Combinatorial Olfactory Signaling in Short-Distance Determines Host Plant Recognition in Locust

Abstract

Selecting palatable plants matters for insect herbivores’ survival, especially for food-restricted oligophagous and monophagous species. However, the definite selection strategy to distinguish host plants from nonhost plants, as well as the underlying sensory basis, remains controversial. Here, we investigated the olfactory recognition of host plants in oligophagous migratory locusts. By establishing one novel behavioral paradigm that allowed the free-moving locusts to make olfactory choices in short-distance, we demonstrated that palps were required to differentiate host plants apart from nonhost counterparts sensitively. Specifically, the characteristic odors between the host plant and nonhost plant defined the behavioral differentiation of food sources, and this process required intact palps. Further, single nonhost odor suppressed the behavioral potency to host plant extraction, while single host odor attenuated the behavioral repulsion to nonhost plant. We also identified the palps odorant receptors (ORs) repertoire that modulated the short-range recognition of key volatiles from host plants and nonhost and demonstrated that combinatorial olfactory signaling controls food choice. Our results support a “pull–push” model in which olfactory signaling on locust palps acts as a key tuning modulator in host plant recognition, expanding the knowledge of insect chemosensation.