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 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.

Fig. 1.

A time-calibrated phylogeny of the attine fungus-growing ants with age estimates for the origins of the five known ant agricultural systems. Agricultural systems, indicated by colored rectangles, are defined by phylogenetically distinct groups of associated fungal cultivars and were reconstructed under likelihood and parsimony methods with identical results. Tree topology is the maximum-likelihood reconstruction, identical with regard to attine phylogeny to the Bayesian codon-model result. Numbers on branches indicate support values from four analyses: parsimony bootstraps, ML bootstraps, Bayesian nucleotide-model posterior probabilities, and Bayesian codon-model posterior probabilities (“−,” < 50; “*,” 100). The three solid circles represent node assignments for Dominican amber fossil calibrations, and the open circle marks the root of the dating-analysis tree. Bars below the time scale summarize four separate relaxed-molecular-clock analyses dating the origin of the five agricultural systems. Black bars represent the most recent node containing all members of the system (“crown-group”) and red bars additionally include the branch leading to that node (“stem-group”). For each system, pairs of red and black bars from top to bottom correspond to (i) Bayesian uncorrelated lognormal, root age prior to 73.5 ± 4.5 mya; (ii) penalized likelihood, root age 81 mya; (iii) penalized likelihood, root age 73.5 mya; (iv) penalized likelihood, root age 66 mya. The tree shown here is the result of dating analysis (iii). Ant head photos (top to bottom): Mycocepurus tardus, Myrmicocrypta infuscata, Apterostigma collare, Mycetophylax emeryi, Cyphomyrmex rimosus, Cyphomyrmex longiscapus, Trachymyrmex opulentus, Trachymyrmex cornetzi, Acromyrmex octospinosus, Atta laevigata. Fungus gardens: (A) Lower attine agriculture. (B) Coral fungus agriculture. (C) Yeast agriculture. (D) Higher leaf-cutter agriculture. Country abbreviations: ARG, Argentina; AUS, Australia; BRAZ, Brazil; CR, Costa Rica; MAD, Madagascar; CR, Costa Rica; JAP, Japan; PAN, Panama; GUAT, Guatemala; GUY, Guayana; TRI, Trinidad; MEX, Mexico. Photo credits are given in Acknowledgments.