Hearn Katherine E, Koch Eva L, Stankowski Sean, Butlin Roger K, Faria Rui, Johannesson Kerstin, Westram Anja M
Ecology and Evolutionary Biology, School of Biosciences University of Sheffield Sheffield S10 2TN United Kingdom.
Department of Zoology University of Cambridge Cambridge CB2 3EJ United Kingdom.
Evol Lett. 2022 Aug 12;6(5):358-374. doi: 10.1002/evl3.295. eCollection 2022 Oct.
Sexual antagonism is a common hypothesis for driving the evolution of sex chromosomes, whereby recombination suppression is favored between sexually antagonistic loci and the sex-determining locus to maintain beneficial combinations of alleles. This results in the formation of a sex-determining region. Chromosomal inversions may contribute to recombination suppression but their precise role in sex chromosome evolution remains unclear. Because local adaptation is frequently facilitated through the suppression of recombination between adaptive loci by chromosomal inversions, there is potential for inversions that cover sex-determining regions to be involved in local adaptation as well, particularly if habitat variation creates environment-dependent sexual antagonism. With these processes in mind, we investigated sex determination in a well-studied example of local adaptation within a species: the intertidal snail, . Using SNP data from a Swedish hybrid zone, we find novel evidence for a female-heterogametic sex determination system that is restricted to one ecotype. Our results suggest that four putative chromosomal inversions, two previously described and two newly discovered, span the putative sex chromosome pair. We determine their differing associations with sex, which suggest distinct strata of differing ages. The same inversions are found in the second ecotype but do not show any sex association. The striking disparity in inversion-sex associations between ecotypes that are connected by gene flow across a habitat transition that is just a few meters wide indicates a difference in selective regime that has produced a distinct barrier to the spread of the newly discovered sex-determining region between ecotypes. Such sex chromosome-environment interactions have not previously been uncovered in and are known in few other organisms. A combination of both sex-specific selection and divergent natural selection is required to explain these highly unusual patterns.
性拮抗是驱动性染色体进化的一个常见假说，即性拮抗基因座与性别决定基因座之间的重组抑制受到青睐，以维持有利的等位基因组合。这导致了性别决定区域的形成。染色体倒位可能有助于重组抑制，但其在性染色体进化中的精确作用仍不清楚。由于局部适应常常通过染色体倒位抑制适应性基因座之间的重组来促进，因此覆盖性别决定区域的倒位也有可能参与局部适应，特别是如果栖息地差异产生环境依赖性性拮抗的话。考虑到这些过程，我们在一个物种内局部适应的深入研究实例中调查了性别决定：潮间带蜗牛。利用来自瑞典杂交带的单核苷酸多态性（SNP）数据，我们发现了一种仅限于一种生态型的雌性异配性别决定系统的新证据。我们的结果表明，四个假定的染色体倒位，两个先前已描述，两个新发现，跨越假定的性染色体对。我们确定了它们与性别的不同关联，这表明了不同年龄的不同层次。在第二种生态型中也发现了相同的倒位，但没有显示出任何性别关联。在仅几米宽的栖息地过渡区域通过基因流连接的生态型之间，倒位与性别的关联存在显著差异，这表明选择机制存在差异，这为新发现的性别决定区域在生态型之间的传播产生了明显的障碍。这种性染色体与环境的相互作用此前在[具体物种名称未提及]中尚未被发现，在其他生物中也很少见。需要结合性别特异性选择和分歧性自然选择来解释这些极其不寻常的模式。
