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

Abstract

Attracting and securing potential mating partners is of fundamental importance for reproduction. 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 widespread 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 two fatty acid synthase genes that most likely evolved by tandem gene duplication and that simultaneously impact sexual attractiveness and complex chemical surface profiles in parasitic wasps. Gene knockdown 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 mating response. Intriguingly, this suggests a potential coding mechanism for sexual attractiveness mediated by specific methyl-branching patterns in complex cuticular hydrocarbon (CHC) profiles. So far, the genetic underpinnings of methyl-branched CHCs 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.

eLife digest

Attracting a mate is critical in all species that sexually reproduce. Most animals, particularly insects, do this using chemical compounds called pheromones which can be sensed by potential mates. But how these vast range of different compounds encode and convey the information needed to secure a partner is not fully understood, and the genes that drive this complex communication mechanism are largely unknown.

To address this knowledge gap, Sun et al. studied the parasitic wasp Nasonia vitripennis. Like other insects, female N. vitripennis contain a wide range of chemical compounds on their cuticle, the outer waxy layer coating their surface. Sun et al. set out to find exactly which of these compounds, known as cuticular hydrocarbons, are involved in sexual communication.

They did this by simultaneously inactivating two related genes that they hypothesized to be responsible for synthesizing and maintaining chemical compounds on the cuticle of insects. The genetic modification altered the pattern of chemicals on the surface of the female wasps by specifically up- and down-regulating compounds with similar branching structures. The mutant females were also much less sexually attractive to male wasps.

These findings suggest that the chemical pattern identified by Sun et al. is responsible for communicating and maintaining sexual attractiveness in N. vitripennis female wasps. This is a significant stepping stone towards unravelling how sexual attractiveness can be encoded in complex mixtures of pheromones.

The results also have important implications for agriculture, as this parasitic wasp species is routinely used to exterminate particular fly populations that cause agricultural damage. The work by Sun et al. provides new insights into how these wasps sexually communicate, which may help scientists improve their rearing conditions and sustain them over multiple generations. This could contribute to a wider application of this more sustainable, eco-friendly alternative to destructive agricultural pesticides.