Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5486 No. 1: 24 Jul. 2024
Type: Article
Published: 2024-07-24
DOI: 10.11646/zootaxa.5486.1.3
Page range: 71-108
Abstract views: 219
PDF downloaded: 6

Integrative taxonomy reveals two new species of karst-dwelling Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) from the border region of Laos and Vietnam

Faculty of Forest Resources and Environmental Management; Vietnam National University of Forestry; Xuan Mai; Chuong My; Hanoi; Vietnam
Faculty of Forest Resources and Environmental Management; Vietnam National University of Forestry; Xuan Mai; Chuong My; Hanoi; Vietnam
College of Forestry Biotechnology; Vietnam National University of Forestry; Hanoi; Vietnam
Herpetology Laboratory; Department of Biology; La Sierra University; 4500 Riverwalk Parkway; Riverside; California 92505; USA
Herpetology Laboratory; Department of Biology; La Sierra University; 4500 Riverwalk Parkway; Riverside; California 92505; USA
Faculty of Forestry; National University of Laos; Dong Dok Campus; Vientiane; Lao PDR
Faculty of Forestry; National University of Laos; Dong Dok Campus; Vientiane; Lao PDR
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; Jalan UMS; 88400; Kota Kinabalu; Sabah; Malaysia
Reptilia genetics Indochina karst forest Laos phylogenetics systematics Vietnam

Abstract

An integrative taxonomic analysis of the gekkonid lizard genus Hemiphyllodactylus was conducted using molecular, morphological, color pattern, and ecological data on a clade of 19 species, including two new species from karst landscapes in northern Laos and Vietnam. Hemiphyllodactylus houaphanensis sp. nov. (Laos) and H. vanhoensis sp. nov. (Vietnam) are karst-dwelling species whose discovery further emphasizes the unrealized herpetological diversity and site-specific endemism in karst ecosystems across Southeast Asia and the need for increased field work to protect these biodiverse landscapes.

 

References

  1. Agarwal, I., Khandekar, A., Giri, V.B., Ramakrishnan, U. & Karanth, K.P. (2019) The hills are alive with geckos! A radiation of a dozen species on sky islands across peninsular India (Squamata: Gekkonidae, Hemiphyllodactylus) with the description of three new species. Organisms Diversity & Evolution, 19, 341–361. https://doi.org/10.1007/s13127-019-00392-5
  2. Agung, A.P., Chornelia, A., Grismer, L.L., Grismer, J.L., Quah, E.S.H., Lu, J., Tomlinson, K.W. & Hughes, A.C. (2022) Description of two new species of Hemiphyllodactylus (Reptilia: Gekkonidae) from karst landscapes in Yunnan, China, highlights complex conservation needs. Zoological Research, 43 (5), 767–786. https://doi.org/10.24272/j.issn.2095-8137.2022.105
  3. Agung, A.P., Grismer, L.L., Grismer, J.L., Quah, E.S., Chornelia, A., Lu, J.M. & Hughes, A.C. (2021) A new species of Hemiphyllodactylus Bleeker (Squamata: Gekkonidae) from Yunnan, China and its phylogenetic relationship to other congeners. Zootaxa, 4980 (1), 1–27. https://doi.org/10.11646/zootaxa.4980.1.1
  4. Barraclough, T.G., Birky Jr., C.W. & Burt, A. (2003) Diversification in sexual and asexual organisms. Evolution, 57, 2166–2172. https://doi.org/10.1111/j.0014-3820.2003.tb00394.x
  5. 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
  6. Boulenger, G.A. (1903) Descriptions of new lizards in the collection of the British Museum. The Annals and Magazine of Natural History Series 7, 12 (70), 429–435.
  7. Chan, K.O. & Grismer, L.L. (2022) GroupStruct: An R package for allometric size correction. Zootaxa, 5124 (4), 471–482. https://doi.org/10.11646/zootaxa.5124.4.4
  8. De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886. https://doi.org/10.1080/10635150701701083
  9. Do, Q.H., Nguyen, K.V., Le, M.D., Pham, C.T., Ziegler, T. & Nguyen, T.Q. (2021) A new species of Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) from Da Lat Plateau, Vietnam. Zootaxa, 5023 (1), 93–106. https://doi.org/10.11646/zootaxa.5023.1.5
  10. Do, Q.H., Pham, C.T., Phan, T.Q., Le, M.D., Ziegler, T. & Nguyen, T.Q. (2020) A new species of Hemiphyllodactylus (Squamata: Gekkonidae) from Tuyen Quang Province, Vietnam. Zootaxa, 4821 (3), 511–532. https://doi.org/10.11646/zootaxa.4821.3.5
  11. 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
  12. Eliades, S.J., Phimmachak, S., Sivongxay, N., Siler, C.D. & Stuart, B.L. (2019) Two new species of Hemiphyllodactylus (Reptilia: Gekkonidae) from Laos. Zootaxa, 4577 (1), 131–147. https://doi.org/10.11646/zootaxa.4577.1.8
  13. Frost, D.R. & Hillis, D.M. (1990) Species in concept and practice: herpetological application. Herpetologica, 46, 87–104.
  14. 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/10.1006/clad.1994.1018
  15. Grismer, L.L. (1999) An evolutionary classification of reptiles on islands in The Gulf of California, Mexico. Herpetologica, 55(4), 446–469. [https://www.jstor.org/stable/3893312]
  16. Grismer, L.L., Wood, P.L. Jr., Anuar, S., Muin, M.A., Quah, E.S.H., McGuire, J.A., Brown, R.M., Ngo, T.V. & Pham, T.H. (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/zoj12064
  17. Grismer, L.L., Wood, P.L. Jr., Quah, E.S.H., Thura, M.K., Oaks, J.R. & Lin, A. (2020) Four new Burmese species of Hemiphyllodactylus Bleeker (Squamata: Gekkonidae) from distantly unrelated parapatric clades from the Shan Plateau and Salween Basin. Zootaxa, 4758 (1), 45–82. https://doi.org/10.11646/zootaxa.4758.1.2
  18. Grismer, L., Wood Jr., P.L., Poyarkov, N.A., Le, M.D., Karunarathna, S., Chomdej, S. & Grismer, J.L. (2021) 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
  19. Grismer, L.L., Yushchenko, P.V., Pawangkhanant, P., Naiduangchan, M., Nazarov, R.A., Orlova, V.F. & Poyarkov, N.A. (2020) A new species of Hemiphyllodactylus Bleeker (Squamata; Gekkonidae) from Peninsular Thailand that converges in morphology and color pattern on Pseudogekko smaragdinus (Taylor) from the Philippines. Zootaxa, 4816 (2), 171–190. https://doi.org/10.11646/zootaxa.4816.2.2
  20. Grismer, L.L., Wood, P.L. Jr., Zug, G.R., Thura, M.K., Grismer, M.S., Murdoch, M.L., Quah, E.S.H. & Lin, A. (2018) Two more new species of Hemiphyllodactylus Bleeker (Squamata: Gekkonidae) from the Shan Hills of eastern Myanmar (Burma). Zootaxa, 4483 (2), 295–316. https://doi.org/10.11646/zootaxa.4883.2.4
  21. Guo, W., Zhou, K., Yan, J. & Li, P. (2015) A new species of Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) from western Yunnan, China. Zootaxa, 3974 (3), 377–390. https://doi.org/10.11646/zootaxa.3760.1.4
  22. Hillis, D.M. (2019) Species delimitation in herpetology. Journal of Herpetology, 53, 3–12. https://doi.org/10.1670/18-123
  23. 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
  24. 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.
  25. https://doi.org/10.1126/science.1065889
  26. Husson, F., Josse, J., Le, S. & Mazet, J. (2017) FactoMineR: Exploratory 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, 1–15. [http://www.biomedcentral.com/1471-2156/11/94] https://doi.org/10.1186/1471-2156-11-94
  28. 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
  29. Kassambara, A. & Mundt, F. (2017) Factoextra: Extract and Visualize the Result of Multivariate Data Analyses. R package version 1.0.5.999. [program]
  30. Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular evolutionary genetics analysis version 11.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874. https://doi.org/10.1093/molbev/msw054
  31. Le, M., Raxworthy, C.J., McCord, W.P. & Mertz, L. (2006) A molecular phylogeny of tortoises (Testudines: Testudinidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 40, 517−531. https://doi.org/10.1016/j.ympev.2006.03.003
  32. 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
  33. Luu, V.Q., Nguyen, T.H., Do, Q.H., Pham, C.T., Hoang, T.T., Nguyen, T.Q., Le, D.M., Ziegler, T., Grismer, J.L. & Grismer, L.L. (2023) A new species of Hemiphyllodactylus (Squamata, Gekkonidae) from Ha Giang Province, Vietnam. ZooKeys, 1167, 353–382. https://doi.org/10.3897/zookeys.1167.103713
  34. Macey, J.R., 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
  35. McCoy, M.W., Bolker, B.M., Osenberg, C.W., Miner, B.G. & Vonesh, J.R. (2006) Size correction: Comparing morphological traits among populations and environments. Oecologia, 148, 547–554. https://doi.org/10.1007/s00442-006-0403-6
  36. 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, 14 November 2010, 1–8. https://doi.org/10.1109/GCE.2010.5676129
  37. 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
  38. Ngo, T.V., Grismer, L.L., Pham, T.H. & Wood, P.L. Jr. (2014) A new species of Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) from Ba Na–Nui Chua Nature Reserve, Central Vietnam. Zootaxa, 3760 (4), 539–552. https://doi.org/10.11646/zootaxa.3760.4.3
  39. 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
  40. Nguyen, T.Q., Botov, A., Le, M.D., Nophaseud, L., Zug, G., Bonkowski, M. & Ziegler, T. (2014) A new species of Hemiphyllodactylus (Reptilia: Gekkonidae) from northern Laos. Zootaxa, 3827 (1), 45–56. https://doi.org/10.11646/zootaxa.3827.1.4
  41. Nguyen, T.Q., Do, Q.H., Ngo, H.T., Pham, A.V., Pham, C.T., Le, M.D. & Ziegler, T. (2020) Two new species of Hemiphyllodactylus (Squamata: Gekkonidae) from Hoa Binh Province, Vietnam. Zootaxa, 4801 (3), 513–536. https://doi.org/10.11646/zootaxa.4801.3.5
  42. Nguyen, T.Q., Lehmann, T., Le, M.D., Duong, H.T., Bonkowski, M. & Ziegler, T. (2013) A new species of Hemiphyllodactylus (Reptilia: Gekkonidae) from northern Vietnam. Zootaxa, 3736 (1), 89–98. https://doi.org/10.11646/zootaxa.3736.1.5
  43. Pagès, J. (2015) Multiple Factor Analysis by Example Using R. CRC Press, New York, New York, 272 pp. https://doi.org/10.1201/b17700
  44. R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. [2018]
  45. Rambaut, A. & Drummond, A.J. (2013) TreeAnnotator. Version 1.7.3. MCMC Output Analysis. Available from: https://beast. community/treeannotator (accessed 15 January 2023)
  46. Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer. Version 1.7. Available from: http://tree.bio.ed.ac.uk/ software/tracer/ (accessed 15 January 2023)
  47. Reist, J.D. (1986) An 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
  48. Ronquist, F., Teslenko, 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
  49. Simmons, J.E. (2002) Herpetological Collecting and Collections Management. Revised Edition. Society for the Study of Amphibians and Reptiles. Herpetological Circular, 31, 1–153.
  50. Sung, Y.H., Lee, W., Ng, H., Zhang, Y. & Yang, J. (2018) A new species of Hemiphyllodactylus (Squamata: Gekkonidae) from Hong Kong. Zootaxa, 4392 (2), 361–373. https://doi.org/10.11646/zootaxa.4392.2.8
  51. Thorpe, R.S. (1975) Quantitative handling of characters useful in snake systematics with particular reference to interspecific 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
  52. Thorpe, R.S. (1983) A review of the numerical methods for recognizing and analyzing racial differentiation. In: Felsenstein, J. (Ed.), Numerical Taxonomy. NATO ASI Series (Series G: Ecological Sciences). Vol. 1. Springer Verlag, Berlin, pp. 404–423. https://doi.org/10.1007/978-3-642-69024-2_43
  53. 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, W232–W235. https://doi.org/10.1093/nar/gkw256
  54. Turan, C. (1999) A note on the examination of morphometric differentiation among fish populations: The Truss System. Turkish Journal of Zoology, 23, 259–263.
  55. Uetz, P., Freed, P., Aguilar, R., Reyes, F. & Hošek, J. (Eds.) (2022) The Reptile Database. Available from: http://www.reptile–database.org (accessed 22 February 2023)
  56. 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
  57. Wood, P.L. Jr., Grismer, L.L., Aowphol, A., Aguilar, C.A., Cota, M., Grismer, M.S. & Sites Jr., J.W. (2017) Three new karst-dwelling Cnemaspis Strauch, 1887 (Squamata; Gekkoniade) from Peninsular Thailand and the phylogenetic placement of C. punctatonuchalis and C. vandeventeri. PeerJ, 5, e2884. https://doi.org/10.7717/peerj.2884
  58. Yan, J., Lin, Y., Guo, W., Li, P. & Zhou, K.Y. (2016) A new species of Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) from Mount Gaoligong, southwestern China. Zootaxa, 4136 (3), 567–576. https://doi.org/10.11646/zootaxa.3974.3.5
  59. Zhang, B., Qian, T., Jiang, X., Cai, B., Deng, X. & Yang, D. (2020) A new species of Hemiphyllodactylus Bleeker, 1860 (Reptilia: Squamata) from Hunan Province, China. Asian Herpetological Research, 11 (3), 183–197. https://doi.org/10.16373/j.cnki.ahr.190066
  60. Zhou, K.Y., Liu, Y.Z. & Yang, G.P. (1981) Three new subspecies of Hemiphyllodactylus yunnanensis (Boulenger) from China (Lacertiformes: Gekkonidae). Acta Zootaxonomica Sinica, 6, 202–209. [in Chinese, English translation by H. Ota (1996) in Smithsonian Herpetological Information Service 110, 1–8, 1 pl.]
  61. Zug, G.R. (2010) Speciation and dispersal in a low diversity taxon: the Slender geckos Hemiphyllodactylus (Reptilia, Gekkonidae). Smithsonian Contributions to Zoology, 631, 1–70.