Mate discrimination among subspecies through a conserved olfactory pathway

Signaling mechanisms underlying the sexual isolation of species are poorly understood. Using four subspecies of Drosophila mojavensis as a model, we identify two behaviorally active male-specific pheromones. One functions as a conserved male anti-aphrodisiac in all subspecies and acts via gustation. The second induces female receptivity via olfaction exclusively in the two subspecies that produce it. Genetic analysis of the cognate receptor for the olfactory pheromone indicates an important role for this sensory pathway in promoting sexual isolation of subspecies, in collaboration with auditory signals. Surprisingly, the peripheral sensory pathway detecting this pheromone is conserved molecularly, physiologically and anatomically across subspecies. These observations imply that subspecies-specific behaviors arise from differential interpretation of the same peripheral cue, reminiscent of sexually conserved detection but dimorphic interpretation of male pheromones in D. melanogaster. Our results reveal that, during incipient speciation, pheromone production, detection and interpretation do not necessarily evolve in a coordinate manner.