The key role of cheaters in the persistence of cooperation.

Unlabelled: Evolution of cooperation is a major, extensively studied problem in evolutionary biology. Cooperation is beneficial for a population as a whole but costly for the bearers of social traits such that cheaters enjoy a selective advantage over cooperators. Here we focus on coevolution of cooperators and cheaters in a multi-level selection framework, by modeling competition among groups composed of cooperators and cheaters. Cheaters enjoy a reproductive advantage over cooperators at the individual level, independent of the presence of cooperators in the group. Cooperators carry a social trait that provides a fitness advantage to the respective groups. In the case of absolute fitness advantage, where the survival probability of a group is independent of the composition of other groups, the survival of cooperators does not correlate with the presence of cheaters. By contrast, in the case of relative fitness advantage, where the survival probability of a group depends on the composition of all groups, the survival of cooperators positively correlates with the presence of cheaters. Increasing the strength of the social trait alone fails to ensure survival of cooperators, and the increase of the reproduction advantage of the cheaters is necessary to avoid population extinction. We validate these theoretical results with an agent-based model of a bacterial biofilm where emergence of the cooperative trait is facilitated by the presence of cheaters, leading to evolution of spatial organization. This finding contrasts the classical view that spatial organization facilitates cooperation. Our results suggest that, counterintuitively, cheaters often promote, not destabilize, evolution of cooperation.

Significance: Cooperation is central to the evolution of life and the emergence of multicellularity. Social traits stabilize populations against environmental volatility and enable division of labor. However, evolution of cooperation is beset by cheaters that benefit from cooperation without paying the cost. Analysis of a multilevel selection model of population evolution shows that, counterintuitively, the presence of cheaters can be beneficial or even essential for the survival of cooperators. This unexpected effect comes from multilevel selection whereby cheaters at the individual level become altruists at the group level, enabling overall growth of the population that is essential for the persistence of cooperators. These findings have broad implications for understanding the emergence of cooperation and host-parasite coevolution throughout the history of life.