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Asymmetric hybridization and introgression between sibling species of the pufferfish Takifugu that have undergone explosive speciation

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Abstract

Pufferfishes belonging to the genus Takifugu are a prominent example of recent adaptive radiations of marine fishes. Using amplified fragment length polymorphism (AFLP) and mitochondrial DNA (mtDNA) markers, the genetic characteristics of natural hybrids between two sibling species, Takifugu snyderi and Takifugu stictonotus, were investigated to gain insights into the role of hybridization in rapid diversification. Numerous early generations of hybrids (131 F1 hybrids and 18 first-generation backcrosses) were screened by Bayesian assignment procedures from samples collected at three sites off the Pacific coast of eastern Honshu, Japan (Ibaraki: 36°21′N, 140°37′E; Fukushima: 37°03′N, 141°03′E; Iwate: 40°02′N, 141°59′E), during 2012–2014. Analysis of mtDNA indicated that hybridization is highly directional, as the majority of the F1 hybrids (75.6%) were offspring between T. stictonotus females and T. snyderi males. Among the 18 backcrosses, 17 were toward T. snyderi and one was toward T. stictonotus. Two of 118 individuals classified as genetically pure T. snyderi based on AFLP markers were affected by mtDNA introgression from T. stictonotus. These results suggest that interspecific gene flow has been highly asymmetrical toward T. snyderi, which may partly explain the marked difference in intraspecific genetic diversity between the two species. The proportion of F1 hybrids in the Ibaraki and Fukushima areas is exceptionally high compared with that of other marine fishes, indicating the need for continuous monitoring of hybridization and its impact on integrity of each parental species under the changing marine environment.

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Acknowledgements

We are grateful to Kazuhiko Kurimoto, Naoto Itou, Tadahiro Soutome, Toru Sakuma, Shinichiro Ikeguchi, Hiroyuki Doi, and Harumi Sakai for their help in obtaining the samples and Youta Hazama, Kyoji Fijiwara, Tomoko Sato, and Yuko Nozaki for their help in the laboratory work. This work was supported in part by JSPS KAKENHI (Nos. 19580229 and 25440227) and by Grants from the Project of the NARO Bio-oriented Technology Research Advancement Institution (the special scheme project on regional developing strategy, Project No. 16822337).

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  1. National Fisheries University, 2-7-1 Nagata-Honmachi, Shimonoseki, Yamaguchi, 759-6595, Japan

    Hiroshi Takahashi, Airi Toyoda, Taku Yamazaki & Shusaku Narita

  2. Ibaraki Prefectural Fisheries Research Institute, Hitachinaka, Ibaraki, 311-1203, Japan

    Tsuyoshi Mashiko & Yukio Yamazaki

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  1. Hiroshi Takahashi
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  2. Airi Toyoda
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  3. Taku Yamazaki
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  4. Shusaku Narita
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Correspondence to Hiroshi Takahashi.

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All animals have been sampled and/or treated according to the national legislation in Japan. This article does not contain studies with human participants by any of the authors.

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Takahashi, H., Toyoda, A., Yamazaki, T. et al. Asymmetric hybridization and introgression between sibling species of the pufferfish Takifugu that have undergone explosive speciation. Mar Biol 164, 90 (2017). https://doi.org/10.1007/s00227-017-3120-2

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