Transcriptome Differences between Alternative Sex Determining Genotypes in the House Fly, Musca domestica

Sex determination evolves rapidly, often because of turnover of the genes at the top of the pathway. The house fly, Musca domestica, has a multifactorial sex determination system, allowing us to identify the selective forces responsible for the evolutionary turnover of sex determination in action. There is a male determining factor, M, on the Y chromosome (Y-M), which is probably the ancestral state. An M factor on the third chromosome (IIIM) has reached high frequencies in multiple populations across the world, but the evolutionary forces responsible for the invasion of IIIM are not resolved. To test whether the IIIM chromosome invaded because of sex-specific selection pressures, we used mRNA sequencing to determine whether isogenic males that differ only in the presence of the Y-M or IIIM chromosome have different gene expression profiles. We find that more genes are differentially expressed between Y-M and IIIM males in testis than head, and that genes with male-biased expression are most likely to be differentially expressed between Y-M and IIIM males. We additionally find that IIIM males have a masculinized gene expression profile, suggesting that the IIIM chromosome has accumulated an excess of male-beneficial alleles because of its male-limited transmission. These results are consistent with the hypothesis that sex-specific selection acts on alleles linked to the male-determining locus driving evolutionary turnover in the sex determination pathway.