1. Institute of Integrative Biology, ETH Zurich, 8092 Zürich, Switzerland
2. Institute of Microbiology, ETH Zurich, 8093 Zürich, Switzerland
3. Department of Zoology and Department of Mathematics, University of British Columbia, Vancouver BC V6T 1Z4, Canada

Correspondence to: Martin Ackermann¹Wolf-Dietrich Hardt²Michael Doebeli³ Correspondence and requests for materials should be addressed to M.A. (Email: martin.ackermann@env.ethz.ch), W.-D.H. (Email: hardt@micro.biol.ethz.ch) or M.D. (Email: doebeli@zoology.ubc.ca).

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 noise^{1, 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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