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

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.

Automated summary

Choosing palatable plants is crucial for insect herbivores' survival, especially for restricted-feeders that specialize on few types of plants. However, the definitive strategy and sensory basis for distinguishing between host and nonhost plants remains controversial. In this study, we investigated the olfactory recognition of host plants in migratory locusts that feed on a limited range of plants. By using a novel behavioral paradigm, we found that the palps of locusts are necessary for differentiating between host and nonhost plants. The characteristic odors of the plants determined the behavioral differentiation, and intact palps were required for this process. We also identified the odorant receptors in the palps that modulate the recognition of key volatiles from host and nonhost plants, demonstrating the role of olfactory signaling in food choice.