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A domestication history of dynamic adaptation and genomic deterioration in Sorghum

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 in S.bicolor type bicolor.
Fig. 2: Total recessive GERP load over time in S.bicolor type bicolor.
Fig. 3: Selection signals across S. bicolor chromosomes 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.

Data availability

Sequence data were deposited in the European Molecular Biology Laboratory European Bioinformatics Institute (project code PRJEB24962).

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.

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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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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.

Corresponding author

Correspondence to Robin G. Allaby.

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The authors declare no competing interests.

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Journal peer review information: Nature Plants thanks 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 1,046 Sorghum lines 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 in Sorghum. Nat. Plants 5, 369–379 (2019). https://doi.org/10.1038/s41477-019-0397-9

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