Microbial signaling coordinates group oviposition and predator defense in migratory locusts

Abstract

Reproductive synchronization is suggested to enhance fitness in many insects, yet the mechanisms enabling such coordination remain unknown. In Locusta migratoria, we identify a microbiota-derived volatile, 2,4,6-trimethylpyridine (2,4,6-TMP) that coordinates communal oviposition in gregarious females while simultaneously deterring egg predators. Eggs laid by gregarious females emit 2,4,6-TMP, which attracts conspecifics by activating the olfactory receptors LmOR34 and LmOR36; disruption of either receptor abolishes attraction and alters oviposition behavior. 2,4,6-TMP is synthesized by the egg-associated bacterium Enterobacter roggenkampii through a lysine degradation pathway. Deletion of lysine decarboxylase abolishes 2,4,6-TMP production and associated behavioral responses. Beyond facilitating reproduction, 2,4,6-TMP repels soil-dwelling predators, including ants, beetles, and potworms. In the ant Solenopsis invicta, avoidance is mediated by the olfactory receptor SinOR43a-1; RNA interference (RNAi) knockdown of this receptor abolishes repellence. Semi-field assays confirm the ecological relevance of 2,4,6-TMP. These findings reveal an egg-associated bacterial signaling mechanism that couples reproductive coordination with predator defense in L. migratoria.