Cooperators trade off ecological resilience and evolutionary stability in public goods games

Abstract

Microbial populations often rely on the cooperative production of extracellular ‘public goods’ molecules. The cooperative nature of public good production may lead to minimum viable population sizes, below which populations collapse. In addition, ‘cooperator’ public goods producing individuals face evolutionary competition from non-producing mutants, or ‘freeloaders’. Thus, public goods cooperators should be resilient not only to the invasion of freeloaders, but also to ecological perturbations that may push their populations below a sustainable threshold. Through a mathematical analysis of the Ecological Public Goods Game, we show that game parameters that improve the cooperating population's stability to freeloader invasion also lead to a low ecological resilience. Complex regulatory strategies mimicking those used by microbes in nature may allow cooperators to beat this trade-off and become evolutionarily stable to invading freeloaders while at the same time maximizing their ecological resilience. Our results thus identify the coupling between resilience to evolutionary and ecological challenges as a key factor for the long-term viability of public goods cooperators.

Artificially selecting bacterial communities using propagule strategies†

“…For both of these experiments, it is reasonable to speculate that an improvement in the community-level function is likely to align against selection at the individual (cellular) level. For instance, a mutant with a higher amylase production than its ancestor may engage in an ecological public-goods evolutionary game (Hauert et al 2006;Hauert et al 2008;Rauch et al 2017), and be selected against due to the higher cost of amylase production (West et al 2006;Harrington and Sanchez 2014). In the second experiment, mutants that are capable of using the metabolic byproducts secreted by other species in their community would have a growth advantage, by being able to expand into open niches.…”

“…A second important challenge was pointed out by Goldman and Brown: engineered functions in synthetic consortia can be affected both by ecological processes (e.g., invasions, species extinctions, and population dynamics) as well as by rapid evolution within the community (Goldman and Brown 2009;Escalante et al 2015). As a result, a microbial consortium that is engineered to carry out a desired function must be also designed to be both evolutionarily and ecologically stable (a problem that is far from trivial [Shade et al 2012;Rauch et al 2017]), if we want that function to be stable over time.…”

Tragedy of the commons in the chemostat

“…We note that this model does not explicitly model nutrients, nor the way in which the public goods chemically interact with the organisms, whereas these processes are explicitly modeled in our model. In another recent paper [ 37 ], the tradeoff between the population’s resilience to ecological perturbations that may induce population collapse via Allee effects, and its resistance to cheater invasion is investigated in the context of an Ecological Public Goods Game. Whereas low population numbers promote cooperative behavior, they may lead to population collapse due to ecological perturbations; on the other hand, high population numbers provide a buffer to ecological perturbations, but invite invasion by cheaters.…”

Artificially selecting microbial communities using propagule strategies

“…For both of these experiments, it is reasonable to speculate that an improvement in the community-level function is likely to align against selection at the individual (cellular) level. For instance, a mutant with a higher amylase production than the ancestral population may engage in an ecological public-goods evolutionary game (Hauert et al 2006(Hauert et al , 2008Rauch et al 2017) , and be selected against due to the higher cost of amylase production (West et al 2006;Harrington and Sanchez 2014) . Similarly, in the second experiment, mutants that appear in a population which are capable of using the metabolic byproducts secreted by other species in the community may in principle have a growth advantage, by being able to expand into open niches.…”