Reciprocal genomic evolution in the ant–fungus agricultural symbiosis

• Published in: Nature communications 2016-07, Vol.7 (1), p.12233-12233, Article 12233
• Main Authors: Nygaard, Sanne, Hu, Haofu, Li, Cai, Schiøtt, Morten, Chen, Zhensheng, Yang, Zhikai, Xie, Qiaolin, Ma, Chunyu, Deng, Yuan, Dikow, Rebecca B., Rabeling, Christian, Nash, David R., Wcislo, William T., Brady, Seán G., Schultz, Ted R., Zhang, Guojie, Boomsma, Jacobus J.
• Format: Article
• Language: English
• Subjects: 631/158/2456; 631/181/2481; 631/208/212/2304; Agriculture; Animals; Ants - genetics; Calibration; Carbohydrate Metabolism - genetics; Chitin - metabolism; Crops, Agricultural - genetics; Cultivars; Domestication; Evolution; Evolution, Molecular; Farmers; Fungi; Fungi - genetics; Genome; Genome, Insect; Genome, Plant; Genomes; Humanities and Social Sciences; multidisciplinary; Phylogenetics; Phylogeny; Science; Science (multidisciplinary); Sequence Analysis, DNA; Symbiosis - genetics; Time Factors
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/ncomms12233

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. Attine ants, including the leaf-cutting ants, cultivate fungi as their sole source of food. Here, Nygaard et al . use whole genome and transcriptome sequences from seven ant species and their fungal cultivars to reconstruct the reciprocal genetic changes underlying the evolution of the ant-fungus mutualism.