Parasitism as a selective force shaping the ecology and evolution of an ancient ant-fungal-bacterial mutualism.

摘要

Beneficial and antagonistic symbioses have been key sources of evolutionary innovation over the history of life. Although parasitic and mutualistic host-microbe interactions have been studied extensively, studies investigating the interactions between parasites and mutualists are currently lacking. Here I argue that exploitation of mutualisms is an important selective pressure shaping the ecology and evolution of symbioses. I explore this idea using the fungus-growing ant-microbe symbiosis as a model system. Fungus-growing ants have an obligate mutualism with the fungi they cultivate for food, which is exploited by parasites in the genus Escovopsis. To protect their crops from infection ants form a second mutualism with antibiotic-producing bacteria that have activity specific to Escovopsis. I detail the discovery of another level of parasitism within the ant-microbe symbiosis; black yeasts that exploit the ants' mutualistic bacteria and ultimately determine the success of the ant-fungal mutualism by altering symbiont dynamics. I then test the hypothesis that fungus-growing ants have evolved specialized behavioral responses to parasitism and reveal that the ants infrabuccal pocket functions as a specialized sterilization device, killing spores of Escovopsis. This is apparently achieved through symbiotic bacteria in the pocket, which produce antibiotics that inhibit Escovopsis, illustrating that the combination of behavior and microbial symbionts can be a successful host defense strategy. I then investigate how parasitism influences cooperative dynamics in the ant-fungus mutualism. Through empirical experiments and computer simulations I show that parasites help align the selfish interests of mutualists. My results suggest that when two mutualists have a 'common foe' selection favors cooperation over cheating, helping explain the evolutionary stability of mutualisms. Finally, I discuss instances of microbial symbiosis in which the microbe protects its host from natural enemies through secondary metabolite production. I explore ecological and evolutionary pressures that make microbes good defensive partners and suggest that developing of such relationships has been a common theme in the evolution of life. Collectively, these data show that parasitism has profoundly influenced the ecological and evolutionary dynamics of the fungus-growing ant symbiosis. Further, this work clearly illustrates that to better understand symbiosis, we need to research interactions in the symbionts' ecological community.