Molecular evolution of sex-biased genes in the Drosophila ananassae subgroup

BACKGROUND: Genes with sex-biased expression often show rapid molecular evolution between species. Previous population genetic and comparative genomic studies of Drosophila melanogaster and D. simulans revealed that male-biased genes have especially high rates of adaptive evolution. To test if this is also the case for other lineages within the melanogaster group, we investigated gene expression in D. ananassae, a species that occurs in structured populations in tropical and subtropical regions. We used custom-made microarrays and published microarray data to characterize the sex-biased expression of 129 D. ananassae genes whose D. melanogaster orthologs had been classified previously as male-biased, female-biased, or unbiased in their expression and had been studied extensively at the population-genetic level. For 43 of these genes we surveyed DNA sequence polymorphism in a natural population of D. ananassae and determined divergence to the sister species D. atripex and D. phaeopleura. RESULTS: Sex-biased expression is generally conserved between D. melanogaster and D. ananassae, with the majority of genes exhibiting the same bias in the two species. However, about one-third of the genes have either gained or lost sex-biased expression in one of the species and a small proportion of genes (~4%) have changed bias from one sex to the other. The male-biased genes of D. ananassae show evidence of positive selection acting at the protein level. However, the signal of adaptive protein evolution for male-biased genes is not as strong in D. ananassae as it is in D. melanogaster and is limited to genes with conserved male-biased expression in both species. Within D. ananassae, a significant signal of adaptive evolution is also detected for female-biased and unbiased genes. CONCLUSIONS: Our findings extend previous observations of widespread adaptive protein evolution to an independent Drosophila lineage, the D. ananassae subgroup. However, the rate of adaptive evolution is not greater for male-biased genes than for female-biased or unbiased genes, which suggests that there are differences in sex-biased gene evolution between the two lineages.