Can the evolution of plant defense lead to plant-herbivore mutualism?

Moderate rates of herbivory can enhance primary production. This hypothesis has led to a controversy as to whether such positive effects can result in mutualistic interactions between plants and herbivores. We present a model for the ecology and evolution of plant-herbivore systems to address this q uestion. In this model, herbivores have a positive indirect effect on plant s through recycling of a limiting nutrient. Plants can evolve but are const rained by a trade-off between growth and antiherbivore defense. Although ev olution generally does not lead to optimal plant performance, our evolution ary analysis shows that, under certain conditions, the plant-herbivore inte raction can be considered mutualistic. This requires in particular that her bivores efficiently recycle nutrients and that plant reproduction be positi vely correlated with primary production. We emphasize that two different de finitions of mutualism need to be distinguished. A first ecological definit ion of mutualism is based on the short-term response of plants to herbivore removal, whereas a second evolutionary definition rests on the long-term r esponse of plants to herbivore removal, allowing plants to adapt to the abs ence of herbivores. The conditions for an evolutionary mutualism are more s tringent than those for an ecological mutualism. A particularly counterintu itive result is that higher herbivore recycling efficiency results both in increased plant benefits and in the evolution of increased plant defense. T hus, antagonistic evolution occurs within a mutualistic interaction.