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Molecular phylogeny of obligate fish parasites of the family Cymothoidae (Isopoda, Crustacea): evolution of the attachment mode to host fish and the habitat shift from saline water to freshwater

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Abstract

In host–parasite coevolution, parasite innovations including the acquisition of new habitats and novel traits can trigger evolutionary breakthroughs and enhance parasite diversification via accumulation of new hosts. All species of the family Cymothoidae are obligate fish parasites, attaching to exterior body surfaces of fish, the buccal or opercular cavities, or burrowing into abdominal muscle tissue. In the present study, we constructed a molecular phylogeny of 27 cymothoid species that parasitise 38 fish species, combined with 2 prior cymothoid datasets, based on the sequences of mitochondrial 16S rRNA and COI genes. We explored the evolution of the host attachment mode, and the habitat shift from saline water to freshwater. Our evolutionary trees include two freshwater clades, an abdominal burrower clade, and cymothoid clades that are closer to the base of Cymothoidae than those initially analysed. We found that the basal clade of Cymothoidae was Elthusa sacciger, which is parasitic in the opercular cavity of synaphobranchid eels. This result suggests that cymothoids may have originated in deep seas, subsequently expanded to shallow seas, and then to brackish and/or freshwater, by shifting host species. Invasion of freshwater habitats has occurred at least twice; freshwater abdominal muscle burrowers living on armoured catfish constitute a clade allied to E. sacciger. The ancestral host attachment site, based on our dataset, was the opercular cavity, followed (sequentially) by buccal colonisation and attachment to the external body.

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Acknowledgements

We sincerely thank J. Akahane, G. Akinaga, S. N. Chiba, R. Dohi, A. Fujii, K. Goto, H. Hamaoka, T. Hattori, T. Hayakawa, N. Hayashida, I. Hirabayashi, H. Hirasaka, S. Isozaki, G. Itani, M. Ito, M. Ito, H. Matsuba, Kanagawa Prefectural Museum of Natural History, H. Katahira, E. Katayama, Y. Kimura, K. Koeda, T. Kunishima, H. Mishima, K. Miyamoto, Y. Miyazaki, T. Moritaki, F. Nakao, N. Nakayama, M. Nishiguchi, M. Ogishi, J. Ohtomi, T. Oka, T. Okada, I. Oura, K. Sakai, T. Sakai, T. Sakumoto, M. Sakurai, T. Sato, T. P. Satoh, Seikai National Fisheries Research Institute, H. Senou, T. Shigeta, S. Sodeyama, R. Shimomura, T. Shinonome, K. Tachihara, R. Tagashira, M. Takami, T. Takaya, F. Tashiro, Toba Aquarium, Tohoku National Fisheries Research Institute, T. Tsukayama, A. Umemoto, M. Utsunomiya, Y. Yagi, A. Yasui, and S. Yoshimi for providing specimens and/or assisting sample collection. Photos in Figs. 1, 4 courtesy of I. Seidel and H. Hirasaka. We are also grateful to members of the Maneno Team (Tanganyika Research Project Team) and staffs of Lake Tanganyika Research Unit, Mpulungu, Zambia, for their support. Research in Lake Tanganyika was conducted under permission from the Zambian Ministry of Agriculture, Food, and Fisheries. This study was supported by Showa Seitoku Memorial Foundation (Grant No. H26) and the Mikimoto Fund for marine Ecology (Grant No. H24).

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Authors and Affiliations

  1. Graduate School of Science and Engineering, Ehime University, 2-5 Bunkyo, Matsuyama, Ehime, 790-8577, Japan

    Hiroki Hata & Shinya Tada

  2. Department of Biology, Faculty of Agriculture and Life Science, Hirosaki University, 1-1 Bunkyo, Hirosaki, Aomori, 036-8560, Japan

    Atsushi Sogabe

  3. Department of Biology, Faculty of Science, Ehime University, 2-5 Bunkyo, Matsuyama, Ehime, 790-8577, Japan

    Ryohei Nishimoto, Reina Nakano & Nobuhiko Kohya

  4. Research Institute for Humanity and Nature, 457-4 Motoyama, Kamigamo, Kita-ku, Kyoto, 603-8047, Japan

    Hirohiko Takeshima

  5. Faculty of Environmental Earth Science, Hokkaido University, N10W5 Kita-ku, Sapporo, 060-0810, Japan

    Ryota Kawanishi

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  1. Hiroki Hata
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Hata, H., Sogabe, A., Tada, S. et al. Molecular phylogeny of obligate fish parasites of the family Cymothoidae (Isopoda, Crustacea): evolution of the attachment mode to host fish and the habitat shift from saline water to freshwater. Mar Biol 164, 105 (2017). https://doi.org/10.1007/s00227-017-3138-5

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