Lund-Hansen, K. K. | Search bioRxiv

bioRxiv2020

Feminisation of complex traits in Drosophila melanogaster via female-limited X chromosome evolution

A handful of studies have investigated sexually antagonistic constraints on obtaining sex-specific fitness optima, though exclusively through male-genome-limited evolution experiments. In this paper, we established a female-limited X chromosome evolution experiment, where we used an X chromosome balancer to enforce the inheritance of the X chromosome through the matriline, thus removing exposure to male selective constraints. This approach eliminates the effects of sexually antagonistic selection on the X chromosome, permitting evolution towards a single sex-specific optimum. After multiple generations of selection, we found strong evidence that body size and development time had moved towards a female-specific optimum, whereas reproductive fitness and locomotion activity remained unchanged. The changes in body size and development time are consistent with previous results, and suggest that the X chromosome is enriched for sexually antagonistic genetic variation controlling these traits. The lack of change in reproductive fitness and locomotion activity could be due to a number of mutually non-exclusive explanations, including a lack of sexually antagonistic variance on the X chromosome or confounding effects of the use of the balancer chromosome. This study is the first to employ female-genome-limited selection and adds to the understanding of the complexity of sexually antagonistic genetic variation.

evolutionary biology↗

bioRxiv2019

Sexually antagonistic coevolution between the sex chromosomes of Drosophila melanogaster

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.

evolutionary biology↗