Third-party mutualists have contrasting effects on host invasion under the enemy-release and biotic-resistance hypotheses

Plants engage in complex multipartite interactions with mutualists and antagonists, but these interactions are rarely included in studies that explore plant invasiveness. When considered in isolation, we know that beneficial microbes can enhance an exotic plant’s invasive ability and that herbivorous insects often decrease an exotic plant’s likeliness of success. However, the effect of these partners on plant fitness has not been well characterized when all three species coevolve. We use computational evolutionary modeling of a trait-based system to test how microbes and herbivores simultaneously coevolving with an invading plant affect the invaders’ probability of becoming established. Specifically, we designed a model that explores how a beneficial microbe would influence the outcome of an interaction between a plant and herbivore. To model novel interactions, we included a phenotypic trait shared by each species. Making this trait continuous and selectable allows us to explore how trait similarities between coevolving plants, herbivores and microbes affect fitness. Using this model, we answer the following questions: (1) Can a beneficial plant-microbe interaction influence the evolutionary outcome of antagonistic interactions between plants and herbivores? (2) How does the initial trait similarity between interacting organisms affect the likelihood of plant survival in novel locations? (3) Does the effect of tripartite interactions on the invasion success of a plant depend on whether organisms interact through trait similarity Enemy Release Hypothesis (ERH)] or dissimilarity (Biotic Resistance Hypothesis)? We found that it was much more difficult for plants to invade under the ERH but that beneficial microbes increase the probability of plant survival in a novel range under both hypotheses. To our knowledge, this model is the first to use tripartite interactions to explore novel species introductions. It represents a step towards gaining a better understanding of the factors influencing establishment of exotic species to prevent future invasions.