While the diversity of sex pheromone communication systems across insects is well documented, the mechanisms that lead to such diversity are not well understood. Sex pheromones constitute a species-specific system of sexual communication that reinforces interspecific reproductive isolation. When odor blends evolve, the efficacy of male-female communication becomes compromised, unless preference for novel blends also evolves. We explore odor learning as a possible mechanism leading to changes in sex pheromone preferences in the butterfly Bicyclus anynana. Our experiments reveal mating patterns suggesting that mating bias for new blends can develop following a short learning experience, and that this maternal experience impacts the mating outcome of offspring without further exposure. We propose that odor learning can be a key factor in the evolution of sex pheromone blend recognition and in chemosensory speciation.

Insects use species-specific sex pheromone blends to attract members of the opposite sex which express the corresponding molecular receptors. Given this lock and key mechanism used for species identification and mate choice, it is currently not well understood how pheromone blends or receptor systems evolve. One possibility is that insects develop preferences for new sex pheromone blends via the process of learning, and that these learned preferences may be passed on to the next generation. We tested these hypotheses by exposing newly emerged Bicyclus anynana female butterflies to either wild type or to modified male sex pheromone blends. A few days later, we scored female mating outcome in a choice trial involving both male types. We also assessed the mating outcome of naïve offspring of females that underwent distinct odor learning trials to test for a potential inheritance of learned odor preferences. Naïve (parental) females mated preferentially with Wt-blend males, but females pre-exposed to new blends either shifted their preference to new-blend males, or mated equally with males of either blend type; the response depending on the new blend they were introduced to. Naïve daughters of females who were exposed to new-blend males behaved similarly to their experienced mothers. We demonstrate that females are able to learn preferences for novel pheromone blends in response to a short social experience, and pass that learned preference down to the next generation. This suggests that learning can be a key factor in the evolution of sex pheromone blend recognition and in chemosensory speciation.Significance statementWhile the diversity of sex pheromone communication systems across insects is well documented, the mechanisms that lead to such diversity are not well understood. Sex pheromones constitute a species-specific system of sexual communication that reinforces interspecific reproductive isolation. When odor blends evolve, the efficacy of male-female communication becomes compromised, unless preference for novel blends also evolves. We explore odor learning as a possible mechanism leading to changes in sex pheromone preferences. We show that preferences for new blends can develop following a short learning experience, and that these novel preferences can be transmitted to the next generation. To our knowledge, this is the first investigation of sex pheromone blend preference learning impacting mate choice and being inherited in an insect.