Decoding the genetic and chemical basis of sexual attractiveness in parasitic wasps

Abstract

Attracting and securing potential mating partners is of fundamental importance for successfully initiating reproduction and thus assuring the passing of genes to the next generation. Therefore, signaling sexual attractiveness is expected to be tightly coordinated in communication systems synchronizing senders and receivers. Chemical signaling has permeated through all taxa of life as the earliest and most wide-spread form of communication and is particularly prevalent in insects. However, it has been notoriously difficult to decipher how exactly information related to sexual signaling is encoded in complex chemical profiles. Similarly, our knowledge of the genetic basis of sexual signaling is very limited and usually restricted to a few case studies with comparably simple pheromonal communication mechanisms. The present study jointly addresses these two knowledge gaps by characterizing a single gene simultaneously impacting sexual attractiveness and complex chemical surface profiles in parasitic wasps. Knocking down a fatty acid synthase gene in female wasps dramatically reduces their sexual attractiveness coinciding with a drastic decrease in male courtship and copulation behavior. Concordantly, we found a striking shift of methyl-branching patterns in the female surface pheromonal compounds, which we subsequently demonstrate to be the main cause for the greatly reduced male response. Intriguingly, this suggests a potential coding mechanism for sexual attractiveness mediated by specific methyl-branching patterns, whose genetic underpinnings are not well understood despite their high potential for encoding information. Our study sheds light on how biologically relevant information can be encoded in complex chemical profiles and on the genetic basis of sexual attractiveness. Significance StatementUnraveling the genetic basis of chemical signaling is one of the most prevalent yet challenging topics in functional genetics and animal communication studies. Here we present the characterization of a biosynthetic gene in parasitoid wasps that simultaneously impacts sexual attractiveness as well as majorly shifts complex surface pheromone compositions. The shifted pattern primarily constitutes up- and down-regulated methyl-branched compounds with very distinct branching positions. Therefore, these findings immediately suggest a potential coding mechanism for sexual attractiveness in complex chemical profiles. This advances our understanding of how genetic information can be translated into biologically relevant chemical information and reveals that sexual attractiveness can have a comparably simple genetic basis.