The evolutionary maintenance of cooperative behaviors requires the suppression of exploitive strategies. It remains a challenge to identify the forces that bring this suppression and the social strategies that persist. In bacterial quorum-sensing (QS), cell-cell signaling circuits regulate the production of public goods that benefit the whole community. Many bacterial species show high levels of standing genetic variation and rapid horizontal transfer of functional QS alleles, called pherotypes, where a signal encoded by one pherotype will specifically activate its cognate receptor but not the receptor of another pherotype. Here we combine mathematical modeling with experiments and sequence analysis of the Bacillus subtilis ComQXP system to show that ComQXP has the highest level of divergence and horizontal transfer rate among core genes of this species and that both could be explained by selection for minority pherotype through exploitation of the majority pherotype. We show that in an unstructured population, both a minority pherotype and a QS null mutant invade the wild-type. QS null mutants cannot cheat the wild-type if QS regulates the production of private goods or if population structure impose high relatedness between interacting cells. We show that selection for minority pherotype will persist in structured populations owing to its facultative nature – pherotypes cheat as minority but cooperate in pure culture. In contrast, a minority pherotype will be selected against if QS regulates private goods. hese results provide a first mechanistic example for microbial facultative cheating behavior, and show how it can lead to the maintenance of high level of standing genetic variability and cooperation.
