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A domestication history of dynamic adaptation and genomic deterioration inSorghum

Nature Plants volume5,pages369–379 (2019)Cite this article

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Abstract

The evolution of domesticated cereals was a complex interaction of shifting selection pressures and repeated episodes of introgression. Genomes of archaeological crops have the potential to reveal these dynamics without being obscured by recent breeding or introgression. We report a temporal series of archaeogenomes of the crop sorghum (Sorghum bicolor) from a single locality in Egyptian Nubia. These data indicate no evidence for the effects of a domestication bottleneck, but instead reveal a steady decline in genetic diversity over time coupled with an accumulating mutation load. Dynamic selection pressures acted sequentially to shape architectural and nutritional domestication traits and to facilitate adaptation to the local environment. Later introgression between sorghum races allowed the exchange of adaptive traits and achieved mutual genomic rescue through an ameliorated mutation load. These results reveal a model of domestication in which genomic adaptation and deterioration were not focused on the initial stages of domestication but occurred throughout the history of cultivation.

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Fig. 1: Genomic heterozygosity over time inS. bicolortype bicolor.
Fig. 2: Total recessive GERP load over time inS. bicolortype bicolor.
Fig. 3: Selection signals acrossS. bicolorchromosomes 1–10.
Fig. 4: Principal coordinate analysis of 1,894 SNPs from 23 genomes in this study and 1,046 sorghum lines described in Thurber et al.33.
Fig. 5: Genome rescue between bicolor and durra lineages.

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Data availability

Sequence data were deposited in the European Molecular Biology Laboratory European Bioinformatics Institute (project codePRJEB24962).

Code availability

The serial founder event simulation was executed using the program founderv6.pl available for download at:https://warwick.ac.uk/fac/sci/lifesci/research/archaeobotany/downloads/founderv6.

References

  1. Larson, G. et al. Current perspectives and the future of domestication studies.Proc. Natl Acad. Sci. USA111,6139–6146 (2014).

    Article CAS Google Scholar

  2. Purugganan, M. D. & Fuller, D. Q. The nature of selection during plant domestication.Nature457,843–848 (2009).

    Article CAS Google Scholar

  3. Fuller, D. Q. et al. Convergent evolution and parallelism in plant domestication revealed by an expanding archaeological record.Proc. Natl Acad. Sci. USA111,6147–6152 (2014).

    Article CAS Google Scholar

  4. Allaby, R. G., Stevens, S., Lucas, L., Maeda, O. & Fuller, D. Q. Geographic mosaics and changing rates of cereal domestication.Phil. Trans. R. Soc. B372,20160429 (2017).

    Article Google Scholar

  5. Poets, A. M., Fang, Z., Clegg, M. T. & Morell, P. L. Barley landraces are characterized by geographically heterogeneous genomic origins.Genome Biol.16,173 (2015).

    Article Google Scholar

  6. Hardigan, M. A. et al. Genome diversity of tuber-bearing solanum uncovers complex evolutionary history and targets of domestication in the cultivated potato.Proc. Natl Acad. Sci. USA114,E9999–E10008 (2017).

    Article CAS Google Scholar

  7. Hufford, M. et al. The genomic signature of crop-wild introgression in maize.PLoS Genet.9,e1003477 (2013).

    Article CAS Google Scholar

  8. The World Sorghum and Millet Economies: Facts, Trends and Outlook(FAO and ICRISAT, 1996)..

  9. Winchell, F., Stevens, C. J., Murphy, C., Champion, L. & Fuller, D. Q. Evidence for sorghum domestication in fourth millennium BC eastern Sudan: spikelet morphology from ceramic impressions of the Butana group.Curr. Anthropol.58,673–683 (2017).

    Article Google Scholar

  10. Doggett, H.Sorghum2nd edn (Longman, 1988).

  11. Brown, P. J., Myles, S. & Kresowich, S. Genetic support for a phenotype-based racial classification in sorghum.Crop Sci.51,224–230 (2011).

    Article Google Scholar

  12. Morris, G. et al. Population genomic and genome-wide association studies of agroclimatic traits in sorghum.Proc. Natl Acad. Sci. USA110,453–458 (2013).

    Article CAS Google Scholar

  13. Fuller, D. Q. & Stevens, C. J. inPlants and People in Africa’s Past: Progress in African Archaeobotany(eds Mercuri, A. M. et al.) 427–452 (Springer, 2017).

  14. Clapham, A. J. & Rowley-Conwy, P. A. inFields of Change: Progress in African Archaeobotany(ed. Cappers, R.) 157–164 (Barkhuis & Groningen University Library, 2007).

  15. de Wet, J. M. L., Harlan, J. R. & Price, E. G. inOrigins of African Plant Domestication(eds Harlan, J. R. et al.) 453–463 (Mouton Press, 1976).

  16. Harlan, J. R. & Stemler, A. B. L. inOrigins of African Plant Domestication(eds Harlan, J. R. et al.) 465–478 (Mouton Press, 1976).

  17. Ohadi, S., Hodnett, G., Rooney, W. & Bagavathiannan, M. Gene flow and its consequences inSorghumspp.Crit. Rev. Plant Sci.36,367–385 (2017).

    Article Google Scholar

  18. Meyer, R. & Purugganan, M. Evolution of crop species: genetics of domestication and diversification.Nat. Rev. Genet.14,840–852 (2013).

    Article CAS Google Scholar

  19. Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences.Nature475,493–496 (2011).

    Article CAS Google Scholar

  20. Wang, L. et al. The interplay of demography and selection during maize domestication and expansion.Genome Biol.18,215 (2017).

    Article Google Scholar

  21. Meyer, R. S. et al. Domestication history and geographical adaptation inferred from a SNP map of African rice.Nat. Genet.48,1083–1088 (2016).

    Article CAS Google Scholar

  22. Mazet, O., Rodríguez, W., Grusea, S., Boitard, S. & Chikhi, L. On the importance of being structured: instantaneous coalescence rates and human evolution—lessons for ancestral population size inference.Heredity (Edinb.)116,362–371 (2016).

    Article CAS Google Scholar

  23. Orozco-terWengel, P. The devil is in the details: the effect of population structure on demographic inference.Heredity (Edinb.)116,349–350 (2016).

    Article CAS Google Scholar

  24. Renault, S. & Rieseberg, L. The accumulation of deleterious mutations as a consequence of domestication and improvement in sunflower and other Compositae crops.Mol. Biol. Evol.32,2273–2283 (2015).

    Article Google Scholar

  25. Liu, Q., Zhou, Y., Morrell, P. L. & Gaut, B. S. Deleterious variants in Asian rice and the potential cost of domestication.Mol. Biol. Evol.34,908–924 (2017).

    Article CAS Google Scholar

  26. Cooper, G. M. et al. Distribution and intensity of constraint in mammalian genomic sequence.Genome Res.15,901–913 (2005).

    Article CAS Google Scholar

  27. Smith, O. et al. Genomic methylation patterns in archaeological barley show de-methylation as a time-dependent diagenetic process.Sci. Rep.4,5559 (2014).

    Article CAS Google Scholar

  28. Pavlidis, P., Živkovic, D., Stamatakis, A. & Alachiotis, N. SweeD: likelihood-based detection of selective sweeps in thousands of genomes.Mol. Biol. Evol.30,2224–2234 (2013).

    Article CAS Google Scholar

  29. Hudson, M., Ringli, C., Boylan, M. T. & Quail, P. H. TheFAR1locus encodes a novel nuclear protein specific to phytochrome a signaling.Genes Dev.13,2017–2027 (1999).

    Article CAS Google Scholar

  30. Zhu, Q. H., Ramm, K., Shivakkumar, R., Dennis, E. S. & Upadhyahya, N. M. TheANTHER INDEHISCENCE1gene encoding a single MYB domain protein is involved in anther development in rice.Plant Physiol.135,1514–1525 (2004).

    Article CAS Google Scholar

  31. Martin, S., Davey, J. & Jiggins, C. Evaluating the use of ABBA–BABA statistics to locate introgressed loci.Mol. Biol. Evol.32,244–257 (2014).

    Article Google Scholar

  32. Mace, E. S. et al. Whole genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum.Nat. Commun.4,2320 (2013).

    Article Google Scholar

  33. Thurber, C. S., Ma, J. M., Higgins, R. H. & Brown, P. J. Retrospective genomic analysis of sorghum adaptation to temperate-zone grain production.Genome Biol.14,R68 (2013).

    Article Google Scholar

  34. DeGiorgio, M., Jakobsson, M. & Rosenberg, N. Explaining worldwide patterns of human genetic variation using a coalescent-based serial founder model of migration outward from Africa.Proc. Natl Acad. Sci. USA106,16057–16062 (2009).

    Article CAS Google Scholar

  35. Alvarez, N. et al. Farmers’ practices, metapopulation dynamics, and conservation of agricultural biodiversity on-farm: a case study of sorghum among the Duupa in sub-sahelian Cameroon.Biol. Conserv.121,533–543 (2005).

    Article Google Scholar

  36. Westengen, O. T. et al. Ethnolinguistic structuring of sorghum genetic diversity in Africa and the role of local seed systems.Proc. Natl Acad. Sci. USA111,14100–14105 (2014).

    Article CAS Google Scholar

  37. Allaby, R. G., Ware, R. & Kistler, L. A re-evaluation of the domestication bottleneck from archaeogenomic evidence.Evol. Appl.12,29–37 (2018).

    Article Google Scholar

  38. Kremling, K. A. et al. Dysregulation of expression correlates with rare-allele burden and fitness loss in maize.Nature555,520–523 (2018).

    Article CAS Google Scholar

  39. Rogers & Slatkin Excess defects in a woolly mammoth on Wrangel Island.PLoS Genet.13,e1006601 (2017).

    Article Google Scholar

  40. Shennan, S. et al. Regional population collapse followed initial agricultural booms in mid-Holocene Europe.Nat. Commun.4,2486 (2013).

    Article Google Scholar

  41. Allaby, R. G., Kitchen, J. L. & Fuller, D. Q. Surprisingly low limits of selection in plant domestication.Evol. Bioinform. Online11,41–51 (2016).

    PubMed PubMed Central Google Scholar

  42. Alexander, J. The Saharan divide in the Nile Valley: the evidence from Qasr Ibrim.Afr. Archaeol. Rev.6,73–90 (1988).

    Article Google Scholar

  43. Rose, P. inThe Encyclopedia of Ancient History(eds Bagnall, R. S. et al.) 5695–5697 (Wiley, 2013).

  44. Palmer, S. A., Moore, J. D., Clapham, A. J., Rose, P. & Allaby, R. G. Archaeogenetic evidence of ancient Nubian barley evolution from six to two-row indicates local adaptation.PLoS ONE4,e6301 (2009).

    Article Google Scholar

  45. Palmer, S. A. et al. Archaeogenomic evidence of punctuated genome evolution inGossypium.Mol. Biol. Evol.29,2031–2038 (2012).

    Article CAS Google Scholar

  46. O’Donoghue, K., Clapham, A., Evershed, R. P. & Brown, T. A. Remarkable preservation of biomolecules in ancient radish seeds.Proc. Biol. Sci.263,541–547 (1996).

    Article Google Scholar

  47. Alexander, J. & Driskell, B. Qasr Ibrim 1984.J. Egypt. Archaeol.71,12–26 (1985).

    Google Scholar

  48. Rowley-Conwy, P. Nubia AD 0-550 and the ‘Islamic’ agricultural revolution: preliminary botanical evidence from Qasr Ibrim, Egyptian Nubia.Archeol. du Nil Moyen3,131–138 (1989).

    Google Scholar

  49. Clapham, A. & Rowley-Conwy, P. inFrom Foragers to Farmers: Papers in Honour of Gordon C. Hillman(eds Fairbairn, A. S. & Weiss, E.) 244–253 (Oxbow Books, 2009).

  50. Adams, W. Y.Ceramic Industries of Medieval Nubia(Univ. Kentucky Press, 1986).

  51. Hanghøj, K. et al. Fast, accurate and automatic ancient nucleosome and methylation maps with epiPALEOMIX.Mol. Biol. Evol.33,3248–3298 (2016).

    Article Google Scholar

  52. Paterson, A. H. et al. TheSorghum bicolorgenome and the diversification of grasses.Nature457,551–556 (2009).

    Article CAS Google Scholar

  53. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2.Nat. Methods9,357–359 (2012).

    Article CAS Google Scholar

  54. Li, H. et al. The sequence alignment/map (SAM) format and SAMtools.Bioinformatics25,2078–2079 (2009).

    Article Google Scholar

  55. Bouyer, D. et al. DNA methylation dynamics during early plant life.Genome Biol.18,179 (2017).

    Article Google Scholar

  56. Clark, R. M., Tavare, S. & Doebley, J. Estimating a nucleotide substitution rate for maize from polymorphism at a major domestication locus.Mol. Biol. Evol.22,2304–2312 (2005).

    Article CAS Google Scholar

  57. Van der Auwera, G. A. et al. From FastQ data to high-confidence variant calls: the genome analysis toolkit best practices pipeline.Curr. Protoc. Bioinformatics43,11.10.1–11.10.33 (2013).

    Google Scholar

  58. da Fonseca, R. R. et al. The origin and evolution of maize in the southwestern United States.Nat. Plants1,14003 (2015).

    Article Google Scholar

  59. Koslov, A. M., Aberer, A. & Alexandros, S. ExaML version 3: a tool for phylogenomic analysis on supercomputers.Bioinformatics31,2577–2579 (2015).

    Article Google Scholar

  60. Felsenstein, J. Evolutionary trees from DNA sequences: a maximum likelihood approach.J. Mol. Evol.17,368–376 (1981).

    Article CAS Google Scholar

  61. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Bioinformatics22,2688–2690 (2006).

    Article CAS Google Scholar

  62. R:A Language and Environment for Statistical Computing(R Core Team, 2017);https://www.r-project.org

  63. Pfeifer, B., Wittelsbürger, U., Ramos-Onsins, S. & Lercher, M. PopGenome: an efficient Swiss army knife for population genomic analyses in R.Mol. Biol. Evol.31,1929–1936 (2014).

    Article CAS Google Scholar

  64. Wolfe, K. H., Sharpe, P. M. & Li, W. H. Rates of synonymous substitution in plant nuclear genes.J. Mol. Evol.29,208–211 (1989).

    Article CAS Google Scholar

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Acknowledgements

The authors thank M. Nesbitt for permitting the use of herbaria material from Kew Gardens. O.S., W.V.N., G.B. and R.G.A. were supported by the NERC (NE/L006847/1), and L.K. was also supported by NERC (NE/L012030/1). The work by C.S. and D.Q.F. with archaeobotanical materials was supported by a European Research Council grant (no. 323842).

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Authors and Affiliations

  1. School of Life Sciences, University of Warwick, Coventry, UK

    Oliver Smith, William V. Nicholson, Logan Kistler, Alan Clapham, Roselyn Ware, Siva Samavedam, Guy Barker & Robin G. Allaby

  2. Natural History Museum of Denmark, Copenhagen, Denmark

    Oliver Smith

  3. Warwick Medical School, University of Warwick, Coventry, UK

    William V. Nicholson

  4. Department of Anthropology, Smithsonian Institution, National Museum of Natural History, Washington, D.C., USA

    Logan Kistler

  5. Department of Agriculture, Fisheries and Forestry Queensland (DAFFQ), Warwick, Queensland, Australia

    Emma Mace

  6. The Austrian Archaeological Institute, Cairo Branch, Zamalek, Cairo, Egypt

    Pamela Rose

  7. Institute of Archaeology, UCL, London, UK

    Chris Stevens & Dorian Q. Fuller

  8. Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, Warwick, Queensland, Australia

    David Jordan

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Contributions

R.G.A. conceived and designed the project. R.G.A., O.S., R.W. and L.K. wrote the manuscript. R.G.A., O.S., W.V.N., L.K., E.M., R.W., G.B. and S.S. interpreted the genomic data; C.S., A.C. and D.Q.F. interpreted the archaeological data. O.S. performed DNA extractions; genome sequencing; baseline bioinformatics, including mapping heterozygosity calls across genomes and specific domestication genes; methylation analysis; and PSMC analysis. P.R., A.C. and D.Q.F. supplied archaobotanical material; C.S., A.C. and D.Q.F. selected archaobotanical material. W.V.N. performed phylogenetic, SweeD and linear regression analyses. L.K. and R.G.A. performed GERP analyses. E.M. and D.J. performed principal component analysis and provided access to datasets. R.G.A. performed heterozygosity, heterozygosity gradient and population simulation analyses. R.W. performed linear regression analysis. S.S. performed D statistic analysis.

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Correspondence to Robin G. Allaby.

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Journal peer review information:Nature Plantsthanks Terence Brown, Xuehui Huang and other anonymous reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Tables 1–15, Supplementary Figures 1–18 and Supplementary Video Legend.

Reporting Summary

Supplementary Video

A three-dimensional file showing principal coordinate analysis of 1,894 SNPs from 23 genomes in this study and 1,046Sorghumlines described in ref. 25.

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Smith, O., Nicholson, W.V., Kistler, L.et al.A domestication history of dynamic adaptation and genomic deterioration inSorghum. Nat. Plants5,369–379 (2019). https://doi.org/10.1038/s41477-019-0397-9

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