The role of host switching in the evolution of the fungus-gardening ant symbiosis

Mikheyev, Alexander Sergeyevich
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The fungus-growing ants have long provided a spectacular example of co-evolutionary integration between distantly related taxa. Their ecological success has been thought to depend largely on the evolutionary alignment of reproductive interests between ants and fungi, following vertical transmission and the ancient suppression of fungal sexuality. In my dissertation I explored the role of lateral cultivar switching on the evolution of the fungus-gardening ant mutualism. First, I provided the first evidence for sexual reproduction in the attine cultivars, together with evidence of extensive independent long-distance horizontal transmission of fungal genes. In fact, fungi have greater gene flow relative to their host ants, crossing the Gulf of Mexico between Latin America and Cuba, over which the ants cannot readily disperse. Second, for the special case of leaf-cutting ants, I show that the cultivar population was largely unstructured with respect to host ant species, and leaf-cutting ants interact largely with a single species of fungus. Finally, I examined the effect of post-glacial expansion on the population structure of the northern fungus-gardening ant Trachymyrmex septentrionalis and compared it with that of its two microbial mutualists: a community of lepiotaceous fungal cultivars and associated antibiotic-producing Pseudonocardia bacteria. This comparison allowed me to examine the effect of historical biogeographic forces, such as climate-driven range shifts, on the population structure of the ants and their microbial symbionts. While neither the cultivar nor the Pseudonocardia genetic structure was correlated with that of the ants, they were significantly, though weakly, correlated with each other. These results suggest that biogeographic forces may act differently on macro- and microscopic organisms, even in the extreme case where some microbial mutualists may be vertically transmitted from generation to generation and share the same joint ecological niche. Thus, binding forces that appear to enforce host fidelity are relatively weak and pairwise associations between cultivar lineages and ant species have little opportunity for evolutionary persistence. Taken together, my studies suggest that mechanisms other than long-term pairwise interactions between ants and fungi (so-called partner fidelity feedback) govern the evolution of the mutualism over evolutionary time.