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

Background/Question/Methods

Social species that rely on the cooperative production of public goods may be challenged by the evolutionary emergence of “free-rider” individuals, which take advantage of the public goods but do not contribute to their production. We sought to investigate the ecological consequences of the evolutionary competition between cooperators and free-rider individuals in experimental laboratory populations of budding yeast (S. cerevisiae). These populations grow in the sugar sucrose by collectively degrading it into glucose and fructose, which are then shared by all cells in the population. By using high throughput culturing and analysis methods, we have simultaneously tracked the evolutionary dynamics of the social gene responsible for public goods production, as well as the total population size for hundreds of independent populations. We mapped the joint eco-evolutionary dynamics on the eco-evolutionary phase space formed by the frequency of the cooperative gene and the total population size. These phase diagrams were obtained at different environmental qualities characterized by a higher or lower death rate. This allowed us to inquire about bifurcations in our system, and how the eco-evolutionary dynamics behave near critical points.

Results/Conclusions

Visual inspection of the trajectories on the phase diagrams reveals a striking behavior:  trajectories either spiral towards an eco-evolutionary equilibrium vortex, or go to extinction depending on their starting point in the phase diagram. We determined all of the eco-evolutionary fixed points, as well as their stability. By analyzing our phase diagrams, we found that invasion of a pure cooperator population by free-riders does not lead to population collapse, but it significantly reduces the resilience of the population to perturbations. We determined the phase diagram for different environmental qualities (death-rates) and found that, surprisingly, the size of the sub-population of cooperative individuals in equilibrium increases with the death rate, up until a critical point where the death-rate becomes too large and the whole population collapses. By linearizing the trajectories on the phase diagram, we determined the characteristic eigenvalues of the eco-evolutionary dynamics around equilibrium. We found that as the death-rate approaches its critical value, the collective ecosystem dynamics –as characterized by the absolute magnitude of the eigenvalue, slows down. In addition, demographic noise increases dramatically as the death rate approaches its critical value, providing an early warning indicator of ecosystem collapse.