Dual mechanisms of olfactory plasticity: Transient modulation by phosphatidylcholine and D-chiro-inositol and sustained regulation via the sex peptide-juvenile hormone system.

Abstract

Insects exhibit olfactory plasticity to optimize their survival and reproduction, which ensures that their sensory preferences flexibly meets their needs. However, a comprehensive understanding of the sequential regulatory mechanisms driving these sensory adjustments is lacking. Addressing this knowledge gap is crucial for clarifying how the olfactory system of insect flexibly meets their reproductive needs. Using electroantennogram (EAG) and single-sensillum recordings, we found that female Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) displayed distinct olfactory preferences for oviposition cues, host volatiles, and sex pheromones before and after mating. The injection of synthesized sex peptide (SP) or juvenile hormone (JH) into virgin females, as well as the knockdown of SP- or JH-receptors in mated females, reversed the olfactory preferences in both groups of flies. The onset of the effect of JH was relatively gradual, as evidenced by the lack of changes observed during the first 6 h after mating. The rapid changes in antennal sensitivities may involve specific neuromolecules, such as phosphatidylcholine (PC) and D-chiro-inositol (DCI), which were identified through metabolomics screening, and their functions were further validated by microinjection. Our findings reveal a post-mating regulatory mechanism where immediate olfactory adjustments are facilitated by rapid signaling molecules, while long-term sensitivity modifications rely on the gradual action of JH.