Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones

Abstract

Sex pheromones play a pivotal role in the communication of many sexually reproducing organisms. Accordingly, speciation is often accompanied by pheromone diversification enabling proper mate finding and recognition. Current theory implies that chemical signals are under stabilizing selection by the receivers who thereby maintain the integrity of the signals. How the tremendous diversity of sex pheromones seen today evolved is poorly understood. Here we unravel the genetics of a newly evolved pheromone phenotype in wasps and present results from behavioural experiments indicating how the evolution of a new pheromone component occurred in an established sender-receiver system. We show that male Nasonia vitripennis evolved an additional pheromone compound differing only in its stereochemistry from a pre-existing one. Comparative behavioural studies show that conspecific females responded neutrally to the new pheromone phenotype when it evolved. Genetic mapping and gene knockdown show that a cluster of three closely linked genes accounts for the ability to produce this new pheromone phenotype. Our data suggest that new pheromone compounds can persist in a sender's population, without being selected against by the receiver and without the receiver having a pre-existing preference for the new pheromone phenotype, by initially remaining unperceived. Our results thus contribute valuable new insights into the evolutionary mechanisms underlying the diversification of sex pheromones. Furthermore, they indicate that the genetic basis of new pheromone compounds can be simple, allowing them to persist long enough in a population for receivers to evolve chemosensory adaptations for their exploitation.