Title: A time-calibrated phylogenetic approach to assessing the phylogeography, colonization history and phenotypic evolution of snakes in the Japanese Izu Islands
Abstract: Journal of BiogeographyVolume 38, Issue 2 p. 259-271 A time-calibrated phylogenetic approach to assessing the phylogeography, colonization history and phenotypic evolution of snakes in the Japanese Izu Islands Takeo Kuriyama, Takeo Kuriyama Faculty of Science, Toho University, Funabashi City, Chiba 274-8510, JapanSearch for more papers by this authorMatthew C. Brandley, Matthew C. Brandley Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520-8105, USA, Present address: School of Biological Sciences, University of Sydney, NSW 2006, AustraliaSearch for more papers by this authorAkira Katayama, Akira Katayama Department of Zoology, Graduate School of Science, Kyoto University, Sakyo, Kyoto 606-8502, JapanSearch for more papers by this authorAkira Mori, Akira Mori Department of Zoology, Graduate School of Science, Kyoto University, Sakyo, Kyoto 606-8502, JapanSearch for more papers by this authorMasanao Honda, Masanao Honda Graduate School of Life and Environmental Sciences, University of Tsukuba, Ibaraki 305-8577, JapanSearch for more papers by this authorMasami Hasegawa, Corresponding Author Masami Hasegawa Faculty of Science, Toho University, Funabashi City, Chiba 274-8510, Japan Masami Hasegawa, Faculty of Science, Toho University, Funabashi City, Chiba, 274-8510, Japan.E-mail: [email protected]Search for more papers by this author Takeo Kuriyama, Takeo Kuriyama Faculty of Science, Toho University, Funabashi City, Chiba 274-8510, JapanSearch for more papers by this authorMatthew C. Brandley, Matthew C. Brandley Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520-8105, USA, Present address: School of Biological Sciences, University of Sydney, NSW 2006, AustraliaSearch for more papers by this authorAkira Katayama, Akira Katayama Department of Zoology, Graduate School of Science, Kyoto University, Sakyo, Kyoto 606-8502, JapanSearch for more papers by this authorAkira Mori, Akira Mori Department of Zoology, Graduate School of Science, Kyoto University, Sakyo, Kyoto 606-8502, JapanSearch for more papers by this authorMasanao Honda, Masanao Honda Graduate School of Life and Environmental Sciences, University of Tsukuba, Ibaraki 305-8577, JapanSearch for more papers by this authorMasami Hasegawa, Corresponding Author Masami Hasegawa Faculty of Science, Toho University, Funabashi City, Chiba 274-8510, Japan Masami Hasegawa, Faculty of Science, Toho University, Funabashi City, Chiba, 274-8510, Japan.E-mail: [email protected]Search for more papers by this author First published: 15 October 2010 https://doi.org/10.1111/j.1365-2699.2010.02403.xCitations: 27Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstract Aim We infer the biogeography and colonization history of a dispersal-limited terrestrial vertebrate, the Japanese four-lined ratsnake (Elaphe quadrivirgata), to reveal the number of times mainland populations have invaded the Izu Archipelago of Japan, the mainland sources of these colonists, and the time-scale of colonization. We compare these results with those of past studies in an attempt to uncover general biogeographical patterns. Moreover, we briefly examine the significance of colonization history when evaluating the evolution of body size and melanism of the Izu Island E. quadrivirgata populations. Location The Izu Islands (Oshima, Toshima, Niijima, Shikine, Kozu, Tadanae and Mikura), a volcanic archipelago off the Pacific coast of central Japan. Methods We obtained DNA sequences of the mitochondrial cytochrome b gene (1117 base pairs) from 373 individual snakes sampled from seven of the Izu Islands and 25 mainland localities. We employed partitioned Bayesian phylogenetic analyses assuming a relaxed molecular clock to estimate phylogenetic relationships among extant haplotypes and to give an explicit temporal scale to the timing of clade divergence, colonization history and tempo of body-size evolution. Moreover, we employed model-based biogeographical analysis to calculate the minimum number of times E. quadrivirgata colonized the Izu Islands. Results We found evidence that three separate regions of the Izu Archipelago have been colonized independently from mainland ancestors within the past 0.58–0.20 Ma. The Izu Peninsula plus Oshima and Mikura were both colonized independently from lineages inhabiting eastern mainland Japan. The Toshima, Niijima, Shikine, Kozu and Tadanae populations all derive from a single colonization from western mainland Japan. Oshima has been subject to three or possibly four colonizations. Main conclusions These results support the hypothesis that the extreme body-size disparity among island populations of this ratsnake evolved in situ. Moreover, the fact that the dwarf, melanistic population inhabiting Oshima descends from multiple mainland colonization events is evidence of an extremely strong natural selection pressure resulting in the rapid evolution of this unique morphology. These results contrast with theoretical predictions that natural selection pressures should play a decreased role on islands close to the mainland and/or subject to frequent or recent immigration. References Abe, H., Matsuki, R., Ueno, S., Nashimoto, M. & Hasegawa, M. (2006) Dispersal of Camellia japonica seeds by Apodemus speciosus speciosus revealed by maternity analyses of plants and behavioral observations of animal vectors. Ecological Research, 21, 732– 740. Brandley, M.C., Schmitz, A. & Reeder, T.W. (2005) Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Systematic Biology, 54, 373– 390. Brandley, M.C., Wang, Y., Guo, X., Nieto Montes de Oca, A., Fería Ortíz, M., Hikida, T. & Ota, H. (in press) Accommodating locus-specific heterogeneity in molecular dating methods: an example using inter-continental dispersal of Plestiodon (Eumeces) lizards. Systematic Biology. Burbrink, F.T. & Lawson, R. (2007) How and when did Old World ratsnakes disperse into the New World? Molecular Phylogenetics and Evolution, 43, 173– 189. Burbrink, F.T., Lawson, R. & Slowinksi, J.B. (2000) Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept. Evolution, 54, 2107– 2118. Camin, J.H. & Ehrlich, P.R. (1958) Natural selection in water snakes (Natrix sipedon L.) on islands in Lake Erie. Evolution, 12, 504– 511. Carstens, B.C. & Knowles, L.L. (2007) Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers. Systematic Biology, 56, 400– 411. Castoe, T.A., Doan, T.M. & Parkinson, C.L. (2004) Data partitions and complex models in Bayesian analysis: the phylogeny of gymnophthalmid lizards. Systematic Biology, 53, 448– 469. Chase, J.M. (2003) Community assembly: when should history matter? Oecologia, 136, 489– 498. Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214. Drummond, A.J., Ho, S.Y.W., Phillips, M.J. & Rambaut, A. (2006) Relaxed phylogenetics and dating with confidence. PLOS Biology, 4, e88. Emerson, B.C. (2002) Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Molecular Ecology, 11, 951– 966. Emerson, B.C., Oromí, P. & Hewitt, G.M. (2000) Tracking colonization and diversification of insect lineages on islands: mitochondrial DNA phylogeography of Tarphius canariensis (Coleoptera: Colydiidae) on the Canary Islands. Proceedings of the Royal Society B: Biological Sciences, 267, 2199– 2205. Fukami, T., Beaumont, H.J.E., Zhang, X.X. & Rainey, P.B. (2007) Immigration history controls diversification in experimental adaptive radiation. Nature, 446, 436– 439. Gillespie, R.G. (2004) Community assembly through adaptive radiation in Hawaiian spiders. Science, 303, 356– 359. Gillespie, R.G. & Roderick, G.K. (2002) Arthropods on islands: colonization, speciation, and conservation. Annual Review of Entomology, 47, 595– 632. Grant, P.R. & Grant, B.R. (2008) How and why species multiply: the radiation of Darwin’s finches. Princeton University Press, Princeton, NJ. Graur, D. & Martin, W. (2004) Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends in Genetics, 20, 80– 86. Hasegawa, M. (1990) Demography of an island population of the lizard, Eumeces okadae, on Miyake, Izu Islands. Researches on Population Ecology, 32, 119– 133. Hasegawa, M. (1994) Insular radiation in life history of the lizard Eumeces okadae in the Izu Islands, Japan. Copeia, 1994, 732– 747. Hasegawa, M. (1999) Impacts of introduced weasel on the insular food web. Diversity of reptiles, amphibians and other terrestrial animals on tropical islands: origin, current status and conservation (ed. by H. Ota), pp. 129– 154. Elsevier Science, New York. Hasegawa, M. (2003) Ecological diversification of insular terrestrial reptiles: a review of the studies on the lizard and snakes of the Izu Islands. Global Environmental Research, 7, 59– 67. Hasegawa, M. & Mori, A. (2008) Does a gigantic insular snake grow faster or live longer to be gigantic? Evidence from a long-term field study. South American Journal of Herpetology, 3, 145– 154. Hasegawa, M. & Moriguchi, H. (1989) Geographic variation in food habits, body size, and life-history traits of the snakes on the Izu Islands. Current herpetology in East Asia (ed. by M. Matsui, T. Hikida and R.C. Goris), pp. 414– 432. Herpetological Society of Japan, Kyoto. Hayashi, M. & Chiba, S. (2004) Enhanced colour polymorphisms in island populations of the land snail Euhadra peliomphala. Biological Journal of the Linnean Society, 81, 417– 425. Higuchi, H. (1976) Comparative study on the breeding of mainland and island subspecies of the varied tit, Parus varius. Tori, 25, 11– 20. Ho, S.Y.W., Phillips, M.J., Cooper, A. & Drummond, A.J. (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Molecular Biology and Evolution, 22, 1561– 1568. Ho, S.Y.W., Shapiro, B., Phillips, M.J., Cooper, A. & Drummond, A.J. (2007) Evidence for time dependency of molecular rate estimates. Systematic Biology, 56, 515– 522. Huelsenbeck, J.P. & Rannala, B. (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology, 53, 904– 913. Inoue, K. & Amano, M. (1986) Evolution of Campanula punctata Lam. in the Izu Islands: change of pollinators and evolution of breeding systems. Plant Species Biology, 1, 89– 97. Inoue, K. & Kawahara, T. (1990) Allozyme differentiation and genetic structure in island and mainland Japanese populations of Campanula punctata (Campanulaceae). American Journal of Botany, 77, 1140– 1448. Isobe, I. & Yasuda, A. (1995) Large coastal cliff recession at the southeastern part of Niijima Island, central Japan: measurement of erosional volume of a pyroclastic cone using aerial photography. Bulletin of the Geological Survey of Japan, 46, 457– 475 (in Japanese). Isshiki, M. (1987) Geology of the Niijima District, Quadrangle Series. Geological Survey of Japan, Tsukuba. Kageyama, M., Motokawa, M. & Hikida, T. (2009) Geographic variation in morphological traits of the large Japanese field mouse, Apodemus speciosus (Rodentia, Muridae) from the Izu Island group, Japan. Zoological Science, 26, 266– 276. Kaneoka, I., Isshiki, N. & Zashu, S. (1970) K–Ar ages of the Izu–Bonin Islands. Geochemical Journal, 4, 53– 60. King, R.B. & Lawson, R. (1995) Color-pattern variation in Lake Erie water snakes: the role of gene flow. Evolution, 49, 885– 896. Kitazato, H. (1997) Paleogeographic changes in central Honshu, Japan, during the late Cenozoic in relation to the collision of the Izu–Ogasawara Arc with the Honshu Arc. Island Arc, 6, 144– 157. Kocher, T.D. (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nature Review Genetics, 5, 288– 298. Leaché, A.D. (2009) Species tree discordance traces to phylogeographic clade boundaries in North American fence lizards (Sceloporus). Systematic Biology, 58, 547– 559. Lomolino, M.V. (1990) The target area hypothesis: the influence of island area on immigration rates of non-volant mammals. Oikos, 57, 297– 300. Losos, J.B. & Ricklefs, R.E. (2009) Adaptation and diversification on islands. Nature, 457, 830– 835. MacArthur, R. & Wilson, E.O. (1967) The theory of island biogeography. Princeton University Press, Princeton, NJ. Maddison, D. & Maddison, W. (2008) MacClade version 4.08. Sinauer Associates, Inc., Sunderland, MA. Maddison, W.P. (1997) Gene trees in species trees. Systematic Biology, 46, 523– 536. McGuire, J.A., Linkem, C.W., Koo, M., Hutchison, D.W., Lappin, A.K., Orange, D.O., Lemos-Espinal, J., Riddle, B.R. & Jaeger, J. (2007) Mitochondrial introgression and incomplete lineage sorting through space and time: phylogenetics of crotaphytid lizards. Evolution, 61, 2879– 2897. Mori, A. & Hasegawa, M. (1999) Geographic differences in behavioral responses of hatchling lizards (Eumeces okadae) to snake-predator chemicals. Japanese Journal of Herpetology, 18, 45– 56. Mori, A. & Hasegawa, M. (2002) Early growth of Elaphe quadrivirgata from an insular gigantic population. Current Herpetology, 21, 43– 50. Niitsuma, N. (1991) Collision tectonics in the South Fossa Magna; central Japan (II). Modern Geology, 15, 314– 411. Nylander, J.A.A., Ronquist, F., Huelsenbeck, J.P. & Nieves-Aldrey, J.L. (2004) Bayesian phylogenetic analysis of combined data. Systematic Biology, 53, 47– 67. Nylander, J.A.A., Wilgenbusch, J.C., Warren, D.L. & Swofford, D.L. (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics, 24, 581– 583. Oiki, S., Kawahara, T., Inoue, K., Ohara, M. & Maki, M. (2001) Random amplified polymorphic DNA (RAPD) variation among populations of the insular endemic plant Campanula microdonta (Campanulaceae). Annals of Botany, 87, 661– 667. Okamoto, T., Motokawa, J., Toda, M. & Hikida, T. (2006) Parapatric distribution of the lizards Plestiodon (formerly Eumeces) latiscutatus and P. japonicus (Reptilia: Scincidae) around the Izu Peninsula, central Japan, and its biogeographic implications. Zoological Science, 23, 419– 425. Parent, C.E., Caccone, A. & Petren, K. (2008) Colonization and diversification of Galápagos terrestrial fauna: a phylogenetic and biogeographical synthesis. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 3347– 3361. Ree, R.H. & Smith, S.A. (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology, 57, 4– 14. Ree, R.H., Moore, B.R., Webb, C.O. & Donoghue, M.J. (2005) A likelihood framework for inferring the evolution of geographic range on phylogenetic trees. Evolution, 59, 2299– 2311. Schwarz, G. (1978) Estimating the dimension of a model. Annals of Statistics, 6, 461– 464. Shaw, K.L. (1995) Biogeographic patterns of two independent Hawaii cricket radiations (Laupala and Prognathogryllus). Hawaiian biogeography: evolution on a hot spot archipelago (ed. by W.L. Wagner and V.A. Funk), pp. 39– 56. Smithsonian Institution Press, Washington, DC. Sugihara, S., Fukuoka, T. & Ookawara, R. (2001) Volcanic eruption of Tenjosan Volcano at Kozushima and Mukaiyama volcano at Niijima, Izu Islands. Journal of Geography, 110, 94– 105 (in Japanese). Suzuki, H., Yasuda, S.P., Sakaizumi, M., Wakana, S., Motokawa, M. & Tsuchiya, K. (2004) Differential geographic patterns of mitochondrial DNA variation in two sympatric species of Japanese wood mice, Apodemus speciosus and A. argenteus. Genes and Genetic Systems, 79, 165– 176. Swofford, D.L. (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, MA. Takada, Y., Sakai, E., Uematsu, Y. & Tateishi, T. (2006) Morphological variation of large Japanese field mice, Apodemus speciosus on the Izu and Oki Islands. Mammal Study, 31, 29– 40. Tanaka, K., Mori, A. & Hasegawa, M. (2001) Apparent decoupling of prey recognition ability with prey availability in an insular snake population. Journal of Ethology, 19, 27– 32. Tomozawa, M. & Suzuki, H. (2008) A trend of central versus peripheral structuring in mitochondrial and nuclear gene sequences of the Japanese wood mouse, Apodemus speciosus. Zoological Science, 25, 273– 285. Tsukui, M., Saito, K. & Hayashi, K. (2006) Frequent and intensive eruptions in the 9th century, Izu Islands, Japan: revision of volcano-stratigraphy based tephras and historical document. Bulletin of Volcanological Society of Japan, 1, 327– 338 (in Japanese with English abstract). Whittaker, R.J. & Fernández-Palacios, J.M. (2007) Island biogeography, ecology, evolution, and conservation, 2nd edn. Oxford University Press, Oxford. Whittaker, R.J., Triantis, K.A. & Ladle, R.J. (2008) A general dynamic theory of oceanic island biogeography. Journal of Biogeography, 35, 977– 994. Yoshida, H. (1992) Eruptive history of Nii-jima volcano. Program and abstracts of the annual meeting of the Volcanological Society of Japan in autumn of 1992, 2, 63 (in Japanese). Citing Literature Supporting Information Appendix S1 Geographical locality and haplotype of Elaphe quadrivirgata tissue samples used in this study. Appendix S2 The complete time-calibrated ratsnake phylogeny used for secondary calibrations. Appendix S3 Complete results of the lagrange analysis. As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer-reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors. Filename Description JBI_2403_sm_AppS1.doc562 KB Supporting info item JBI_2403_sm_AppS2.doc134.5 KB Supporting info item JBI_2403_sm_AppS3.doc45 KB Supporting info item Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article. Volume38, Issue2February 2011Pages 259-271 ReferencesRelatedInformation
Publication Year: 2010
Publication Date: 2010-10-15
Language: en
Type: article
Indexed In: ['crossref']
Access and Citation
Cited By Count: 35
AI Researcher Chatbot
Get quick answers to your questions about the article from our AI researcher chatbot