Feedback between population and evolutionary dynamics determines the fate of social microbial populations

Abstract

The evolutionary spread of cheater strategies can destabilize populations engaging in cooperative behaviors, thus demonstrating that evolutionary changes can have profound implications for populations dynamics. At the same time, the relative fitness of cooperative traits often depends upon population density, thus leading to the potential for bidirectional coupling between population density and the evolution of a cooperative trait. Despite the potential importance of these eco evolutionary feedback loops, they have not yet been demonstrated experimentally in social species and their ecological implications are poorly understood. Here, we demonstrate the presence of a strong feedback loop between population dynamics and the evolutionary dynamics of a social microbial gene, SUC2, in laboratory yeast populations whose cooperative growth is mediated by the SUC2 gene. We directly visualize eco evolutionary trajectories of hundreds of populations over fifty generations, allowing us to characterize the phase space describing the interplay of evolution and ecology in this system. Small populations collapse despite continual evolution towards increased cooperative allele frequencies; large populations with a sufficient number of cooperators spiral to a stable state of coexistence between cooperator and cheater strategies. The presence of cheaters does not significantly affect the equilibrium population density, but it does reduce the resilience of the population as well as its ability to adapt to a rapidly deteriorating environment. Our results demonstrate the potential ecological importance of coupling between evolutionary dynamics and the population dynamics of cooperatively growing organisms, particularly in microbes.