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Issue: Vol. 5501 No. 1: 29 Aug. 2024
Type: Article
Published: 2024-08-29
DOI: 10.11646/zootaxa.5501.1.2
Page range: 39-55
Abstract views: 728
PDF downloaded: 29

Incorporating New Datatypes to Enhance Species Delimitation: A Case Study in Rice Paddy Snakes (Homalopsidae: Hypsiscopus)

University of Kansas; Center for Genomics; 1345 Jayhawk Blvd; Lawrence; Kansas 66045; United States; Department of Biology; University of Texas at Arlington; Arlington; Texas; 76010; United States
Reptilia Zoo and Education Centre; 2501 Rutherford Rd.; Vaughn; Ontario; Canada L4K 2N6; State Key Laboratory of Genetic Resources and Evolution; Kunming Institute of Zoology; The Chinese Academy of Sciences; Kunming; China; Department of Natural History; Royal Ontario Museum; Toronto; ON; Canada
Department of Natural History; Royal Ontario Museum; Toronto; ON; Canada
Institute of Tropical Biology; Vietnam Academy of Science and Technology; Ho Chi Minh City; Vietnam
Department of Herpetology; Zoological Institute; Russian Academy of Sciences; St. Petersburg; Russia
Section of Research & Collections; North Carolina Museum of Natural Sciences; North Carolina; 27601; USA
Reptilia China east Asia mud snakes phylogenetics systematics red river vietnam

Abstract

Homalopsids (Old World Mud Snakes) include 59 semiaquatic species in Asia and Australasia that display an array of morphological adaptations, behaviors, and microhabitat preferences. These attributes make homalopsids an ideal model system for broader questions in evolutionary biology, but the diversity of this understudied group of snakes is still being described. Recognized species diversity in rice paddy snakes (Hypsiscopus) has recently doubled after nearly 200 years of taxonomic stability. However, the evolutionary distinctiveness of some populations remains in question. In this study, we compare mainland Southeast Asian populations of Hypsiscopus east and west of the Red River Basin in Vietnam, a known biogeographic barrier in Asia, using an iterative approach with molecular phylogenetic reconstruction, machine-learning morphological quantitative statistics, and ecological niche modeling. Our analyses show that populations west of the Red River Basin represent an independent evolutionary lineage that is distinct in genetics, morphospace, and habitat suitability, and so warrants species recognition. The holotype of H. wettsteini, a species originally described in error from Costa Rica, grouped morphometrically with the population at the Red River Basin and eastward, and those west of the Red River Basin are referred to the recently described H. murphyi. The two species may have diversified due to a variety of geological and environmental factors, and their recognition exemplifies the importance of multifaceted approaches in taxonomy for downstream biogeographic studies on speciation scenarios.

 

References

  1. Ahmadzadeh, F., Flecks, M., Carretero, M.A., Böhme, W., Ilgaz, C., Engler, J.O., James Harris, D., Üzüm, N. & Rödder, D. (2013) Rapid lizard radiation lacking niche conservatism: ecological diversification within a complex landscape. Journal of Biogeography, 40, 1807–1818. https://doi.org/10.1111/jbi.12121
  2. Aiello-Lammens, M.E., Boria, R.A., Radosavljevic, A., Vilela, B. & Anderson, R.P. (2015) spThin: an R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography, 38, 541–545. https://doi.org/10.1111/ecog.01132
  3. 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, 2011, 1–138. https://doi.org/10.1206/360.1
  4. Becker, R.A., Wilks, A.R., Brownrigg, R., Minka, T.P. & Deckmyn, A. (2018) Maps: Draw Geographical Maps. Available from: https://cran.r-project.org/web/packages/maps/maps.pdf (accessed 29 February 2024)
  5. Bernstein, J.M., Murphy, J.C., Voris, H.K., Brown, R.M. & Ruane, S. (2021) Phylogenetics of mud snakes (Squamata: Serpentes: Homalopsidae): A paradox of both undescribed diversity and taxonomic inflation. Molecular Phylogenetics and Evolution, 160, 107109. https://doi.org/10.1016/j.ympev.2021.107109
  6. Bernstein, J.M. & Ruane, S. (2022) Maximizing molecular data from low-quality fluid-preserved specimens in natural history collections. Frontiers in Ecology and Evolution, 10, 893088. https://doi.org/10.3389/fevo.2022.893088
  7. Bernstein, J.M., de Souza, H.F., Murphy, J.C., Voris, H.K., Brown, R.M., Myers, E.A., Harrington, S., Shanker, K. & Ruane, S. (2023) Phylogenomics using fresh and formalin specimens resolves the systematics of Old World Mud Snakes (Serpentes: Homalopsidae) and expands biogeographic inference. Bulletin of the Society of Systematic Biologists, 2 (1), 1–24. https://doi.org/10.18061/bssb.v2i1.9393
  8. Bernstein, J.M., Voris, H.K., Stuart, B.L., Karns, D.R., McGuire, J.A., Iskandar, D.T., Riyanto, A., Calderón-Acevedo, C.A., Brown, R.M., Gehara, M., Soto-Centeno, J.A. & Ruane, S. (2024) Integrative methods reveal multiple drivers of diversification in rice paddy snakes. Scientific Reports, 14, 4727. https://doi.org/10.1038/s41598-024-54744-z
  9. Bernstein, J.M., Voris, H.K., Stuart, B.L., Phimmachak, S., Seateun, S., Sivongxay, N., Neang, T., Karns, D.R., Andrews, H.L., Osterhage, J., Phipps, E.A. & Ruane, S. (2022) Undescribed diversity in a widespread, common group of Asian mud snakes (Serpentes: Homalopsidae: Hypsiscopus). Ichthyology & Herpetology, 110 (3), 561–574. https://doi.org/10.1643/h2022015
  10. Bivand, R., Keitt, T., Rowlingson, B., Pebesma, E., Sumner, M., Hijmans, R., Baston, D., Rouault, E., Warmerdam, F., Ooms, J. & Rundel, C. (2021) rgdal: Bindings for the “Geospatial” Data Abstraction Library. Available from: https://rgdal.r-forge.r-project.org/ (accessed 29 February 2024)
  11. Bivand, R. & Lewin-Koh, N. (2021) maptools: Tools for Handling Spatial Objects. Available from: https://maptools.r-forge.r-project.org/ (accessed 29 February 2024)
  12. Breitfeld, H.T., Hennig-Breitfeld, J., BouDagher-Fadel, M.K., Hall, R. & Galin, T. (2020) Oligocene-Miocene drainage evolution of NW Borneo: Stratigraphy, sedimentology and provenance of Tatau-Nyalau province sediments. Journal of Asian Earth Sciences, 195, 104331. https://doi.org/10.1016/j.jseaes.2020.104331
  13. Burbrink, F.T., Bernstein, J.M., Kuhn, A., Gehara, M. & Ruane, S. (2021) Ecological divergence and the history of gene flow in the Nearctic milksnakes (Lampropeltis triangulum complex). Systematic Biology, 71 (4), 839–858. https://doi.org/10.1093/sysbio/syab093
  14. Catania, K.C., Leitch, D.B. & Gauthier, D. (2010) Function of the appendages in tentacled snakes ( Erpeton tentaculatus ). Journal of Experimental Biology, 213, 359–367. https://doi.org/10.1242/jeb.039685
  15. Chan, K.O., Sind, L.I., Thong, L.I., Ananthanarayanan, S., Rasu, S., Aowphol, A., Rujirawan, A., Anuar, S., Mulcahy, D., Grismer, J.L. & Grismer, L.L. (2022) Phylogeography of mangrove pit vipers (Viperidae, Trimeresurus erythrurus‐purpureomaculatus complex). Zoologica Scripta, 51, 664–675. https://doi.org/10.1111/zsc.12562
  16. Chen, D. & Chen, H.W. (2013) Using the Köppen classification to quantify climate variation and change: An example for 1901–2010. Environmental Development, 6, 69–79. https://doi.org/10.1016/j.envdev.2013.03.007
  17. Cox, M.J. (1991) Snakes of Thailand and their husbandry. Krieger Pub Co, Malabar, Florida, 526 pp.
  18. David, P. & Vogel, G. (2024) On the status of Helicops wettsteini Amaral, 1929, a senior synonym of Hypsiscopus murphyi (SERPENTES: Homalopsidae). Zootaxa, 5415 (2), 300–308. https://doi.org/10.11646/zootaxa.5415.2.4
  19. De Bruyn, M., Rüber, L., Nylinder, S., Stelbrink, B., Lovejoy, N.R., Lavoué, S., Tan, H.H., Nugroho, E., Wowor, D., Ng, P.K.L., Azizah, M.N.S., von Rintelen, T., Hall, R . & Carvalho, G. R. (2013) Paleo-drainage basin connectivity predicts evolutionary relationships across three Southeast Asian biodiversity hotspots. Systematic Biology, 62 (3), 398–410.
  20. De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886. https://doi.org/10.1080/10635150701701083
  21. Di Cola, V., Broennimann, O., Petitpierre, B., Breiner, F.T., D’Amen, M., Randin, C., Engler, R., Pottier, J., Pio, D., Dubuis, A., Pellissier, L., Mateo, R.G., Hordijk, W., Salamin, N. & Guisan, A. (2017) ecospat: an R package to support spatial analyses and modeling of species niches and distributions. Ecography, 40, 774–787. https://doi.org/10.1111/ecog.02671
  22. Enriquez‐Urzelai, U., Martínez‐Freiría, F., Freitas, I., Perera, A., Martínez‐Solano, Í., Salvi, D., Velo‐Antón, G. & Kaliontzopoulou, A. (2022) Allopatric speciation, niche conservatism and gradual phenotypic change in the evolution of European green lizards. Journal of Biogeography, 49, 2193–2205. https://doi.org/10.1111/jbi.14497
  23. Fabre, A.-C., Bickford, D., Segall, M. & Herrel, A. (2016) The impact of diet, habitat use, and behaviour on head shape evolution in homalopsid snakes. Biological Journal of the Linnean Society, 118, 634–647. https://doi.org/10.1111/bij.12753
  24. Favre, A., Päckert, M., Pauls, S.U., Jähnig, S.C., Uhl, D., Michalak, I. & Muellner‐Riehl, A.N. (2015) The role of the uplift of the Qinghai‐Tibetan Plateau for the evolution of Tibetan biotas. Biological Reviews, 90, 236–253. https://doi.org/10.1111/brv.12107
  25. Fick, S.E. & Hijmans, R.J. (2017) WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302–4315. https://doi.org/10.1002/joc.5086
  26. Fu, J. & Wen, L. (2023) Impacts of Quaternary glaciation, geological history and geography on animal species history in continental East Asia: A phylogeographic review. Molecular Ecology, 32, 4497–4514. https://doi.org/10.1111/mec.17053
  27. Garnier, S., Ross, N., Rudis, R., Camargo, A.P., Sciaini, M. & Scherer, C. (2021) Rvision - Colorblind-Friendly Color Maps for R. R package version 0.6.2. Available from: https://sjmgarnier.github.io/viridis/authors.html (accessed 29 February 2024)
  28. Gressitt, J.L. (1941) Amphibians and reptiles from southeastern China. Philippine Journal of Science, 75, 1–58.
  29. Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321. https://doi.org/10.1093/sysbio/syq010
  30. Hall, R. (1996) Reconstructing Cenozoic SE Asia. In: Hall, R. & Blundell, D. (Eds.), Tectonic Evolution of Southeast Asia. Geological Society of London, London, pp. 153–184.
  31. Hall, R. (1998) The plate tectonics of Cenzoic SE Asia and the distribution of land and sea. In: Hall, R. & Holloway, J.D. (Eds.), Biogeography and geological Evolution of SE Asia. Backbuys Publishers, Leiden, pp. 99–131.
  32. Hall, R. (2009) Southeast Asia’s changing palaeogeography. Blumea - Biodiversity, Evolution and Biogeography of Plants, 54, 148–161. https://doi.org/10.3767/000651909X475941
  33. Hamidy, A., Zakky, Q., Fitriyana, N. & Endarwin, W. (2023) A new species of water snake genus Hypsiscopus (Serpentes: Homalopsidae) from Sulawesi, Indonesia. TREUBIA, 50, 21–38. https://doi.org/10.14203/treubia.v50i1.4511
  34. Hijmans, R.J., Etten, J. van, Sumner, M., Cheng, J., Baston, D., Bevan, A., Bivand, R., Busetto, L., Canty, M., Fasoli, B., Forrest, D., Ghosh, A., Golicher, D., Gray, J., Greenberg, J.A., Hiemstra, P., Hingee, K., Ilich, A., Geosciences, I. for M.A., Karney, C., Mattiuzzi, M., Mosher, S., Naimi, B., Nowosad, J., Pebesma, E., Lamigueiro, O.P., Racine, E.B., Rowlingson, B., Shortridge, A., Venables, B. & Wueest, R. (2022) raster: Geographic Data Analysis and Modeling. Available from: https://cran.r-project.org/web/packages/raster/index.html (accessed 29 February 2024)
  35. Hijmans, R.J. & Graham, C.H. (2006) The ability of climate envelope models to predict the effect of climate change on species distributions: comparing climate envelope and mechanistic models. Global Change Biology, 12, 2272–2281. https://doi.org/10.1111/j.1365-2486.2006.01256.x
  36. Hijmans, R.J., Phillips, S. & Elith, J.L.J. (2021) dismo: Species Distribution Modeling. Available from: https://cran.r-project.org/web/packages/dismo/index.html (accessed 29 February 2024)
  37. Hua, X. & Wiens, J.J. (2010) Latitudinal variation in speciation mechanisms in frogs. Evolution, 64, 429–443. https://doi.org/10.1111/j.1558-5646.2009.00836.x
  38. Hutchison, C.S. (1989) Geological Evolution of South-east Asia. 2nd Edition. Claredon Press, Oxford, 406 pp.
  39. Jayne, B.C., Voris, H.K. & Ng, P.K.L. (2018) How big is too big? Using crustacean-eating snakes (Homalopsidae) to test how anatomy and behaviour affect prey size and feeding performance. Biological Journal of the Linnean Society, 123, 636–650. https://doi.org/10.1093/biolinnean/bly007
  40. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
  41. Karin, B.R., Gamble, T. & Jackman, T.R. (2020) Optimizing phylogenomics with rapidly evolving long exons: comparison with anchored hybrid enrichment and ultraconserved elements. Molecular Biology and Evolution, 37, 904–922. https://doi.org/10.1093/molbev/msz263
  42. Karns, D.R., Lukoschek, V., Osterhage, J., Murphy, J.C. & Voris, H.K. (2010) Phylogeny and biogeography of the Enhydris clade (Serpentes: Homalopsidae). Zootaxa, 2452 (1), 18–30. https://doi.org/10.11646/zootaxa.2452.1.2
  43. Karsen, S.J., Wai-neng Lau, M. & Bogadek, A. (1986) Hong Kong Amphibians and Reptiles. Provisional Urban Council Publication, Hong Kong, 136 pp.
  44. Kass, J.M., Muscarella, R., Galante, P.J., Bohl, C.L., Pinilla-Buitrago, G.E., Boria, R.A., Soley-Guardia, M. & Anderson, R.P. (2021) ENMeval 2.0: Redesigned for customizable and reproducible modeling of species’ niches and distributions. Methods in Ecology and Evolution, 12, 1602–1608. https://doi.org/10.1111/2041-210X.13628
  45. Knouft, J.H., Losos, J.B., Glor, R.E. & Kolbe, J.J. (2006) Phylogenetic analysis of the evolution of the niche in lizards of the Anolis sagrei group. Ecology, 87, S29–S38. https://doi.org/10.1890/0012-9658(2006)87[29:PAOTEO]2.0.CO;2
  46. Kunts, R.E. (1983) Snakes of Taiwan. United States Navy Medical Research Unit No. 2, Taipei, 44 pp.
  47. Lamigueiro, O.P. & Hijmans, R. (2022) rasterVis: Visualization Methods for Raster Data. Available from: https://cran.r-project.org/web/packages/rasterVis/index.html (accessed 29 February 2024)
  48. Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T . & Calcott, B. (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular biology and evolution, 34 (3), 772–773.
  49. Leloup, P.H., Lacassin, R., Tapponnier, P., Schärer, U., Zhong, D., Liu, X., Zhang, L., Ji, S. & Trinh, P.T. (1995) The Ailao Shan-Red River shear zone (Yunnan, China), Tertiary transform boundary of Indochina. Tectonophysics, 251, 3–84. https://doi.org/10.1016/0040-1951(95)00070-4
  50. Li, J.-N., He, C., Guo, P., Zhang, P. & Liang, D. (2017) A workflow of massive identification and application of intron markers using snakes as a model. Ecology and Evolution, 7, 10042–10055. https://doi.org/10.1002/ece3.3525
  51. Li, J.-N., Liang, D., Wang, Y.-Y., Guo, P., Huang, S. & Zhang, P. (2020) A large-scale systematic framework of Chinese snakes based on a unified multilocus marker system. Molecular Phylogenetics and Evolution, 148, 106807. https://doi.org/10.1016/j.ympev.2020.106807
  52. Mell, R. (1922) Beiträge zur Fauna sinica. Die Vertebraten Südchinas: Feldlisten und Feldnoten der Säuger, Vögel, Reptilien, Batrachier, 122 pp.
  53. Minh, B.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
  54. Mulch, A. & Chamberlain, C.P. (2006) The rise and growth of Tibet. Nature, 439, 670–671. https://doi.org/10.1038/439670a
  55. Muñoz, M.M., Crawford, N.G., McGreevy, T.J., Messana, N.J., Tarvin, R.D., Revell, L.J., Zandvliet, R.M., Hopwood, J.M., Mock, E., Schneider, A.L. & Schneider, C.J. (2013) Divergence in coloration and ecological speciation in the Anolis marmoratus species complex. Molecular Ecology, 22, 2668–2682. https://doi.org/10.1111/mec.12295
  56. Murphy, J.C. (2007) Homalopsid Snakes: Evolution in the Mud. Krieger Publishing Company, Malabar, 260 pp.
  57. Murphy, J.C. & Voris, H.K. (2014) A checklist and key to the homalopsid snakes (Reptilia, Squamata, Serpentes), with the description of new genera. Fieldiana Life and Earth Sciences, 2014, 1–43. https://doi.org/10.3158/2158-5520-14.8.1
  58. Murphy, J.C. & Voris, H.K. (2021) A new species of Brachyorrhos from Seram, Indonesia and notes on fangless homalopsids (Squamata, Serpentes). Philippine Journal of Systematic Biology, 14 (2), 1–8 + i–ii. https://doi.org/10.26757/pjsb2020b14015
  59. Murphy, J.C., Voris, H.K. & Karns, D.R. (2012a) The dog-faced water snakes, a revision of the genus Cerberus Cuvier, (Squamata, Serpentes, Homalopsidae), with the description of a new species. Zootaxa, 3484 (1), 1–34. https://doi.org/10.11646/zootaxa.3484.1.1
  60. Murphy, J.C., Voris, H.K., Karns, D.R., Chan-ard, T. & Suvunrat, K. (1999) The ecology of the water snakes of Ban Tha Hin, Songkhla Province, Thailand. Natural History Bulletin of the Siam Society, 47, 129–147.
  61. Murphy, J.C., Voris, H.K., Murthy, B.H.C.K., Traub, J. & Cumberbatch, C. (2012b) The masked water snakes of the genus Homalopsis Kuhl & van Hasselt, 1822 (Squamata, Serpentes, Homalopsidae), with the description of a new species. Zootaxa, 3208 (1), 1–26. https://doi.org/10.11646/zootaxa.3208.1.1
  62. Neuwirth, E. (2022) RColorBrewer: ColorBrewer Palettes. Available from: https://r-graph-gallery.com/38-rcolorbrewers-palettes.html (accessed 29 February 2024)
  63. 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
  64. O’Connell, K.A., Mulder, K.P., Wynn, A., Queiroz, K. & Bell, R.C. (2021) Genomic library preparation and hybridization capture of formalin‐fixed tissues and allozyme supernatant for population genomics and considerations for combining capture‐ and RADseq‐based single nucleotide polymorphism data sets. Molecular Ecology Resources, 22 (2), 487–502. https://doi.org/10.1111/1755-0998.13481
  65. Ogden, R. & Thorpe, R.S. (2002) Molecular evidence for ecological speciation in tropical habitats. Proceedings of the National Academy of Sciences, 99, 13612–13615. https://doi.org/10.1073/pnas.212248499
  66. Pebesma, E. (2018) Simple Features for R: Standardized Support for Spatial Vector Data. The R Journal, 10, 439. https://doi.org/10.32614/RJ-2018-009
  67. Peel, M.C., Finlayson, B.L. & McMahon, T.A. (2007) Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences, 11, 1633–1644. https://doi.org/10.5194/hess-11-1633-2007
  68. Phillips, S.J., Anderson, R.P. & Schapire, R.E. (2006) Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190, 231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
  69. Phillips, S.J., Dudík, M. & Schapire, R.E. (2004) A maximum entropy approach to species distribution modeling. In: Proceedings of the twenty-first international conference on Machine learning. ICML ’04. Association for Computing Machinery, New York, New York, pp. 83. https://doi.org/10.1145/1015330.1015412
  70. Pope, C.H. (1929) A list of reptiles known to occur in Fukien Province, China. Proceedings of the Natural History Society of Fukien, 2, 20–22.
  71. Pyron, A.R. & Burbrink, F.T. (2009) Lineage diversification in a widespread species: roles for niche divergence and conservatism in the common kingsnake, Lampropeltis getula. Molecular Ecology, 18, 3443–3457. https://doi.org/10.1111/j.1365-294X.2009.04292.x
  72. Qu, Y., Song, G., Gao, B., Quan, Q., Ericson, P.G.P. & Lei, F. (2015) The influence of geological events on the endemism of East Asian birds studied through comparative phylogeography B. Riddle (Ed). Journal of Biogeography, 42, 179–192. https://doi.org/10.1111/jbi.12407
  73. Quah, E.S.H., Grismer, L.L., Wood, P.L., Jr., Thura, M.K., Zin, T., Kyaw, H., Lwin, N., Grismer, M.S. & Murdoch, M.L. (2017) A new species of Mud Snake (Serpentes, Homalopsidae, Gyiophis Murphy & Voris, 2014) from Myanmar with a first molecular phylogenetic assessment of the genus. Zootaxa, 4238 (4), 571–582. https://doi.org/10.11646/zootaxa.4238.4.5
  74. Quah, E.S.H., Wood, P.L.Jr., Grismer, L.L. & Sah, S.A.M. (2018) On the taxonomy and phylogeny of the rare Selangor Mud Snake (Raclitia indica) Gray (Serpentes, Homalopsidae) from Peninsular Malaysia. Zootaxa, 4514 (1), 53. https://doi.org/10.11646/zootaxa.4514.1.4
  75. Rambaut, A. (2014) FigTree v1.4.2. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 29 February 2024)
  76. Ramos, E.K.S., Magalhães, R.F. de, Marques, N.C.S., Baêta, D., Garcia, P.C.A. & Santos, F.R. (2019) Cryptic diversity in Brazilian endemic monkey frogs (Hylidae, Phyllomedusinae, Pithecopus) revealed by multispecies coalescent and integrative approaches. Molecular Phylogenetics and Evolution, 132, 105–116. https://doi.org/10.1016/j.ympev.2018.11.022
  77. Raxworthy, C.J., Ingram, C.M., Rabibisoa, N. & Pearson, R.G. (2007) Applications of ecological niche modeling for species delimitation: a review and empirical evaluation using day geckos (Phelsuma) from Madagascar. Systematic Biology, 56, 907–923. https://doi.org/10.1080/10635150701775111
  78. Richards, C.L., Carstens, B.C. & Lacey Knowles, L. (2007) Distribution modelling and statistical phylogeography: an integrative framework for generating and testing alternative biogeographical hypotheses. Journal of Biogeography, 34, 1833–1845. https://doi.org/10.1111/j.1365-2699.2007.01814.x
  79. Rissler, L.J. & Apodaca, J.J. (2007) Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the Black Salamander (Aneides flavipunctatus). Systematic Biology, 56, 924–942. https://doi.org/10.1080/10635150701703063
  80. Ronquist, F.M., 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 (3), 539–542. https://doi.org/10.1093/sysbio/sys029
  81. Rossman, D.A. & Scott, N. J. (1968) Identity of Helicopes wettsteini Amaral (Serpentes: Colubridae). Herpetologica, 24 (3), 262–263.
  82. Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J.C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S.E. & Sánchez-Gracia, A. (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution, 34, 3299–3302. https://doi.org/10.1093/molbev/msx248
  83. Ruane, S. & Austin, C.C. (2017) Phylogenomics using formalin-fixed and 100+ year-old intractable natural history specimens. Molecular Ecology Resources, 17, 1003–1008. https://doi.org/10.1111/1755-0998.12655
  84. Sabaj, M.H. (2016) Standard symbolic codes for institutional resource collections in herpetology and ichthyology: an online reference. Version 6.5. American Society of Ichthyologists and Herpetologists, 108, 593–669. https://doi.org/10.1643/ASIHCODONS2020
  85. Salles, T., Mallard, C., Husson, L., Zahirovic, S., Sarr, A.-C. & Sepulchre, P. (2021) Quaternary landscape dynamics boosted species dispersal across Southeast Asia. Communications Earth & Environment, 2, 240. https://doi.org/10.1038/s43247-021-00311-7
  86. Schmidt, K.P. (1927) The reptiles of Hainan. Bulletin of the American Museum of Natural History, 54, 395–465.
  87. Schneider, C.J., Smith, T.B., Larison, B. & Moritz, C. (1999) A test of alternative models of diversification in tropical rainforests: Ecological gradients vs. rainforest refugia. Proceedings of the National Academy of Sciences, 96, 13869–13873. https://doi.org/10.1073/pnas.96.24.13869
  88. Shen, X.X., Liang, D., Feng, Y.J., Chen, M.Y. & Zhang, P. (2013) A versatile and highly efficient toolkit including 102 nuclear markers for vertebrate phylogenomics, tested by resolving the higher level relationships of the Caudata. Molecular Biology and Evolution, 30, 2235–2248. https://doi.org/10.1093/molbev/mst122
  89. Simmons, J.E. (2015) Herpetological collecting and collections management. Society for the Study of Amphibians and Reptiles Herpetological Circular, 42, 1–191.
  90. Soto-Centeno, J.A. (2022) ENMpipe: a tutorial pipeline for building and testing ecological niche models. Available from: https://github.com/mormoops/ENMpipe (accessed 29 February 2024)
  91. Urbanek, S. (2021) rJava: Low-Level R to Java Interface. Available from: https://cran.r-project.org/web/packages/rJava/index.html (accessed 29 February 2024)
  92. Voris, H.K. (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography, 27, 1153–1167. https://doi.org/10.1046/j.1365-2699.2000.00489.x
  93. Weijola, V., Vahtera, V., Lindqvist, C. & Kraus, F. (2019) A molecular phylogeny for the Pacific monitor lizards (Varanus subgenus Euprepiosaurus) reveals a recent and rapid radiation with high levels of cryptic diversity. Zoological Journal of the Linnean Society, 186, 1053–1066. https://doi.org/10.1093/zoolinnean/zlz002
  94. Wickham, H. (2011) ggplot2: ggplot2. Wiley Interdisciplinary Reviews: Computational Statistics, 3, 180–185. https://doi.org/10.1002/wics.147
  95. Wickham, H., Averick, M., Bryan, J., Chang, W., McGowan, L.D., François, R., Grolemund, G., Hayes, A., Henry, L., Hester, J., Kuhn, M., Pedersen, T.L., Miller, E., Bache, S.M., Müller, K., Ooms, J., Robinson, D., Seidel, D.P., Spinu, V., Takahashi, K., Vaughan, D., Wilke, C., Woo, K. & Yutani, H. (2019) Welcome to the Tidyverse. Journal of Open Source Software, 4, 1686. https://doi.org/10.21105/joss.01686
  96. Wickham, H., François, R., Henry, K. & Müller, K. (2020) dplyr: a grammar of data manipulation. Available from: https://dplyr.tidyverse.org/ (accessed 29 February 2024)
  97. Wiens, J.J. (2004) Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution, 58, 193–197. https://doi.org/10.1111/j.0014-3820.2004.tb01586.x
  98. Wiens, J.J. & Graham, C.H. (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics, 36, 519–539. https://doi.org/10.1146/annurev.ecolsys.36.102803.095431
  99. Yuan, Z.-Y., Suwannapoom, C., Yan, F., Poyarkov, N.A., Nguyen, S.N., Chen, H., Chomdej, S., Murphy, R.W. & Che, J. (2016) Red River barrier and Pleistocene climatic fluctuations shaped the genetic structure of Microhyla fissipes complex (Anura: Microhylidae) in southern China and Indochina. Current Zoology, 62, 531–543. https://doi.org/10.1093/cz/zow042
  100. Zhang, D.-R., Chen, M.-Y., Murphy, R.W., Che, J., Pang, J.-F., Hu, J.-S., Luo, J., Wu, S.-J., Ye, H. & Zhang, Y.-P. (2010a) Genealogy and palaeodrainage basins in Yunnan Province: Phylogeography of the Yunnan spiny frog, Nanorana yunnanensis (Dicroglossidae). Molecular Ecology, 19, 3406–3420. https://doi.org/10.1111/j.1365-294X.2010.04747.x
  101. Zhang, M., Rao, D., Yang, J., Yu, G. & Wilkinson, J.A. (2010b) Molecular phylogeography and population structure of a mid-elevation montane frog Leptobrachium ailaonicum in a fragmented habitat of southwest China. Molecular Phylogenetics and Evolution, 54, 47–58. https://doi.org/10.1016/j.ympev.2009.10.019