title: Dry habitats were crucibles of domestication in the evolution of agriculture in ants.
abstract: The evolution of ant agriculture, as practised by the fungus-farming 'attine' ants, is thought to have arisen in the wet rainforests of South America about 55-65 Ma. Most subsequent attine agricultural evolution, including the domestication event that produced the ancestor of higher attine cultivars, is likewise hypothesized to have occurred in South American rainforests. The 'out-of-the-rainforest' hypothesis, while generally accepted, has never been tested in a phylogenetic context. It also presents a problem for explaining how fungal domestication might have occurred, given that isolation from free-living populations is required. Here, we use phylogenomic data from ultra-conserved element (UCE) loci to reconstruct the evolutionary history of fungus-farming ants, reduce topological uncertainty, and identify the closest non-fungus-growing ant relative. Using the phylogeny we infer the history of attine agricultural systems, habitat preference and biogeography. Our results show that the out-of-the-rainforest hypothesis is correct with regard to the origin of attine ant agriculture; however, contrary to expectation, we find that the transition from lower to higher agriculture is very likely to have occurred in a seasonally dry habitat, inhospitable to the growth of free-living populations of attine fungal cultivars. We suggest that dry habitats favoured the isolation of attine cultivars over the evolutionary time spans necessary for domestication to occur.
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112, USA mgbranstetter@gmail.com.|Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA.
authors.forename: Michael G
authors.identifier: http://orcid.org/0000-0002-3734-6166
authors.initials: MG
authors.lastname: Branstetter
authors.affiliation: Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA.|Department of Entomology, University of Maryland, College Park, MD 20742, USA.
authors.forename: Ana
authors.identifier: http://orcid.org/0000-0002-4514-1478
authors.initials: A
authors.lastname: Ješovnik
authors.affiliation: Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA.|Center for Social Insect Research, School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA.
authors.forename: Jeffrey
authors.identifier: http://orcid.org/0000-0003-3995-7275
authors.initials: J
authors.lastname: Sosa-Calvo
authors.affiliation: Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA.
authors.forename: Michael W
authors.identifier: http://orcid.org/0000-0003-1021-8129
authors.initials: MW
authors.lastname: Lloyd
authors.affiliation: Department of Biological Sciences and Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803, USA.
authors.forename: Brant C
authors.identifier: http://orcid.org/0000-0002-1943-0217
authors.initials: BC
authors.lastname: Faircloth
authors.affiliation: Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA.
authors.forename: Seán G
authors.identifier: http://orcid.org/0000-0003-0468-940X
authors.initials: SG
authors.lastname: Brady
authors.affiliation: Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA schultzt@si.edu.
authors.forename: Ted R
authors.identifier: http://orcid.org/0000-0002-6244-7233
authors.initials: TR
authors.lastname: Schultz
mesh_terms: D000818:Animals; D001000:Ants / Q000235:genetics / Q000502:physiology*; D005075:Biological Evolution; D000071278:Domestication; D017753:Ecosystem; D005658:Fungi / Q000502:physiology*; D019476:Insect Proteins / Q000235:genetics; D010802:Phylogeny; D065947:Rainforest; D017422:Sequence Analysis, DNA; D013020:South America; D013559:Symbiosis
chemical_list: D019476:Insect Proteins
keywords: attine ants; fungus farming; phylogenomics; symbiosis; ultraconserved elements