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Major Evolutionary Transitions in Ant Agriculture SEE COMMENTARY Major evolutionary transitions in ant agriculture SEE COMMENTARY Ted R. Schultz† and Sea´ n G. Brady Department of Entomology and Laboratories of Analytical Biology, National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, Washington, DC 20013-7012 Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved January 30, 2008 (received for review November 20, 2007) Agriculture is a specialized form of symbiosis that is known to have Based on nearly monolithic associations between broad phy- evolved in only four animal groups: humans, bark beetles, ter- logenetic groups of attine ants, cultivars, and Escovopsis para- mites, and ants. Here, we reconstruct the major evolutionary sites, attine agriculture has been divided into five biologically transitions that produced the five distinct agricultural systems of distinct agricultural systems, each representing a major transi- the fungus-growing ants, the most well studied of the nonhuman tion in the evolution of ant agriculture. These systems are: (i) agriculturalists. We do so with reference to the first fossil- lower agriculture, practiced by species in the majority of attine calibrated, multiple-gene, molecular phylogeny that incorporates genera (76 species), including those thought to retain more the full range of taxonomic diversity within the fungus-growing primitive features, which cultivate a wide range of fungal species ant tribe Attini. Our analyses indicate that the original form of ant in the tribe Leucocoprineae; (ii) coral fungus agriculture, prac- s agriculture, the cultivation of a diverse subset of fungal species in ticed by species in the ‘‘pilosum group’’ (34 species), a subset of the tribe Leucocoprineae, evolved Ϸ50 million years ago in the the attine genus Apterostigma, which cultivate a clade of fungi in Neotropics, coincident with the early Eocene climatic optimum. the Pterulaceae; (iii) yeast agriculture, practiced by species in the During the past 30 million years, three known ant agricultural ‘‘rimosus group’’ (18 species), a subset of the attine genus systems, each involving a phylogenetically distinct set of derived Cyphomyrmex, which cultivate a distinct clade of leucocoprinea- fungal cultivars, have separately arisen from the original agricul- ceous fungi derived from the lower attine fungi; (iv) generalized tural system. One of these derived systems subsequently gave rise higher agriculture, practiced by species in the three genera of to the fifth known system of agriculture, in which a single fungal non-leaf-cutting ‘‘higher attine’’ ants (63 species), which cultivate species is cultivated by leaf-cutter ants. Leaf-cutter ants evolved another distinct clade of leucocoprineaceous fungi separately remarkably recently (Ϸ8–12 million years ago) to become the derived from the lower attine fungi; and (v) leaf-cutter agricul- dominant herbivores of the New World tropics. Our analyses ture, a subdivision of higher attine agriculture practiced by identify relict, extant attine ant species that occupy phylogenetic species of ecologically dominant ants in the genera Atta and positions that are transitional between the agricultural systems. Acromyrmex (40 species), which cultivate a single highly derived Intensive study of those species holds particular promise for species of higher attine fungus (4, 12–14). clarifying the sequential accretion of ecological and behavioral In contrast to important advances in other areas of attine characters that produced each of the major ant agricultural biology, including molecular phylogenies for the other three EVOLUTION systems. symbionts (10, 13–25), major features of fungus-growing ant phylogeny remain poorly understood (1, 26, 27). A well sup- Attini ͉ divergence dating ͉ Formicidae ͉ phylogeny ͉ symbiosis ported, resolved phylogeny of the attine ants is necessary for analyzing the coevolution of the ants and their three microbial ttine ants (subfamily Myrmicinae, tribe Attini) comprise a symbionts as well as for understanding the historical sequence of Amonophyletic group of Ͼ230 described species, exclusively evolutionary change that produced each of the five attine New World and primarily Neotropical in distribution (1–4). All agricultural systems. To address this problem, we reconstructed attine ants obligately depend on the cultivation of fungus gardens the evolution of attine agriculture by inferring the first fossil- for food. So complete is this dependence that, upon leaving the calibrated molecular phylogeny for the fungus-growing ants, maternal nest, a daughter queen must carry within her mouth a based on data from four nuclear protein-coding genes and nucleus of fungus that serves as the starting culture for her new incorporating the full range of attine taxonomic diversity, par- garden (5–7). Attine agriculture achieves its evolutionary apex in ticularly with regard to poorly understood, rarely collected, and the leaf-cutting ants of the genera Acromyrmex and Atta, the potentially paraphyletic or polyphyletic taxa (1). dominant herbivores of the New World tropics (8, 9). Unlike Results and Discussion more primitive attine ants that forage for and cultivate their fungus gardens on organic detritus, leaf-cutting ants have ac- Origin of Ant Agriculture. Based on the monophyly of the attine quired the ability to cut and process fresh vegetation (leaves, ants, on their exclusively New World distribution, and on their flowers, and grasses) to serve as the nutritional substrate for apparent center of diversity in the wet Neotropics, some re- their fungal cultivars. This key evolutionary innovation renders searchers have speculated that ant agriculture arose a single time a mature Atta colony the ecological equivalent of a large mammalian herbivore in terms of collective biomass, lifespan, Author contributions: T.R.S. and S.G.B. designed research, performed research, contributed and quantity of plant material consumed (9). new reagents/analytic tools, analyzed data, and wrote the paper. Attine ant agriculture is the product of an ancient, quadri- The authors declare no conflict of interest. partite, symbiotic relationship between three mutualists and one This article is a PNAS Direct Submission. parasite. The mutualists include the attine ants, their fungal Data deposition: The DNA sequences reported in this paper have been deposited in the cultivars (Leucocoprineae and Pterulaceae), and filamentous GenBank database (accession nos. EU204145–EU204615). bacteria in the genus Pseudonocardia (Actinomycetes) that grow See Commentary on page 5287. on the integuments of the ants. The parasite, a fungus in the †To whom correspondence should be addressed at: Smithsonian Institution, P.O. Box 37012, genus Escovopsis (Ascomycetes) known only from attine fungus NHB, CE516, MRC 188, Washington, DC 20013-7012. E-mail: [email protected]. gardens, infects those gardens as a ‘‘crop disease’’ and is con- This article contains supporting information online at www.pnas.org/cgi/content/full/ trolled, at least in part, by an antibiotic produced by the 0711024105/DCSupplemental. Pseudonocardia bacterial symbiont (4, 10, 11). © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0711024105 PNAS ͉ April 8, 2008 ͉ vol. 105 ͉ no. 14 ͉ 5435–5440 Outgroup: Pogonomyrmex sp. (GUY) + 2 Myrmica spp. (USA) Cataulacus MAD02 (MAD) Acanthognathus ocellatus (CR) –/60/98/73 Monomorium pharaonis (USA) Tetramorium caespitum (USA) /99/ / Proatta butteli (BORNEO) * * * –/–/80/– Meranoplus sp. (AUS) 84/63/99/82 –/–/63/– Crematogaster sp (GUY) 71/89/*/90 50/66/78/91 Pristomyrmex pungens (JAP) Strumigenys propiciens (TRI) Pyramica hoplites (MAD) –/–/72/– */*/*/* 98/97/*/* Strumigenys dicomas (MAD) –/–/ Blepharidatta brasiliensis (BRAZ) 99/99 Wasmannia auropunctata (CR) 84/86/*/* Wasmannia sp. (ARG) */*/*/* –/–/ /– Basiceros manni (CR) * Tranopelta cf. gilva (PAN) Cephalotes atratus (GUY) –/–/96/– 95/98/*/* Procryptocerus scabriusculus (GUAT) –/–/ Pheidole clydei (USA) 86/66 */*/*/* Pheidole hyatti (USA) –/–/–/50 Daceton armigerum (GUY) Orectognathus sp (AUS) –/–/–/– */*/*/* Orectognathus versicolor (AUS) Mycocepurus smithi (GUY) 99/96/ Mycocepurus smithi (ARG) –/–/–/– */* 62/70/99/97 */*/*/* Mycocepurus tardus (PAN) –/62/63/– Mycocepurus curvispinosus (CR) Myrmicocrypta infuscata (GUY) Myrmicocrypta new sp (BRAZ) Lower */*/*/* –/–/82/89 Myrmicocrypta new sp (PAN) Myrmicocrypta buenzlii (GUY) Agriculture –/–/–/– 81/69/97/* 68/52/92/94 Myrmicocrypta urichi (TRI) 67/68/*/* */*/*/* Myrmicocrypta ednaella (PAN) 96/99/*/* Apterostigma new sp. (PERU) Apterostigma auriculatum (BRAZ) */*/*/* Apterostigma auriculatum (PAN) Apterostigma dentigerum (PAN) / / / Apterostigma dorotheae (GUY) * * * * 97/98/*/* Coral Fungus PALEOATTINI 99/*/*/* Apterostigma p.c. sp 1 (PAN) –/–/78/99 91/91/*/* Apterostigma collare (CR) (Pterulaceae) –/–/–/– Apterostigma p.c. sp 4 (PAN) –/–/62/– Apterostigma manni (PAN) Agriculture 95/94/ / Apterostigma cf. goniodes (PAN) * * Mycetophylax emeryi (GUY) */*/*/* */*/*/* Mycetophylax emeryi gp (ARG) Mycetarotes cf. parallelus (BRAZ) 92/ / / */*/*/* Mycetarotes acutus (BRAZ) * * * Mycetosoritis hartmanni (USA) Mycetosoritis clorindae (BRAZ) 64/77/97/* Cyphomyrmex fanulus (GUY) Mycetophylax conformis (TRI) –/–/76/94 95/99/*/* */*/*/* Cyphomyrmex morschi (BRAZ) Cyphomyrmex rimosus (USA) NEOATTINI */*/*/* Cyphomyrmex minutus (GUY) Yeast –/–/–/99 */*/*/* Cyphomyrmex new sp (BRAZ) 79/80/98/* Cyphomyrmex cornutus (PAN) Agriculture –/55/–/* */*/*/na Cyphomyrmex cornutus
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