Cooperation and exploitation: Exploring how parasites shape the success and stability of mutualisms

The fungus-growing ant–microbe symbiosis is a paradigmatic example of coevolution between microbial symbionts and their hosts resulting in unique innovations and a high degree of biological complexity.  The ants tend their fungal mutualist (Basidiomycota: mostly Lepiotaceae), providing it with optimal conditions for growth.  In exchange, the fungus serves as the main food source for the ants.  The origin of this mutually beneficial interaction is likely more than 45–65 million years ago, and the subsequent evolutionary history of this ancient mutualism has resulted in complex associations. In addition to the ants and their fungal crops, the gardens of fungus-growing ants are host to specialized and virulent fungal pathogens in the genus Escovopsis (Ascomycota: Hypocreales).  Extensive molecular phylogenetic analyses of the garden pathogen reveal both an early origin and tightly coevolved relationship with the ants and their fungal mutualist. To deal with the pathogen the ants have evolved a mutualistic association with filamentous bacteria (actinomycetes) that produce antibiotics that suppress the growth of Escovopsis.  Recent experimental and molecular ecology work indicates that the presence of these additional symbionts greatly influences the success and specificity of the ant-fungal mutualism. In addition, experimentally enforced cheating by either the ants or their fungal partner, results in higher parasite-induced morbidity of the fungus garden, suggesting that the garden parasite may even help stabilize the ant-fungus mutualism.