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Population genetics of Haminoea (Haloa) japonica Pilsbry, 1895, a widespread non-indigenous sea slug (Mollusca: Opisthobranchia) in North America and Europe

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Abstract

Haminoea japonica is an opisthobranch mollusk with a large non-indigenous range. This species is a vector for a parasite that causes the human skin disease cercarial dermatitis, and may have negative effects on populations of native species. Molecular evidence from the mitochondrial cytochrome c oxidase I gene and the histone 3 nuclear gene indicates that previously published morphology-based hypotheses on the spread of H. japonica out of Japan are correct. The most likely explanation for the current range of the species, which includes Japan, Korea, France, Spain, Italy, Canada and the USA is a recent, human-mediated dispersal from Japanese populations. The highest levels of nucleotide and haplotype diversity are found in Japan. Non-indigenous populations have low levels of genetic diversity (indicating bottlenecking). Haplotypes that were detected in the non-indigenous range of H. japonica have only been found in two localities in the native range; these two localities are in north-eastern Japan. In addition, the haplotype network structure and Spatial Analysis of Molecular Variance results confirm the origins of non-indigenous populations most likely trace to north-eastern Japan, which is where most Pacific oyster exports to North America also originated. Because there are no major shipping ports in north-eastern Japan, ballast water is less likely to be the mechanism of dispersal. The results of this study provide important data for the development of policies and regulations aimed to prevent further spread of this species in non-indigenous ranges.

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Acknowledgments

We would like to thank all those colleagues who provided or assisted in the collection of specimens used in this study: Kenji Okoshi, Tomohiro Kuwae, Masato Owada, Rie Nakano, Michiaki Hon-ma, Koh Dong Bum, Satoshi Wada, Douglas Eernisse, Patrick Krug, Atsuko Kuramochi, Takashi Kuramochi, Glenys Gibson, Annette Klussmann-Kolb, Jessica Goodheart, Jennifer Alexander, Jermaine Mahguib, Elysse Ornelas, Duncan Hanson, Jill Walker, Paul Callomon, Terry Gosliner, Kenji Kito, Kenji Ito, Kevin Lee, and Isabel Rey Fraile. Ryan Kelly provided COI sequences for comparison. This work was supported by the California State University Agricultural Research Institute (ARI), the Ernest Prete, Jr. Student Environmental Research Fellowship, the Southern California Academy of Sciences, Conchologists of America, the Houston Conchology Society, the Research, Scholarship and Creative Activity (RSCA) Program at California State University, and the California State University Council on Ocean Affairs, Science, and Technology (COAST). Andrew Cohen, Manami Kanno and Carol Stepien provided valuable comments that greatly improved the quality of this manuscript.

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  1. Department of Biological Sciences, California State Polytechnic University, 3801 Temple Avenue, Pomona, CA, 91768, USA

    Dieta Hanson & Ángel Valdés

  2. Graduate School of Science, Chiba University, Yayoi-cho, Inage-ku, Chiba, 263-8522, Japan

    Yayoi Hirano

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  1. Dieta Hanson
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  3. Ángel Valdés
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Correspondence to Ángel Valdés.

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Hanson, D., Hirano, Y. & Valdés, Á. Population genetics of Haminoea (Haloa) japonica Pilsbry, 1895, a widespread non-indigenous sea slug (Mollusca: Opisthobranchia) in North America and Europe. Biol Invasions 15, 395–406 (2013). https://doi.org/10.1007/s10530-012-0294-x

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