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Nat Commun. 2016 Jul 20;7:12233. doi: 10.1038/ncomms12233.

Reciprocal genomic evolution in the ant-fungus agricultural symbiosis.

Author information

1
Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.
2
China National Genbank, BGI-Shenzhen, Shenzhen 518083, China.
3
Smithsonian Institute for Biodiversity Genomics, Smithsonian Institution, Washington DC 20013-7012, USA.
4
Department of Biology, University of Rochester, Rochester, New York 14627, USA.
5
Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, USA.
6
Smithsonian Tropical Research Institute, Balboa, Ancón 03092, Panama.
7
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.

Abstract

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.

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