Data from: Opposing patterns of intraspecific and interspecific differentiation in sex chromosomes and autosomes

Linking intraspecific and interspecific divergence is an important challenge in speciation research. X chromosomes are expected to evolve faster than autosomes and disproportionately contribute to reproductive barriers, and comparing genetic variation on X and autosomal markers within and between species can elucidate evolutionary processes that shape genome variation. We performed RADseq on a 16-population transect of two closely-related Australian cricket species, Teleogryllus commodus and T. oceanicus, covering allopatry and sympatry. This classic study system for sexual selection provides a rare exception to Haldane’s rule, as hybrid females are sterile. We found no evidence of recent introgression, despite the fact that the species co-exist in overlapping habitats in the wild and interbreed in the laboratory. Putative X-linked loci showed greater differentiation between species compared to autosomal loci. However, population differentiation within species was unexpectedly lower on X-linked markers than autosomal markers, and relative X-to-autosomal genetic diversity was inflated above neutral expectations. Populations of both species showed genomic signatures of recent population expansions, but these were not strong enough to account for the inflated X/A diversity. Instead, most of the excess polymorphism on the X could better be explained by sex-biased processes that increase the relative effective population size of the X, such as interspecific variation in the strength of sexual selection among males. Taken together, the opposing patterns of diversity and differentiation at X versus autosomal loci implicate a greater role for sex-linked genes in maintaining species boundaries in this system.

在物种形成研究领域，联结种内与种间分化是一项关键的科学挑战。X染色体的演化速率通常被认为快于常染色体，且会显著不成比例地参与生殖屏障的构建；比较物种内外X染色体与常染色体遗传标记的遗传变异，可阐明塑造基因组变异的核心演化过程。我们对两种亲缘关系紧密的澳大利亚蟋蟀物种——Teleogryllus commodus和T. oceanicus的16个种群样带开展了RADseq（限制性位点相关DNA测序）研究，样带覆盖了异域分布与同域分布区域。该类群是性选择研究的经典模式系统，同时也是霍尔丹法则（Haldane's rule）的罕见例外：其杂交雌性表现为不育。尽管这两个物种在野外共享重叠生境且可在实验室中完成杂交，但我们未发现近期发生基因渐渗的证据。与常染色体位点相比，推定的X连锁位点在物种间呈现出更高的遗传分化水平。然而，种内种群的遗传分化在X连锁标记上却意外低于常染色体标记，且X染色体与常染色体的相对遗传多样性水平超出中性演化预期，呈现过度升高的现象。两个物种的种群均展现出近期种群扩张的基因组特征，但该信号强度不足以解释X/A相对遗传多样性的升高现象。取而代之的是，X染色体上过多的多态性可更好地由性别偏向性演化过程解释——这类过程会提升X染色体的相对有效种群大小，例如雄性间性选择强度在物种间存在差异。综合来看，X染色体与常染色体位点在遗传多样性与分化水平上呈现出的相反模式，表明性连锁基因在该系统的物种边界维持中发挥了更为重要的作用。