Sex pheromones are pivotal for insect reproduction. However, the mechanism of sex pheromone communication remains enigmatic in hymenopteran parasitoids. Here we have identified the sex pheromone and elucidated the olfactory basis of sex pheromone communication in Campoletis chlorideae (Ichneumonidae), a solitary larval endoparasitoid of over 30 lepidopteran pests. Using coupled gas chromatography-electroantennogram detection, we identified two female-derived pheromone components, tetradecanal (14:Ald) and 2-heptadecanone (2-Hep) (1:4.6), eliciting strong antennal responses from males but weak responses from females. We observed that males but not females were attracted to both single components and the blend. The hexane-washed female cadavers failed to arouse males, and replenishing 14:Ald and 2-Hep could partially restore the sexual attraction of males. We further expressed six C. chlorideae male-biased odorant receptors in Drosophila T1 neurons and found that CchlOR18 and CchlOR47 were selectively tuned to 14:Ald and 2-Hep, respectively. To verify the biological significance of this data, we knocked down CchlOR18 and CchlOR47 individually or together in vivo and show that the attraction of C. chlorideae to their respective ligands was abolished. Moreover, the parasitoids defective in either of the receptors were less likely to court and copulate. Finally, we show that the sex pheromone and ( Z )-jasmone, a potent female attractant, can synergistically affect behaviors of virgin males and virgin females and ultimately increase the parasitic efficiency of C. chlorideae . Our study provides new insights into the molecular mechanism of sex pheromone communication in C. chlorideae that may permit manipulation of parasitoid behavior for pest control.

Insects use olfaction to detect ecologically relevant chemicals in their environment. To maintain useful responses over a variety of stimuli, olfactory receptor neurons are desensitized to prolonged or high concentrations of stimuli. Depending on the timescale, the desensitization is classified as short-term, which typically spans a few seconds; or long-term, which spans from minutes to hours. Compared with the well-studied mechanisms of desensitization in vertebrate olfactory neurons, the mechanisms underlying invertebrate olfactory sensitivity regulation remain poorly understood. Recently, using a large-scale functional screen, a conserved critical receptor phosphorylation site has been identified in the model insect Drosophila melanogaster, providing new insight into the molecular basis of desensitization in insects. Here, we summarize the progress in this area and provide perspectives on future directions to determine the molecular mechanisms that orchestrate the desensitization in insect olfaction.