Sexually antagonistic coevolution between the sex chromosomes of Drosophila melanogaster

Abstract

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. Here we build on previous theory and suggest that when these two loci 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 in which we reciprocally exchanged the sex chromosomes between five wild-type populations in a round-robin design. Disrupting putatively coevolved sex chromosome pairs resulted in increased male reproductive success in 16 out of 20 experimental populations (10 of which were 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 have been resolved. To help formalise our hypothesis, we developed population genetic models of antagonistic coevolution using fitness expressions based on our empirical results. Our models 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 a cycle of antagonistic coevolution can occur between sex chromosomes and illustrates how this process may drive genetic and phenotypic divergence between populations. SignificanceSex chromosomes are not only involved in genetic sex determination - they are also important factors in sexual conflict and speciation. Here, using a combination of experiments and population genetic models, we show that the sex chromosomes in Drosophila melanogaster can coevolve antagonistically. We found that swapping sex chromosomes between five Drosophila melanogaster populations increased male fitness at the cost of reduced offspring survival. After 25 generations, the increase had disappeared, consistent with the completion of a cycle of antagonistic coevolution. Using parameter values based on these empirical data, our models show that antagonistic coevolution between the sex chromosomes is a biologically plausible explanation for the results. Thus, our results point to a potentially important path to speciation through sexual conflict.