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Self-destructive cooperation mediated by phenotypic noise

Nature volume 454, pages 987–990 (2008)Cite this article

Abstract

In many biological examples of cooperation, individuals that cooperate cannot benefit from the resulting public good. This is especially clear in cases of self-destructive cooperation, where individuals die when helping others. If self-destructive cooperation is genetically encoded, these genes can only be maintained if they are expressed by just a fraction of their carriers, whereas the other fraction benefits from the public good. One mechanism that can mediate this differentiation into two phenotypically different sub-populations is phenotypic noise1,2. Here we show that noisy expression of self-destructive cooperation can evolve if individuals that have a higher probability for self-destruction have, on average, access to larger public goods. This situation, which we refer to as assortment, can arise if the environment is spatially structured. These results provide a new perspective on the significance of phenotypic noise in bacterial pathogenesis: it might promote the formation of cooperative sub-populations that die while preparing the ground for a successful infection. We show experimentally that this model captures essential features of Salmonella typhimurium pathogenesis. We conclude that noisily expressed self-destructive cooperative actions can evolve under conditions of assortment, that self-destructive cooperation is a plausible biological function of phenotypic noise, and that self-destructive cooperation mediated by phenotypic noise could be important in bacterial pathogenesis.

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Figure 1: The evolutionary dynamics of stochastic self-destructive cooperation.
Figure 2: Testing biological assumptions of self-destructive cooperation mediated by phenotypic noise with a mouse model for S. typhimurium enterocolitis.

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Acknowledgements

We are grateful to Markus Schlumberger, K. Aktories, I. Just, S. Hammerschmidt and J. Fletcher for discussions, and M. Barthel and the RCHCI team for professional help with the animal experiments. M.A. and N.E.F. were supported by the Swiss National Science Foundation, and M.A. was also supported by the Roche Research Foundation and the Novartis Foundation. M.D. is supported by NSERC (Canada). B.S. and W.-D.H. were supported by the UBS foundation. Salmonella work in the Hardt laboratory is supported by grants from the ETH research foundation (TH-10 06-1), the Swiss National Science Foundation (310000-113623/1) and the European Union (SavinMucoPath number 032296).

Author Contributions M.A., W.-D.H. and M.D. formulated the question; M.A. and M.D. wrote the mathematical model; M.D. analysed the mathematical model; M.A., B.S., N.E.F. and W.-D.H. planned the experiments and interpreted the results; B.S. performed the experiments for Fig. 2b, d; P.S. performed the experiment for Fig. 2f; and M.A., W.-D.H. and M.D. wrote the manuscript.

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Authors and Affiliations

  1. Institute of Integrative Biology, ETH Zurich, 8092 Zürich, Switzerland ,

    Martin Ackermann & Nikki E. Freed

  2. Institute of Microbiology, ETH Zurich, 8093 Zürich, Switzerland ,

    Bärbel Stecher, Pascal Songhet & Wolf-Dietrich Hardt

  3. Department of Zoology and Department of Mathematics, University of British Columbia, Vancouver BC V6T 1Z4, Canada

    Michael Doebeli

Authors
  1. Martin Ackermann
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  2. Bärbel Stecher
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  3. Nikki E. Freed
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  4. Pascal Songhet
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  5. Wolf-Dietrich Hardt
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  6. Michael Doebeli
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Corresponding authors

Correspondence to Martin Ackermann, Wolf-Dietrich Hardt or Michael Doebeli.

Supplementary information

Supplementary Information

The file contains Supplementary Notes, Supplementary Figures 1-2 with Legends and additional references. Part I contains an additional mathematical analysis of the model for the evolution of self-destructive cooperation mediated by phenotypic noise. Part II contains methods and additional information on the mouse infection experiments with S. typhimurium (PDF 1037 kb)

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Ackermann, M., Stecher, B., Freed, N. et al. Self-destructive cooperation mediated by phenotypic noise. Nature 454, 987–990 (2008). https://doi.org/10.1038/nature07067

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