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Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

Significance The evolution of cooperation is a central issue in biology and the social sciences. Study of model systems of social microbes has focused on how “cooperators” and “cheats” interact but rarely accounts for the surrounding environment. We demonstrate how environmental stress in the form of antibiotics alters the evolution of public goods cooperation in a bacterium. Antibiotics accentuate the costs to cooperators, resulting in their rapid demise relative to cheats. In a more applied vein, antibiotic resistance was maximal in the presence of both producers and cheats, suggesting that knowledge about social strategies can be used to improve therapies. Our work emphasizes ecoevolutionary feedback in social evolution and demonstrates that social interactions may be considerably modified in natural, stressful environments. Cheats are a pervasive threat to public goods production in natural and human communities, as they benefit from the commons without contributing to it. Although ecological antagonisms such as predation, parasitism, competition, and abiotic environmental stress play key roles in shaping population biology, it is unknown how such stresses generally affect the ability of cheats to undermine cooperation. We used theory and experiments to address this question in the pathogenic bacterium, Pseudomonas aeruginosa. Although public goods producers were selected against in all populations, our competition experiments showed that antibiotics significantly increased the advantage of nonproducers. Moreover, the dominance of nonproducers in mixed cultures was associated with higher resistance to antibiotics than in either monoculture. Mathematical modeling indicates that accentuated costs to producer phenotypes underlie the observed patterns. Mathematical analysis further shows how these patterns should generalize to other taxa with public goods behaviors. Our findings suggest that explaining the maintenance of cooperative public goods behaviors in certain natural systems will be more challenging than previously thought. Our results also have specific implications for the control of pathogenic bacteria using antibiotics and for understanding natural bacterial ecosystems, where subinhibitory concentrations of antimicrobials frequently occur.