Natural evolution of intermale sexual behavior by multiple pheromone switches among Drosophila species

We have identified a Drosophila species in which males exhibit spontaneous, elaborate, and robust intermale sexual behavior. Males of D. santomea, a West African island endemic, distinguish conspecific sexes but court males and females promiscuously and seldom attack. Elevated intermale courtship derives from at least three changes in two separate pheromone systems. In males, the sexually monomorphic cuticular pheromone 7-tricosene promotes rather than inhibits courtship and the courtship-inhibiting olfactory pheromone cVA is reduced 84-92% compared to close relatives, including the sibling species D. yakuba. The third change is surprisingly in D. santomea females, where cVA suppresses rather than promotes sexual receptivity. The female cVA switch and male cVA reduction may have co-evolved to maintain efficient intraspecific mating in D. santomea but prevent sympatric hybridization with D. yakuba, or to reduce intraspecific aggression. We find that high intermale courtship and low cVA also co-occur and appear selectively derived in a distant monomorphic species D. persimilis, implying pheromonal and behavioral convergence in the two recently speciated taxa. The data suggest that sequential changes in the behavioral valence and levels of pheromones explain the recent evolutionary emergence of intermale sexual behavior in Drosophila.