The nature of parasite specialization in the fungus-growing ant symbiosis

Host-parasite coevolution is intricately coupled with parasite specialization. As hosts become resistant, parasites may adapt and overcome that resistance or may become specialized on a narrow range of susceptible hosts. Ultimately, a parasite’s host range will dictate ecological host-parasite dynamics and host-parasite coevolution. Here, I use the system of fungus-growing ants and their symbionts to study host-specialization by Escovopsis, a parasite of the ants’ cultivated fungus. In recent years, the fungus-growing ant symbiosis has emerged as a model system for studying coevolution, speciation, cooperation and conflict between the ants and their fungal cultivars. In chapter one, I outline how this system has also proven to be an easily tractable system for studying the ecological and evolutionary dynamics of hosts and parasites. In chapters two and five, I combine molecular analysis of phylogenetic relationships of host and parasites with finer analysis of population differences within species to identify specialization by parasites on particular host-species and host-genotypes. At the host-species level, Escovopsis that attack gardens of Cyphomyrmex ants are specific to a narrow range of fungal cultivars propagated by the ants. At the host-genotype level, however, there is little evidence that genotypically similar strains of Escovopsis that attack Apterostigma dentigerum gardens are specialized on within-species host cultivar genotypes. In chapters three and four, knowledge of such patterns of specialization is used as a foundation for experiments in which the host fungi and the parasitic fungi are confronted to determine patterns of host resistance and parasite infectivity. I demonstrate that host cultivars can chemically defend themselves against some Escovopsis spp., but Escovopsis spp. can overcome the defenses of host-species on which they are specialized and can efficiently recognize and be attracted to these susceptible hosts. These host and parasite adaptations are consistent with patterns of parasite specialization and host-switching in the Apterostigma ant symbiosis. Thus, this comprehensive approach reveals both process and pattern, demonstrating how mechanisms of resistance and infectivity shape parasite hostspecialization and ultimately population dynamics of interacting organisms.