Evolutionary stability of social commitment

The social amoeba Dictyostelium discoideum switches between the phase of solitary growth and social fruitification depending on nutrient availability. Under non-nutrient conditions, cells enter the social phase where they aggregate and differentiate to form fruiting bodies consisting of spores on top of non-viable altruistic stalk cells. Once cells aggregate, they complete fruiting body formation even with a renewed source of nutrients. This social commitment is puzzling because it deprives individual cells of the benefits of quickly resuming solitary growth. One idea posits that traits that facilitate premature dedifferentiation in response to nutrient recovery are somehow hindered from being selected in a social context. In this study, we studied the outcomes of premature dedifferentiation by forced refeeding. We show that when refed cells were allowed to resume sociality together with non-refed cells, besides some successfully becoming solitary outside of fruiting bodies, a large fraction was redirected to a sub-region of altruistic stalk regardless of their original cell fate. The lower cohesiveness of prestalk cells relative to prespore cells and comparably reduced cohesivity in refed cells was consistent with the redirection. Furthermore, application of a game theoretical model, which describes fruiting body formation among cells with differences in cell-cell association strategies, revealed a valley in the fitness landscape that prevents the invasion of mutants with the ability to dedifferentiate completely into a socially committed population. Our results provide a general scheme that naturally penalizes withdrawal from a society by evolving a specific division of labor such that less cohesive individuals become altruists. Significance Statement Evolution of unicellular to multicellular organisms must resolve conflicts of reproductive interests between individual cells and the group. In the social amoeba Dictyostelium, a transition from a solitary to multicellular group occurs under starvation. Once cells commit themselves to multicellular organization, the process continues even when shifting to an environment that favors solitary growth. Our study revealed that cells forced to partially revert to a de-committed state take an altruistic role through interaction with socially committed cells. The de-committed cells exhibited reduced cohesivity and were sorted out to altruistic positions in morphogenesis. This inevitably penalizes ‘selfish’ cells that revert to solitary growth too quickly. Our results explain group-level behaviors that is apparently difficult to understand from an individual-level fitness.