Symbiont-mediated adaptation: Evolution of cold-tolerant fungi permits winter fungiculture by leafcutter ants at the northern frontier of a tropical ant-fungus symbiosis

The obligate mutualism between leafcutter ants and their Attamyces fungi originated in the tropics but extends today also into temperate regions. The northernmost leafcutter ant Atta texana sustains fungiculture during winter temperatures that would harm the cold-sensitive Attamyces cultivars of tropical leafcutter ants. Cold-tolerance of Attamyces cultivars increases with winter harshness along a latitudinal temperature gradient across the range of A. texana in the southern USA, indicating selection for cold-tolerant Attamyces variants along the temperature cline. Ecological niche modeling corroborates winter temperature as a key range-limiting factor impeding northward expansion of A. texana. The northernmost A. texana populations are able to sustain fungiculture throughout winter because of their cold-adapted fungi and because of seasonal garden relocation. Although the origin of leafcutter fungiculture was an evolutionary breakthrough that revolutionized the food niche of tropical fungus-growing ants, the ants' dependence on cold-sensitive fungal symbionts eventually constrained this host-microbe symbiosis during the expansion into temperate habitats. Evolution of cold-tolerant fungi within the symbiosis relaxed constraints on winter fungiculture at the northern frontier of the leafcutter ant distribution, thereby expanding the ecological niche of an obligate host-microbe symbiosis.