A predator-derived odor specifically triggers avoidance in gregarious mated female Locusta migratoria.
BACKGROUND: Insects possess a highly specialized olfactory system. The migratory locust (Locusta migratoria), a major agricultural pest, is thought to emit odors that serve as aposematic signals to protect gregarious individuals from predation. However, whether locusts can detect the odors of their natural enemies to preemptively avoid predation remains unclear. RESULTS: Here, we show that gregarious mated female locusts exhibit strong avoidance behavior toward the odors of two avian predators, Numida meleagris and Anas platyrhynchos. Through volatile compound profiling, we identified 1-octen-3-ol, a key predator-released odor, which elicited significant aversive responses specifically in gregarious mated females; notably, virgin females showed no behavioral response to this odor. Through screening 82 olfactory receptors in L. migratoria, we identified two receptors, LmOR1 and LmOR17, that detect 1-octen-3-ol. A temporal expression study of LmOR1 and LmOR17 across different developmental stages of two locust phases using quantitative real-time polymerase chain reaction (qRT-PCR) showed that both genes are significantly more highly expressed in the gregarious mated females. Genome editing of these receptors revealed that knockout of LmOR1 significantly reduced both the electrophysiological response and the behavioral avoidance of 1-octen-3-ol, whereas knockout of LmOR17 had no effect. In our results we thus uncover a striking mating-state dependence of an innate avoidance behavior to a predator-derived odor, and further we identify LmOR1 as the major receptor mediating this olfactory-driven defense. CONCLUSION: Our findings provide crucial insights into the behavioral and olfactory mechanisms underlying insect-predator interactions, as well as the role of mating status in modulating defensive responses, offering potential olfactory targets for locust management. © 2026 Society of Chemical Industry.