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A role for a neo-sex chromosome in stickleback speciation

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  • Jun Kitano

    (Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, Seattle, Washington 98109, USA
    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.))

  • Joseph A. Ross

    (Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, Seattle, Washington 98109, USA
    Graduate Program in Molecular and Cellular Biology, University of Washington, Seattle, Washington 98195, USA
    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.))

  • Seiichi Mori

    (Biological Laboratory, Gifu-keizai University, Ogaki, Gifu 503-8550, Japan)

  • Manabu Kume

    (Aqua Restoration Research Center, Public Works Research Institute, Kakamigahara, Gifu 501-6021, Japan)

  • Felicity C. Jones

    (Stanford University, Stanford, California 94305, USA)

  • Yingguang F. Chan

    (Stanford University, Stanford, California 94305, USA)

  • Devin M. Absher

    (Stanford University, Stanford, California 94304, USA
    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.))

  • Jane Grimwood

    (Stanford University, Stanford, California 94304, USA
    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.))

  • Jeremy Schmutz

    (Stanford University, Stanford, California 94304, USA
    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.))

  • Richard M. Myers

    (Stanford University, Stanford, California 94304, USA
    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.))

  • David M. Kingsley

    (Stanford University, Stanford, California 94305, USA)

  • Catherine L. Peichel

    (Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, Seattle, Washington 98109, USA)

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.

Suggested Citation

  • Jun Kitano & Joseph A. Ross & Seiichi Mori & Manabu Kume & Felicity C. Jones & Yingguang F. Chan & Devin M. Absher & Jane Grimwood & Jeremy Schmutz & Richard M. Myers & David M. Kingsley & Catherine L, 2009. "A role for a neo-sex chromosome in stickleback speciation," Nature, Nature, vol. 461(7267), pages 1079-1083, October.
    • Handle: RePEc:nat:nature:v:461:y:2009:i:7267:d:10.1038_nature08441
    DOI: 10.1038/nature08441
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    Cited by:

    1. Lulu Xu & Yandong Ren & Jiahong Wu & Tingting Cui & Rong Dong & Chen Huang & Zhe Feng & Tianmin Zhang & Peng Yang & Jiaqing Yuan & Xiao Xu & Jiao Liu & Jinhong Wang & Wu Chen & Da Mi & David M. Irwin , 2024. "Evolution and expression patterns of the neo-sex chromosomes of the crested ibis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Zhen Huang & Ivanete De O. Furo & Jing Liu & Valentina Peona & Anderson J. B. Gomes & Wan Cen & Hao Huang & Yanding Zhang & Duo Chen & Ting Xue & Qiujin Zhang & Zhicao Yue & Quanxi Wang & Lingyu Yu & , 2022. "Recurrent chromosome reshuffling and the evolution of neo-sex chromosomes in parrots," Nature Communications, Nature, vol. 13(1), pages 1-11, December.

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