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.

Selection on male sex pheromone composition contributes to butterfly reproductive isolation

“…First, we found similar pMSP components in distantly related Bicyclus lineages and most pMSP components in one Bicyclus species could be found scattered as trace compounds in a few other Bicyclus lineages (in 14% of the species on average, noted by grey cells in figure 2b). This large phenotypic standing variation, as found in other species [41,57], suggests that each Bicyclus rspb.royalsocietypublishing.org Proc. R. Soc.…”

Genetic and epigenetic architecture of sex-biased expression in the jewel wasps Nasonia vitripennis and giraulti

“…2B and SI Appendix, Table S3) (35). Linoleic acid is an essential unsaturated fatty acid in other insects that lack Δ12-desaturase activity, and in Nasonia it is the precursor of the male-derived sex pheromone (4R,5R)-and (4R,5S)-5-hydroxy-4-decanolides, which is highly attractive to virgin females (36,37). Male mating success positively correlates with the amount of pheromone that they produce (38), which likely explains the high levels of expression of these genes.…”

Does early learning drive ecological divergence during speciation processes in parasitoid wasps?

“…We are currently testing alternative mechanisms of reproductive isolation, for example hybrid breakdown based on genetic differences [51], cytoplasmic incompatibility caused by Wolbachia infection [52] and sexual isolation owing to different pheromones [53]. Remarkably, a recent study revealed that cuticular hydrocarbons, which are used as mate recognition rspb.royalsocietypublishing.org Proc.…”