Molecular and regulatory properties of a public good shape the evolution of cooperation

Public goods cooperation abounds in nature, occurring in organisms ranging from bacteria to humans. Although previous research focused on the behavioral and ecological conditions favoring cooperation, the question of whether the molecular and regulatory properties of the public good itself can influence selection for cooperation has received little attention. Using a metapopulation model, we show that extended molecular durability of a public good—allowing multiple reuse across generations—greatly reduces selection for cheating if (and only if) the production of the public good is facultatively regulated. To test the apparent synergy between public goods durability and facultative regulation, we examined the production of iron-scavenging pyoverdin molecules by the bacterium Pseudomonas aeruginosa, a cooperative behavior that is facultatively regulated in response to iron availability. We show that pyoverdin is a very durable public good and that extended durability significantly enhances fitness. Consistent with our model, we found that nonsiderophore-producing mutants (cheats) had a relative fitness advantage over siderophore producers (cooperators) when pyoverdin durability was low but not when durability was high. This was because cooperators facultatively reduced their investment in pyoverdin production when enough pyoverdin had accumulated in the media—a cost-saving strategy that minimized the ability of cheats to invade. These findings show how molecular properties of cooperative acts can shape the costs and benefits of cooperation.