Cheater suppression and spite through quorum sensing

The evolutionary consequences of quorum sensing in regulating bacterial cooperation are not fully understood. In this study, we reveal unexpected consequences of regulating public good production through quorum sensing on bacterial population dynamics, showing that quorum sensing can be a “spiteful” alternative to unregulated production. We analyze a birth-death model of bacterial population dynamics accounting for public good production and the presence of non-producing cheaters. Our model demonstrates that when demographic noise is a factor, the consequences of controlling public good production according to quorum sensing depend on the cost of public good production and the presence of alternative sources of the fitness benefits provided by public goods. When public good production is inexpensive, quorum sensing is a spiteful alternative to unconditional production, in terms of the mean population extinction time. When costs are higher, quorum sensing becomes a selfish strategy for the producing strain, both stabilizing cooperation and decreasing the risk of population extinction. Cooperative behavior is widespread in bacteria [1], including coordinated swarming and public good production. These behaviors are often regulated through quorum sensing (QS) [2], in which individual bacteria produce and export small molecules called autoinducers (AI). When AI molecules accumulate to a sufficiently high concentration in the environment, and consequently within the bacteria producing them, they activate operons controlling the expression of genes critical for cooperation. While the biochemistry of some QS systems is well understood [2], there are many proposed biological functions of QS which have been the subject of debate [3, 4, 5, 6, 7]. Evolutionary questions concerning QS function have largely focused on the ability of QS-controlled cooperation to combat invasion by non-cooperating cheaters in bacterial populations [8, 9]. The question of how cooperation can evolve and be maintained in populations is a general problem in evolutionary biology [10], and the role of QS in the evolution of bacterial cooperation is of great interest in understanding bacterial social interactions. A number of possible resolutions to the problem of social cheaters in bacterial public good production include punishment of cheaters [11], dispersal into subpopulations [12], and the use of QS to regulate cooperation [1, 13, 6]. Regulation of public good production through QS has been shown to reduce the ability of cheaters to invade a population of producers [14]. The role of QS in maximizing population growth in the absence of cheaters has also been investigated as a rationale for QS-control of public good production. Because public goods produced by bacteria can have density-dependent fitness benefits [15], regulation of public good production based on population density can be seen as an optimal control solution to maintaining a maximal population size balancing metabolic costs and benefits [16, 17]. By maintaining a maximal population size, a population also maximizes its mean time to extinction, which is especially important with the possibility of unpredictable environmental changes. Considering the threat of both cheater invasion and the onset of harmful environmental conditions that could lead to population extinction, there is a tension in the degree to which public good production is regulated. Unconditional public good production appears to be a self-defeating strategy, where non-producing