A tradeoff between the ecological and evolutionary stabilities of public goods genes in microbial populations

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 cells face evolutionary competition from non-producing mutants, or " freeloaders ". Thus, public goods cooperators have to be stable not only to the invasion of freeloaders, but also to ecological perturbations that may push their numbers too small to be sustainable. Through a combination of experiments with microbial populations and mathematical analysis of the Ecological Public Goods Game, we show that game parameters and experimental conditions that improve the evolutionary stability of cooperators also lead to a low ecological stability of the cooperator population. Complex regulatory strategies mimicking those used by microbes in nature may allow cooperators to beat this eco-evolutionary stability tradeoff and become resistant to freeloaders while at the same time maximizing their ecological stability. Our results thus identify the coupled eco-evolutionary stability as being key for the long-term viability of microbial public goods cooperators.. CC-BY 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not. 2 INTRODUCTION Populations often require individuals to contribute to their maintenance. Frequently, this involves the production of " public goods " , whose costs are born by the producing individuals but whose benefits are shared by all individuals in the population [1]. Historically, cooperation has been mostly studied as an evolutionary problem. A vast body of work in the field of evolutionary game theory has been devoted to understanding the conditions that lead to the emergence and stability of cooperation, most of which involve some form of self-assortment of cooperators [2– 12]. A less appreciated but equally important aspect of social dilemmas is that cooperation may present ecological challenges [13–16]. Populations that require the expression of cooperative traits for their survival, such as the production of a public good, often require large numbers of cooperating individuals in order for the positive effects of their contributions to be significant. When population sizes are too small, the overall production of the public good may not be large enough to sustain the population. This may lead to a minimum viable population size, below which the population collapses [13]. Indeed, the presence of an Allee effect (a positive effect of population size on …