Social Evolution Selects for Redundancy in Bacterial Quorum Sensing

Quorum sensing is a process of chemical communication that bacteria use to monitor cell density and coordinate cooperative behaviors. Quorum sensing relies on extracellular signal molecules and cognate receptor pairs. While a single quorum-sensing system is sufficient to probe cell density, bacteria frequently use multiple quorum-sensing systems to regulate the same cooperative behaviors. The potential benefits of these redundant network structures are not clear. Here, we combine modeling and experimental analyses of the Bacillus subtilis and Vibrio harveyi quorum-sensing networks to show that accumulation of multiple quorum-sensing systems may be driven by a facultative cheating mechanism. We demonstrate that a strain that has acquired an additional quorum-sensing system can exploit its ancestor that possesses one fewer system, but nonetheless, resume full cooperation with its kin when it is fixed in the population. We identify the molecular network design criteria required for this advantage. Our results suggest that increased complexity in bacterial social signaling circuits can evolve without providing an adaptive advantage in a clonal population.The accumulation of multiple, seemingly redundant, bacterial quorum-sensing systems is promoted by facultative cheating behavior; the strain with multiple systems cheats its single quorum-sensing system ancestor as a minority but returns to cooperation when in the majority.Author Summary: Quorum sensing is a mechanism through which bacteria communicate by producing, releasing, and detecting signal molecules encoding information about cell population density. Quorum sensing allows bacteria to synchronize their behaviors and act as collectives. Often, quorum sensing controls cooperative behaviors that benefit the entire community, such as the production and secretion of costly metabolites. Some bacteria release multiple signal molecules which, once detected, funnel information into the same cellular response. Thus, the benefit of using multiple rather than a single signal is mysterious since the signals seem redundant. Here, we combine modeling and experiments to show that the evolutionary accumulation of multiple quorum-sensing systems can be attributed to social exploitation and kin recognition. When in low abundance, a strain that has acquired an additional quorum-sensing system can avoid cooperating and can exploit its ancestor strain, which contains one less quorum-sensing system. The cheater containing the additional system returns to a cooperative behavior when it is abundant. We also identify the molecular mechanisms necessary for the acquisition of an additional signaling system. Our work demonstrates that increased complexity in bacterial social signaling circuits can evolve without providing an adaptive advantage in a clonal population.