Comparative population structure in species of bats differing in ecology and morphology in the Andaman Islands, India

• Autorzy: Chakravarty R. , Chattopadhyay B. , Ramakrishnan U. , Ramakrishnan U. , Sivasundar A.
• Języki publikacji: EN

Abstrakty

EN

Gene flow results from movement between populations, homogenising gene pools and impacting genetic variation and evolution. Growing evidence suggests that movement of individuals among populations may be more strongly determined by ecological traits. We compared genetic and morphometric differentiation in four species of bats — Eonycteris spelaea, Cynopterus sphinx, Rhinolophus affinis and Hipposideros pomona — which differ in their flight capability and roosting requirement to understand their effects in shaping genetic structure. Hypervariable region I of the mitochondrial control region was amplified from 40 E. spelaea, 28 C. sphinx, 44 R. affinis and 57 H. pomona sampled from locations spread across the Andaman archipelago. Populations of E. spelaea were nearly panmictic; R. affinis were differentiated into two clusters, and H. pomona were differentiated into three clusters. Consistent genetic and morphometric clusters were obtained for C. sphinx and the genetic break for C. sphinx occurs between Middle and South Andaman Islands, coincided with the Jarawa Tribal Reserve. In conclusion, poorly-dispersing, caveroosting species show high population structure, but when flight capability is very well-developed, the effect of disjunct roost availability is offset. The genetic structure of C. sphinx where we expected panmixia, is possibly confounded by the colonization history of its two genetic lineages and its habitat use which may prevent significant gene flow between the two lineages.

• Wydawca: -
• Czasopismo: Acta Chiropterologica
• Rocznik: 2018
• Tom: 20
• Numer: 1
• Opis fizyczny: p.85-98,fig.,ref.

Twórcy

autor

Chakravarty R.

• Post-Graduate Program in Wildlife Biology and Conservation, Wildlife Conservation Society-India, Bangalore 560097, India and National Centre for Biological Sciences, Bangalore 560065, India

autor

Chattopadhyay B.

• Department of Biological Sciences, National University of Singapore, 16 Science Drive 4, Singapore 117558

autor

Ramakrishnan U.

• National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bellary Road, Bangalore 560065, India

autor

Ramakrishnan U.

• National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bellary Road, Bangalore 560065, India

autor

Sivasundar A.

• National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bellary Road, Bangalore 560065, India

Bibliografia

• 1. Altringham, J. D. 2011. Bats: from evolution to conservation. Oxford University Press, Oxford, xv + 324 pp. Google Scholar
• 2. Aul, B., P. J. J. Bates, D. L. Harrison, and G. Marimuthu. 2014. Diversity, distribution and status of bats on the Andaman and Nicobar Islands, India. Oryx, 48: 204–212. Google Scholar
• 3. Bates, P. J. J. 2012. Bats. Pp. 68–93, in Mammals of South Asia ( A. J. T. Johnsingh and N. Manjrekar, eds.). Universities Press, Telangana, India, 766 pp. Google Scholar
• 4. Bates, P. J. J., and D. L. Harrison. 1997. Bats of the Indian Subcontinent. Harrison Zoological Museum, Sevenoaks, Kent, xvi + 258 pp. Google Scholar
• 5. Bohonak, A. J. 1999. Dispersal, gene flow and population structure. Quarterly Reviews of Biology, 74: 21–45. Google Scholar
• 6. Burland, T. M, and J. Worthington-Wilmer. 2001. Seeing in the dark: molecular approaches to the study of bat populations. Biological Reviews, 76: 389–409. Google Scholar
• 7. Burney, T. M., and R. T. Brumfield. 2009. Ecology predicts levels of genetic differentiation in Neotropical birds. American Naturalist, 174: 358–368. Google Scholar
• 8. Campbell, P., C. J. Schneider, A. M. Adnan, A. Zubaid, and T. H. Kunz. 2004. Phylogeny and phylogeography of Old World fruit bats in the Cynopterus brachyotis complex. Molecular Phylogenetics and Evolution, 33: 764–781. Google Scholar
• 9. Campbell, P., C. J. Schneider, A. M. Adnan, A. Zubaid and T. H. Kunz. 2006. Comparative population structure of Cynopterus fruit bats in peninsular Malaysia and southern Thailand. Molecular Ecology, 15: 29–47. Google Scholar
• 10. Campbell, S., P. Guay, P. John, and R. Mulder. 2009. Genetic differentiation among populations of a specialist fishing bat suggests lack of suitable habitat connectivity. Biological Conservation, 142: 2657–2664. Google Scholar
• 11. Carstens, B. C., J. Sullivan, L. M. Davalos, P. A. Larsen, and S. C. Pedersen. 2004. Exploring population genetic structure in three species of Lesser Antillean bats. Molecular Ecology, 13: 2557–2566. Google Scholar
• 12. Castella, V., M. Ruedi, L. Excoffier, C. Ibañez, R. Arlettaz, and J. Hausser. 2000. Is the Gibraltar strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vespertilionidae)? Molecular Ecology, 9: 1761–1772. Google Scholar
• 13. Castella, V., M. Ruedi, and L. Excoffier. 2008. Contrasted pat terns of mitochondrial and nuclear structure among nursery colonies of the bat Myotis myotis. Journal of Evolutionary Biology, 14: 708–720. Google Scholar
• 14. Champion, H. G., and S. K. Seth. 1968. Revised survey of the forest types of India. Natraj Publishers, Dehradun, India, 404 pp. Google Scholar
• 15. Chattopadhyay, B., K. M. Garg, A. K. V. Kumar, D. P. S. Doss, F. E. Rheindt, S. Kandula, and U. Ramakrishnan. 2016. Gen n ome-wide data reveal cryptic diversity and genetic introgression in an Oriental Cynopterine fruit bat radiation. BMC Evolutionary Biology, 16: 41. Google Scholar
• 16. Chen, J., S. J. Rossiter, J. R. Flanders, Y. Sun, P. Hua, C. Miller-Butterworth, X. Liu, K. E. Rajan, and S. Zhang. 2010. Contrasting genetic structure in two co-distributed species of old world fruit bat. PLoS ONE, 5: e13903. Google Scholar
• 17. Chen, S.-F., S. J. Rossiter, C. G. Faulkes, and G. Jones. 2006. Population genetic structure and demographic history of the endemic Formosan lesser horseshoe bat (Rhinolophus monoceros). Molecular Ecology, 15: 1643–1656. Google Scholar
• 18. Chen, S.-F., G. Jones, and S. J. Rossiter. 2008. Sex-biased gene flow and colonization in the Formosan lesser horseshoe bat: inference from nuclear and mitochondrial markers. Journal of Zoology (London), 274: 207–215. Google Scholar
• 19. Das, I. 1999. A noteworthy collection of mammals from Mount Harriet, Andaman Islands, India. Journal of South Asian Nat ural History. 4: 181–185. Google Scholar
• 20. Douangboubpha, B., S. Bumrungsri, C. Satasook, P. Soisook, S. S. H. Bu, B. Aul, D. L. Harrison, M. J. Pearch, N. M. Thomas, and P. J. J. Bates. 2011. A new species of small Hipposideros (Chiroptera: Hipposideridae) from Myanmar and a revaluation of the taxon H. nicobarulae Miller, 1902 from the Nicobar Islands. Acta Chiropterologica, 13: 61–78. Google Scholar
• 21. Excoffier, L., and H. E. L. Lischer. 2010. Arlequin suite ver. 3.5: a new series of programs to perform population genetic analyses under Linux and Windows. Molecular Ecology Resources. 10: 564–567. Google Scholar
• 22. Excoffier, L., P. E. Smouse, and J. M. Quattro. 1992. Analysis of Molecular Variance inferred from metric distances among DNA haplotypes. Genetics, 131: 479–491. Google Scholar
• 23. Fenton, M. B., and N. B. Simmons. 2014. Bats. A world of science and mystery. University of Chicago Press, Chicago, IL, 240 pp. Google Scholar
• 24. Furey, N. M., and P. A. Racey. 2016. Can wing morphology inform conservation priorities for Southeast Asian cave bats? Biotropica, 48: 545–556. Google Scholar
• 25. Furmankiewicz, J., and J. A. Altringham. 2006. Genetic structure in a swarming brown long-eared bat (Plecotus auritus) population: evidence for mating at swarming sites. Conservation Genetics, 8: 913–923. Google Scholar
• 26. Futuyma, D. J. 2009. Evolution, 2nd edition. Sinauer Associates Inc. Sunderland, Massachusetts, 614 pp. Google Scholar
• 27. Heaney, L. R., and T. E. Roberts. 2009. New perspectives on long-term biogeographic dynamics and conservation of Philippine fruit bats, Pp. 17–58, in Island bats: Evolution, Ecology and Conservation ( T. H. Kunz and P. A. Racey, eds.). University of Chicago Press, Chicago, IL, 568 pp. Google Scholar
• 28. Kumar, S., G. Stecher, and K. Tamura. 2016. MEGA 7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33: 1870–1874. Google Scholar
• 29. Kunz, T. H., and S. Parsons (eds.). 2009. Ecological and behavioural methods for the study of bats, 2nd edition. Johns Hopkins University Press, Baltimore, 920 pp. Google Scholar
• 30. Li, G., G. Jones, S. J. Rossiter, S.-F. Chen, S. Parsons, and S. Zhang. 2006. Phylogenetics of small horseshoe bats from East Asia based on mitochondrial DNA sequence variation. Journal of Mammalogy, 87: 1234–1240. Google Scholar
• 31. Lin, A. Q, G. Csorba, L.-F. Li, T.-L. Jiang, G.-J. Lu, V. D. Thong, P. Soisook, K.-P. Sun, and J. Feng. 2013. Phylogeography of Hipposideros armiger (Chiroptera: Hipposideridae) in the Oriental region: the contribution of multiple Pleistocene glacial refugia and intrinsic factors to con temporary population genetic structure. Journal of Biogeography, 41: 317–327. Google Scholar
• 32. Loveless, M. D. and J. L. Hamrick. 1984. Ecological determinants of genetic structure in plant populations. Annual Reviews of Ecology, Evolution and Systematics, 15: 65–95. Google Scholar
• 33. Maharadatunkamsi, S. Hisheh, D. J. Kitchener and L. H. Schmitt. 2000. Genetic and morphometric diversity in Walla cea: Geographical patterning in the horseshoe bat, Rhinolophus affinis. Journal of Biogeography, 27: 193–201. Google Scholar
• 34. Maharadatunkamsi, S. Hisheh, D. J. Kitchener and L. H. Schmitt. 2003. Relationships between morphology, genetics and geography in the cave fruit bat Eonycteris spelaea (Dobson, 1871) from Indonesia. Biological Journal of the Linnean Society, 79: 511–522. Google Scholar
• 35. McCracken, G. F., and M. F. Gassel. 1997. Genetic structure in migratory and non-migratory populations of Brazilian free-tailed bats. Journal of Mammalogy, 78: 348–357. Google Scholar
• 36. Menon, V. 2014. Indian Mammals: a field guide. Hachette India, Gurgaon, India, 528 pp. Google Scholar
• 37. Meyer, C. F. J., E. K. V. Kalko, and G. Kerth. 2009. Smallscale fragmentation effects on local genetic diversity in two phyllostomid bats with different dispersal abilities in Panama. Biotropica, 41: 95–102. Google Scholar
• 38. Miller-Butterworth, C. M., D. S. Jacobs, and E. H. Harley. 2003. Strong population substructure is correlated with morphology and ecology in a migratory bat. Nature, 424: 187–191. Google Scholar
• 39. Moussy, C., D. J. Hosken, F. Mathews, G. C. Smith, J. N. Aegerter and S. Bearhop. 2013. Migration and dispersal patterns of bats and their influence on genetic structure. Mammal Reviews, 43: 183–195. Google Scholar
• 40. Newton, L. R., J. M. Nassar, and T. H. Fleming. 2003. Genetic population structure and mobility of two nectar-feeding bats from Venezuelan deserts: inferences from mitochondrial DNA. Molecular Ecology, 12: 3191–3198. Google Scholar
• 41. Norberg, U. M., and J. M. V. Rayner. 1987. Ecological morphology and flight in bats (Mammalia: Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philosophical Transactions of the Royal Society of London, 316B: 335–427. Google Scholar
• 42. Olival, K. J. 2012. Evolutionary and ecological correlates of population genetic structure in bats, Pp. 267–316, in Evolutionary history of bats: fossils, molecules and morphology ( G. F. Gunnell and N. B. Simmons, eds.). Cambridge University Press, Cambridge, 560 pp. Google Scholar
• 43. Petit, E., F. Balloux, and J. Goudet. 2001. Sex-biased dispersal in a migratory bat: a characterization using sex-specific demographic parameters. Evolution, 55: 635–640. Google Scholar
• 44. R Core Team. 2016. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/ . Google Scholar
• 45. Ripperger, S. P., M. Tschapka, E. K. V. Kalko, B. Rodriguez-Herrera, and F. Mayer. 2013. Life in a mosaic landscape: anthropogenic habitat fragmentation affects genetic population structure in a frugivorous bat species. Conservation Genetics, 14: 925–934. Google Scholar
• 46. Ripperger, S. P., M. Tschapka, E. K. V. Kalko, B. Rodriguez-Herrera, and F. Mayer. 2014. Resisting habitat fragmentation: high genetic connectivity among populations of the frugivorous bat Carollia castanea in an agricultural landscape. Agriculture, Ecosystems and Environment, 185: 9–15. Google Scholar
• 47. Rivers, N. M., R. K. Butlin, and J. D. Altringham. 2005. Genetic population structure of Natterer's bats explained by mating at swarming sites and philopatry. Molecular Ecology, 14: 4299–4312. Google Scholar
• 48. Rossiter, S. J., G. Jones, R. D. Ransome, and E. M. Barratt. 2000. Genetic variation and population structure in the endangered greater horseshoe bat Rhinolophus ferrumequinum. Molecular Ecology, 9: 1131–1135. Google Scholar
• 49. Rozas, J., and R. Rozas. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics, 15: 174–175. Google Scholar
• 50. Russell, A. L., R. A. Medellin, and G. F. McCracken. 2005. Genetic variation and migration in the Mexican free-tailed bat (Tadarida brasiliensis mexicana). Molecular Ecology, 14: 2207–2222. Google Scholar
• 51. Sagot, M., and G. Chaverri. 2015. Effects of roost specialization on extinction risk in bats. Conservation Biology, 29: 1666–1673. Google Scholar
• 52. Schmitt, L., S. Hisheh, A. Suyanto, Maharadatunkamsi, C. Newbound, D. J. Kitchener, and R. How. 2009. Crossing the line: The impact of contemporary and historical sea barriers on the population structure of bats in Southern Wallacea. Pp. 59–96, in Island bats: evolution, ecology and conservation ( T. H. Kunz and P. A. Racey, eds.). University of Chicago Press, Chicago, IL, 568 pp. Google Scholar
• 53. Schneider, C. A., W. S. Rasband, and K. W. Eliceiri. 2012. NIH Image to Image J: 25 years of image analysis. Nature Methods, 9: 671–675. Google Scholar
• 54. Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science, 236: 787–792. Google Scholar
• 55. Speer, K. A., B. J. Petronio, N. B. Simmons, R. Richey, K. Magrini, J. A. Soto-Centeno, and D. L. Reed. 2017. Population structure of a widespread bat (Tadarida brasiliensis) in an island system. Ecology and Evolution, 7: 7585–7598. Google Scholar
• 56. Srinivasulu, C., and B. Srinivasulu. 2002. Greater shortnosed fruit bat (Cynopterus sphinx) foraging and damage in vineyards in India. Acta Chiropterologica, 4: 167–171. Google Scholar
• 57. Srinivasulu, C., A. Srinivasulu, B. Srinivasulu, A. Gopi, T. H. Dar, P. J. J. Bates, S. J. Rossiter, and G. Jones. 2017. Recent surveys of bats from the Andaman Islands, India: diversity, distribution, and echolocation characteristics. Acta Chiropterologica, 19: 419–437. Google Scholar
• 58. Storz, J. F. 2002. Contrasting patterns of divergence in quantitative traits and neutral DNA markers: analysis of clinal variation. Molecular Ecology, 11: 2537–2551. Google Scholar
• 59. Storz, J. F., J. Balasingh, H. R. Bhat, P. T. Nathan, D. P. S. Doss, A. A. Prakash, and T. H. Kunz. 2001. Clinal variation in body size and sexual dimorphism in an Indian fruit bat, Cynopterus sphinx (Chiroptera: Pteropodidae). Biological Journal of the Linnean Society, 72: 17–31. Google Scholar
• 60. Varudkar, A., and U. Ramakrishnan. 2015. Commensalism facilitates gene flow in mountains: a comparison between two Rattus species. Heredity, 115: 253–261. Google Scholar
• 61. Veith, M., N. Beer, A. Kiefer, J. Johannsen, and A. Sietz. 2004. The role of swarming sites for maintaining gene flow in the brown long-eared bat (Plecotus auritus). Heredity, 93: 342–349. Google Scholar
• 62. VonHoldt, B. M., D. R. Stahler, E. E. Bangs, D. W. Smith, M. D. Jimenez, C. M. Mack, C. C. Niemeyer, J. P. Pollinger, and R. K. Wayne. 2010. A novel assessment of population structure and gene flow in grey wolf populations of the Northern Rocky Mountains of the United States. Molecular Ecology, 19: 4412–4427. Google Scholar
• 63. Weir, B. S., and C. C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38: 1358–1370. Google Scholar
• 64. Wilson, D. E., and D. M. Reeder. 2005. Mammal species of the World. Smithsonian Institution Press, Washington, D.C., xvii + 1207 pp. Google Scholar
• 65. Worthington-Wilmer, J., and E. Barratt. 1996. A non-lethal method of tissue sampling for genetic studies of chiropterans. Bat Research News, 37: 1–3. Google Scholar
• 66. Worthington-Wilmer, J., L. Hall, E. Barratt, C. Moritz, S. Url, and L. E. S. Hall. 1999. Genetic structure and male-mediated gene flow in the ghost bat (Macroderma gigas). Evolution, 53: 1582–1591.

Identyfikatory

DOI

10.3161/15081109ACC2018.20.1.006