Cultivation of fungus for food originated about 45-65 million years ago in the ancestor of fungus-growing ants (Formicidae, tribe Attini), representing an evolutionary transition from the life of a hunter-gatherer of arthropod prey, nectar, and other plant juices, to the life of a farmer subsisting on cultivated fungi. Seven hypotheses have been suggested for the origin of attine fungiculture, each differing with respect to the substrate used by the ancestral attine ants for fungal cultivation. Phylogenetic information on the cultivated fungi, in conjunction with information on the nesting biology of extant attine ants and their presumed closest relatives, reveal that the attine ancestors probably did not encounter their cultivars-to-be in seed stores (von Ihering 1894), in rotting wood (Forel 1902), as mycorrhizae (Garling 1979), on arthropod corpses (von Ihering 1894) or ant faeces in nest middens (Wheeler 1907). Rather, the attine ant-fungus mutualism probably arose from adventitious interactions with fungi that grew on walls of nests built in leaf litter (Emery 1899), or from a system of fungal myrmecochory in which specialized fungi relied on ants for dispersal (Bailey 1920) and in which the ants fortuitously vectored these fungi from parent to offspring nests prior to a true fungicultural stage.

Cultivars of fungus-growing (attine) ants are vertically transmitted through inheritance from parent to offspring nest, but horizontal cultivar transfer between ant nests occurs occasionally, resulting in cultivar replacement within ant lineages. Two mechanisms could theoretically prevent the invasion of suboptimal cultivar strains and thus stabilize ant–cultivar coevolution: first, partner feedback inherent in vertical cultivar transmission and second, partner (symbiont) choice if the ants differentiate between productive and inferior cultivars during replacements. To elucidate the nature of symbiont choice, we presented workers of Cyphomyrmex muelleri with novel cultivars representing a phylogenetic cline of close and distant relatives of the native C. muelleri cultivar. Workers invariably preferred their native cultivar, discriminating against even very close relatives of the native cultivar. When given a choice between two non-native cultivar strains, workers accepted the strain most closely related to their native cultivar. Two conclusions emerge. First, colony switches to distantly related cultivars are behaviorally unlikely and may not be preference-based; rather, distant switches may occur under constrained choice, such as pathogen-related garden losses that force colonies to import novel cultivars. Second, the ability of attine ants to differentiate between closely related cultivar strains suggests that the ant–fungus mutualism is stabilized evolutionarily not only by partner feedback inherent in vertical cultivar transmission, but possibly also by symbiont choice through which the ants select against unwanted, presumably inferior, cultivars. The efficacy of symbiont choice now needs to be tested experimentally. Such research may benefit from application of theory and experimental paradigms that have been developed within the areas of mate choice and sexual selection.

Almost all of the more than 200 species of fungus-growing ants (Formicidae: Attini) cultivate litter-decomposing fungi in the family Lepiotaceae (Basidiomycota: Agaricales). The single exception to this rule is a subgroup of ant species within the lower attine genus Apterostigma, which cultivate pterulaceous fungi distantly related to the Lepiotaceae. Comparison of cultivar and ant phylogenies suggests that a switch from lepiotaceous to pterulaceous fungiculture occurred only once in the history of the fungus-growing ants. This unique switch occurred after the origin of the genus Apterostigma, such that the basal Apterostigma lineages retained the ancestral attine condition of lepiotaceous fungiculture, and none of the Apterostigma lineages in the monophyletic group of pterulaceous fungiculturists are known to have reverted back to lepiotaceous fungiculture. The origin of pterulaceous fungiculture in attine ants may have involved a unique transition from the ancestral cultivation of litter-decomposing lepiotaceous fungi to the cultivation of wood-decomposing pterulaceous fungi. Phylogenetic analyses further indicate that distantly related Apterostigma ant species sometimes cultivate the same cultivar lineage, indicating evolutionarily frequent, and possibly ongoing, exchanges of fungal cultivars between Apterostigma ant species. The pterulaceous cultivars form two sister clades, and different Apterostigma ant lineages are invariably associated with, and thus specialized on, only one of the two cultivar clades. However, within clades Apterostigma ant species are able to switch between fungi. This pattern of broad specialization by attine ants on defined cultivar clades, coupled with flexible switching between fungi within cultivar clades, is also found in other attine lineages and appears to be a general phenomenon of fungicultural evolution in all fungus-growing ants.