Reciprocal genomic evolution in the ant–fungus agricultural symbiosis

Sanne Nygaard (), Haofu Hu, Cai Li, Morten Schiøtt, Zhensheng Chen, Zhikai Yang, Qiaolin Xie, Chunyu Ma, Yuan Deng, Rebecca B. Dikow, Christian Rabeling, David R. Nash, William T. Wcislo, Seán G. Brady, Ted R. Schultz, Guojie Zhang () and Jacobus J. Boomsma ()
Additional contact information
Sanne Nygaard: Centre for Social Evolution, University of Copenhagen
Haofu Hu: China National Genbank, BGI-Shenzhen
Cai Li: China National Genbank, BGI-Shenzhen
Morten Schiøtt: Centre for Social Evolution, University of Copenhagen
Zhensheng Chen: China National Genbank, BGI-Shenzhen
Zhikai Yang: China National Genbank, BGI-Shenzhen
Qiaolin Xie: China National Genbank, BGI-Shenzhen
Chunyu Ma: China National Genbank, BGI-Shenzhen
Yuan Deng: China National Genbank, BGI-Shenzhen
Rebecca B. Dikow: Smithsonian Institute for Biodiversity Genomics, Smithsonian Institution
Christian Rabeling: University of Rochester
David R. Nash: Centre for Social Evolution, University of Copenhagen
William T. Wcislo: Smithsonian Tropical Research Institute
Seán G. Brady: National Museum of Natural History, Smithsonian Institution
Ted R. Schultz: National Museum of Natural History, Smithsonian Institution
Guojie Zhang: Centre for Social Evolution, University of Copenhagen
Jacobus J. Boomsma: Centre for Social Evolution, University of Copenhagen

Nature Communications, 2016, vol. 7, issue 1, 1-9

Abstract: 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.

Date: 2016
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DOI: 10.1038/ncomms12233

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