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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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.
KeywordsCodon Position Host Fish Attachment Mode Bayesian Inference Method Armoured Catfish
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).
Compliance with ethical standards
Conflict of interest
All authors declare that they have no conflict of interest.
All experiments were conducted in accordance with the Ethical Guidelines for Animal Experiments of Ehime University.
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