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Multiple colonizations of Lake Biwa by Sarcocheilichthys fishes and their population history

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Abstract

Rapid adaptation and speciation have not been well documented for organisms in Lake Biwa, Japan, the oldest ancient lake in East Asia. To examine these processes, we focused on the divergence of Sarcocheilichthys gudgeons and conducted phylogeographic and population genetic analyses using mitochondrial DNA sequences and microsatellite data. No remarkable genetic differentiation was found between two species, S. biwaensis and S. variegatus microoculus, both endemic to Lake Biwa, whereas this species group, including S. v. variegatus, was genetically divided into three major regional groups: the Lake Biwa, Ise Bay, and western groups. Divergent mtDNA haplotypes were included within the Lake Biwa and western groups, strongly suggesting secondary contacts among allopatrically isolated populations. Dating for mtDNA phylogeny using a geological constraint suggested the colonization of Lake Biwa by multiple Sarcocheilichthys lineages that diverged from each other in the early–middle Pleistocene. Coalescent-based population analyses indicated that the local populations colonized the rocky bottom habitat in Lake Biwa from other habitats after the Last Glacial Maximum, likely reflecting past environmental changes in the lake, including the disappearance of rocky areas during the glacial climate. Divergent morphological adaptation in Sarcocheilichthys associated with substrate type may have rapidly proceeded along with environmental changes.

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Acknowledgments

We express sincere thanks to professional fishermen of Lake Biwa for cooperation in fish sampling, to Lake Biwa Museum, Shiga Prefecture, for the kind permission to use stocking samples, to S. Kanao, J. Nakajima, C. Oshiumi and J. Kitamura for providing fish samples, and to K. Hosoya, T. Kokita, R. Kakioka, M. Nishida, H. Takeshima, M. Hori and the members of Laboratory of Animal Ecology of Kyoto University for their valuable advice during this study. This study was supported by the Grants-in-Aid from the Ministry of Education, Culture, Sports, Science, and Technology, Japan (nos. 18570086, 21370035, Biodiversity Research of the 21st Century COE: A14, and “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem” of the GCOE), the Core Stage Backup Research Fund of Kyoto University, and the Foundation of Ito Grant for Ichthyology, Fujiwara Natural History Foundation. This study complies with current laws in Japan and the Regulation on Animal Experimentation at Kyoto University.

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  1. Division of Biological Science, Graduate School of Science, Kyoto University, Kitashirakawa-Oiwakecho, Sakyo-ku, Kyoto, 606-8502, Japan

    Takefumi Komiya, Sari Fujita-Yanagibayashi & Katsutoshi Watanabe

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  1. Takefumi Komiya
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  2. Sari Fujita-Yanagibayashi
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  3. Katsutoshi Watanabe
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Correspondence to Katsutoshi Watanabe.

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ESM Table S1

Average expected heterozygosity (± SD) and number of loci that showed the deviation from Hardy–Weinberg equilibrium (XLS 32 kb)

ESM Table S2

Matrix of geographical distances as shorter coastal distances (km) for “geofile” in Migrate-n analysis (XLS 32 kb)

ESM Table S3

Pairwise F ST for the Sarcocheilichthys samples with sample sizes ≥8 based on mtDNA and microsatellite data (XLS 42 kb)

ESM Table S4

Results of mismatch distribution analysis and neutrality tests by Tajima’s D and Fu’s FS for pooled and respective samples of Sarcocheilichthys species (XLS 43 kb)

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Komiya, T., Fujita-Yanagibayashi, S. & Watanabe, K. Multiple colonizations of Lake Biwa by Sarcocheilichthys fishes and their population history. Environ Biol Fish 97, 741–755 (2014). https://doi.org/10.1007/s10641-013-0176-9

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