Quorum sensing provides a molecular mechanism for evolution to tune and maintain investment in cooperation

Abstract

As selection frequently favors non-cooperating defectors in mixed populations with cooperators, mechanisms that promote cooperation stability clearly exist. One potential mechanism is bacterial cell-to-cell communication, quorum sensing (QS), which can allow cooperators to prevent invasion by defectors. However, the impact of QS on widespread maintenance of cooperation in well-mixed conditions has not been experimentally demonstrated over extended evolutionary timescales. Here, we use wild-type ( WT) Vibrio harveyi that regulates cooperation with QS and an unconditionally cooperating ( UC) mutant to examine the evolutionary origins and subsequent dynamics of novel defectors during a long-term evolution experiment. We found that UC lineages were completely outcompeted by defectors, whereas functioning QS enabled the maintenance of cooperative variants in most WT populations. Sequencing of evolved populations revealed multiple luxR mutations that swept the UC lineages. However, the evolution of mutant lineages with reduced levels of bioluminescence ( dims) occurred in many WT lineages. These dim variants also decreased other cooperative phenotypes regulated by QS, such as protease production, indicating they result from changes to QS regulation. This diminished investment phenotype optimizes a trade-off between cooperative input and growth output, allowing cooperation to be maintained under QS control even in the presence of evolved defectors.