Data from: Genomic islands of differentiation in two songbird species reveal candidate genes for hybrid female sterility

Hybrid sterility is a common first step in the evolution of postzygotic reproductive isolation. According to Haldane’s Rule it affects predominantly the heterogametic sex. While the genetic basis of hybrid male sterility in organisms with heterogametic males has been studied for decades, the genetic basis of hybrid female sterility in organisms with heterogametic females has received much less attention. We investigated the genetic basis of reproductive isolation in two closely related avian species, the Common Nightingale (Luscinia megarhynchos) and the Thrush Nightingale (L. luscinia), that hybridize in a secondary contact zone and produce viable hybrid progeny. In accordance with Haldane’s Rule, hybrid females are sterile, while hybrid males are fertile, allowing gene flow to occur between the species. Using transcriptomic data from multiple individuals of both nightingale species we identified genomic islands of high differentiation (FST) and of high divergence (Dxy), and we analyzed gene content and patterns of molecular evolution within these islands. Interestingly, we found that these islands were enriched for genes related to female meiosis and metabolism. The islands of high differentiation and divergence were also characterized by higher levels of linkage disequilibrium than the rest of the genome in both species indicating that they might be situated in genomic regions of low recombination. This study provides one of the first insights into genetic basis of hybrid female sterility in organisms with heterogametic females.

杂种不育是合子后生殖隔离演化过程中常见的初始阶段。根据霍尔丹法则（Haldane’s Rule），该效应主要作用于异配性别（heterogametic sex）。尽管针对异配性别为雄性的生物，其杂种雄性不育的遗传机制已被研究数十年，但异配性别为雌性的生物中，杂种雌性不育的遗传基础却极少受到关注。我们对两种近缘鸟类——普通夜莺（*Luscinia megarhynchos*）与歌鸲夜莺（*L. luscinia*）——的生殖隔离遗传基础展开了研究。这两个物种在次生接触带发生杂交，可产生可存活的杂交后代。研究结果符合霍尔丹法则：杂交雌性不育，而杂交雄性可育，使得两物种间能够发生基因交流。我们利用两种夜莺多个个体的转录组数据（transcriptomic data），鉴定出了高分化（FST，固定指数）与高分歧（Dxy，核苷酸分歧度）的基因组岛，并分析了这些区域内的基因组成与分子演化模式。有趣的是，我们发现这些基因组岛富集有与雌性减数分裂及代谢相关的基因。相较于两物种的基因组其余区域，高分化与高分歧基因组岛同样表现出更高的连锁不平衡（linkage disequilibrium）水平，这表明它们可能位于重组率较低的基因组区域内。本研究为解析异配性别为雌性的生物的杂种雌性不育遗传基础提供了首批认知之一。