Abstract
All crops are the product of a domestication process that started less than 12,000 years ago from one or more wild populations1,2. Farmers selected desirable phenotypic traits (such as improved energy accumulation, palatability of seeds and reduced natural shattering3) while leading domesticated populations through several more or less gradual demographic contractions2,4. As a consequence, the erosion of wild genetic variation5 is typical of modern cultivars, making them highly susceptible to pathogens, pests and environmental change6,7. The loss of genetic diversity hampers further crop improvement programmes to increase food production in a changing world, posing serious threats to food security8,9. Using both ancient and modern seeds, we analysed the temporal dynamics of genetic variation and selection during the domestication process of the common bean (Phaseolus vulgaris) in the southern Andes. Here, we show that most domestic traits were selected for before 2,500 years ago, with no or only minor loss of whole-genome heterozygosity. In fact, most of the changes at coding genes and linked regions that differentiate wild and domestic genomes are already present in the ancient genomes analysed here, and all ancient domestic genomes dated between 600 and 2,500 years ago are highly variable (at least as variable as modern genomes from the wild). Single seeds from modern cultivars show reduced variation when compared with ancient seeds, indicating that intensive selection within cultivars in the past few centuries probably partitioned ancestral variation within different genetically homogenous cultivars. When cultivars from different Andean regions are pooled, the genomic variation of the pool is higher than that observed in the pool of ancient seeds from north and central western Argentina. Considering that most desirable phenotypic traits are probably controlled by multiple polymorphic genes10, a plausible explanation of this decoupling of selection and genetic erosion is that early farmers applied a relatively weak selection pressure2 by using many phenotypically similar but genetically diverse individuals as parents. Our results imply that selection strategies during the past few centuries, as compared with earlier times, more intensively reduced genetic variation within cultivars and produced further improvements by focusing on a few plants carrying the traits of interest, at the cost of marked genetic erosion within Andean landraces.
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Data availability
The sequenced raw reads from the ancient samples are publicly available as NCBI Bioproject (ID: PRJNA574560). The modern sample genomic data are available with the following NCBI accession codes: SRR10161640, SRR10161629, SRR10161767, SRR10161647, SRR10161646, SRR10161645, SRR10161601, SRR10161592, SRR10161584, SRR10161684, SRR10161683, SRR10161697, SRR10161690, SRR10161688, SRR10161651, SRR10161745 and SRR10161723.
Code availability
The custom scripts developed in this study are publicly available in the GitHub repository at https://github.com/anbena/ancient-beans.
Change history
04 March 2021
A Correction to this paper has been published: https://doi.org/10.1038/s41477-021-00892-3
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Acknowledgements
This study was supported by the University of Ferrara, the CUIA (Consorzio Universitario Italiano per l’Argentina, 5^ Research Program), the ERA-CAPS project Bean_Adapt, internal grants from the Marche Polytechnic University and the University of Firenze, the Italian Ministry of Education, University and Research (project Dipartimenti di Eccellenza 2018–2022, PRIN2017 grant no. 20174BTC4R), the Swedish Research Council grant no. VR-UF E0347601 and the Norwegian Research Council grant no. 262777. We also thank CONICET (Consejo Nacional de Investigaciones Cientificas y Técnicas) and the Institutions and Museums in Argentina for their support in the fieldwork, and in particular for recovering the archaeo-botanical specimens and studying the archaeological sites. M.D.L. sadly passed away during the preparation of this paper. One of the seeds we sequenced was kindly donated by the Archaeological Museum Pío Pablo Díaz in Cachi (Salta, Argentina), where M.D.L. was Director for many years.
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G.B. and R.P. conceived the project. G.B., E.T. and A.B. designed the research. M.L., S.V., L.C. and S.B. performed the experiments. E.T., A.B., M.L., S.B., A.I. and C.X. analysed the data. G.B., E.T., A.B., M.L., F.R., B.S. and S.B. contributed to the manuscript preparation. V.L., P.B., N.O., A.G., G.N., C.T.M. and M.D.L. collected the samples. G.B., E.T., A.B., R.P., M.L., S.B. and B.S. interpreted the data. G.B. and E.T. wrote the manuscript. All authors revised and approved the manuscript.
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Peer review information Nature Plants thanks Robin Allaby, Kelly Swarts and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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Supplementary information
Supplementary Information
Supplementary Sections 1–11, references, Figs. 1–13 and Tables 2–6.
Supplementary Table 1
Ancient seed information: AMS dates and basic sequencing statistics.
Supplementary Table 7
Results of selection scan using different accessions as the outgroup.
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Trucchi, E., Benazzo, A., Lari, M. et al. Ancient genomes reveal early Andean farmers selected common beans while preserving diversity. Nat. Plants 7, 123–128 (2021). https://doi.org/10.1038/s41477-021-00848-7
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DOI: https://doi.org/10.1038/s41477-021-00848-7
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