The origin of the attine ant-fungus mutualism

Cultivation of fungus for food originated about 45-65 million years ago in the ancestor of fungus-growing ants (Formicidae, tribe Attini), representin g an evolutionary transition from the life of a hunter-gatherer of anthropo d 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 bio logy of extant attine ants and their presumed closest relatives, reveal tha t the attine ancestors probably did not encounter their cultivars-to-be in seed stores (von Ihering 1894), in rotting wood (Forel 1902), as mycorrhiza e (Garling 1979), an arthropod corpses (von Ihering 1894) or ant faeces in nest middens (Wheeler 1907). Rather, the attine ant-fungus mutualism probab ly arose from adventitious interactions with fungi that grew on walls of ne sts built in leaf litter (Emery 1899), or from a system of fungal myrmecoch ory in which specialized fungi relied on ants for dispersal (Bailey 1920) a nd in which the ants fortuitously vectored these fungi from parent to offsp ring nests prior to a true fungicultural stage. Reliance on fungi as a dominant food source has evolved only twice in ants: first in the attine ants, and second in some ant species in the solenopsid ine genus Megalomyrmex that either coexist as trophic parasites in gardens of attine hosts or aggressively usurp gardens from them. All other known an t-fungus associations are either adventitious or have nonnutritional functi ons (e.g. strengthening of carton-walls in ant nests). There exist no unamb iguous reports of facultative mycophagy in ants, but such trophic ant-fungu s interactions would most likely occur underground or in leaf litter and th us escape easy observation. Indirect evidence of fungivory can be deduced f rom contents of the ant alimentary canal and particularly from the contents of the infrabuccal pocket, a pharyngeal device that filters out solids bef ore liquids pass into the intestine. Infrabuccal pocket contents reveal tha t ants routinely ingest fungal spores and hyphal material. Infrabuccal cont ents are eventually expelled as a pellet on nest middens or away from the n est by foragers, suggesting that the pellet provides fungi with a means for the dispersal of spores and hyphae. Associations between such "buccophilou s" fungi and ants may have originated multiple times and may have become el aborated and externalized in the case of the attine ant-fungus mutualism. T hus, contrary to the traditional model in which attine fungi are viewed as passive symbionts that happened to come under ant control, this alternative model of a myrmecochorous origin of the attine mutualism attributes an imp ortant role to evolutionary modifications of the fungi that preceded the an t transition from hunter-gatherer to fungus farmer.