A handful of studies have investigated sexually antagonistic constraints on achieving sex-specific fitness optima, although exclusively through male-genome-limited evolution experiments. In this article, we established a female-limited X chromosome evolution experiment, where we used an X chromosome balancer to enforce the inheritance of the X 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 toward a single sex-specific optimum. After multiple generations of selection, we found strong evidence that body size and development time had moved toward 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 particular traits. The lack of change in reproductive fitness and locomotion activity could be due to a number of mutually nonexclusive explanations, including a lack of sexually antagonistic variance on the X chromosome for those traits 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.
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.
1A handful of studies have investigated sexually antagonistic constraints on obtaining 2 sex-specific fitness optima, though exclusively through male-genome-limited 3 evolution experiments. In this paper, we established a female-limited X chromosome 4 evolution experiment, where we used an X chromosome balancer to enforce the 5 inheritance of the X chromosome through the matriline, thus removing exposure to 6 male selective constraints. This approach eliminates the effects of sexually 7 antagonistic selection on the X chromosome, permitting evolution towards a single 8 sex-specific optimum. After multiple generations of selection, we found strong 9 evidence that body size and development time had moved towards a female-specific 10 optimum, whereas reproductive fitness and locomotion activity remained unchanged. 11The changes in body size and development time are consistent with previous results, 12 and suggest that the X chromosome is enriched for sexually antagonistic genetic 13 variation controlling these traits. The lack of change in reproductive fitness and 14 locomotion activity could be due to a number of mutually non-exclusive explanations, 15 including a lack of sexually antagonistic variance on the X chromosome or 16 confounding effects of the use of the balancer chromosome. This study is the first to 17 employ female-genome-limited selection and adds to the understanding of the 18 complexity of sexually antagonistic genetic variation. 19 20 21
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