The Origin of the Attine Ant-Fungus Mutualism

Abstract

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. 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 solenopsidine genus Megalomyrmex that either coexist as trophic parasites in gardens of attine hosts or aggressively usurp gardens from them. All other known ant-fungus associations are either adventitious or have nonnutritional functions (e.g., strengthening of carton-walls in ant nests). There exist no unambiguous reports of facultative mycophagy in ants, but such trophic ant-fungus interactions would most likely occur underground or in leaf litter and thus escape easy observation. Indirect evidence of fungivory can be deduced from contents of the ant alimentary canal and particularly from the contents of the infrabuccal pocket, a pharyngeal device that filters out solids before liquids pass into the intestine. Infrabuccal pocket contents reveal that ants routinely ingest fungal spores and hyphal material. Infrabuccal contents are eventually expelled as a pellet on nest middens or away from the nest by foragers, suggesting that the pellet provides fungi with a means for the dispersal of spores and hyphae. Associations between such "buccophilous" fungi and ants may have originated multiple times and may have become elaborated and externalized in the case of the attine ant-fungus mutualism. Thus, 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 important role to evolutionary modifications of the fungi that preceded the ant transition from hunter-gatherer to fungus farmer.

Rapid shifts in Atta cephalotes fungus-garden enzyme activity after a change in fungal substrate (Attini, Formicidae)

“…The most highly advanced and complex agricultural systems are found in the leaf-cutting ant genera Atta and Acromyrmex (Weber, 1966;Mueller et al, 2001;Mueller et al, 2005), which evolved 8-12 million years ago (Schultz and Brady, 2008) and are characterized by mainly collecting fresh plant material . Atta and Acromyrmex workers carry freshly cut leaves to the nest where they process this material into substrate for their crop symbiont Leucocoprinus gongylophorus, by chewing it into minute pieces that are mixed with ''saliva''.…”

Symbiont fidelity and the origin of species in fungus-growing ants

“…However, empirical work over the past two decades has shown that cultivars are frequently transmitted horizontally between different ant colonies (sometimes between colonies of different ant species) and that lower-attine cultivars are closely related to, and in some cases identical to, free-living fungal species, suggesting frequent import of fungi into the symbiosis from free-living sources [12][13][14]17,21,23,[25][26][27][28][29] . This apparent absence of one-to-one host fidelity (that is, long-term association of ant and fungal genotypes), combined with the recent discovery that the lower-attine fungal Clade 2 ( Fig.…”

Isolation and molecular characterization of symbiotic fungus from Acromyrmex ambiguus and Acromyrmex heyeri ants of Rio Grande do Sul State, Brazil

“…Moreover, it showed the formation of two distinct groups (Ah and AA) determined by the ant species independently of the geographical region studied. Agreeing with the results, other studies also claimed that different strains of leaf-cutting ants can cultivate in their nests the same symbiotic fungus (MUELLER, 2001;MIKhEYEV et al, 2007). On the other hand, DOhERTY et al (2003) using the RAPD (Random amplified polymorphic DNA) observed genetic variability in isolates originated from symbiotic fungus of Atta cephalotes from Panama and Trinidad.…”

“…The genera Atta and Acromyrmex stands out due to the damage they cause, both in native plants and at cultivated plants, in which they cut fresh material that serves as a substrate for the cultivation of the symbiotic fungus inside their nests (ChAPELLA et al, 1994;MUELLER et al, 2001). All Attine ants (that includes about 256 described species in 15 genera) (SOSA-CALVO et al, 2013) are mandatory dependent on this symbiosis, which involves Lepiotaceaeous fungi (order Agaricales, Basidiomycota division) (ChAPELA et al, 1994).…”

“…All Attine ants (that includes about 256 described species in 15 genera) (SOSA-CALVO et al, 2013) are mandatory dependent on this symbiosis, which involves Lepiotaceaeous fungi (order Agaricales, Basidiomycota division) (ChAPELA et al, 1994). This fungus is considered of monophyletic origin, having co-evolved with the ants for 50 million years through vertical transmission (ChAPELA et al, 1994;MUELLER et al, 2001).…”