Major evolutionary transitions in ant agriculture

Abstract

Agriculture is a specialized form of symbiosis that is known to have evolved in only four animal groups: humans, bark beetles, termites, and ants. Here, we reconstruct the major evolutionary transitions that produced the five distinct agricultural systems of the fungus-growing ants, the most well studied of the nonhuman agriculturalists. We do so with reference to the first fossilcalibrated, multiple-gene, molecular phylogeny that incorporates the full range of taxonomic diversity within the fungus-growing ant tribe Attini. Our analyses indicate that the original form of ant agriculture, the cultivation of a diverse subset of fungal species in the tribe Leucocoprineae, evolved Ϸ50 million years ago in the Neotropics, coincident with the early Eocene climatic optimum. During the past 30 million years, three known ant agricultural systems, each involving a phylogenetically distinct set of derived fungal cultivars, have separately arisen from the original agricultural system. One of these derived systems subsequently gave rise to the fifth known system of agriculture, in which a single fungal species is cultivated by leaf-cutter ants. Leaf-cutter ants evolved remarkably recently (Ϸ8 -12 million years ago) to become the dominant herbivores of the New World tropics. Our analyses identify relict, extant attine ant species that occupy phylogenetic positions that are transitional between the agricultural systems. Intensive study of those species holds particular promise for clarifying the sequential accretion of ecological and behavioral characters that produced each of the major ant agricultural systems.Attini ͉ divergence dating ͉ Formicidae ͉ phylogeny ͉ symbiosis A ttine ants (subfamily Myrmicinae, tribe Attini) comprise a monophyletic group of Ͼ230 described species, exclusively New World and primarily Neotropical in distribution (1-4). All attine ants obligately depend on the cultivation of fungus gardens for food. So complete is this dependence that, upon leaving the maternal nest, a daughter queen must carry within her mouth a nucleus of fungus that serves as the starting culture for her new garden (5-7). Attine agriculture achieves its evolutionary apex in the leaf-cutting ants of the genera Acromyrmex and Atta, the dominant herbivores of the New World tropics (8, 9). Unlike more primitive attine ants that forage for and cultivate their fungus gardens on organic detritus, leaf-cutting ants have acquired the ability to cut and process fresh vegetation (leaves, flowers, and grasses) to serve as the nutritional substrate for their fungal cultivars. This key evolutionary innovation renders a mature Atta colony the ecological equivalent of a large mammalian herbivore in terms of collective biomass, lifespan, and quantity of plant material consumed (9).Attine ant agriculture is the product of an ancient, quadripartite, symbiotic relationship between three mutualists and one parasite. The mutualists include the attine ants, their fungal cultivars (Leucocoprineae and Pterulaceae), and filamentous bacteria in the genus ...

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

“…Instead, it might best be characterized as narrowly diffuse, 'one-to-few' coevolution. The C. wheeleri ant clade is closely related to the higher Attini 20 , which includes the leafcutting ants whose fungal cultivars are highly derived, obligate symbionts that exhibit coevolved modifications 16,20,22 . If C. wheelerigroup ant-fungus associations are more specific than those found in other lower Attini, they may represent an intermediate condition linking the broadly diffuse associations found in other lower-attine ants with the narrow associations that led to the evolution of higherattine fungiculture.…”

“…The root node was assigned a lognormal prior of log(mean) = 1.6, log (s.d.) = 1.0, offset = 15 (equivalent to a minimum bound of 15 Ma, median value of 20 Ma and a 95% quantile of 40 Ma) based on the presence of Cyphomyrmex maya and C. taino, both members of the C. rimosus group, in Dominican amber 20,51 . The crown group of the C. wheeleri group was also assigned a normal prior of mean = 20, s.d.…”

“…The crown group of the C. wheeleri group was also assigned a normal prior of mean = 20, s.d. = 5 (equivalent to a median of 20 Ma and a 95% confidence interval of 1.8-18.2 Ma) based on prior divergence dates from a largely independent data set 20 . Elimination of this second prior, which is not directly linked to the fossil record, altered resulting ages by less than 1 Ma.…”

“…Although all attine ants are obligate symbionts, the cultivated fungi vary from facultative to obligate in their associations with ants. In 'lower' attine fungiculture, the ancestral fungicultural system for attine ants 12,19,20 , fungal cultivars belong to two distinct, separate lineages ('Clade 1' and 'Clade 2') within the tribe Leucocoprineae. Lower-attine fungi are thought to facultatively associate with ants because the fungi can also live outside the symbiosis 12,21 .…”

Unraveling Trichoderma species in the attine ant environment: description of three new taxa

“…Attine ants maintain a mutualistic interaction with basiodiomycetous fungi in an obligatory association originated about 50 million years ago (Schultz and Brady 2008). In this mutualism, workers collect various types of substrates (fresh leaves, seeds or insect carcasses) to nourish the fungal cultivar, besides favoring fungal dispersion during the ants' reproductive stage.…”