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      Multiregional origins of the domesticated tetraploid wheats

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          Abstract

          We used genotyping-by-sequencing (GBS) to investigate the evolutionary history of domesticated tetraploid wheats. With a panel of 189 wild and domesticated wheats, we identified 1,172,469 single nucleotide polymorphisms (SNPs) with a read depth ≥3. Principal component analyses (PCAs) separated the Triticum turgidum and Triticum timopheevii accessions, as well as wild T. turgidum from the domesticated emmers and the naked wheats, showing that SNP typing by GBS is capable of providing robust information on the genetic relationships between wheat species and subspecies. The PCAs and a neighbour-joining analysis suggested that domesticated tetraploid wheats have closest affinity with wild emmers from the northern Fertile Crescent, consistent with the results of previous genetic studies on the origins of domesticated wheat. However, a more detailed examination of admixture and allele sharing between domesticates and different wild populations, along with genome-wide association studies (GWAS), showed that the domesticated tetraploid wheats have also received a substantial genetic input from wild emmers from the southern Levant. Taking account of archaeological evidence that tetraploid wheats were first cultivated in the southern Levant, we suggest that a pre-domesticated crop spread from this region to southeast Turkey and became mixed with a wild emmer population from the northern Fertile Crescent. Fixation of the domestication traits in this mixed population would account for the allele sharing and GWAS results that we report. We also propose that feralization of the component of the pre-domesticated population that did not acquire domestication traits has resulted in the modern wild population from southeast Turkey displaying features of both the domesticates and wild emmer from the southern Levant, and hence appearing to be the sole progenitor of domesticated tetraploids when the phylogenetic relationships are studied by methods that assume a treelike pattern of evolution.

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          qqman: an R package for visualizing GWAS results using Q-Q and manhattan plots

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            Distribution of wild wheats and barley.

            If we accept the evidence at face value, we are led to conclude that emmer was probably domesticated in the upper Jordan watershed and that einkorn was domesticated in southeast Turkey. Barley could have been domesticated almost anywhere within the arc bordering the fertile crescent. All three cereals may well have been harvested in the wild state throughout their regions of adaptation long before actual farming began. The primary habitats for barley, however, are not the same as those for the wheats. Wild barley is more xerophytic and extends farther downslope and into the steppes and deserts along the wadis. It seems likely that, while all three early cereals were domesticated within an are flanking the fertile crescent, each was domesticated in a different subregion of the zone. Lest anyone should be led to think the problem is solved, we wish to close with a caveat. Domestication may not have taken place where the wild cereals were most abundant. Why should anyone cultivate a cereal where natural stands are as dense as a cultivated field? If wild cereal grasses can be harvested in unlimited quantities, why should anyone bother to till the soil and plant the seed? We suspect that we shall find, when the full story is unfolded, that here and there harvesting of wild cereals lingered on long after some people had learned to farm, and that farming itself may have orig inated in areas adjacent to, rather than in, the regions of greatest abundance of wild cereals. We need far more specific information on the climate during incipient domestication and many more carefully conducted excavations of sites in the appropriate time range. The problem is far from solved, but some knowledge of the present distribution of the wild forms should be helpful.
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              The genetic expectations of a protracted model for the origins of domesticated crops.

              Until recently, domestication has been interpreted as a rapid process with little predomestication cultivation and a relatively rapid rise of the domestication syndrome. This interpretation has had a profound effect on the biological framework within which investigations into crop origins have been carried out. A major underlying assumption has been that artificial selection pressures were substantially stronger than natural selection pressures, resulting in genetic patterns of diversity that reflect genetic independence of geographic localities. Recent archaeobotanical evidence has overturned the notion of a rapid transition, resulting in a protracted model that undermines these assumptions. Conclusions of genome-wide multilocus studies remain problematic in their support of a rapid-transition model by indicating that domesticated crops appear to be associated by monophyly with only a single geographic locality. Simulations presented here resolve this conflict, indicating that the results observed in such studies are inevitable over time at a rate that is largely influenced by the long-term population size. Counterintuitively, multiple origin crops are shown to be more likely to produce monophyletic clades than crops of a single origin. Under the protracted transition, the importance of the rise of the domestication syndrome becomes paramount in producing the patterns of genetic diversity from which crop origins may be deduced. We identify four different interacting levels of organization that now need to be considered to track crop origins from modern genetic diversity, making crop origins a problem that could be addressed through system-based approaches.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: Writing – original draft
                Role: Formal analysisRole: Writing – review & editing
                Role: Formal analysisRole: MethodologyRole: Writing – review & editing
                Role: Formal analysisRole: Writing – original draft
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                22 January 2020
                2020
                : 15
                : 1
                : e0227148
                Affiliations
                [001]School of Earth and Environmental Sciences, Manchester Institute of Biotechnology, University of Manchester, Manchester, England, United Kingdom
                Institute of Genetics and Developmental Biology Chinese Academy of Sciences, CHINA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                [¤]

                Current address: Interdisciplinary Center for Archaeology and Evolution of Human Behaviour, Universidade do Algarve, Faro, Portugal

                Author information
                http://orcid.org/0000-0002-8596-9288
                http://orcid.org/0000-0002-1006-1099
                Article
                PONE-D-19-23497
                10.1371/journal.pone.0227148
                6975532
                31968001
                a0943f3e-a114-41d0-9285-dff8da053a08
                © 2020 Oliveira et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 20 August 2019
                : 12 December 2019
                Page count
                Figures: 5, Tables: 0, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100010663, H2020 European Research Council;
                Award ID: 339941
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000270, Natural Environment Research Council;
                Award ID: NE/M010805/1
                Award Recipient :
                This work was supported by: TAB, 339941, European Research Council, https://erc.europa.eu/, No involvement; TAB, NE/M010805/1, Natural Environment Research Council, https://nerc.ukri.org/, No involvement.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Animal Types
                Domestic Animals
                Biology and Life Sciences
                Zoology
                Animal Types
                Domestic Animals
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Grasses
                Wheat
                Biology and Life Sciences
                Genetics
                Departures from Diploidy
                Polyploidy
                Tetraploidy
                Biology and Life Sciences
                Computational Biology
                Genome Analysis
                Genome-Wide Association Studies
                Biology and Life Sciences
                Genetics
                Genomics
                Genome Analysis
                Genome-Wide Association Studies
                Biology and Life Sciences
                Genetics
                Human Genetics
                Genome-Wide Association Studies
                Biology and Life Sciences
                Agriculture
                Crop Science
                Crops
                Cereal Crops
                Biology and Life Sciences
                Genetics
                Plant Genetics
                Crop Genetics
                Biology and Life Sciences
                Plant Science
                Plant Genetics
                Crop Genetics
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Computer and Information Sciences
                Data Management
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Computational Biology
                Genome Analysis
                Genomic Libraries
                Biology and Life Sciences
                Genetics
                Genomics
                Genome Analysis
                Genomic Libraries
                Custom metadata
                The GBS data are available at the European Nucleotide Archive, study PRJEB42105.

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