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MBE Advance Access published online on June 30, 2009

Molecular Biology and Evolution, doi:10.1093/molbev/msp128
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© The Author 2009. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

Application of the isolation with migration model demonstrates the Pleistocene origin of geographic differentiation in Cardamine nipponica (Brassicaceae), an endemic Japanese alpine plant

Hajime Ikeda1, Noriyuki Fujii2 and Hiroaki Setoguchi1

1 Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-nihonmatsu-cho, Sakyo-ku, Kyoto 606-8501, Japan
2 Graduate School of Science and Technology, Kumamoto University, Kurokami2-39-1, Kumamoto, Kumamoto 860-8555, Japan

Corresponding Author Hajime Ikeda, Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-nihonmatsu-cho, Sakyo-ku, Kyoto 606-8501, Japan. Telephone: +81-75-753-6858, Fax: +81-75-753-6858. Email: h.ikeda0927{at}h02.mbox.media.kyoto-u.ac.jp

Received for publication February 12, 2009. Revision received April 19, 2009. Revision received June 23, 2009. Accepted for publication June 23, 2009.

The Pleistocene was characterized by a cyclic pattern of cold and warm climatic periods, or climatic oscillations, which caused fluctuations in the distributions of organisms. This resulted in drastic changes in demography, thereby accelerating the genetic divergence of populations. Phylogeographic studies have elucidated the history of populations during the Pleistocene. However, given the lack of model-based analysis of population histories, previous phylogeographic studies could not adequately evaluate the effect of these Pleistocene climatic oscillations on the genetic divergence and migration events between populations. Populations of Japanese alpine plants in central and northern Japan are highly differentiated, and a history of isolation between regions during the Pleistocene was inferred. Using sequences of ten nuclear genes (approximately 7,000 bp in total) from Cardamine nipponica (Brassicaceae), we applied an isolation with migration (IM) model to test the significance of the isolation history between central and northern Japan and to assess whether range shifts during the Pleistocene climatic oscillations were involved in the genetic differentiation between regions. The estimated divergence time indicates that the two regions were separated about 100,000–110,000 years ago. The exclusive occurrence of closely related haplotypes within each region (parsimony network) and the high level of genetic differentiation between the regions (mean FST = 0.417) indicate that genetic divergence occurred following the isolation of the two regions. Therefore, the genetic differentiation between regions was shaped during the Pleistocene, especially during the last glacial and inter- and post-glacial periods. In addition, our multilocus analysis showed that populations in central and northern Japan were completely isolated after they split. Geographic separation and subsequent restricted migration events among mountains could explain this isolation history between regions. Furthermore, genetic drift in the reduced populations would remove evidence of occasional migration, emphasizing the isolation history. Therefore, our application of a demographic model demonstrated the Pleistocene origin of geographic differentiation statistically and provided a plausible migration history for C. nipponica.

Key Words: alpine plants • Cardamine nipponica • IM model • Pleistocene climatic oscillations • phylogeography


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