Microbial Mediation Of Herbivory In Leaf Cutter Ant Fungus Gardens

Most metazoans lack the physiological capacity to use plants as their sole source of energy and nutrients. To compensate for this, metazoans associate with microbial symbionts, which aid their hosts with the breakdown of recalcitrant biomass, remediation of plant defense compounds, and nutrient supplementation. Leaf-cutter ants, dominant herbivores in the Neotropics, are a paradigmatic example of this microbial mediation of herbivory. The ants cut foliar biomass from their surroundings and provide it as a growth substrate to their fungal cultivar Leucoagaricus gongylophorus. The cultivar breaks down the plant biomass and provides specialized hyphal swellings called gongylidia, which the ants consume as their primary source of energy. In this dissertation, I explore the relationships between the different types of substrates ants incorporate into their fungus gardens and how both the fungal cultivar and the bacterial community facilitate the ants' breadth in substrate use. I approach these investigations through an ecological and evolutionary lens using contemporary 'omics' tools. In chapter 1, I present the context in which this dissertation work was completed. I describe trends in the microbial mediation of herbivory and review the current state of understanding of how this relates to leaf-cutter ants. In chapter 2, I use metaproteomics to compare the proteins that the cultivar secretes when provided with different plant substrates. I show that the fungus responds in a flexible, substrate-specific manner to the material that the ants incorporate into their gardens. In chapter 3, I focus on the bacterial community in the fungus gardens of ants and how they may facilitate the ants' transition from using dicots to grasses. Using metagenomics, I show a shift in the bacterial community between these two types of substrate specialization and an associated shift in the functional capacity of the bacteria. In chapter 4, I continue investigating the ants' evolutionary transition to a novel substrate by examining the genomes of the fungal cultivars from the colonies of ants with grass and dicot substrate specializations. In this chapter I present preliminary results that further support the fungus' capacity for biomass degradation and present future directions into the evolution of this fungus, in terms of its transition to symbiosis, its transition to novel substrates, and its polykaryotic life history. In sum, the work presented in this dissertation expands our knowledge into the microbial mediation of herbivory in the leaf-cutter ant system.