Evolutionary adaptation in three-way interactions between plants, microbes and arthropods

Evolutionary adaptations in interactions between plants, microbes and arthropods are generally studied in interactions that involve only two of these groups, that is, plants and microbes, plants and arthropods or arthropods and microbes. We review the accumulating evidence from a wide variety of systems, including plant- and arthropod-associated microbes, and symbionts as well as antagonists, that selection and adaptation in seemingly two-way interactions between plants and microbes, plants and arthropods and arthropods and microbes are often driven by the biotic context of a third partner. We extend the concept of local adaptation from two-way interactions to scenarios for three-way interactions. We show that consumers can locally adapt to specific host phenotypes that are induced by a third species with which they do not directly interact. This emphasizes that indirect interactions have not only ecological but also important evolutionary consequences, and stresses the need to conduct studies of local adaptation in the proper ecological context of the species involved. Overall, our review underlines the importance of three-way interactions in the evolution of plantmicrobe, plantarthropod and arthropodmicrobe interactions, and we outline some promising directions for future research.