The microevolutionary response to male-limited X-chromosome evolution in Drosophila melanogaster reflects macroevolutionary patterns

Abstract

Due to its hemizygous inheritance and role in sex determination, the X chromosome is expected to play an important role in the evolution of sexual dimorphism, and to be enriched for sexually antagonistic genetic variation. By forcing the X chromosome to only be expressed in males over >40 generations, we changed the selection pressures on the X to become similar to those experienced by the Y. This releases the X from any constraints arising from selection in females, and should lead to specialization for male fitness, which could occur either via direct effects of X-linked loci or trans-regulation of autosomal loci by the X. We found evidence of masculinization via upregulation of male-benefit sexually antagonistic genes, and downregulation of X-linked female benefit genes. Interestingly, we could detect evidence of microevolutionary changes consistent with previously documented macroevolutionary patterns, such as changes in expression consistent with previously established patterns of sexual dimorphism, an increase in the expression of metabolic genes related to mitonuclear conflict, and evidence that dosage compensation effects can be rapidly altered. These results confirm the importance of the X in the evolution of sexual dimorphism and as a source for sexually antagonistic genetic variation, and demonstrate that experimental evolution can be a fruitful method for testing theories of sex chromosome evolution.