Comparative Dating of Attine Ant and Lepiotaceous Cultivar Phylogenies Reveals Coevolutionary Synchrony and Discord

The mutualistic symbiosis between fungus-gardening ants and their cultivars has made fundamental contributions to our understanding of the coevolution of complex species interactions. Reciprocal specialization and vertical symbiont cotransmission are thought to promote a pattern of largely synchronous coevolutionary diversification in attines. Here we test this hypothesis by inferring the first time-calibrated multigene phylogeny of the lepiotaceous attine cultivars and comparing it with the recently published fossil-anchored phylogeny of the attine ants. While this comparison reveals some possible cases of synchronous origins of ant and fungal clades, there were a number of surprising asynchronies. For example, leaf-cutter cultivars appear to be significantly younger than the corresponding ant genera. Similarly, a clade of fungi interacting with primitive fungus-gardening ants-thought to be ancestral to the more derived leaf-cutter symbionts-appears instead to be a more recent acquisition from free-living stock. These macroevolutionary patterns are consistent with recent population-level studies suggesting occasional acquisition of novel cultivar types from environmental sources and horizontal transmission of cultivars between different ant species. Horizontal transmission events, even if rare, appear to form loose ecological connections between diffusely coevolving ant and fungus lineages that permit punctuated changes in the topology of the mutualistic ant-fungus interaction network.