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Self-destructive cooperation mediated by phenotypic noise

Author

Listed:
  • Martin Ackermann

    (Institute of Integrative Biology, ETH Zurich, 8092 Zürich, Switzerland)

  • Bärbel Stecher

    (Institute of Microbiology, ETH Zurich, 8093 Zürich, Switzerland)

  • Nikki E. Freed

    (Institute of Integrative Biology, ETH Zurich, 8092 Zürich, Switzerland)

  • Pascal Songhet

    (Institute of Microbiology, ETH Zurich, 8093 Zürich, Switzerland)

  • Wolf-Dietrich Hardt

    (Institute of Microbiology, ETH Zurich, 8093 Zürich, Switzerland)

  • Michael Doebeli

    (University of British Columbia)

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.

Suggested Citation

  • Martin Ackermann & Bärbel Stecher & Nikki E. Freed & Pascal Songhet & Wolf-Dietrich Hardt & Michael Doebeli, 2008. "Self-destructive cooperation mediated by phenotypic noise," Nature, Nature, vol. 454(7207), pages 987-990, August.
    • Handle: RePEc:nat:nature:v:454:y:2008:i:7207:d:10.1038_nature07067
    DOI: 10.1038/nature07067
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    Cited by:

    1. Manalee Vishnu Surve & Smita Bhutda & Akshay Datey & Anjali Anil & Shalini Rawat & Athira Pushpakaran & Dipty Singh & Kwang Sik Kim & Dipshikha Chakravortty & Anirban Banerjee, 2018. "Heterogeneity in pneumolysin expression governs the fate of Streptococcus pneumoniae during blood-brain barrier trafficking," PLOS Pathogens, Public Library of Science, vol. 14(7), pages 1-29, July.
    2. Si Tang & Yaqing Liu & Jianming Zhu & Xueyu Cheng & Lu Liu & Katrin Hammerschmidt & Jin Zhou & Zhonghua Cai, 2024. "Bet hedging in a unicellular microalga," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Te Wu & Long Wang & Feng Fu, 2017. "Coevolutionary dynamics of phenotypic diversity and contingent cooperation," PLOS Computational Biology, Public Library of Science, vol. 13(1), pages 1-16, January.
    4. Karl P. Gerhardt & Satyajit D. Rao & Evan J. Olson & Oleg A. Igoshin & Jeffrey J. Tabor, 2021. "Independent control of mean and noise by convolution of gene expression distributions," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    5. Maxime Batsch & Isaline Guex & Helena Todorov & Clara M. Heiman & Jordan Vacheron & Julia A. Vorholt & Christoph Keel & Jan Roelof van der Meer, 2024. "Fragmented micro-growth habitats present opportunities for alternative competitive outcomes," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    6. Peña, Jorge & Cooper, Guy Alexander & Liu, Ming & West, Stuart Andrew, 2020. "Dividing labour in social microorganisms: coordinated or random specialisation?," IAST Working Papers 20-104, Institute for Advanced Study in Toulouse (IAST).
    7. Jan J. Kreider & Thijs Janzen & Abel Bernadou & Daniel Elsner & Boris H. Kramer & Franz J. Weissing, 2022. "Resource sharing is sufficient for the emergence of division of labour," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    8. Czuppon, Peter & Gokhale, Chaitanya S., 2018. "Disentangling eco-evolutionary effects on trait fixation," Theoretical Population Biology, Elsevier, vol. 124(C), pages 93-107.
    9. Patrick Kaiser & Emma Slack & Andrew J Grant & Wolf-Dietrich Hardt & Roland R Regoes, 2013. "Lymph Node Colonization Dynamics after Oral Salmonella Typhimurium Infection in Mice," PLOS Pathogens, Public Library of Science, vol. 9(9), pages 1-12, September.
    10. Anne-Stéphanie Rueff & Renske Raaphorst & Surya D. Aggarwal & Javier Santos-Moreno & Géraldine Laloux & Yolanda Schaerli & Jeffrey N. Weiser & Jan-Willem Veening, 2023. "Synthetic genetic oscillators demonstrate the functional importance of phenotypic variation in pneumococcal-host interactions," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    11. Peña, Jorge & Nöldeke, Georg & Lehmann, Laurent, 2014. "Relatedness and synergies of kind and scale in the evolution of helping," Working papers 2014/09, Faculty of Business and Economics - University of Basel.

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