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  • Review Article
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Enforcement is central to the evolution of cooperation

Nature Ecology & Evolution volume 3, pages 1018–1029 (2019)Cite this article

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Matters Arising to this article was published on 10 February 2020

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Abstract

Cooperation occurs at all levels of life, from genomes, complex cells and multicellular organisms to societies and mutualisms between species. A major question for evolutionary biology is what these diverse systems have in common. Here, we review the full breadth of cooperative systems and find that they frequently rely on enforcement mechanisms that suppress selfish behaviour. We discuss many examples, including the suppression of transposable elements, uniparental inheritance of mitochondria and plastids, anti-cancer mechanisms, reciprocation and punishment in humans and other vertebrates, policing in eusocial insects and partner choice in mutualisms between species. To address a lack of accompanying theory, we develop a series of evolutionary models that show that the enforcement of cooperation is widely predicted. We argue that enforcement is an underappreciated, and often critical, ingredient for cooperation across all scales of biological organization.

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Fig. 1: The importance of enforcement is revealed by its absence at all levels of biological organization.

Jon Ågren (b); Andrea Case (c); Dave Watts/Alamy Stock Photo (d); Tom Wenseleers (e); Christian Ziegler and Charlotte Jandér (f); Nature Picture Library/Alamy Stock Photo (g)

Fig. 2: Models of enforcement across the levels of biological organization.

Lena London, used under creative commons license (Meerkats in d)

Fig. 3: The evolution of enforcement is predicted to reduce selfishness and promote cooperation across all levels of biological organization.

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  • 05 July 2019

    Owing to a technical error, for a short period of time the Published Online date displaying for the HTML version of this Review Article was incorrect as 28 June 2019; it should have read 24 June 2019. This has now been corrected. The PDF was unaffected.

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Acknowledgements

The authors thank M. Bentley, A. Bourke, J. Boomsma and S. West for discussions that were central to the project; S. Frank and two anonymous referees for thoughtful comments on the paper; and C. Jandér, A. Case, J. Ågren, and T. Wenseleers for images. J.A.Å. was supported by fellowships from the Sweden-America Foundation and the Wenner-Gren Foundations. K.R.F. is funded by European Research Council Grant 787932 and Wellcome Trust Investigator award 209397/Z/17/Z. K.R.F. also thanks D. Newman and members of the Caltech Evolution class for stimulating discussions.

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Author notes

  1. These authors contributed equally: J. Arvid Ågren, Nicholas G. Davies.

Authors and Affiliations

  1. Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY, USA

    J. Arvid Ågren

  2. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA

    J. Arvid Ågren

  3. Department of Infectious Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, UK

    Nicholas G. Davies

  4. Department of Zoology, University of Oxford, Oxford, UK

    Kevin R. Foster

  5. Department of Biochemistry, University of Oxford, Oxford, UK

    Kevin R. Foster

Authors
  1. J. Arvid Ågren
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  2. Nicholas G. Davies
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  3. Kevin R. Foster
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Contributions

All authors contributed to the writing of the article. J.A.Å. and K.R.F. conceived the article, N.G.D. and K.R.F. developed the models and N.G.D. did the analysis.

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Correspondence to Kevin R. Foster.

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Supplementary Information

Supplementary Text, Supplementary Equations, Supplementary Tables 1–3 and Supplementary Box 1

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Ågren, J.A., Davies, N.G. & Foster, K.R. Enforcement is central to the evolution of cooperation. Nat Ecol Evol 3, 1018–1029 (2019). https://doi.org/10.1038/s41559-019-0907-1

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  • DOI: https://doi.org/10.1038/s41559-019-0907-1

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