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EVOLUTION
Major evolutionary transitions in ant agriculture

Ted R. Schultz and Seán 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)

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 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 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 (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.

Attini | divergence dating | Formicidae | phylogeny | symbiosis

Author contributions: T.R.S. and S.G.B. designed research, performed research, contributed new reagents/analytic tools, analyzed data, and wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

To whom correspondence should be addressed at: Smithsonian Institution, P.O. Box 37012, NHB, CE516, MRC 188, Washington, DC 20013-7012. E-mail: schultzt{at}si.edu

© 2008 by The National Academy of Sciences of the USA

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