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Recent demography drives changes in linked selection across the maize genome

Nature Plants volume 2, Article number: 16084 (2016) Cite this article

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Abstract

Genetic diversity is shaped by the interaction of drift and selection, but the details of this interaction are not well understood. The impact of genetic drift in a population is largely determined by its demographic history, typically summarized by its long-term effective population size (Ne). Rapidly changing population demographics complicate this relationship, however. To better understand how changing demography impacts selection, we used whole-genome sequencing data to investigate patterns of linked selection in domesticated and wild maize (teosinte). We produce the first whole-genome estimate of the demography of maize domestication, showing that maize was reduced to approximately 5% the population size of teosinte before it experienced rapid expansion post-domestication to population sizes much larger than its ancestor. Evaluation of patterns of nucleotide diversity in and near genes shows little evidence of selection on beneficial amino acid substitutions, and that the domestication bottleneck led to a decline in the efficiency of purifying selection in maize. Young alleles, however, show evidence of much stronger purifying selection in maize, reflecting the much larger effective size of present day populations. Our results demonstrate that recent demographic change—a hall-mark of many species including both humans and crops—can have immediate and wide-ranging impacts on diversity that conflict with expectations based on long-term Ne alone.

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Figure 1: Genetic diversity in maize and teosinte.
Figure 2: Estimated demographic history of maize and teosinte.
Figure 3: Relative diversity versus distance to nearest substitution in maize and teosinte.
Figure 4: Relative diversity versus distance to nearest gene in maize and teosinte.

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Acknowledgements

We are indebted to G. Coop and S. Aeschbacher for their constructive input during this study. We thank R. Bukowski and Q. Sun for providing early-access data from maize HapMap3. Funding was provided by National Science Foundation Plant Genome Research Project 1238014, the US Department of Agriculture (USDA) Agricultural Research Service, and USDA Hatch project CA-D-PLS-2066-H.

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Authors and Affiliations

  1. Department of Plant Sciences, University of California, Davis, 95616, California, USA

    Timothy M. Beissinger, Kate Crosby, Arun Durvasula & Jeffrey Ross-Ibarra

  2. US Department of Agriculture, Agricultural Research Service, Columbia, 65211, Missouri, USA

    Timothy M. Beissinger

  3. Division of Plant Sciences, University of Missouri, Columbia, 65211, Missouri, USA

    Timothy M. Beissinger

  4. Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, 50011, Iowa, USA

    Li Wang & Matthew B. Hufford

  5. Genome Center and Center for Population Biology, University of California, Davis, 95616, California, USA

    Jeffrey Ross-Ibarra

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  1. Timothy M. Beissinger
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Contributions

T.M.B. and J.R.I. devised this study. T.M.B., L.W., J.R.-I. and K.C. analysed the data. A.D. performed early-stage simulations. T.M.B., J.R.-I. and M.B.H. wrote the manuscript.

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Correspondence to Timothy M. Beissinger or Jeffrey Ross-Ibarra.

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Beissinger, T., Wang, L., Crosby, K. et al. Recent demography drives changes in linked selection across the maize genome. Nature Plants 2, 16084 (2016). https://doi.org/10.1038/nplants.2016.84

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