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Evidence of long-term gene flow and selection during domestication from analyses of Eurasian wild and domestic pig genomes

Nature Genetics volume 47, pages 11411148 (2015) | Download Citation

Abstract

Traditionally, the process of domestication is assumed to be initiated by humans, involve few individuals and rely on reproductive isolation between wild and domestic forms. We analyzed pig domestication using over 100 genome sequences and tested whether pig domestication followed a traditional linear model or a more complex, reticulate model. We found that the assumptions of traditional models, such as reproductive isolation and strong domestication bottlenecks, are incompatible with the genetic data. In addition, our results show that, despite gene flow, the genomes of domestic pigs have strong signatures of selection at loci that affect behavior and morphology. We argue that recurrent selection for domestic traits likely counteracted the homogenizing effect of gene flow from wild boars and created 'islands of domestication' in the genome. Our results have major ramifications for the understanding of animal domestication and suggest that future studies should employ models that do not assume reproductive isolation.

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European Nucleotide Archive

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Acknowledgements

We thank B. Peter for his help and guidance during the model-fitting step of the analysis as well as for kindly sharing his code. We are also indebted to D. Wegmann for providing us with the latest version of ABCtoolbox. We also thank K. Lohse for his insights during the conception of the project and D. Caspani for his help with the figures. We thank B. Dibbits for his help during the laboratory work. This project is financially supported by the European Research Council under the European Community's 256 Seventh Framework Programme (FP7/2007–2013)/ERC (SelSweep), grant agreements 249894 and ERC-2013-StG 337574-UNDEAD. J.G.S. was supported by US National Institutes of Health grant R01-GM40282 and National Science Foundation postdoctoral fellowship DBI-1402120.

Author information

Affiliations

  1. Animal Breeding and Genomics Group, Wageningen University, Wageningen, the Netherlands.

    • Laurent A F Frantz
    • , Ole Madsen
    • , Hendrik-Jan Megens
    • , Mirte Bosse
    • , Yogesh Paudel
    • , Richard P M A Crooijmans
    •  & Martien A M Groenen
  2. Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, UK.

    • Laurent A F Frantz
    •  & Greger Larson
  3. Department of Integrative Biology, University of California, Berkeley, Berkeley, California, USA.

    • Joshua G Schraiber
  4. Department of Genome Sciences, University of Washington, Seattle, Washington, USA.

    • Joshua G Schraiber
  5. Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

    • Alex Cagan

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Contributions

M.A.M.G., L.A.F.F. and G.L. designed the study. R.P.M.A.C. provided the samples. L.A.F.F., H.-J.M., O.M., M.B. and Y.P. aligned and filtered the data. L.A.F.F. and J.G.S. performed the modeling. L.A.F.F., J.G.S. and A.C. performed the selection scan. L.A.F.F., J.G.S., G.L. and M.A.M.G. wrote the manuscript with input from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Laurent A F Frantz.

Integrated supplementary information

Supplementary information

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  1. 1.

    Supplementary Text and Figures

    Supplementary Figures 1–11, Supplementary Tables 4–6 and Supplementary Note.

Excel files

  1. 1.

    Supplementary Table 1

    List of samples used in this study.

  2. 2.

    Supplementary Table 2

    Support for each model in Supplementary Figure 3.

  3. 3.

    Supplementary Table 3

    Prior and posterior distributions for the full model. All population size (N) and migration rate (m) parameters are in log scale. All other models (Supplementary Fig. 3) use the same prior bound. RMSE is the root mean square error. P_value_KS corresponds to the P value of the Kolomogorov-Smirnov test of uniformity of the posterior quantiles (see “Validation of ABC procedure” in the Supplementary Note).

  4. 4.

    Supplementary Table 7

    List of genes with GO term enrichment (P < 0.01) in sweep regions in EUD.

  5. 5.

    Supplementary Table 8

    List of genes with GO term enrichment (P < 0.01) in sweep regions in ASD.

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DOI

https://doi.org/10.1038/ng.3394

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