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.

在部分生物类群中，性染色体更替速度极快，近缘物种间往往拥有截然不同的性染色体系统。尽管已有诸多性染色体更替的案例被报道，但我们对其在表型多样化与基因组进化中发挥的功能性作用仍知之甚少。日本三棘刺鱼（Gasterosteus aculeatus）的同域物种对为解答上述问题提供了绝佳研究体系：其中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系统，而同域共存的太平洋种群则仅具备简单的XY性染色体系统。此外，既往数量性状位点（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过程。为探究新X染色体上富集物种形成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。目前新Y染色体尚未出现显著的退化现象，但新X与新Y染色体的核苷酸序列已开始出现分化，且该分化在融合位点附近区域尤为显著。新性染色体上还富集了一批具有性别偏向性表达特征的基因。此外，日本海种群谱系中，新X染色体上的基因相较于常染色体基因，展现出更高的非同义替换率。跨物种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，以及介导物种间表型差异的QTL位点，不仅分布于融合位点附近区域，也广泛存在于新X染色体的其他区段。由此可见，即便新Y染色体尚未发生显著退化，新性染色体仍可积累导致物种间产生差异的碱基替换。