Herbivore-Induced Volatiles Orchestrate Oviposition Plasticity in Geometrid Moths to Counteract Direct Resistance in...

The coevolutionary arms race between plants and herbivores drives the diversification of reciprocal adaptations. However, the transgenerational plasticity of insect behavioral responses to induced plant defenses remains poorly understood. Here, we elucidate a synchronized defense-counterdefense dynamic between tea plants (Camellia sinensis) and the geometrid moth (Ectropis grisescens). We found that larval herbivory rapidly triggers an integrated defense cascade in tea plants, involving Ca²⁺ signaling, MAPK activation, and jasmonate biosynthesis. This coordinated signaling leads to the accumulation of specific defensive metabolites (luteoloside, galangin, rhofolin, and vitexin), which collectively impair larval growth. Crucially, this herbivore-induced chemical defense creates a selective pressure that drives a reciprocal adaptation in the insect. Gravid E. grisescens females have evolved the ability to detect two characteristic volatiles, (E)-β-ocimene and linalool, emitted by attacked plants. These volatiles serve as reliable oviposition deterrent signals, enabling females to avoid defended hosts and thereby enhance offspring fitness. Our study integrates plant physiological signaling, phytohormone-mediated metabolomic changes, and insect behavioral ecology to reveal a novel paradigm of intergenerational coevolution. It demonstrates how plant induced defenses directly shape insect oviposition strategies, sustaining a dynamic equilibrium in agroecosystems.