Learning individual signatures: rove beetle males discriminate unreceptive females by cuticular hydrocarbon patterns

Abstract

Pheromones elicit a species-wide, class-specific and stereotyped reaction. By learning class- or individual-specific cues in association with pheromones and subsequently using the cues alone for discrimination, a receiver may react more effectively to its social environment than if its only reaction to pheromones was stereotyped. In the rove beetle Aleochara curtula , recently mated females are inappropriate mating partners; nevertheless they elicit male sexual reactions owing to olfactory excitation by the female sex pheromone. During physical contact, mated females can be discerned by gustatory perception of an antiaphrodisiac pheromone via the clasper-like parameres of the male genitalia. Males transfer the antiaphrodisiac pheromone during copulation, together with the spermatophore, onto their mate. Our experiments showed that in association with antiaphrodisiac pheromone perception, males learned the scent of a mated female and relied on this chemical signature to refrain from sexual grasping responses in subsequent encounters. Habituation–dishabituation experiments further showed that the learned patterns were individual specific. The application of cuticular extracts to alter the scent of females, and the resulting inability of males to discriminate between similar-smelling females, demonstrated that males relied on cuticular hydrocarbons for individual discrimination. Chemical analysis of the cuticular profiles revealed higher variation in female than in male patterns. Learning the scent of mated females in association with the antiaphrodisiac pheromone allows males to reduce the time and energy spent on sexual reactions towards inappropriate mating partners and hence gives them more time to search for a receptive female at the mating site. ► Male rove beetles Aleochara curtula learn the individual-specific scent of mated females. ► The scent of females is only learned in association with the antiaphrodisiac pheromone. ► The scent cues are provided by the cuticular hydrocarbons of females. ► Males refrain from sexual grasping response when perceiving the scent of a learned female.