Coevolutionary arms races: Is victory possible?

Plants are embattled in a war with rasping, sucking, and chewing insects, deadly viruses, debilitating bacteria, and castrating fungi. This war costs billions of dollars in crop losses each year, making the study of plant-pathogen and plant-herbivore interactions one of the most significant branches of applied biology (1). But the study of how plants and their enemies interact also has inspired major advances in fundamental research regarding species interactions, particularly concerning the interplay of evolution and ecology. Especially influential has been the idea that herbivorous insects have driven the evolution of plants, and in turn, plant adaptations to insect attack have stimulated a diversification of insects (2). This evolutionary dance between insects and plants is a widely cited example of what generally is referred to as “coevolution”—that is, reciprocal adaptive genetic changes within populations of interacting species that act as selective agents for one another. Coevolution fascinates biologists because it suggests a view of nature in which close associations between species have shaped their life histories and ecologies in a way that fundamentally alters how they interact. If coevolution is a widespread and dominant process, then one of humankind’s more insidious impacts on the world is likely to be the perturbation of coevolved systems. Original ideas about coevolution were inspired by studies of plant-insect and plant-pathogen interactions, and those who study the impact of diseases or herbivores on plants inevitably are indoctrinated with the notion of coevolution. Ironically, even though coevolution is conceptually compelling, we lack definitive empirical studies that show how it works. Alternative hypotheses for the course of coevolution include: (i) escalating arms races in which plants relentlessly add to their chemical arsenals, whereas herbivores follow suit with new mechanisms for overriding those defenses, (ii) cyclical selection in which highly defended plants are favored in times when virulent …