Department of Biology, Section for Evolutionary Ecology, Lund University, 223 62 Lund, Sweden;
School of Life Sciences, University of Sussex, Brighton BN1 9QG, United Kingdom.
Proc Natl Acad Sci U S A. 2021 Feb 23;118(8). doi: 10.1073/pnas.2003359118.
Antagonistic interactions between the sexes are important drivers of evolutionary divergence. Interlocus sexual conflict is generally described as a conflict between alleles at two interacting loci whose identity and genomic location are arbitrary, but with opposite fitness effects in each sex. We build on previous theory by suggesting that when loci under interlocus sexual conflict are located on the sex chromosomes it can lead to cycles of antagonistic coevolution between them and therefore between the sexes. We tested this hypothesis by performing experimental crosses using where we reciprocally exchanged the sex chromosomes between five allopatric wild-type populations in a round-robin design. Disrupting putatively coevolved sex chromosome pairs resulted in increased male reproductive success in 16 of 20 experimental populations (10 of which were individually significant), but also resulted in lower offspring egg-to-adult viability that affected both male and female fitness. After 25 generations of experimental evolution these sexually antagonistic fitness effects appeared to be resolved. To formalize our hypothesis, we developed population genetic models of antagonistic coevolution using fitness expressions based on our empirical results. Our model predictions support the conclusion that antagonistic coevolution between the sex chromosomes is plausible under the fitness effects observed in our experiments. Together, our results lend both empirical and theoretical support to the idea that cycles of antagonistic coevolution can occur between sex chromosomes and illustrate how this process, in combination with autosomal coadaptation, may drive genetic and phenotypic divergence between populations.
性别间的相互拮抗作用是进化分歧的重要驱动因素。基因间性冲突通常被描述为两个相互作用的基因座之间的等位基因冲突,其身份和基因组位置是任意的,但在每个性别中的适应性效应相反。我们在前人的理论基础上提出,当基因间性冲突的基因座位于性染色体上时,它可能导致它们之间以及性别之间的拮抗协同进化循环。我们通过使用 进行实验杂交来检验这一假设,其中我们在轮次设计中相互交换了五个隔离野生型种群的性染色体。破坏可能协同进化的性染色体对导致 20 个实验种群中的 16 个(其中 10 个具有个体显著性)雄性繁殖成功增加,但也导致后代卵到成虫的存活率降低,影响雄性和雌性适应性。经过 25 代的实验进化,这些性拮抗适应性效应似乎得到了解决。为了正式提出我们的假设,我们使用基于我们的经验结果的适应性表达来开发拮抗协同进化的群体遗传模型。我们的模型预测支持这样的结论,即在我们实验中观察到的适应性效应下,性染色体之间的拮抗协同进化是合理的。总之,我们的研究结果为性染色体之间的拮抗协同进化的观点提供了实证和理论上的支持,并说明了这个过程如何与常染色体的协同适应相结合,可能导致种群之间的遗传和表型分歧。