Theoretical analyses for the evolution of biogenic volatile organic compounds (BVOC) emission strategy.

ABSTRACT

Plants emit biogenic volatile organic compounds (BVOCs) as signaling molecules, playing a crucial role in inducing resistance against herbivores. Neighboring plants that eavesdrop on BVOC signals can also increase defenses against herbivores or alter growth patterns to respond to potential risks of herbivore damage. Despite the significance of BVOC emissions, the evolutionary rationales behind their release and the factors contributing to the diversity in such emissions remain poorly understood. To unravel the conditions for the evolution of BVOC emission, we developed a spatially explicit model that formalizes the evolutionary dynamics of BVOC emission and non-emission strategies. Our model considered two effects of BVOC signaling that impact the fitness of plants intra-individual communication, which mitigates herbivore damage through the plant's own BVOC signaling incurring emission costs, and inter-individual communication, which alters the influence of herbivory based on BVOC signals from other individuals without incurring emission costs. Employing two mathematical models-the lattice model and the random distribution model-we investigated how intra-individual communication, inter-individual communication, and spatial structure influenced the evolution of BVOC emission strategies. Our analysis revealed that the increase in intra-individual communication promotes the evolution of the BVOC emission strategy. In contrast, the increase in inter-individual communication effect favors cheaters who benefit from the BVOCs released from neighboring plants without bearing the costs associated with BVOC emission. Our analysis also demonstrated that the narrower the spatial scale of BVOC signaling, the higher the likelihood of BVOC evolution. This research sheds light on the intricate dynamics governing the evolution of BVOC emissions and their implications for plant-plant communication.