Putting theory to the test: An integrated computational/experimental chemostat model of the tragedy of the commons.

Cooperation via shared public goods is ubiquitous in nature, however, noncontributing social cheaters can exploit the public goods provided by cooperating individuals to gain a fitness advantage. Theory predicts that this dynamic can cause a Tragedy of the Commons, and in particular, a 'Collapsing' Tragedy defined as the extinction of the entire population if the public good is essential. However, there is little empirical evidence of the Collapsing Tragedy in evolutionary biology. Here, we experimentally demonstrate this outcome in a microbial model system, the public good-producing bacterium Pseudomonas aeruginosa grown in a continuous-culture chemostat. In a growth medium that requires extracellular protein digestion, we find that P. aeruginosa populations maintain a high density when entirely composed of cooperating, protease-producing cells but completely collapse when non-producing cheater cells are introduced. We formulate a mechanistic mathematical model that recapitulates experimental observations and suggests key parameters, such as the dilution rate and the cost of public good production, that define the stability of cooperative behavior. We combine model prediction with experimental validation to explain striking differences in the long-term cheater trajectories of replicate cocultures through mutational events that increase cheater fitness. Taken together, our integrated empirical and theoretical approach validates and parametrizes the Collapsing Tragedy in a microbial population, and provides a quantitative, mechanistic framework for generating testable predictions of social behavior.

Division of labor in bacterial populations.

Cooperating behaviors abound across all domains of life, but are vulnerable to invasion by cheaters. An important evolutionary question is to determine mechanisms that stabilize and maintain cooperation levels and prevent population collapse. Policing is one strategy populations may employ to achieve this goal, and it has been observed in many natural populations including microbes. Here we present and analyze a division of labor model to investigate if, when and how policing can be a cooperation-stabilizing mediator. The model represents a chemostat where cooperators produce a public good that benefits all individuals, and where toxin-producers produce a toxin that harms both cooperators and cheaters. We show that in many cases, the mere presence of toxin-producers is not enough to avoid a Tragedy of the Commons in which all individuals go extinct. The main focus of our work is to identify conditions on various model parameters which ensure that a mixed population of cooperators and toxin-producers can stably coexist and can avoid invasion by a cheater population. This happens when all of the following conditions hold: (i) The cost of policing must exceed the cost of cooperation. (ii) There is enough "collateral damage" caused by policing, i.e. the toxicity rate experienced by cooperators is sufficiently high, and (iii) The toxin affects cheaters even more than cooperators, and we provide a precise mathematical condition of how much stronger this effect should be.

Bacterial Cheaters Evade Punishment by Cyanide.

In all domains of life, mechanisms exist that protect cooperating groups from exploitation by cheaters. Recent observations with the bacterium Pseudomonas aeruginosa have suggested a paradigmatic cheater control mechanism in which cooperator cells punish or "police" cheater cells by cyanide poisoning. These cheater cells are deficient in a pleiotropic quorum-sensing regulator that controls the production of cooperative secretions including cyanide, and presumably also cyanide resistance. In this study, we directly tested and refuted the cyanide policing model. Contrary to the hypothesis, cheater fitness was unaffected by the presence of cyanide. Cheater mutants grew equally well in co-cultures with either cyanide-proficient or cyanide-deficient cooperators, and they were as resistant to exogenous cyanide as wild-type cells. We show that these behaviors are the result of quorum-sensing-independent and cyanide-responsive resistance gene regulation. Our results highlight the role of genetic architecture in the evolution of cooperative behavior.