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.
Fungal cultivars of fungus-growing ants (Attini, Formicidae) are carried by dispersing queens from parent to offspring nest. This vertical cultivar transmission between generations is thought to result in long-term ant-fungus coevolution and selection for beneficial cultivar traits that maximize harvests and thus colony productivity. In contrast to this traditional view of vertical cultivar transmission, frequent horizontal cultivar transmission between ant species is implicated by a phylogenetic analysis of 72 cultivars propagated by two fungus-growing ant species coexisting sympatrically in central Panama. The two ant species are specialized on the same group of closely related cultivars, but in six of 12 cultivar clades identifiable within this group, cultivars from both ant species were united in the same clade. Five of these 'mixed' clades were supported by bootstrap values of about 90% or higher. In one instance, colonies from the two ant species cultivated the same, genetically identical, cultivar clone. These phylogenetic patterns indicate that: (i) cultivar exchanges between the two ant species occur routinely throughout ecological time; and that (ii) coevolutionary processes between ants and their fungi are more diffuse than previously assumed. Because the two ant species are specialized on a narrow group of closely related cultivars that they regularly exchange among each other, but not with other sympatric ant species, cultivar exchanges are constrained, most likely, by ant preferences for their own cultivar group or by stringent selection against transitions of ant lineages to distantly related cultivars.
Leafcutter ants propagate co-evolving fungi for food. The nearly 50 species of leafcutter ants (Atta, Acromyrmex) range from Argentina to the United States, with the greatest species diversity in southern South America. We elucidate the biogeography of fungi cultivated by leafcutter ants using DNA sequence and microsatellite-marker analyses of 474 cultivars collected across the leafcutter range. Fungal cultivars belong to two clades (Clade-A and Clade-B). The dominant and widespread Clade-A cultivars form three genotype clusters, with their relative prevalence corresponding to southern South America, northern South America, Central and North America. Admixture between Clade-A populations supports genetic exchange within a single species, Leucocoprinus gongylophorus. Some leafcutter species that cut grass as fungicultural substrate are specialized to cultivate Clade-B fungi, whereas leafcutters preferring dicot plants appear specialized on Clade-A fungi. Cultivar sharing between sympatric leafcutter species occurs frequently such that cultivars of Atta are not distinct from those of Acromyrmex. Leafcutters specialized on Clade-B fungi occur only in South America. Diversity of Clade-A fungi is greatest in South America, but minimal in Central and North America. Maximum cultivar diversity in South America is predicted by the Kusnezov-Fowler hypothesis that leafcutter ants originated in subtropical South America and only dicot-specialized leafcutter ants migrated out of South America, but the cultivar diversity becomes also compatible with a recently proposed hypothesis of a Central American origin by postulating that leafcutter ants acquired novel cultivars many times from other nonleafcutter fungus-growing ants during their migrations from Central America across South America. We evaluate these biogeographic hypotheses in the light of estimated dates for the origins of leafcutter ants and their cultivars.
Abstract.•Almost all of the more than 200 species of fungus-growing ants (Formicidae: Attini) cultivate litterdecomposing 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 oí 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. Fungus-growing ants (Formicidae, tribe Attini) are well In contrast, the lower attine ants (eight genera, including the known for their habit of cultivating fungi for food, a behavior genus Apterostigma) cultivate morphologically unspecialized that originated in the common ancestor of attine ants about fungi (called G3 fungi) from which the Gl fungi arose (S.A. 50-60 million years ago (Wilson 1971; Schultz and Meier Rehner, pers. comm.; P. Abbott, N. Gerardo, and U. Mueller, 1995;Mueller et al. 2001). Since then, attine ants have un-unpubl. data), and which are therefore evolutionarily pledergone an adaptive radiation that has resulted in 13 extant siomorphic with respect to the G1 group (Chapela et al. 1994; genera containing more than 210 described species, all ob-Mueller et al. 1998). There is only one known exception to ligately dependent on the farming of mutualistic fungi, usu-this lepiotaceous cultivation of Gl and G3 fungi: some but ally in nests excavated in the soil (Schultz and Meier 1995; not all ant species in the genus Apterostigma cultivate fungi Weiterer et al. 1998; Brandâo and Mayhé-Nunes 2001). Do-that are distantly rel...
We used mark-resight data and amplified fragment length polymorphism (AFLP) markers to assess movements and gene flow between Central Pacific breeding colonies of the great frigatebird, Fregata minor. Of 715 adult frigatebirds marked on Tern Island and Johnston Atoll, 21.3% were resighted at other frigatebird colonies at least 582 km away. Mark-resight data indicated regular movement of males and females between Tern Island and Johnston Atoll (873 km apart), and less frequent movements to other islands; no birds marked on Tern or Johnston were seen on Christmas Island, but one was seen in the Philippines, 7627 km from where it was marked. Despite the regular occurrence of interisland movements, Bayesian analyses of AFLP data showed significant genetic differentiation between Tern Island and Johnston Atoll, and more pronounced differentiation between these two islands and the more distant Christmas Island. The AFLP profiles of three birds breeding on Tern Island fell within the profile-cluster typical for Christmas Island birds, both in a nonmetric multidimensional scaling analysis and in a population assignment test, suggesting dispersal events from Christmas Island to Tern Island. Several factors could explain the persistence of genetic structure despite frequent movements between colonies: many movements occurred during the nonbreeding season, many breeding-season movements did not involve mate-acquisition behaviours and individuals that do disperse may be selected against, as suggested by morphometric differences between colonies. The persistence of genetic structure among breeding colonies despite significant interisland movements suggests limits to the effectiveness of migration as a homogenizing force in this broadly distributed, extremely mobile species.
Significance We document the behavioral interactions among three ant species: a fungus-growing host ant, a permanently associated parasitic guest ant, and a raiding agro-predator ant. We show that the presence of guest ants becomes advantageous when host ants are attacked by raider ants, because guest ants use alkaloid venom to defend their host ant colony. Furthermore, detection of the guest ant odors is sufficient to discourage raider scouts from recruiting nestmates to host colonies. Guest ants likely have evolved this protective behavior because they also perish when their host colony dies.
Abstract.•Almost all of the more than 200 species of fungus-growing ants (Formicidae: Attini) cultivate litterdecomposing 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 oí 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. Fungus-growing ants (Formicidae, tribe Attini) are well In contrast, the lower attine ants (eight genera, including the known for their habit of cultivating fungi for food, a behavior genus Apterostigma) cultivate morphologically unspecialized that originated in the common ancestor of attine ants about fungi (called G3 fungi) from which the Gl fungi arose (S.A. 50-60 million years ago (Wilson 1971; Schultz and Meier Rehner, pers. comm.; P. Abbott, N. Gerardo, and U. Mueller, 1995;Mueller et al. 2001). Since then, attine ants have un-unpubl. data), and which are therefore evolutionarily pledergone an adaptive radiation that has resulted in 13 extant siomorphic with respect to the G1 group (Chapela et al. 1994; genera containing more than 210 described species, all ob-Mueller et al. 1998). There is only one known exception to ligately dependent on the farming of mutualistic fungi, usu-this lepiotaceous cultivation of Gl and G3 fungi: some but ally in nests excavated in the soil (Schultz and Meier 1995; not all ant species in the genus Apterostigma cultivate fungi Weiterer et al. 1998; Brandâo and Mayhé-Nunes 2001). Do-that are distantly rel...
A new ant species of Megalomyrmex conducts mass raids to usurp gardens of the fungus-growing ant Cyphomyrmex longiscapus, then lives in the gardens and consumes the cultivated fungus. Unlike attine ants, however, Megalomyrmex sp. does not forage for substrate to manure the gardens; therefore, when gardens become depleted, Megalomyrmex sp. must locate and usurp new gardens. Megalomyrmex sp. workers feed their larvae with attine brood, but only after removing the fungal mycelium that covers the attine larval integument, suggesting that this fungal coat may provide partial protection against other predators. Unlike other known Megalomyrmex species, which coexist as social parasites in attine colonies, Megalomyrmex sp. expels its attine hosts during the garden raids. Megalomyrmex sp. thus maintains a unique agro-predatory lifestyle that is described here for the first time.
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