Data from: Sex chromosome turnover contributes to genomic divergence between incipient stickleback species

Sex chromosomes turn over rapidly in some taxonomic groups, where closely related species have different sex chromosomes. Although there are many examples of sex chromosome turnover, we know little about the functional roles of sex chromosome turnover in phenotypic diversification and genomic evolution. The sympatric pair of Japanese threespine stickleback (Gasterosteus aculeatus) provides an excellent system to address these questions: the Japan Sea species has a neo-sex chromosome system resulting from a fusion between an ancestral Y chromosome and an autosome, while the sympatric Pacific Ocean species has a simple XY sex chromosome system. Furthermore, previous quantitative trait locus (QTL) mapping demonstrated that the Japan Sea neo-X chromosome contributes to phenotypic divergence and reproductive isolation between these sympatric species. To investigate the genomic basis for the accumulation of genes important for speciation on the neo-X chromosome, we conducted whole genome sequencing of males and females of both the Japan Sea and the Pacific Ocean species. No substantial degeneration has yet occurred on the neo-Y chromosome, but the nucleotide sequence of the neo-X and the neo-Y has started to diverge, particularly at regions near the fusion. The neo-sex chromosomes also harbor an excess of genes with sex-biased expression. Furthermore, genes on the neo-X chromosome showed higher non-synonymous substitution rates than autosomal genes in the Japan Sea lineage. Genomic regions of higher sequence divergence between species, genes with divergent expression between species, and QTL for inter-species phenotypic differences were found not only at the regions near the fusion site, but also at other regions along the neo-X chromosome. Neo-sex chromosomes can therefore accumulate substitutions causing species differences even in the absence of substantial neo-Y degeneration.

在部分分类类群中，性染色体更替速度极快，亲缘关系相近的物种往往拥有不同的性染色体。尽管已有诸多性染色体更替的研究案例，但学界对其在表型多样化与基因组进化过程中发挥的功能性作用仍所知有限。同域分布的日本三刺棘鱼（Gasterosteus aculeatus）物种对为解答这类问题提供了绝佳的研究体系：日本海种群拥有由祖先Y染色体与常染色体融合形成的新性染色体（neo-sex chromosome）系统，而同域分布的太平洋种群则仅具备简单的XY性染色体系统。此前的数量性状位点（quantitative trait locus, QTL）定位研究已证实，日本海种群的新X染色体参与了这两个同域物种间的表型分化与生殖隔离形成。为探究新X染色体上积累与物种形成相关关键基因的基因组基础，我们对日本海与太平洋种群的雌雄个体开展了全基因组测序。研究结果显示，目前新Y染色体尚未出现明显的退化，但新X与新Y染色体的核苷酸序列已开始出现分化，尤其是在融合位点附近的区域。新性染色体上还富集了大量具有性别偏向性表达的基因。此外，在日本海种群谱系中，新X染色体上的基因非同义替换率高于常染色体基因。物种间序列分化程度更高的基因组区域、物种间表达模式存在差异的基因，以及调控物种间表型差异的QTL位点，不仅分布于融合位点附近区域，也出现在新X染色体的其他区段。因此，即便新Y染色体尚未出现显著退化，新性染色体仍可积累引发物种间差异的碱基替换。