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      Turnover of sex chromosomes and speciation in fishes

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          Abstract

          Closely related species of fishes often have different sex chromosome systems. Such rapid turnover of sex chromosomes can occur by several mechanisms, including fusions between an existing sex chromosome and an autosome. These fusions can result in a multiple sex chromosome system, where a species has both an ancestral and a neo-sex chromosome. Although this type of multiple sex chromosome system has been found in many fishes, little is known about the mechanisms that select for the formation of neo-sex chromosomes, or the role of neo-sex chromosomes in phenotypic evolution and speciation. The identification of closely related, sympatric species pairs in which one species has a multiple sex chromosome system and the other has a simple sex chromosome system provides an opportunity to study sex chromosome turnover. Recently, we found that a population of threespine stickleback ( Gasterosteus aculeatus) from Japan has an X 1X 2Y multiple sex chromosome system resulting from a fusion between the ancestral Y chromosome and an autosome, while a sympatric threespine stickleback population has a simple XY sex chromosome system. Furthermore, we demonstrated that the neo-X chromosome ( X 2) plays an important role in phenotypic divergence and reproductive isolation between these sympatric stickleback species pairs. Here, we review multiple sex chromosome systems in fishes, as well as recent advances in our understanding of the evolutionary role of sex chromosome turnover in stickleback speciation.

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          A role for a neo-sex chromosome in stickleback speciation

          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. In this study, we show that a newly evolved sex chromosome harbours 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 harbours loci for male courtship display traits that contribute to behavioural isolation, while 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 suggest that sex chromosome turnover might play a greater role in speciation than previously appreciated.
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            Sex chromosomes and speciation in Drosophila.

            Two empirical rules suggest that sex chromosomes play a special role in speciation. The first is Haldane's rule - the preferential sterility and inviability of species hybrids of the heterogametic (XY) sex. The second is the disproportionately large effect of the X chromosome in genetic analyses of hybrid sterility. Whereas the causes of Haldane's rule are well established, the causes of the 'large X-effect' have remained controversial. New genetic analyses in Drosophila confirm that the X is a hotspot for hybrid male sterility factors, providing a proximate explanation for the large X-effect. Several other new findings -- on faster X evolution, X chromosome meiotic drive and the regulation of the X chromosome in the male-germline -- provide plausible evolutionary explanations for the large X-effect.
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              Turnover of sex chromosomes induced by sexual conflict.

              Sex-determination genes are among the most fluid features of the genome in many groups of animals. In some taxa the master sex-determining gene moves frequently between chromosomes, whereas in other taxa different genes have been recruited to determine the sex of the zygotes. There is a well developed theory for the origin of stable and highly dimorphic sex chromosomes seen in groups such as the eutherian mammals. In contrast, the evolutionary lability of genetic sex determination in other groups remains largely unexplained. In this theoretical study, we show that an autosomal gene under sexually antagonistic selection can cause the spread of a new sex-determining gene linked to it. The mechanism can account for the origin of new sex-determining loci, the transposition of an ancestral sex-determining gene to an autosome, and the maintenance of multiple sex-determining factors in species that lack heteromorphic sex chromosomes.
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                Author and article information

                Contributors
                jkitano@lab.nig.ac.jp
                Journal
                Environ. Biol. Fishes
                Environmental Biology of Fishes
                Springer Netherlands (Dordrecht )
                0378-1909
                1573-5133
                4 June 2011
                4 June 2011
                2012
                : 94
                : 3
                : 549-558
                Affiliations
                [ ]Ecological Genetics Laboratory and JST PRESTO, Center for Frontier Research, National Institute of Genetics, Yata 1111, Mishima, Shizuoka 411–8540 Japan
                [ ]Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, WA 98109–1024 USA
                Article
                9853
                10.1007/s10641-011-9853-8
                4459657
                26069393
                30646816-bc10-46b4-98fc-2644844f7430
                © The Author(s) 2011
                History
                : 1 December 2010
                : 8 May 2011
                Categories
                Article
                Custom metadata
                © Springer Science+Business Media B.V. 2012

                multiple sex chromosomes,neo-sex chromosome,x1x2y,stickleback,sexual conflict,speciation

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