Abstract

Sexual antagonism, or conflict between the sexes, has been proposed as a driving force in both sex-chromosome turnover and speciation. Although closely related species often have different sex-chromosome systems, it is unknown whether sex-chromosome turnover contributes to the evolution of reproductive isolation between species. Here we show that a newly evolved sex chromosome contains genes that contribute to speciation in threespine stickleback fish (Gasterosteus aculeatus). We first identified a neo-sex chromosome system found only in one member of a sympatric species pair in Japan. We then performed genetic linkage mapping of male-specific traits important for reproductive isolation between the Japanese species pair. The neo-X chromosome contains loci for male courtship display traits that contribute to behavioural isolation, whereas the ancestral X chromosome contains loci for both behavioural isolation and hybrid male sterility. Our work not only provides strong evidence for a large X-effect on reproductive isolation in a vertebrate system, but also provides direct evidence that a young neo-X chromosome contributes to reproductive isolation between closely related species. Our data indicate that sex-chromosome turnover might have a greater role in speciation than was previously appreciated.

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Acknowledgements

We thank M. Nishitani, J. Kitajima, M. Nishida, S. Takeyama, T. Andoh, T. Kuwahara, C. Torii, Akkeshi Fisheries Cooperative Association, Akkeshi Waterfowl Center, S. Brady, A. Southwick, all members of the Peichel laboratory, and many field assistants for technical help and discussion. We thank J. Boughman, T. Bradshaw, H. Malik, J. McKinnon, N. Phadnis and D. Schluter for comments on the manuscript. We also thank the Broad Institute for the public release of an initial stickleback genome assembly. This research was supported by the Uehara Memorial Foundation (J.K.), a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, and Water and People Project of Research Institute for Humanity and Nature (S.M.), Akkeshi Town Grants-in-Aid for Scientific Research in the Lake Akkeshi-Bekanbeushi Wetland (M.K.), a Burroughs Wellcome Fund Career Award in the Biomedical Sciences (C.L.P.), and National Institutes of Health grants T32 GM07270 (J.A.R.), R01 GM071854 (C.L.P.) and P50 HG02568 (R.M.M., D.M.K. and C.L.P.).

Author Contributions J.K., S.M. and C.L.P. conceived and designed the study. F.C.J., Y.F.C., D.M.A., J.G., J.S., R.M.M. and D.M.K. contributed new reagents and carried out the SNP genotyping experiments for genome-wide linkage mapping. J.K., J.A.R., S.M., M.K. and C.L.P. performed all other experiments and analysed the data. J.K. and C.L.P. wrote the manuscript.

Author information

Author notes

    • Jun Kitano
    • , Joseph A. Ross
    • , Devin M. Absher
    • , Jane Grimwood
    • , Jeremy Schmutz
    •  & Richard M. Myers

    Present addresses: Department of Ecology and Evolutionary Biology, Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi 980-8578, Japan (J.K.); Department of Biology, University of Maryland, College Park, Maryland 20742, USA (J.A.R.); HudsonAlpha Institute for Biotechnology, Huntsville, Alabama 35806, USA (D.M.A., J.G., J.S. and R.M.M.)

Affiliations

  1. Division of Human Biology, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, Seattle, Washington 98109, USA

    • Jun Kitano
    • , Joseph A. Ross
    •  & Catherine L. Peichel
  2. Graduate Program in Molecular and Cellular Biology, University of Washington, Seattle, Washington 98195, USA

    • Joseph A. Ross
  3. Biological Laboratory, Gifu-keizai University, Ogaki, Gifu 503-8550, Japan

    • Seiichi Mori
  4. Aqua Restoration Research Center, Public Works Research Institute, Kakamigahara, Gifu 501-6021, Japan

    • Manabu Kume
  5. Department of Developmental Biology and Howard Hughes Medical Institute, Stanford University, Stanford, California 94305, USA

    • Felicity C. Jones
    • , Yingguang F. Chan
    •  & David M. Kingsley
  6. Department of Genetics and Stanford Human Genome Center, Stanford University, Stanford, California 94304, USA

    • Devin M. Absher
    • , Jane Grimwood
    • , Jeremy Schmutz
    •  & Richard M. Myers

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Corresponding author

Correspondence to Catherine L. Peichel.

All SNP information has been deposited at http://www.ncbi.nlm.nih.gov/projects/SNP/.

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    Supplementary Information

    This file contains Supplementary Methods, a Supplementary Discussion, Supplementary Figures 1-7 with Legends, Supplementary Tables 1-5 and Supplementary References.

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https://doi.org/10.1038/nature08441

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