Abstract
Cooperation in biological, social, and economic groups is underpinned by public goods that are generated by group members at some personal cost. Theory predicts that public goods will be exploited by cheaters who benefit from the goods by not paying for them, thereby leading to the collapse of cooperation. This situation, described as the "public goods dilemma" in game theory, makes the ubiquity of cooperation a major evolutionary puzzle. Despite this generalization, the demonstration of genetic background and fitness effects of the public goods dilemma has been limited to interactions between viruses and between cells, and thus its relevance at higher levels of organismal complexity is still largely unexplored. Here we provide experimental evidence for the public goods dilemma in a social insect, the ant Pristomyrmex punctatus. In this species, all workers are involved in both asexual reproduction and cooperative tasks. Genetic cheaters infiltrate field colonies, reproducing more than the workers but shunning cooperative tasks. In laboratory experiments, cheaters outcompeted coexisting workers in both survival and reproduction, although a group composed only of cheaters failed to produce offspring. The operations of the public goods dilemma in P. punctatus showed a remarkable convergence with those in microbial societies, not only in fitness consequences but also in behavioral mechanisms. Our study reinforces the evolutionary impact of cheaters on diverse cooperative systems in the laboratory and in the field.