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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References
Rice, W. R. The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution 41, 911–914 (1987)
Rice, W. R. Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116, 161–167 (1987)
Rice, W. R. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38, 735–742 (1984)
Charlesworth, B., Coyne, J. A. & Barton, N. H. The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130, 113–146 (1987)
Presgraves, D. C. Sex chromosomes and speciation in Drosophila . Trends Genet. 24, 336–343 (2008)
Qvarnström, A. & Bailey, R. I. Speciation through evolution of sex-linked genes. Heredity 102, 4–15 (2009)
Charlesworth, D. & Charlesworth, B. Sex differences in fitness and selection for centric fusions between sex-chromosomes and autosomes. Genet. Res. 35, 205–214 (1980)
van Doorn, G. S. & Kirkpatrick, M. Turnover of sex chromosomes induced by sexual conflict. Nature 449, 909–912 (2007)
Ezaz, T., Stiglec, R., Veyrunes, F. & Graves, J. A. M. Relationships between vertebrate ZW and XY sex chromosome systems. Curr. Biol. 16, R736–R743 (2006)
Mank, J. E., Promislow, D. E. L. & Avise, J. C. Evolution of alternative sex-determining mechanisms in teleost fishes. Biol. J. Linn. Soc. 87, 83–93 (2006)
Woram, R. A. et al. Comparative genome analysis of the primary sex-determining locus in salmonid fishes. Genome Res. 13, 272–280 (2003)
Tanaka, K., Takehana, Y., Naruse, K., Hamaguchi, S. & Sakaizumi, M. Evidence for different origins of sex chromosomes in closely related Oryzias fishes: substitution of the master sex-determining gene. Genetics 177, 2075–2081 (2007)
White, M. J. D. Animal Cytology and Evolution (Univ. Press, 1973)
Ross, J. A. et al. Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae). PLoS Genet. 5, e1000391 (2009)
Seehausen, O., van Alphen, J. J. M. & Lande, R. Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection. Ecol. Lett. 2, 367–378 (1999)
Lande, R., Seehausen, O. & van Alphen, J. J. M. Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish. Genetica 112–113, 435–443 (2001)
Kocher, T. D. Adaptive evolution and explosive speciation: the cichlid fish model. Nature Rev. Genet. 5, 288–298 (2004)
Higuchi, M. & Goto, A. Genetic evidence supporting the existence of two distinct species in the genus Gasterosteus around Japan. Environ. Biol. Fishes 47, 1–16 (1996)
Kitano, J., Mori, S. & Peichel, C. L. Phenotypic divergence and reproductive isolation between sympatric populations of anadromous threespine sticklebacks. Biol. J. Linn. Soc. 91, 671–685 (2007)
Kingsley, D. M. & Peichel, C. L. in Biology of the Three-Spined Stickleback (eds Östlund-Nilsson, S., Mayer, I. & Huntingford, F.) 41–81 (CRC Press, 2007)
Peichel, C. L. et al. The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr. Biol. 14, 1416–1424 (2004)
Ross, J. A. & Peichel, C. L. Molecular cytogenetic evidence of rearrangements on the Y chromosome of the threespine stickleback fish. Genetics 179, 2173–2182 (2008)
Foster, S. A. in The Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 381–398 (Oxford Univ. Press, 1994)
Wootton, R. J. A Functional Biology of Sticklebacks (Croom Helm, 1984)
Kitano, J., Mori, S. & Peichel, C. L. Sexual dimorphism in the external morphology of the threespine stickleback (Gasterosteus aculeatus). Copeia 2007, 336–349 (2007)
Wu, C.-I. & Davis, A. W. Evolution of postmating reproductive isolation: the composite nature of Haldane’s rule and its genetic bases. Am. Nat. 142, 187–212 (1993)
Tao, Y., Hartl, D. L. & Laurie, C. C. Sex-ratio segregation distortion associated with reproductive isolation in Drosophila . Proc. Natl Acad. Sci. USA 98, 13183–13188 (2001)
Phadnis, N. & Orr, H. A. A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323, 376–379 (2009)
Orr, H. A. & Irving, S. Complex epistasis and the genetic basis of hybrid sterility in the Drosophila pseudoobscura Bogota-USA hybridization. Genetics 158, 1089–1100 (2001)
Sawamura, K., Roote, J., Wu, C.-I. & Yamamoto, M. T. Genetic complexity underlying hybrid male sterility in Drosophila . Genetics 166, 789–796 (2004)
Gavrilets, S. Fitness Landscapes and the Origin of Species (Princeton Univ. Press, 2004)
Arnqvist, G. & Rowe, L. Sexual Conflict (Princeton Univ. Press, 2005)
Van Ooijen, J. W. & Voorrips, R. E. JoinMap 3.0, Software for the Calculation of Genetic Linkage Maps (Plant Research International, 2001)
Van Ooijen, J. W., Boer, M. P., Jansen, R. C. & Maliepaard, C. MapQTL 4.0, Software for the Calculation of QTL Positions on Genetic Maps (Plant Research International, 2002)
Broman, K. W., Wu, H., Sen, S. & Churchill, G. A. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19, 889–890 (2003)
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.
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All SNP information has been deposited at http://www.ncbi.nlm.nih.gov/projects/SNP/.
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This file contains Supplementary Methods, a Supplementary Discussion, Supplementary Figures 1-7 with Legends, Supplementary Tables 1-5 and Supplementary References. (PDF 2935 kb)
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Kitano, J., Ross, J., Mori, S. et al. A role for a neo-sex chromosome in stickleback speciation. Nature 461, 1079–1083 (2009). https://doi.org/10.1038/nature08441
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DOI: https://doi.org/10.1038/nature08441
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