Parasitoid manipulation as a plant defense strategy

Abstract

From a historical point of view, herbivores have been managed by either increasing a plant's defensive chemicals or through the release or encouragement of biological control agents. More recently, pesticides have become an important management tool. In each case the herbivore is conceptually an enemy that has been managed by manipulation of the plant on one side and by the use of biological control efforts or pesticides on the other, the herbivore being placed between these management strategies. The evolution of the plant and its insect herbivores has been described as an adversarial relationship. The herbivore-parasitoid relationship can be described in the same way. The importance of considering carnivores in understanding the evolution of the plant-herbivore interaction was proposed in the early 1980s. About the same time, a suggestion was made that it is important to consider plants in any effort to understand the herbivore-parasitoid relationship. However, the herbivore has remained in the middle. I suggest here that the specialist plant-herbivore-parasitoid interaction has evolved as a result of a mutualistic tritrophic interaction. As background I present a brief historical look at the management of herbivores followed by an overview of the interactions between the plant and herbivore, the herbivore and parasitoid, and the plant and parasitoid. Next, I consider other interactions between plants and insects where the plants appear to manipulate the insects. Finally, I discuss the mutualistic plant-parasitoid-herbivore interaction as a co-evolved tritrophic system where both the specialist parasitoid and the specialist herbivore have co-evolved together with the plant. The 3 components of the proposed system either interact with each other in a positive way or the potentially negative interactions are neutralized, selection favoring the more successful positive interactions. The proposal is predicated on plants with specialist herbivores and their specialist parasitoids. If this system exists, there is the opportunity for the evolution of subversion, deception, and cheating among the 3 components.