Cheating promotes coexistence in a two-species one-substrate culture model

Abstract

Cheating in microbial communities is often regarded as a precursor to a “tragedy of the commons,” ultimately leading to over-exploitation by a few species and destabilization of the community. While current evidence suggests that cheaters are evolutionarily and ecologically abundant, they can also play important roles in communities, such as promoting cooperative behaviors of other species. We developed a closed culture model with two microbial species and a single, complex nutrient substrate (the metaphorical “common”). One of the organisms, an enzyme producer, degrades the substrate, releasing an essential and limiting resource that it can use both to grow and produce more enzymes, but at a cost. The second organism, a cheater, does not produce the enzyme but can access the diffused resource produced by the other species, allowing it to benefit from the public good without contributing to it. We investigated evolutionarily stable states of coexistence between the two organisms and described how enzyme production rates and resource diffusion influence organism abundances. Our model shows that, in the long-term evolutionary scale, monocultures of the producer species drive themselves extinct because selection always favors mutant invaders that invest less in enzyme production, ultimately driving down the release of resources. However, the presence of a cheater buffers this process by reducing the fitness advantage of lower enzyme production, thereby preventing runaway selection in the producer, and promoting coexistence. Resource diffusion rate controls cheater growth, preventing it from outcompeting the producer. These results show that competition from cheaters can force producers to maintain adequate enzyme production to sustain both itself and the cheater. This is similar to what is known in evolutionary game theory as a “snowdrift game” – a metaphor describing a snow shoveler and a cheater following in their clean tracks. We move further to show that cheating can stabilize communities and possibly be a precursor to cooperation, rather than extinction.