Loss of olfaction reduces caterpillar performance and increases susceptibility to a natural enemy.

Abstract

Insect herbivores such as caterpillars are under strong selection pressure from natural enemies, especially parasitoid wasps. Although the role of olfaction in host-plant seeking has been investigated in great detail in parasitoids and adult lepidopterans, the caterpillar olfactory system and its significance in tri-trophic interactions remain poorly understood. In this study, we investigated the olfactory system of <i>Pieris brassicae</i> caterpillars and the importance of olfactory information in the interactions among this herbivore, its host-plant <i>Brassica oleracea</i>, and its primary natural enemy <i>Cotesia glomerata</i>. To examine the role of olfaction, we utilized CRISPR/Cas9 to knockout (KO) the odorant receptor co-receptor (<i>Orco</i>). This KO impaired olfactory detection and primary processing in the brain. <i>Orco</i> KO caterpillars exhibited reduced weight and lost preference for their optimal food plants. Interestingly, the KO caterpillars also experienced reduced weight when challenged by the parasitoid <i>C. glomerata</i> whose ovipositor had been removed, and the mortality of the KO caterpillars under the attack of unmanipulated parasitoids increased. We then investigated the behavior of <i>P. brassicae</i> caterpillars in response to volatiles from plants attacked by conspecific caterpillars and volatiles from plants on which the caterpillars were themselves attacked by <i>C. glomerata</i>. After analyzing the volatile compounds involved in these interactions, we concluded that olfactory information enables caterpillars to locate suitable food sources more efficiently as well as to select enemy-free spaces. Our results reveal the crucial role of olfaction in caterpillar feeding and natural-enemy avoidance, highlighting the significance of chemoreceptor genes in shaping ecological interactions.