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
Sky Islands are high-elevation environments that are separated by warmer, low elevations, forming natural patches of unique montane habitat that often persist through changing climates. Peninsular India was ancestrally forested and has gradually become more arid since at least the Oligocene, and open landscapes have dominated since the middle-late Miocene. Mesic forests today are largely restricted to coastal mountains and some other montane habitats. A mitochondrial phylogeny and fossil-calibrated timetree of Indian Hemiphyllodactylus reveal an Indochinese origin and an endemic radiation with 12 species-level lineages, where a single species was known, that diversified in the Oligocene-Miocene across montane forest habitats in the Eastern Ghats and south India. The phylogeny also suggests the discontinuous Eastern Ghats mountain range encompasses two distinct biogeographic entities: north and south of the Pennar/Krishna-Godavari River basins. This study highlights the deep history of the region and the importance of montane habitats as islands of unique biodiversity that have persisted through millions of years of changing climates. We describe three new species: Hemiphyllodactylus arakuensis sp. nov., H. jnana sp. nov. and H. kolliensis sp. nov. from montane habitats above 1000 m. The montane habitats of these species are emerging hotspots of reptile endemism, and this study emphasizes the need for systematic biodiversity inventory across India to uncover basic patterns of diversity and distribution.
KeywordsBiogeography Divergence dating Eastern Ghats Systematics Western Ghats
We thank Pratyush P Mohapatra, Aparna Lajmi, R Chaitanya and the Evolutionary Ecology Lab (CES, IISc; Saunak Pal, SP Vijayakumar and Kartik Shanker) for contributing tissues used in this study. We also thank the Andhra Pradesh and Tamil Nadu Forest Departments for collection permits and hospitality and Tarun Khichi, Aniruddha Datta-Roy, V Deepak, R Chaitanya, MS Chaitra, R. Padmawathe and Nikhil Gaitonde for assistance in the field. Lee Grismer helped with r scripts and discussion on multivariate analyses, Maitreya Sil with Lagrange analyses, SR Ganesh with sampling locations in the Shevaroys, and Saunak Pal provided data on BNHS specimens. Joshua Muyiwa, Luis Ceriaco, and Shreya Yadav contributed to nomenclatural discussions. The two reviewers provided useful inputs.
Partial funding came from the Ministry of Environment and Forests, the Department of Atomic Energy (2012/21/06/BRNS to Uma Ramakrishnan), the Department of Science and Technology (DST grant SR/SO/AS-57/2009 to Praveen Karanth), Government of India and National Science Foundation (USA) grant DEB 0844523 to Aaron M Bauer.
Compliance with ethical standards
No live animals were used in experiments, and specimens were collected with permits from the Andhra Pradesh and Tamil Nadu forest Departments, besides from private land and other non-forest areas. Specimens collected for this study were euthanized with halothane, tissue vouchers stored in ethanol and whole specimens fixed with formalin. This study was approved by the National Centre for Biological Sciences, Bangalore (NCBS) animal ethics committee.
- Aengals, R. (2013). First record of Indian slender gecko (Hemiphyllodactylus aurantiacus) from Yelagiri hills, Tamil Nadu. Cobra, 7, 24–26.Google Scholar
- Aengals, R., & Ganesh, S. R. (2013). Rhinophis goweri — a new species of shieldtail snake from the southern Eastern Ghats, India. Russian Journal of Herpetology, 20, 61–65.Google Scholar
- Agarwal, I., Datta-Roy, A., Bauer, A. M., & Giri, V. B. (2012). Rediscovery of Geckoella jeyporensis (Squamata: Gekkonidae), with notes on morphology, coloration and habitat. Hamadryad, 36, 17–24.Google Scholar
- Bauer, A. M., & Das, I. (1999). The systematic status of the endemic South Indian gecko Hemiphyllodactylus aurantiacus (Beddome, 1870). Journal of South Asian Natural History, 4, 213–218.Google Scholar
- Beddome, R. H. (1863). Descriptions of new species of the family Uropeltidae from Southern India, with notes on other little-known species. Proceedings of the Zoological Society of London, 1863, 225–229.Google Scholar
- Beddome, R. H. (1870). Descriptions of some new lizards from the Madras Presidency. Madras Monthly journal of Medical Science, 1, 30–35.Google Scholar
- Beddome, R. H. (1878). Descriptions of new reptiles from the Madras Presidency. Proceedings of the Zoological Society of London, 1877, 685–686.Google Scholar
- Bleeker, P. (1860). Reptilien van Agam. Natuurkundig Tijdschrift voor Nederlandsch Indie. Batavia, 20, 325–329.Google Scholar
- Cobos, A. L., Grismer, L. L., Wood, P. L., Jr., Quah, E. S. H., Anuar, S., & Muin, M. A. (2016). Phylogenetic relationships of geckos of the Hemiphyllodactylus harterti group, a new species from Penang Island, peninsular Malaysia, and a likely case of true cryptic speciation. Zootaxa, 4107, 367–380.CrossRefPubMedGoogle Scholar
- Daniels, R. J. R. (1994). Notes on a rare south Indian Gecko, Hemiphyllodactylus typus Beddome. Dactylus, 2, 132–133.Google Scholar
- Daniels, R. J. R., & Kumar, M. V. R. (1998). Amphibians and reptiles of Kolli Hills. Cobra, 31, 3–5.Google Scholar
- Daniels, R. J. R., & Vencatesan, J. (1998). Ecosystem flips in cultural landscapes: the case of Kolli Hills. Current Science, 75, 353–355.Google Scholar
- Das, I., & Bauer, A. M. (2000). Two new species of Cnemaspis (Sauria: Gekonidae) from Tamil Nadu, southern India. Russian Journal of Herpetology, 7, 17–28.Google Scholar
- Deutsch, C. A., Tewksbury, J. J., Huey, R. B., Sheldon, K. S., Ghalambor, C. K., Haak, D. C., & Martin, P. R. (2008). Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences United States of America, 105, 6668–6672. https://doi.org/10.1073/pnas.0709472105.CrossRefGoogle Scholar
- Drummond, A. J., Rambaut, A., & Suchard M. A. (2016) BEAST 1.8.4. Available from http://beast.bio.ed.ac.uk/. Accessed 24 May 2018.
- Ganesh, S. R., & Arumugam, M. (2015). Microhabitat use and abundance estimates of understorey herpetofauna in the highlands of southern Eastern Ghats, India, with observations on roadkill mortalities. Asian Journal of Conservation Biology, 4, 143–150.Google Scholar
- Ganesh, S. R., & Arumugam, M. (2016). Species richness of montane herpetofauna of southern Eastern Ghats, India: a historical resume and a descriptive checklist. Russian Journal of Herpetology, 23, 7–24.Google Scholar
- Giri, V. B., Agarwal, I., & Bauer, A. M. (2009). Designation of a neotype for Cnemaspis mysoriensis (Jerdon 1853) (Sauria: Gekkonidae), with a redescription and notes on its distribution and habitat. Russian Journal of Herpetology, 16, 256–264.Google Scholar
- Gray, J. E. (1825). A synopsis of the genera of reptiles and Amphibia, with a description of some new species. Annals of Philosophy, 10, 193–217.Google Scholar
- Grismer, L. L., Wood, P. L., Jr., Anuar, S., Muin, M. A., Quah, E. S. H., McGuire, J. A., Brown, R. M., Van Tri, N., & Hong Thai, P. (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 Linnaean Society, 169, 849–880.CrossRefGoogle Scholar
- Grismer, L. L., Wood, P. L., Jr., Anuar, S., Quah, E. S. H., Muin, M. A., Onn, C. K., Sumarli, A. X., & Loredo, A. (2015). Repeated evolution of sympatric, palaeoendemic species in closely related, co-distributed lineages of Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) across a sky island archipelago in peninsular Malaysia. Zoological Journal of the Linnaean Society, 174, 859–876.CrossRefGoogle Scholar
- Grismer, L. L., Wood, P. L., Jr., Thura, M. K., Zin, T., Quah, E. S. H., Murdoch, M. L., Grismer, M. S., Lin, A., Kyaw, H., & Ngwe, L. (2017). 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.CrossRefGoogle Scholar
- Grismer, L. L., Wood, P. L., Jr., Thura, M. K., Zin, T., Quah, E. S. H., Murdoch, M. L., Grismer, M. S., Lin, A., Kyaw, H., & Ngwe, L. (2018a). Phylogenetic taxonomy of Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) with descriptions of three new species from Myanmar. Journal of Natural History, 20, 1–98.Google Scholar
- Grismer, L. L., Wood, P. L., Jr., Thura, M. K., Quah, E. S. H., Murdoch, M. L., Grismer, M. S., Herr, M. W., Lin, A., & Kyaw, H. (2018c). 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.CrossRefGoogle Scholar
- Hutchinson, M. N. (1997). The first fossil pygopod (Squamata, Gekkota), and a review of mandibular variation in living species. Memoirs-Queensland Museum, 41, 355–366.Google Scholar
- Jerdon, T. C. (1853). Catalogue of reptiles inhabiting the peninsula of India. Journal of the Asiatic Society of Bengal, 22, 462–479.Google Scholar
- Karanth, P. K. (2015). An island called India: phylogenetic patterns across multiple taxonomic groups reveal endemic radiations. Current Science, 108, 1847–1851.Google Scholar
- Kluge, A. G. (1995). Cladistic relationships of sphaerodactyl lizards. American Museum Novitates, 3139, 1–23.Google Scholar
- Lee, M. S. Y., Oliver, P. M., and Hutchinson, M. N. (2009a) Phylogenetic uncertainty and molecular clock calibrations: a case study of legless lizards (Pygopodidae, Gekkota). Molecular Phylogenetics and Evolution, 50, 661–666. https://doi.org/10.1016/j.ympev.2008.11.024.
- Licht, A., Cappelle, M. V., Abels, H. A., Ladant, J. B., Alexandre, J. T., Lanord, C. F., Donnadieu, Y., Vandenberghe, J., Rigaudier, T., Lecuyer, C., Terry, D., Jr., Adriaens, R., Boura, A., Guo, Z., Naing Soe, A., Quade, J., DupontNivet, G., & Jaeger, J. J. (2014). Asian monsoons in a late Eocene greenhouse world. Nature, 513, 501–506. https://doi.org/10.1038/nature13704.CrossRefPubMedGoogle Scholar
- Maddison, W. P., Maddison, D. R. (2018). Mesquite: a modular system for evolutionary analysis. Version 3.51 http://www.mesquiteproject.org.
- Mertens, R. (1966). Die nichtmadagassichen Arten und Unterarten der Geckonengattung Phelsuma. Senckenbergiana Biologica, 47, 85–110.Google Scholar
- Morley, R. J. (2000). Origin and evolution of tropical rain forests. Chichester: Wiley.Google Scholar
- Morley, R. J. (2007). Cretaceous and tertiary climate change and the past distribution of megathermal rainforests. In M. B. Bush & J. R. Flenley (Eds.), Tropical rainforest responses to climatic change (pp. 1–31). Berlin: Springer.Google Scholar
- Raheem, D. C., Taylor, H., Ablett, J., Preece, R. C., Aravind, N. A., & Naggs, F. (2014). A systematic revision of the land snails of the Western Ghats of India. Tropical Natural History Supplement, 4, 1–294.Google Scholar
- Rambaut, A., Suchard, M. A., Xie, D., & Drummond, A. J. (2014) Tracer 1.6. Retrieved from: http://beast.bio.ed.ac.uk/Tracer. Accessed 03/13/2016.
- Raxworthy, C. J., Pearson, R. G., Rabibisoa, N., Rakotondrazafy, A. M., Ramanamanjato, J. B., Raselimanana, A. P., Wu, S., Nussbaum, R. A., & Stone, D. A. (2008). Extinction vulnerability of tropical montane endemism from warming and upslope displacement: a preliminary appraisal for the highest massif in Madagascar. Global Change Biology, 14, 1703–1720.CrossRefPubMedCentralGoogle Scholar
- Sanyal, D. P., Gupta, B. D., & Gayen, N. C. (1993). Reptilia. In A. K. Ghosh (Ed.), State Fauna Series 5. Fauna of Andhra Pradesh, Part I (pp. 1–63). Kolkata: Zoological Survey of India.Google Scholar
- Smith, M. A. (1935). The fauna of British India, including Ceylon and Burma. In Reptilia and Amphibia. Volume II. Sauria. London: Taylor and Francis.Google Scholar
- Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739. https://doi.org/10.1093/molbev/msr121.CrossRefPubMedPubMedCentralGoogle Scholar
- Vijayakumar, S. P., Menezes, R. C., Jayarajan, A., & Shanker, K. (2016). Glaciations, gradients, and geography: multiple drivers of diversification of bush frogs in the Western Ghats Escarpment. Proceedings of the Royal Society of London B: Biological Sciences, 283(1836), 20161011.CrossRefGoogle Scholar