinctive karst cave-adapted species based on morphology and color pattern. Its sister species relationship to the intermedius group—to which it is added here—further underscores a growing body of analyses that have recovered a trans-Gulf of Thailand connection across the submerged Sunda Shelf between the southern Thai-Malay Peninsula and southern Indochina. Fragmented karstic archipelagos stretching across Indochina have served as foci for the independent evolution of nearly 25% of the species of Cyrtodactylus. The description of C. disjunctus sp. nov. continues to highlight the fact that karstic habitats support an ever-increasing number of threatened site-specific endemics that compose much of the reptile diversity of many Asian nations but, as of yet, most of these landscapes have no legal protection.

 

References

  1. Agarwal, A., El-Ghazawi, T., El-Askary, H. & Le-Moigne, J (2007) Efficient hierarchical-PCA dimension reduction for hyperspectral imagery. 2007 IEEE International Symposium on Signal Processing and Information Technology, Giza, Egypt, 15–18 December 2007. IEEE, Manhattan, New York City. [published online] https://doi.org/10.1109/isspit.2007.4458191
  2. 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
  3. Bauer, A.M., Sumontha, M. & Pauwels, O.S.G. (2003) Two new species of Cyrtodactylus (Reptilia: Squamata: Gekkonidae) from Thailand. Zootaxa, 376, 1–18
  4. Bouckaert, R.R. & Drummond, A.J. (2017) bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evolutionary Biology, 17, 42. https://doi.org/10.1186/s12862-017-0890-6
  5. Camargo, A. (2022) PCAtest: testing the statistical significance of Principal Component Analysis in R. PeerJ, 10, e12967. https://doi.org/10.7717/peerj.12967
  6. Chen, J.-M., Poyarkov, N.A., 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.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
  7. de Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886. https://doi.org/10.1080/10635150701701083
  8. Drummond, A.J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T. & Wilson, A. (2011) Geneious. Version 5.6. Available from: http://www.geneious.com/ (accessed 9 January 2018)
  9. 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/mss075
  10. Frost, D.R. & Hillis, D.M. (1990) Species in concept and practice: herpetological application. Herpetologica, 46, 86–104.
  11. Frost, D.R. & Kluge, A.G. (1994) A consideration of the epistemology in systematic biology, with special reference to species. Cladistics, 10, 259–294. https://doi.org/10.1111/j.1096-0031.1994.tb00178.x
  12. Gray, J.E. (1827) A Synopsis of the Genera of Saurian Reptiles in which some new Genera are indicated, and the others reviewed by actual Examination. Philosophical Magazine, London, 2, 54–58. https://doi.org/10.1080/14786442708675620
  13. Grismer, L.L., Chan, K., Oaks, J.R., Neang, T., Sokun, L., Murdoch, M.L., Stuart, B.L. & Grismer, J.L. (2020b) A new insular species of the Cyrtodactylus intermedius (Squamata: Gekkonidae) group from Cambodia with a discussion of habitat preference and ecomorphology. Zootaxa, 4830 (1), 75–102. https://doi.org/10.11646/zootaxa.4830.1.3
  14. Grismer, L.L., Geissler, P., Neang, T., Hartmann, T., Wagner, P. & Poyarkov, N.A. (2021c) Molecular phylogenetics, PCA, and MFA recover a new species of Cyrtodactylus (Squamata: Gekkonidae) from an isolated sandstone massif in northwestern Cambodia. Zootaxa, 4949 (2), 261–288. https://doi.org/10.11646/zootaxa.4949.2.3
  15. Grismer, L.L. & Grismer, J.L. (2017) A re-evaluation of the phylogenetic relationships of the Cyrtodactylus condorensis group (Squamata; Gekkonidae) and a suggested protocol for the characterization of rock-dwelling ecomorphology in Cyrtodactylus. Zootaxa, 4300 (4), 486­–504. https://doi.org/10.11646/zootaxa.4300.4.2
  16. Grismer, L.L., Roman, N.A., Vladimir, V.B. & Poyarkov, N.A. (2020c) 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. Zootaxa, 4801 (3), 461–487. https://doi.org/10.11646/zootaxa.4801.3.3
  17. Grismer, L.L., Poyarkov, N.A., Quah, E.S.H., Grismer, J.L. & Wood Jr., P.L. (2022a) The biogeography of bent-toed geckos, Cyrtodactylus (Squamata: Gekkonidae). PeerJ, 10, e13153. https://doi.org/10.7717/peerj.13153
  18. Grismer, L.L., Wood Jr., P.L., Thura, M.K., Quah, E.S.H., Murdoch, M.L., Grismer, M.S., Herr, M.W., Lin, A. & Kyaw, H. (2018) Three more new species of Cyrtodactylus (Squamata: Gekkonidae) from the Salween Basin of eastern Myanmar underscore the urgent need for the conservation of karst habitats. Journal of Natural History, 52, 1243–1294. https://doi.org/10.1080/00222933.2018.1449911
  19. Grismer, L.L., Wood Jr., P.L., Le, M.D., Quah, E.S.H & Grismer, J.L. (2020a). Evolution of habitat preference in 243 species of Bent‐toed geckos (Genus Cyrtodactylus Gray, 1827) with a discussion of karst habitat conservation. Ecology and Evolution, 10, 13717–13730. https://doi.org/10.1002/ece3.6961
  20. Grismer, L.L., Wood Jr., P.L., Poyarkov, N.A., Le, M.D., Kraus, F., Agarwal, I., Oliver, P.M., Nguyen, S.N., Nguyen, T.Q., Karunarathna, S., Welton, L.J., Stuart, B.L., Luu, V.Q., Bauer, A., O’Connell, K.A., Quah, E.S.H., Chan, K.O., Ziegler, T., Ngo, H.T., Nazarov, R.A., Aowphol, A., Chomdej, S., Suwannapoom, C., Siler, C.D., Anuar, S., Ngo, V.T. & Grismer, J.L. (2021a) Phylogenetic partitioning of the third-largest vertebrate genus in the world, Cyrtodactylus Gray, 1827 (Reptilia; Squamata; Gekkonidae) and its relevance to taxonomy and conservation. Vertebrate Zoology, 71, 101–154. https://doi.org/10.3897/vertebrate-zoology.71.e59307.figure30
  21. Grismer, L.L., Wood Jr., P.L., Poyarkov, N.A., Le, M.D., Karunarathna, S., Chomde, S., Suwannapoom, C., Qi, S., Liu, S., Che, J., Quah, E.S.H., Kraus, F., Oliver, P.M., Riyanto, A., Pauwels, O.S.H. & Grismer, J.L. (2021b) Karstic landscapes are foci of species diversity in the world’s third largest vertebrate genus Cyrtodactylus Gray, 1827 (Reptilia: Squamata; Gekkonidae). Diversity, 13 (5), 183. https://doi.org/10.3390/d13050183
  22. 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. (2019) 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
  23. Hillis, D.M. (2019) Species delimitation in herpetology. Journal of Herpetology, 53, 3–12. https://doi.org/10.1670/18-123
  24. 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, 518–522. https://doi.org/10.1093/molbev/msx281
  25. 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
  26. Husson, F., Josse, J., Le, S. & Mazet, J. (2017) FactoMine R: explortory data analysis and data mining. R package, Version 1.36. [program]
  27. 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
  28. Jombart, T. & Collins, C. (2015) A tutorial for discriminant analysis of principal components (DAPC) using adegenet 2.0.0. Available from: http://adegenet.r-forge.r-project.org/files/tutorial-dapc-pdf (accessed 11 September 2023)
  29. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587. https://doi.org/10.1038/nmeth.4285
  30. Kassambara, A. & Mundt, F. (2017) Factoextra: extract and visualize the result of multivariate data analyses. R package, Version 1.0.5.999. [program]
  31. Lleonart, J., Salat, J. & Torres, G.J. (2000) Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology, 205, 85–93. https://doi.org/10.1006/jtbi.2000.2043
  32. Luu, V.Q., Bonkowski, M., Nguyen, T.Q., Le, M.D., Schneider, N., Ngo, H.T. & Ziegler, T. 2016. Evolution in karst massifs: Cryptic diversity among bent-toed geckos along the Truong Son Range with descriptions of three new species and one new country record from Laos. Zootaxa, 4107 (2), 101–140. https://doi.org/10.11646/zootaxa.4107.2.1
  33. Maddison, W.P. & Maddison, D.R. (2015) Mesquite: a modular system for evolutionary analysis. Version 3.04. Available from: http://www.mesquiteproject.org (accessed 25 August 2020) https://doi.org/10.1093/sysbio/42.2.218
  34. Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, Louisiana, 1–8. https://doi.org/10.1109/GCE.2010.5676129
  35. 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
  36. Murdoch, M.L., Grismer, L.L., Wood Jr., P.L., Neang, T., Poyarkov, N.A., Ngo, V.T., Nazarov, R.A., Aowphol, A., Pauwels, O.S.G., Nguyen, H.N. & Grismer, J.L. (2019) Six new species of the Cyrtodactylus intermedius complex (Squamata: Gekkonidae) from the Cardamom Mountains and associated highlands of Southeast Asia. Zootaxa, 4554 (1), 1–62. https://doi.org/10.11646/zootaxa.4554.1.1
  37. Ngo, V.T. (2008) Two new cave-dwelling species of Cyrtodactylus Gray (Squamata: Gekkonidae) from Southwestern Vietnam. Zootaxa, 1909 (1), 37–51. https://doi.org/10.11646/zootaxa.1909.1.4
  38. Ngo, V.T., Grismer, L.L. & Grismer, J.L. (2008) A new endemic cave dwelling species of Cyrtodactylus Gray, 1827 (Squamata: Gekkonidae) in Kien Giang Biosphere Reserve, Southwestern Vietnam. Zootaxa, 1967 (1), 53–62. https://doi.org/10.11646/zootaxa.1967.1.3
  39. Nguyen, A.T., Duong, T.V., Grismer, L.L. & Poyarkov, N.A. (2021) A new granite cave-dwelling Bent-toed Gecko from Vietnam of the Cyrtodactylus irregularis group (Squamata; Gekkonidae) and a discussion on cave ecomorphology. Vertebrate Zoology, 71, 155–174. https://doi.org/10.3897/vz.71.e60225
  40. 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
  41. Nurngsomsri, P., Chuaynkern, C., Duengkae, P., Sanguansombat, W., Grismer, L.L. & Chuaynkern, Y. (2019) Cyrtodactylus leegrismeri Chan and Norhayati, 2010 (Sauria: Gekkonidae): A first country record for Thailand. Songklanakarin Journal of Science and Technology, 41, 1319–1327.
  42. Pagès, J. (2015) Multiple Factor Analysis by Example Using R. CRC Press, New York, New York, 272 pp. https://doi.org/10.1201/b17700
  43. Paradis, E. & Schilep, K. (2018) Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 35, 526–528.
  44. https://doi.org/10.1093/bioinformatics/bty633
  45. Poyarkov, N.A., Geissle, 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. https://doi.org/10.24272/j.issn.2095-8137.2019.052
  46. Quah, E.S.H., Grismer, L.L., Syafiq, M.F., Rujiwawan, A., Aowphol, A., Ahmad, A.B. & Anuar, M.S.S. (2023) Comments on the taxonomic status of Cyrtodactylus zebriacus Taylor, 1962 (Squamata: Gekkonidae) from northern Peninsular Malaysia. Zootaxa, 5318 (4), 489–503. https://doi.org/10.11646/zootaxa.5318.4.3
  47. R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. 2018. Available from: http://www.R-project.org (accessed 1 June 2022)
  48. Rambaut, A. & Drummond, A.J. (2013) TreeAnnotator. Version 1.8.0. MCMC Output Analysis. Available from: https://beast.community/treeannotator (accessed 11 September 2023)
  49. Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901–904. https://doi.org/10.1093/sysbio/syy032
  50. Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer. Version 1.6. Available from: http://gensoft.pasteur.fr/docs/Tracer/v1.6 (accessed 11 September 2023)
  51. Reist, J.D. (1986) A empirical evaluation of coefficients used in residual and allometric adjustment of size covariation. Canadian Journal of Zoology, 64, 1363–1368. https://doi.org/10.1139/z86-203
  52. 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
  53. Ronquist, F., Teslenkom, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 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
  54. Sang, N.N., Orlov, N.L. & Darevsky, I.S. (2006) Descriptions of two New Species of the Genus Cyrtodactylus Gray, 1827 (Squamata: Sauria: Gekkonidae) from Southern Vietnam. Russian Journal of Herpetology, 13, 215–226.
  55. 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
  56. Tamura, K., Stecher, G. & Kumar, S. (2021) MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38, 3022–3027. https://doi.org/10.1093/molbev/msab120
  57. Taylor, E.H. (1962) New oriental reptiles. University of Kansas Science Bulletin, 43, 209–263. https://doi.org/10.5962/bhl.part.13346
  58. Theobald, W. (1876) Descriptive catalogue of the reptiles of British India. Thacker, Spink & Co., Calcutta, xiii + 238 pp. https://doi.org/10.5962/bhl.title.54001
  59. Thorpe, R.S. (1975) Quantitative handling of characters useful in snake systematics with particular reference to intraspecific variation in the Ringed Snake Natrix natrix (L.). Biological Journal of the Linnean Society, 7, 27–43. https://doi.org/10.1111/j.1095-8312.1975.tb00732.x
  60. Thorpe, R.S. (1983) A review of the numerical methods for recognising and analysing racial differentiation. In: Felsenstein, J. (Ed.), Numerical Taxonomy. NATO ASI Series. Vol. 1. Springer, Berlin, Heidelberg, pp. 404–423. https://doi.org/10.1007/978-3-642-69024-2_43
  61. Turan, C. (1999) A note on the examination of morphometric differentiation among fish populations: The Truss System. Turkish Journal of Zoology, 23, 259–263.
  62. Tolentino, P.J., Navidad, J.R.L., Angeles, M.D., Fernandez, D.A.P., Villanueva, E.L.C., Obeña, R.D.R. & Buot, J.I.E. (2020) Review: Biodiversity of forests over limestone in Southeast Asia with emphasis on the Philippines. Biodiversitas Journal of Biodiversity, 21, 1597–1613. https://doi.org/10.13057/biodiv/d210441
  63. Trifinopoulos, J., Nguyen, L.T., von Haeseler, A. & Minh, B.Q. (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44, 232–235. https://doi.org/10.1093/nar/gkw256
  64. Uetz, P., Freed, P. & Hošek, J. (Eds.) (2023) The Reptile Database. Available from: http://www.reptile-database.org (accessed 25 May 2023)
  65. Wilcox, T., 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