Masculinization of gene expression is associated with male quality in Drosophila melanogaster

The signature of sexual selection has been revealed through the study of differences in patterns of genome-wide gene expression, both between the sexes and between alternative reproductive morphs within a single sex. What remains unclear, however, is whether differences in gene expression patterns between individuals of a given sex consistently map to variation in individual quality. Such a pattern, particularly if found in males, would provide unambiguous evidence that the phenotypic response to sexual selection is shaped through sex-specific alterations to the transcriptome. To redress this knowledge gap, we explored whether patterns of sex-biased gene expression are associated with variation in male reproductive quality in Drosophila melanogaster. We measured two male reproductive phenotypes, and their association with sex-biased gene expression, across a selection of inbred lines from the Drosophila Genetic Reference Panel. Genotypes with higher expression of male-biased genes produced males exhibiting shorter latencies to copulation, and higher capacity to inseminate females. Conversely, female-biased genes tended to show negative associations with these male reproductive traits across genotypes. We uncovered similar patterns, by reanalyzing a published dataset from a second D. melanogaster population. Our results reveal the footprint of sexual selection in masculinising the male transcriptome.