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      Dry habitats were crucibles of domestication in the evolution of agriculture in ants

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          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.

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          Most cited references 107

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          Trends, rhythms, and aberrations in global climate 65 Ma to present.

          Since 65 million years ago (Ma), Earth's climate has undergone a significant and complex evolution, the finer details of which are now coming to light through investigations of deep-sea sediment cores. This evolution includes gradual trends of warming and cooling driven by tectonic processes on time scales of 10(5) to 10(7) years, rhythmic or periodic cycles driven by orbital processes with 10(4)- to 10(6)-year cyclicity, and rare rapid aberrant shifts and extreme climate transients with durations of 10(3) to 10(5) years. Here, recent progress in defining the evolution of global climate over the Cenozoic Era is reviewed. We focus primarily on the periodic and anomalous components of variability over the early portion of this era, as constrained by the latest generation of deep-sea isotope records. We also consider how this improved perspective has led to the recognition of previously unforeseen mechanisms for altering climate.
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            ASTRAL: genome-scale coalescent-based species tree estimation

            Motivation: Species trees provide insight into basic biology, including the mechanisms of evolution and how it modifies biomolecular function and structure, biodiversity and co-evolution between genes and species. Yet, gene trees often differ from species trees, creating challenges to species tree estimation. One of the most frequent causes for conflicting topologies between gene trees and species trees is incomplete lineage sorting (ILS), which is modelled by the multi-species coalescent. While many methods have been developed to estimate species trees from multiple genes, some which have statistical guarantees under the multi-species coalescent model, existing methods are too computationally intensive for use with genome-scale analyses or have been shown to have poor accuracy under some realistic conditions. Results: We present ASTRAL, a fast method for estimating species trees from multiple genes. ASTRAL is statistically consistent, can run on datasets with thousands of genes and has outstanding accuracy—improving on MP-EST and the population tree from BUCKy, two statistically consistent leading coalescent-based methods. ASTRAL is often more accurate than concatenation using maximum likelihood, except when ILS levels are low or there are too few gene trees. Availability and implementation: ASTRAL is available in open source form at https://github.com/smirarab/ASTRAL/. Datasets studied in this article are available at http://www.cs.utexas.edu/users/phylo/datasets/astral. Contact: warnow@illinois.edu Supplementary information: Supplementary data are available at Bioinformatics online.
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              Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales.

              Although massively parallel sequencing has facilitated large-scale DNA sequencing, comparisons among distantly related species rely upon small portions of the genome that are easily aligned. Methods are needed to efficiently obtain comparable DNA fragments prior to massively parallel sequencing, particularly for biologists working with non-model organisms. We introduce a new class of molecular marker, anchored by ultraconserved genomic elements (UCEs), that universally enable target enrichment and sequencing of thousands of orthologous loci across species separated by hundreds of millions of years of evolution. Our analyses here focus on use of UCE markers in Amniota because UCEs and phylogenetic relationships are well-known in some amniotes. We perform an in silico experiment to demonstrate that sequence flanking 2030 UCEs contains information sufficient to enable unambiguous recovery of the established primate phylogeny. We extend this experiment by performing an in vitro enrichment of 2386 UCE-anchored loci from nine, non-model avian species. We then use alignments of 854 of these loci to unambiguously recover the established evolutionary relationships within and among three ancient bird lineages. Because many organismal lineages have UCEs, this type of genetic marker and the analytical framework we outline can be applied across the tree of life, potentially reshaping our understanding of phylogeny at many taxonomic levels.
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                Author and article information

                Journal
                Proc Biol Sci
                Proc. Biol. Sci
                RSPB
                royprsb
                Proceedings of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8452
                1471-2954
                12 April 2017
                12 April 2017
                12 April 2017
                : 284
                : 1852
                Affiliations
                [1 ]Department of Biology, University of Utah , Salt Lake City, UT 84112, USA
                [2 ]Department of Entomology, National Museum of Natural History, Smithsonian Institution , Washington, DC 20560, USA
                [3 ]Department of Entomology, University of Maryland , College Park, MD 20742, USA
                [4 ]Center for Social Insect Research, School of Life Sciences, Arizona State University , Tempe, AZ 85287, USA
                [5 ]Department of Biological Sciences and Museum of Natural Science, Louisiana State University , Baton Rouge, LA 70803, USA
                Author notes

                Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.3726862.

                Article
                rspb20170095
                10.1098/rspb.2017.0095
                5394666
                28404776
                © 2017 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                Product
                Funding
                Funded by: National Museum of Natural History, http://dx.doi.org/10.13039/100006271;
                Funded by: Directorate for Biological Sciences, http://dx.doi.org/10.13039/100000076;
                Award ID: DEB-0949689
                Award ID: DEB-1354996
                Award ID: DEB-1456964
                Award ID: DEB-1555905
                Categories
                1001
                183
                70
                198
                Evolution
                Research Article
                Custom metadata
                April 12, 2017

                Life sciences

                attine ants, fungus farming, phylogenomics, ultraconserved elements, symbiosis

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