Regulatory changes in the fatty acid elongase eloF underlie the evolution of sex-specific pheromone profiles in Drosophila prolongata

BACKGROUND: Pheromones play a key role in regulating sexual behavior throughout the animal kingdom. In Drosophila and other insects, many cuticular hydrocarbons (CHCs) are sexually dimorphic, and some are known to perform pheromonal functions. However, the genetic control of sex-specific CHC production is poorly understood outside of the model species D. melanogaster. A recent evolutionary change is found in D. prolongata, which, compared to its closest relatives, shows greatly increased sexual dimorphism in both CHCs and the chemosensory system responsible for their perception. A key transition involves a male-specific increase in the proportion of long-chain CHCs. RESULTS: Perfuming D. prolongata females with the male-biased long-chain CHCs reduces copulation success, suggesting that these compounds function as sex pheromones. The evolutionary change in CHC profiles correlates with a male-specific increase in the expression of multiple genes involved in CHC biosynthesis, including fatty acid elongases, reductases and other key enzymes. In particular, elongase F, which is responsible for producing female-specific pheromones in D. melanogaster, is strongly upregulated in D. prolongata males compared both to females and to males of the sibling species. Mutations in eloF reduce the amount of long-chain CHCs, resulting in a partial feminization of pheromone profiles in D. prolongata males. Transgenic experiments show that sex-biased expression of eloF is caused in part by a putative transposable element honghaier insertion in its regulatory region. CONCLUSIONS: These results show that cis-regulatory changes in the eloF gene, along with other changes in the CHC synthesis pathway, contribute to the evolution of sexual communication.