Optimal Strategies for Signal Sending and Perception in Volatile-mediated Within-Plant Signaling against Herbivory

Abstract

Herbivore-induced plant volatiles (HIPVs) play a critical role in inducible plant defense as information-bearing airborne signals. Released from damaged tissues, HIPVs induce defense responses in undamaged parts of the plant, thereby reducing the risk of subsequent herbivore attack. Although both emission and perception are fundamental components of HIPV-mediated signaling, the co-evolutionary dynamics of these traits under herbivore-driven selection remain poorly understood. Here, we develop a mathematical model of within-plant signaling that explicitly incorporates both inducible signal emission and perception as evolving traits. Using the model, we derived the optimal level of HIPV signal emission and signal perception under successive herbivore attacks. Our results show that the strategy with both signal emission and signal perception, which underlies HIPV-mediated signaling, is favored only under intermediate levels of herbivory. Within this range, increasing herbivory frequency drives the joint evolution of reduced signal emission and enhanced sensitivity to released signal. Furthermore, extending the model to include perception-independent functions of HIPVs, such as the attraction of natural enemies and the deterrence of herbivores, expands the range of conditions under which HIPV-mediated signaling is favored. At the same time, it also allows the emergence of emission-only strategies lacking signal perception, suggesting the potential decoupling of the co-evolution of emission and responsiveness. These findings provide a theoretical framework for understanding how emission and perception jointly shape the evolution of volatile-mediated signaling systems in plants.