Article

Nature 461, 1079-1083 (22 October 2009) | doi:10.1038/nature08441; Received 4 May 2009; Accepted 20 August 2009; Published online 27 September 2009

A role for a neo-sex chromosome in stickleback speciation

Jun Kitano1,7, Joseph A. Ross1,2,7, Seiichi Mori3, Manabu Kume4, Felicity C. Jones5, Yingguang F. Chan5, Devin M. Absher6,7, Jane Grimwood6,7, Jeremy Schmutz6,7, Richard M. Myers6,7, David M. Kingsley5 & Catherine L. Peichel1

  1. Division of Human Biology, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, Seattle, Washington 98109, USA
  2. Graduate Program in Molecular and Cellular Biology, University of Washington, Seattle, Washington 98195, USA
  3. Biological Laboratory, Gifu-keizai University, Ogaki, Gifu 503-8550, Japan
  4. Aqua Restoration Research Center, Public Works Research Institute, Kakamigahara, Gifu 501-6021, Japan
  5. Department of Developmental Biology and Howard Hughes Medical Institute, Stanford University, Stanford, California 94305, USA
  6. Department of Genetics and Stanford Human Genome Center, Stanford University, Stanford, California 94304, USA
  7. 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.)

Correspondence to: Catherine L. Peichel1 Correspondence and requests for materials should be addressed to C.L.P. (Email: cpeichel@fhcrc.org).

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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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