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Facultative cheating supports the coexistence of diverse quorum-sensing alleles

Significance Bacteria cooperate by secretion of public good molecules, which benefit the entire community. Such cooperative behaviors are often regulated by cell–cell signaling mechanisms. In many species, these signaling systems are highly diversified in their signal–receptor specificity, but the causal link between the function of signaling and the maintenance of high genetic diversity was unclear. Here we demonstrate experimentally that signaling diversity is maintained by facultative cheating—a minority strain with one signaling system will exploit the public goods production of a majority strain that possesses a different system, but resumes cooperation on its own. Mutual facultative cheating demonstrates the complexity of social strategies attained by bacteria through the regulation of cooperative behaviors and their impact on population genetics parameters. Bacterial quorum sensing enables bacteria to cooperate in a density-dependent manner via the group-wide secretion and detection of specific autoinducer molecules. Many bacterial species show high intraspecific diversity of autoinducer–receptor alleles, called pherotypes. The autoinducer produced by one pherotype activates its coencoded receptor, but not the receptor of another pherotype. It is unclear what selection forces drive the maintenance of pherotype diversity. Here, we use the ComQXPA system of Bacillus subtilis as a model system, to show that pherotype diversity can be maintained by facultative cheating—a minority pherotype exploits the majority, but resumes cooperation when its frequency increases. We find that the maintenance of multiple pherotypes by facultative cheating can persist under kin-selection conditions that select against “obligate cheaters” quorum-sensing response null mutants. Our results therefore support a role for facultative cheating and kin selection in the evolution of quorum-sensing diversity.