Feature Article: Adaptation to a new environment allows cooperators to purge cheaters stochastically.

Molecular and Cellular Biology Program, University of Washington, Seattle, WA 98195.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 10/2012; 109(47). DOI: 10.1073/pnas.1210190109
Source: PubMed


Cooperation via production of common goods is found in diverse life forms ranging from viruses to social animals. However, natural selection predicts a "tragedy of the commons": Cheaters, benefiting from without producing costly common goods, are more fit than cooperators and should destroy cooperation. In an attempt to discover novel mechanisms of cheater control, we eliminated known ones using a yeast cooperator-cheater system engineered to supply or exploit essential nutrients. Surprisingly, although less fit than cheaters, cooperators quickly dominated a fraction of cocultures. Cooperators isolated from these cocultures were superior to the cheater isolates they had been cocultured with, even though these cheaters were superior to ancestral cooperators. Resequencing and phenotypic analyses revealed that evolved cooperators and cheaters all harbored mutations adaptive to the nutrient-limited cooperative environment, allowing growth at a much lower concentration of nutrient than their ancestors. Even after the initial round of adaptation, evolved cooperators still stochastically dominated cheaters derived from them. We propose the "adaptive race" model: If during adaptation to an environment, the fitness gain of cooperators exceeds that of cheaters by at least the fitness cost of cooperation, the tragedy of the commons can be averted. Although cooperators and cheaters sample from the same pool of adaptive mutations, this symmetry is soon broken: The best cooperators purge cheaters and continue to grow, whereas the best cheaters cause rapid self-extinction. We speculate that adaptation to changing environments may contribute to the persistence of cooperative systems before the appearance of more sophisticated mechanisms of cheater control.

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Available from: Wenying Shou
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    • "What role do adaptations to the abiotic environment, such as the observed reduction in motility, play in the co-evolutionary dynamics between cooperators and cheats? Previous work suggested that cooperative traits could hitchhike along with mutations that provide benefits outside the social context (Morgan et al., 2012; Waite & Shou, 2012; Asfahl et al., 2015). The reasoning is that in cooperative systems cheats must invade from rare, and therefore, any beneficial (nonsocial) mutation is more likely to occur among cooperators because they are more numerous. "
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    ABSTRACT: The production of beneficial public goods is common in the microbial world, and so is cheating - the exploitation of public goods by non-producing mutants. Here, we examine co-evolutionary dynamics between cooperators and cheats and ask whether cooperators can evolve strategies to reduce the burden of exploitation, and whether cheats in turn can improve their exploitation abilities. We evolved cooperators of the bacterium Pseudomonas aeruginosa, producing the shareable iron-scavenging siderophore pyoverdine, together with cheats, defective in pyoverdine production but proficient in uptake. We found that cooperators managed to co-exist with cheats in 56% of all replicates over approximately 150 generations of experimental evolution. Growth and competition assays revealed that co-existence was fostered by a combination of general adaptions to the media and specific adaptions to the co-evolving opponent. Phenotypic screening and whole-genome re-sequencing of evolved clones confirmed this pattern, and suggest that cooperators became less exploitable by cheats because they significantly reduced their pyoverdine investment. Cheats, meanwhile, improved exploitation efficiency through mutations blocking the costly pyoverdine-signalling pathway. Moreover, cooperators and cheats evolved reduced motility, a pattern that likely represents adaptation to laboratory conditions, but at the same time also affects social interactions by reducing strain mixing and pyoverdine sharing. Overall, we observed parallel evolution, where co-existence of cooperators and cheats was enabled by a combination of adaptations to the abiotic and social environment and their interactions. This article is protected by copyright. All rights reserved.
    Full-text · Article · Sep 2015 · Journal of Evolutionary Biology
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    • "The stabilizing ecological interactions could be lost , however , by the evolution of " cheaters " that do not contribute amino acids to the culture media and gain a growth advantage by using the resources for their own growth and reproduction . Waite and Shou ( 2012 ) subsequently showed that the engineered system could be maintained , despite the appearance of cheaters , " . . . if during adaptation to an environment , the fitness gain of cooperators exceeds that of cheaters by at least the fitness cost of coopera - tion . "
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    ABSTRACT: The metabolic capabilities of microbes are the basis for many major biotechnological advances, exploiting microbial diversity by selection or engineering of single strains. However, there are limits to the advances that can be achieved with single strains, and attention has turned toward the metabolic potential of consortia and the field of synthetic ecology. The main challenge for the synthetic ecology is that consortia are frequently unstable, largely because evolution by constituent members affects their interactions, which are the basis of collective metabolic functionality. Current practices in modeling consortia largely consider interactions as fixed circuits of chemical reactions, which greatly increases their tractability. This simplification comes at the cost of essential biological realism, stripping out the ecological context in which the metabolic actions occur and the potential for evolutionary change. In other words, evolutionary stability is not engineered into the system. This realization highlights the necessity to better identify the key components that influence the stable coexistence of microorganisms. Inclusion of ecological and evolutionary principles, in addition to biophysical variables and stoichiometric modeling of metabolism, is critical for microbial consortia design. This review aims to bring ecological and evolutionary concepts to the discussion on the stability of microbial consortia. In particular, we focus on the combined effect of spatial structure (connectivity of molecules and cells within the system) and ecological interactions (reciprocal and non-reciprocal) on the persistence of microbial consortia. We discuss exemplary cases to illustrate these ideas from published studies in evolutionary biology and biotechnology. We conclude by making clear the relevance of incorporating evolutionary and ecological principles to the design of microbial consortia, as a way of achieving evolutionarily stable and sustainable systems.
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    • "However, the underlying mutation was not identified. In a related study, Waite and Shou (2012) engineered a system with obligatory mutualistic cooperation between two nonmating yeast strains. The addition of an obligate cheater strain that exploits a common good shared between the two mutualistic cooperators lead to an adaptive race to either preserve cooperation or fail through population collapse. "
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    ABSTRACT: In a process termed quorum sensing (QS), the opportunistic bacterial pathogen Pseudomonas aeruginosa uses diffusible signaling molecules to regulate the expression of numerous secreted factors or public goods that are shared within the population. But not all cells respond to QS signals. These social cheaters typically harbor a mutation in the QS receptor gene lasR and exploit the public goods produced by cooperators. Here we show that non-social adaptation under growth conditions that require QS-dependent public goods increases tolerance to cheating and defers a tragedy of the commons. The underlying mutation is in the transcriptional repressor gene psdR. This mutation has no effect on public goods expression but instead increases individual fitness by derepressing growth-limiting intracellular metabolism. Even though psdR mutant populations remain susceptible to invasion by isogenic psdR lasR cheaters, they bear a lower cheater load than do wild-type populations, and they are completely resistant to invasion by lasR cheaters with functional psdR. Mutations in psdR also sustain growth near wild-type levels when paired with certain partial loss-of-function lasR mutations. Targeted sequencing of multiple evolved isolates revealed that mutations in psdR arise before mutations in lasR, and rapidly sweep through the population. Our results indicate that a QS-favoring environment can lead to adaptations in non-social, intracellular traits that increase the fitness of cooperating individuals and thereby contribute to population-wide maintenance of QS and associated cooperative behaviors.The ISME Journal (2015) 0, 000-000.advance online publication, 23 January 2015; doi:10.1038/ismej.2014.259.
    No preview · Article · Jan 2015 · The ISME Journal
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