A role for a neo-sex chromosome in stickleback speciation

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. 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.

Community assembly in Nothobranchius annual fishes: Nested patterns, environmental niche and biogeographic history

“…However, Nothobranchius genomes are evolving at a fast rate (Reichwald et al., 2015; Valenzano et al., 2015), with intra‐specific differentiation in the sex determination system in N. furzeri (Valenzano et al., 2015). Divergence in sex determination systems and sex‐linked genes is known to drive speciation across several taxa (Kitano et al., 2009; Qvarnström & Bailey, 2009). Interestingly, species of the R‐clade differ cytogenetically (Shidlovskiy et al., 2010), and it is possible that a combination of allopatric diversification and major cytogenetic incompatibilities during secondary sympatry may promote speciation at least in some Nothobranchius lineages.…”

No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution

“…This apparent association between the function of sex determination and suppression of recombination has led to the suggestion that restricted recombination in sex chromosomes evolves due to selection to resolve sexually antagonistic genetic interactions [2,[9][10][11]. This sexual antagonism hypothesis has assumed the status of conventional wisdom, to the extent that, in many recent publications, sexual antagonism is the only hypothesis suggested to account for restricted recombination in sex chromosomes [1,6,[12][13][14][15][16][17][18][19][20][21][22]. However, empirical support for the sexual antagonism hypothesis is equivocal [1].…”

Independent fusions and recent origins of sex chromosomes in the evolution and diversification of glass knife fishes (Eigenmannia)

“…This is likely to result in a significant level of infertility in potential F 1 hybrids because of abnormal meiotic segregation (Wallace et al, 2002). This effect would likely be compounded if the chromosome happened to harbor sex-determining genes, given the disproportionate importance of sex chromosomes in the evolution of post-mating isolation mechanisms (Presgraves, 2008;Kitano et al, 2009).…”

“…Within fishes, a number of different sex-determining systems may be present even among closely related species (Peichel et al, 2004;Takehana et al, 2007), including those within Eigenmannia (Henning et al, 2008), and have recently been implicated in speciation as well (Kitano et al, 2009). The reason for this evolutionary lability is unknown, but may be related to the multiple redundant gene copies created by whole-genome duplication events (Meyer and Schartl, 1999) and duplications of single sex-determining genes (Nanda et al, 2002).…”