title: Reciprocal genomic evolution in the ant-fungus agricultural symbiosis.
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.
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.
authors.forename: Sanne
authors.initials: S
authors.lastname: Nygaard
authors.affiliation: China National Genbank, BGI-Shenzhen, Shenzhen 518083, China.
authors.forename: Haofu
authors.initials: H
authors.lastname: Hu
authors.affiliation: China National Genbank, BGI-Shenzhen, Shenzhen 518083, China.
authors.forename: Cai
authors.initials: C
authors.lastname: Li
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.
authors.forename: Morten
authors.initials: M
authors.lastname: Schiøtt
authors.affiliation: China National Genbank, BGI-Shenzhen, Shenzhen 518083, China.
authors.forename: Zhensheng
authors.initials: Z
authors.lastname: Chen
authors.affiliation: China National Genbank, BGI-Shenzhen, Shenzhen 518083, China.
authors.forename: Zhikai
authors.initials: Z
authors.lastname: Yang
authors.affiliation: China National Genbank, BGI-Shenzhen, Shenzhen 518083, China.
authors.forename: Qiaolin
authors.initials: Q
authors.lastname: Xie
authors.affiliation: China National Genbank, BGI-Shenzhen, Shenzhen 518083, China.
authors.forename: Chunyu
authors.initials: C
authors.lastname: Ma
authors.affiliation: China National Genbank, BGI-Shenzhen, Shenzhen 518083, China.
authors.forename: Yuan
authors.initials: Y
authors.lastname: Deng
authors.affiliation: Smithsonian Institute for Biodiversity Genomics, Smithsonian Institution, Washington DC 20013-7012, USA.
authors.forename: Rebecca B
authors.initials: RB
authors.lastname: Dikow
authors.affiliation: Department of Biology, University of Rochester, Rochester, New York 14627, USA.|Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, USA.
authors.forename: Christian
authors.initials: C
authors.lastname: Rabeling
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.
authors.forename: David R
authors.identifier: 0000-0002-0462-6794
authors.initials: DR
authors.lastname: Nash
authors.affiliation: Smithsonian Tropical Research Institute, Balboa, Ancón 03092, Panama.
authors.forename: William T
authors.initials: WT
authors.lastname: Wcislo
authors.affiliation: Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, USA.
authors.forename: Seán G
authors.initials: SG
authors.lastname: Brady
authors.affiliation: Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, USA.
authors.forename: Ted R
authors.initials: TR
authors.lastname: Schultz
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.|China National Genbank, BGI-Shenzhen, Shenzhen 518083, China.|State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
authors.forename: Guojie
authors.initials: G
authors.lastname: Zhang
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.
authors.forename: Jacobus J
authors.initials: JJ
authors.lastname: Boomsma
mesh_terms: D000383:Agriculture; D000818:Animals; D001000:Ants / Q000235:genetics*; D002138:Calibration; D050260:Carbohydrate Metabolism / Q000235:genetics; D002686:Chitin / Q000378:metabolism; D018556:Crops, Agricultural / Q000235:genetics; D000071278:Domestication; D019143:Evolution, Molecular; D005658:Fungi / Q000235:genetics*; D016678:Genome; D049750:Genome, Insect; D018745:Genome, Plant; D010802:Phylogeny; D017422:Sequence Analysis, DNA; D013559:Symbiosis / Q000235:genetics*; D013997:Time Factors
chemical_list: D002686:Chitin