Ant Agriculture Research Articles

First experimental evidence for active farming in ambrosia beetles and strong heredity of garden microbiomes.

Fungal cultivation is a defining feature for advanced agriculture in fungus-farming ants and termites. In a third supposedly fungus-farming group, wood-colonizing ambrosia beetles, an experimental proof for the effectiveness of beetle activity for selective promotion of their food fungi over others is lacking and farming has only been assumed based on observations of social and hygienic behaviours. Here, we experimentally removed mothers and their offspring from young nests of the fruit-tree pinhole borer, Xyleborinus saxesenii. By amplicon sequencing of bacterial and fungal communities of nests with and without beetles we could show that beetles are indeed able to actively shift symbiont communities. Although being consumed, the Raffaelea food fungi were more abundant when beetles were present while a weed fungus (Chaetomium sp.) as well as overall bacterial diversity were reduced in comparison to nests without beetles. Core symbiont communities were generally of low diversity and there were strong signs for vertical transmission not only for the cultivars, but also for secondary symbionts. Our findings verify the existence of active farming, even though the exact mechanisms underlying the selective promotion and/or suppression of symbionts need further investigation.

Erratum

Systematic EntomologyVolume 45, Issue 1 p. 224-224 ErratumFree Access Erratum This article corrects the following: The molecular phylogenetics of Trachymyrmex Forel ants and their fungal cultivars provide insights into the origin and coevolutionary history of ‘higher-attine’ ant agriculture Scott E. Solomon, Christian Rabeling, Jeffrey Sosa-Calvo, Cauê T. Lopes, André Rodrigues, Heraldo L. Vasconcelos, Maurício Bacci, Ulrich G. Mueller, Ted R. Schultz, Volume 44Issue 4Systematic Entomology pages: 939-956 First Published online: September 3, 2019 First published: 10 October 2019 https://doi.org/10.1111/syen.12394AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat In [1], the following errors were published in SYEN 44:4. The incorrect reference year “Branstetter et al., 1975,” occurred on pages 940, 941, 944, 945, 946, 949, and 950. In all cases, the citation should have read “Branstetter et al. 2017.” The reference, which was erroneously omitted, should have appeared on pp. 953 in the References section and should have read as follows: ‘Branstetter, M.G., Ješovnik, A., Sosa-Calvo, J., Lloyd, M.W., Faircloth, B.C., Brady, S.G. & Schultz, T.R. (2017) Dry habitats were crucibles of domestication in the evolution of agriculture in ants. Proceedings of the Royal Society of London B, 284, 20170095.’ The following reference, which appeared on pp. 953, was out of place and should have been omitted: ‘Gonçalves, C. (1975) Formigas dos gêneros Sericomyrmex e Trachymyrmex cortando folhas verdes de plantas (Hymenoptera., Formicidae, Myrmicinae, Attini). Reunião Anual da Sociedade Brasileira para o Progresso da Ciência, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil, Vol. 28, p. 1670.’ The reference for Gonçalves 1975 was correctly listed on page 954. We apologize for these errors. Reference 1. Solomon, S.E., Rabeling, C., Sosa-Calvo, J. et al. (2019) The molecular phylogenetics of Trachymyrmex Forel ants and their fungal cultivars provide insights into the origin and coevolutionary history of ‘higher-attine’ ant agriculture. Systematic Entomology, 44, 939– 956. Volume45, Issue1January 2020Pages 224-224 ReferencesRelatedInformation

The molecular phylogenetics ofTrachymyrmexForel ants and their fungal cultivars provide insights into the origin and coevolutionary history of ‘higher‐attine’ ant agriculture

AbstractThe fungus‐growing ants and their fungal cultivars constitute a classic example of a mutualism that has led to complex coevolutionary dynamics spanningc. 55–65 Ma. Of the five agricultural systems practised by fungus‐growing ants, higher‐attine agriculture, of which leaf‐cutter agriculture is a derived subset, remains poorly understood despite its relevance to ecosystem function and human agriculture across the Neotropics and parts of North America. Among the ants practising higher‐attine agriculture, the genusTrachymyrmexForel, as currently defined, shares most‐recent common ancestors with both the leaf‐cutter ants and the higher‐attine generaSericomyrmexMayr andXerolitorSosa‐Calvoet al. Although previous molecular‐phylogenetic studies have suggested thatTrachymyrmexis a paraphyletic grade, until now insufficient taxon sampling has prevented a full investigation of the evolutionary history of this group and limited the possibility of resolving its taxonomy. Here we describe the results of phylogenetic analyses of 38Trachymyrmexspecies, including 27 of the 49 described species and at least 11 new species, using four nuclear markers, as well as phylogenetic analyses of the fungi cultivated by 23 species ofTrachymyrmexusing two markers. We generated new genetic data for 112 ants (402 new gene sequences) and 95 fungi (153 new gene sequences). Our results corroborate previous findings thatTrachymyrmex, as currently defined, is paraphyletic. We propose recognizing two new genera,Mycetomoelleriusgen.n.andParatrachymyrmexgen.n., and restricting the continued use ofTrachymyrmexto the clade of nine largely North American species that contains the type species [Trachymyrmex septentrionalis(McCook)] and that is the sister group of the leaf‐cutting ants. Our fungal cultivar phylogeny generally corroborates previously observed broad patterns of ant–fungus association, but it also reveals further violations of those patterns. Higher‐attine fungi are divided into two groups: (i) the single speciesLeucoagaricus gongylophorus(Möller); and (ii) its sister clade, consisting of multiple species, recently referred to asLeucoagaricusSinger ‘clade B’. Our phylogeny indicates that, although most non‐leaf‐cutting higher‐attine ants typically cultivate species in clade B, some species cultivateL. gongylophorus, whereas still others cultivate fungi typically associated with lower‐attine agriculture. This indicates that the attine agricultural systems, which are currently defined by associations between ants and fungi, are not entirely congruent with ant and fungal phylogenies. They may, however, be correlated with as yet poorly understood biological traits of the ants and/or of their microbiomes.

Farming by ants remodels nutrient uptake in epiphytes

True agriculture - defined by habitual planting, cultivation, harvesting and dependence of a farmer on a crop - is known from fungi farmed by ants, termites or beetles, and plants farmed by humans or ants. Because farmers supply their crops with nutrients, they have the potential to modify crop nutrition over evolutionary time. Here we test this hypothesis in ant/plant farming symbioses. We used field experiments, phylogenetic-comparative analyses and computed-tomography scanning to investigate how the evolution of farming by ants has impacted the nutrition of locally coexisting species in the epiphytic genus Squamellaria (Rubiaceae). Using isotope-labelled mineral and organic nitrogen, we show that specialised ants actively and exclusively fertilise hyperabsorptive warts on the inner walls of plant-formed structures (domatia) where they nest, sharply contrasting with nitrogen provisioning by ants in nonfarming generalist symbioses. Similar hyperabsorptive warts have evolved repeatedly in lineages colonised by farming ants. Our study supports the idea that millions of years of ant agriculture have remodelled plant physiology, shifting from ant-derived nutrients as by-products to active and targeted fertilisation on hyperabsorptive sites. The increased efficiency of ant-derived nutrient provisioning appears to stem from a combination of farming ant behaviour and plant 'crop' traits.

Phylogeny and evolution of the cryptic fungus‐farming ant genusMyrmicocryptaF. Smith (Hymenoptera: Formicidae) inferred from multilocus data

AbstractFungus‐farming ants (Hymenoptera: Formicidae) have become model systems for exploring questions regarding the evolution of symbiosis. However, robust phylogenetic studies of both the ant agriculturalists and their fungal cultivars are necessary for addressing whether or not observed ant–fungus associations are the result of coevolution and, if so, whether that coevolution has been strict or diffuse. Here we focus on the evolutionary relationships of the species within the ant genusMyrmicocryptaand of their fungal cultivars. The fungus‐farming ant genusMyrmicocryptawas created by Fr. Smith in 1860 based on a single alate queen. Since then, 31 species and subspecies have been described. Until now, the genus has not received any taxonomic treatment and the relationships of the species within the genus have not been tested. Our molecular analyses, using ∼40 putative species and six protein‐coding (nuclear and mitochondrial) gene fragments, recoverMyrmicocryptaas monophyletic and as the sister group of the genusMycocepurusForel. The speciesM. tuberculataWeber is recovered as the sister to the rest ofMyrmicocrypta. The time‐calibrated phylogeny recovers the age of stem groupMyrmicocryptaplus its sister group as 45 Ma, whereas the inferred age for the crown groupMyrmicocryptais recovered as 27 Ma. Ancestral character‐state analyses suggest that the ancestor ofMyrmicocryptahad scale‐like or squamate hairs and that, although such hairs were once considered diagnostic for the genus, the alternative state of erect simple hairs has evolved at least seven independent times. Ancestral‐state analyses of observed fungal cultivar associations suggest that the most recent common ancestor ofMyrmicocryptacultivated clade 2 fungal species and that switches to clade 1 fungi have occurred at least five times. It is our hope that these results will encourage additional species‐level phylogenies of fungus‐farming ants and their fungal cultivars, which are necessary for understanding the evolutionary processes that gave rise to agriculture in ants and that produced the current diversity of mutualistic ant–fungus interactions.

Dry habitats were crucibles of domestication in the evolution of agriculture in ants.

The evolution of ant agriculture, as practised by the fungus-farming ‘attine’ ants, is thought to have arisen in the wet rainforests of South America about 55–65 Ma. Most subsequent attine agricultural evolution, including the domestication event that produced the ancestor of higher attine cultivars, is likewise hypothesized to have occurred in South American rainforests. The ‘out-of-the-rainforest’ hypothesis, while generally accepted, has never been tested in a phylogenetic context. It also presents a problem for explaining how fungal domestication might have occurred, given that isolation from free-living populations is required. Here, we use phylogenomic data from ultra-conserved element (UCE) loci to reconstruct the evolutionary history of fungus-farming ants, reduce topological uncertainty, and identify the closest non-fungus-growing ant relative. Using the phylogeny we infer the history of attine agricultural systems, habitat preference and biogeography. Our results show that the out-of-the-rainforest hypothesis is correct with regard to the origin of attine ant agriculture; however, contrary to expectation, we find that the transition from lower to higher agriculture is very likely to have occurred in a seasonally dry habitat, inhospitable to the growth of free-living populations of attine fungal cultivars. We suggest that dry habitats favoured the isolation of attine cultivars over the evolutionary time spans necessary for domestication to occur.

Biology of the relict fungus-farming ant Apterostigma megacephala Lattke, including descriptions of the male, gyne, and larva

Fungus-farming “attine” ant agriculture consists of five distinct agricultural systems characterized by a remarkable symbiont fidelity in which five phylogenetic groups of ants faithfully cultivate five phylogenetic groups of fungi. Across-system garden switching experiments result in colony decline and death, indicating that attine ant-fungus symbiont fidelity is enforced by poorly understood biological constraints. The most dramatic violation of this pattern of symbiont fidelity occurs in the relict species Apterostigma megacephala, the only lower-attine ant known to cultivate a higher-attine fungus. Apterostigma megacephala is the sole surviving representative of an ancient lineage that diverged from all other Apterostigma fungus-farming ants ~39 million years ago, yet it cultivates Leucoagaricus gongylophorus, a highly domesticated fungal species that originated in the gardens of the recently evolved leaf-cutting ants 8–11 million years ago. Understanding the biology of A. megacephala, therefore, may provide important clues about the biological mechanisms that constrain the otherwise seemingly obligate ant-fungus associations that characterize attine ant agriculture. Here, based on field work in the Floresta Nacional de Carajas in the state of Para in Brazil, we report the previously unknown biology of A. megacephala, including nest architecture, colony demography, foraging behavior, and the morphologies of the previously undescribed gyne, male, and larva.

Phylogenomics and Divergence Dating of Fungus-Farming Ants (Hymenoptera: Formicidae) of the Genera Sericomyrmex and Apterostigma.

Fungus-farming ("attine") ants are model systems for studies of symbiosis, coevolution, and advanced eusociality. A New World clade of nearly 300 species in 15 genera, all attine ants cultivate fungal symbionts for food. In order to better understand the evolution of ant agriculture, we sequenced, assembled, and analyzed transcriptomes of four different attine ant species in two genera: three species in the higher-attine genus Sericomyrmex and a single lower-attine ant species, Apterostigma megacephala, representing the first genomic data for either genus. These data were combined with published genomes of nine other ant species and the honey bee Apis mellifera for phylogenomic and divergence-dating analyses. The resulting phylogeny confirms relationships inferred in previous studies of fungus-farming ants. Divergence-dating analyses recovered slightly older dates than most prior analyses, estimating that attine ants originated 53.6–66.7 million of years ago, and recovered a very long branch subtending a very recent, rapid radiation of the genus Sericomyrmex. This result is further confirmed by a separate analysis of the three Sericomyrmex species, which reveals that 92.71% of orthologs have 99% - 100% pairwise-identical nucleotide sequences. We searched the transcriptomes for genes of interest, most importantly argininosuccinate synthase and argininosuccinate lyase, which are functional in other ants but which are known to have been lost in seven previously studied attine ant species. Loss of the ability to produce the amino acid arginine has been hypothesized to contribute to the obligate dependence of attine ants upon their cultivated fungi, but the point in fungus-farming ant evolution at which these losses occurred has remained unknown. We did not find these genes in any of the sequenced transcriptomes. Although expected for Sericomyrmex species, the absence of arginine anabolic genes in the lower-attine ant Apterostigma megacephala strongly suggests that the loss coincided with the origin of attine ants.

Reciprocal genomic evolution in the ant-fungus agricultural symbiosis.

The attine ant–fungus agricultural symbiosis evolved over tens of millions of years, producing complex societies with industrial-scale farming analogous to that of humans. Here we document reciprocal shifts in the genomes and transcriptomes of seven fungus-farming ant species and their fungal cultivars. We show that ant subsistence farming probably originated in the early Tertiary (55–60 MYA), followed by further transitions to the farming of fully domesticated cultivars and leaf-cutting, both arising earlier than previously estimated. Evolutionary modifications in the ants include unprecedented rates of genome-wide structural rearrangement, early loss of arginine biosynthesis and positive selection on chitinase pathways. Modifications of fungal cultivars include loss of a key ligninase domain, changes in chitin synthesis and a reduction in carbohydrate-degrading enzymes as the ants gradually transitioned to functional herbivory. In contrast to human farming, increasing dependence on a single cultivar lineage appears to have been essential to the origin of industrial-scale ant agriculture.

Small genome of the fungus Escovopsis weberi, a specialized disease agent of ant agriculture

Many microorganisms with specialized lifestyles have reduced genomes. This is best understood in beneficial bacterial symbioses, where partner fidelity facilitates loss of genes necessary for living independently. Specialized microbial pathogens may also exhibit gene loss relative to generalists. Here, we demonstrate that Escovopsis weberi, a fungal parasite of the crops of fungus-growing ants, has a reduced genome in terms of both size and gene content relative to closely related but less specialized fungi. Although primary metabolism genes have been retained, the E. weberi genome is depleted in carbohydrate active enzymes, which is consistent with reliance on a host with these functions. E. weberi has also lost genes considered necessary for sexual reproduction. Contrasting these losses, the genome encodes unique secondary metabolite biosynthesis clusters, some of which include genes that exhibit up-regulated expression during host attack. Thus, the specialized nature of the interaction between Escovopsis and ant agriculture is reflected in the parasite's genome.

The most relictual fungus-farming ant species cultivates the most recently evolved and highly domesticated fungal symbiont species.

Fungus-farming (attine) ant agriculture is made up of five known agricultural systems characterized by remarkable symbiont fidelity in which five phylogenetic groups of ants faithfully cultivate five phylogenetic groups of fungi. Here we describe the first case of a lower-attine ant cultivating a higher-attine fungus based on our discovery of a Brazilian population of the relictual fungus-farming ant Apterostigma megacephala, known previously from four stray specimens from Peru and Colombia. We find that A. megacephala is the sole surviving representative of an ancient lineage that diverged ∼39 million years ago, very early in the ∼55-million-year evolution of fungus-farming ants. Contrary to all previously known patterns of ant-fungus symbiont fidelity, A. megacephala cultivates Leucoagaricus gongylophorus, a highly domesticated fungal cultivar that originated only 2-8 million years ago in the gardens of the highly derived and recently evolved (∼12 million years ago) leaf-cutting ants. Because no other lower fungus-farming ant is known to cultivate any of the higher-attine fungi, let alone the leaf-cutter fungus, A. megacephala may provide important clues about the biological mechanisms constraining the otherwise seemingly obligate ant-fungus associations that characterize attine ant agriculture.

A Brazilian population of the asexual fungus-growing ant Mycocepurus smithii (Formicidae, Myrmicinae, Attini) cultivates fungal symbionts with gongylidia-like structures.

Attine ants cultivate fungi as their most important food source and in turn the fungus is nourished, protected against harmful microorganisms, and dispersed by the ants. This symbiosis evolved approximately 50–60 million years ago in the late Paleocene or early Eocene, and since its origin attine ants have acquired a variety of fungal mutualists in the Leucocoprineae and the distantly related Pterulaceae. The most specialized symbiotic interaction is referred to as “higher agriculture” and includes leafcutter ant agriculture in which the ants cultivate the single species Leucoagaricus gongylophorus. Higher agriculture fungal cultivars are characterized by specialized hyphal tip swellings, so-called gongylidia, which are considered a unique, derived morphological adaptation of higher attine fungi thought to be absent in lower attine fungi. Rare reports of gongylidia-like structures in fungus gardens of lower attines exist, but it was never tested whether these represent rare switches of lower attines to L. gonglyphorus cultivars or whether lower attine cultivars occasionally produce gongylidia. Here we describe the occurrence of gongylidia-like structures in fungus gardens of the asexual lower attine ant Mycocepurus smithii. To test whether M. smithii cultivates leafcutter ant fungi or whether lower attine cultivars produce gongylidia, we identified the M. smithii fungus utilizing molecular and morphological methods. Results shows that the gongylidia-like structures of M. smithii gardens are morphologically similar to gongylidia of higher attine fungus gardens and can only be distinguished by their slightly smaller size. A molecular phylogenetic analysis of the fungal ITS sequence indicates that the gongylidia-bearing M. smithii cultivar belongs to the so-called “Clade 1”of lower Attini cultivars. Given that M. smithii is capable of cultivating a morphologically and genetically diverse array of fungal symbionts, we discuss whether asexuality of the ant host maybe correlated with low partner fidelity and active symbiont choice between fungus and ant mutualists.

Cyatta abscondita: Taxonomy, Evolution, and Natural History of a New Fungus-Farming Ant Genus from Brazil

Cyatta abscondita, a new genus and species of fungus-farming ant from Brazil, is described based on morphological study of more than 20 workers, two dealate gynes, one male, and two larvae. Ecological field data are summarized, including natural history, nest architecture, and foraging behavior. Phylogenetic analyses of DNA sequence data from four nuclear genes indicate that Cyatta abscondita is the distant sister taxon of the genus Kalathomyrmex, and that together they comprise the sister group of the remaining neoattine ants, an informal clade that includes the conspicuous and well-known leaf-cutter ants. Morphologically, Cyatta abscondita shares very few obvious character states with Kalathomyrmex. It does, however, possess a number of striking morphological features unique within the fungus-farming tribe Attini. It also shares morphological character states with taxa that span the ancestral node of the Attini. The morphology, behavior, and other biological characters of Cyatta abscondita are potentially informative about plesiomorphic character states within the fungus-farming ants and about the early evolution of ant agriculture.

Nest architecture, fungus gardens, queen, males and larvae of the fungus-growing ant Mycetagroicus inflatus Brandão & Mayhé-Nunes

All known fungus-growing ants (tribe Attini) are obligately symbiotic with their cultivated fungi. The fungal cultivars of “lower” attine ants are facultative symbionts, capable of living apart from ants, whereas the fungal cultivars of “higher” attine ants, including leaf-cutting genera Atta and Acromyrmex, are highly specialized, obligate symbionts. Since higher attine ants and fungi are derived from lower attine ants and fungi, understanding the evolutionary transition from lower to higher attine agriculture requires understanding the historical sequence of change in both ants and fungi. The biology of the poorly known ant genus Mycetagroicus is of special interest in this regard because it occupies a phylogenetic position intermediate between lower and higher ant agriculture. Here, based on the excavations of four nests in Pará, Brazil, we report the first biological data for the recently described species Mycetagroicus inflatus, including the first descriptions of Mycetagroicus males and larvae. Like M. cerradensis, the only other species in the genus for which nesting biology is known, the garden chambers of M. inflatus are unusually deep and the garden is most likely relocated vertically in rainy and dry seasons. Due to the proximity of nests to the Araguaia River, it is likely that even the uppermost chambers and nest entrances of M. inflatus are submerged during the rainy season. Most remarkably, all three examined colonies of M. inflatus cultivate the same fungal species as their congener, M. cerradensis, over 1,000 km away, raising the possibility of long-term symbiont fidelity spanning speciation events within the genus.

Fungal-Fungal Interactions in Leaf-Cutting Ant Agriculture

Many organisms participate in symbiotic relationships with other organisms, yet studies of symbioses typically have focused on the reciprocal costs and benefits within a particular host-symbiont pair. Recent studies indicate that many ecological interactions involve alliances of symbionts acting together as mutualistic consortia against other consortia. Such interacting consortia are likely to be widespread in nature, even if the interactions often occur in a cryptic fashion. Little theory and empirical data exist concerning how these complex interactions shape ecological outcomes in nature. Here, we review recent work on fungal-fungal interactions between two consortia: (i) leaf-cutting ants and their symbiotic fungi (the latter grown as a food crop by the former) and (ii) tropical plants and their foliar endophytes (the cryptic symbiotic fungi within leaves of the former). Plant characteristics (e.g., secondary compounds or leaf physical properties of leaves) are involved in leaf-cutting ant preferences, and a synthesis of published information suggests that these plant traits could be modified by fungal presence. We discuss potential mechanisms for how fungal-fungal interactions proceed in the leaf-cutting ant agriculture and suggest themes for future research.

Rhizolith balls from the Lower Cretaceous of Patagonia: Just roots or the oldest evidence of insect agriculture?

A new type of trace fossil from the Lower Cretaceous of Patagonia that may record the oldest evidence of insect agriculture is represented by biconvex, sub-spherical, carbonate balls composed of a dense mass of rhizoliths. The best preserved balls show an external wall, a tunnel entrance, and vertical, large rhizoliths crossing from top to base, from which a mass of smaller rhizoliths arise. In some cases there is a pelletal surface texture in internal layers of the wall. Some specimens show meniscate tubes attributed to organisms different than the constructors of the chambers, probably attracted by the original organic matter. Micromorphology, analyzed by thin sections and SEM, shows strong evidence of high fungal activity associated to the original roots. Four different hypotheses are analyzed to explain the origin of the balls. The less probable ones are either that the balls were produced only by a self induced and localised overgrowth of secondary and tertiary rootlets from a group of neighbouring primary roots, or that they were crayfishes' feeding chambers. Rhizolith arrangement, as well as other characters, essentially rule out both hypotheses. The hypotheses involving social insects, termites and ants, are more risky, considering the lack of support from the body fossil record, the biogeography of these extant insects, and particularly the lack of definitive evidence of discrete fungus or bacterial gardens in the balls. However, the trace fossils described herein partially resemble the nests and behaviour of the African termite Sphaerothermes sphaerothorax, particularly because of the presence of roots inside a thick lined chamber excavated around them to cultivate bacterial combs. The ant origin of these balls is at least a hypothesis to explore considering the size, shape, wall, entrance tunnel, presence of traces of associated organisms, and particularly roots. The roots and wall relate these balls to hypothesised scenarios for the origin of fungus agriculture in ants. One hypothesis suggests that primitive Attini developed fungus agriculture from the habit of feeding on fungi associated with roots (mycorrhizae) and still other proposes that adventitious fungi on nest walls were responsible for the arise of fungiculture. The balls would supply physical evidence that by the lower Cretaceous some social insects excavated chambers around uncut roots, which in turn provided optimal conditions for fungi development. These rhizolith balls possibly constitute the oldest physical evidence for the origin of fungiculture in social insects, and represent a critical contribution of ichnology to this hot topic intensively discussed on the basis of a scattered body fossil record and molecular phylogeny.

All That Makes Fungus Gardens Grow

The discovery of a parasitic yeast draws attention to the ways that pathogens can stabilize ant agriculture and other symbiotic networks.

Major evolutionary transitions in ant agriculture

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 fossil-calibrated, 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 approximately 50 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 ( approximately 8-12 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.

The evolution of agriculture in ants

Cultivation of fungi for food by fungus-growing ants (Attini: Formicidae) originated about 50 million years ago. The subsequent evolutionary history of this agricultural symbiosis was inferred from phylogenetic and population-genetic patterns of 553 cultivars isolated from gardens of "primitive" fungus-growing ants. These patterns indicate that fungus-growing ants succeeded at domesticating multiple cultivars, that the ants are capable of switching to novel cultivars, that single ant species farm a diversity of cultivars, and that cultivars are shared occasionally between distantly related ant species, probably by lateral transfer between ant colonies.