Jinxi Yuan, Liping Nie, Lei Shang, Zhongqiang Jia, Shuang Shan, Xiaoqing Zhang, Lingzhi Shi, Yuxiao Zeng, Benke Hong, Xu Cheng, Liwei Zhang, Guirong Wang, Bill S Hansson, Hetan Chang
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.