Sexually antagonistic coevolution between the sex chromosomes of Drosophila melanogaster

Abstract

Significance Sex chromosomes are not only involved in genetic sex determination—they are also important factors in sexual conflict and speciation. Using laboratory experiments and population genetic modeling, we show that the sex chromosomes of Drosophila melanogaster can coevolve antagonistically. We found that swapping sex chromosomes between five D. melanogaster populations increased male fitness, apparently at the cost of reduced offspring survival. After 25 generations, these fitness effects had disappeared, consistent with the resolution of conflict after disrupting antagonistically coevolved X- and Y-linked genes. Our population genetic models show that antagonistic coevolution between sex chromosomes is a biologically plausible explanation for our empirical findings. Together, our empirical and theoretical results provide support for a potential path to speciation through sexual conflict. 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 Drosophila melanogaster 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.