Seasonality can induce coexistence of multiple bet-hedging strategies in Dictyostelium discoideum via storage effect

The social amoeba Dictyostelium discoideum has been recently suggested as an example of bet-hedging in microbes. In the presence of resources, amoebae reproduce as unicellular organisms. Resource depletion, however, leads to a starvation phase in which the population splits between aggregators, which form a fruiting body made of a stalk and resistant spores, and non-aggregators, which remain as vegetative cells. Spores are favored when starvation periods are long, but vegetative cells can exploit resources in environments where food replenishes quickly. The investment in aggregators versus non-aggregators can therefore be understood as a bet-hedging strategy that evolves in response to stochastic starvation times. A genotype (or strategy) is defined by the balance between each type of cells. In this framework, if the ecological conditions on a patch are defined in terms of the mean starvation time (i.e. time between the onset of starvation and the arrival of a new food pulse), a single genotype dominates each environment, which is inconsistent with the huge genetic diversity observed in nature. Here we investigate whether seasonality, represented by a periodic, wet-dry alternation in the mean starvation times, allows the coexistence of several strategies in a single patch. We study this question in a non-spatial (well-mixed) setting in which different strains compete for a common pool of resources over a sequence of growth-starvation cycles. We find that seasonality induces a temporal storage effect that can promote the stable coexistence of multiple genotypes. Two conditions need to be met in our model. First, there has to be a temporal niche partitioning (two well-differentiated habitats within the year), which requires not only different mean starvation times between seasons but also low variance within each season. Second, each season's well-adapted strain has to grow and create a large enough population that permits its survival during the subsequent unfavorable season, which requires the number of growth-starvation cycles within each season to be sufficiently large. These conditions allow the coexistence of two bet-hedging strategies. Additional tradeoffs among life-history traits can expand the range of coexistence and increase the number of coexisting strategies, contributing toward explaining the genetic diversity observed in D. discoideum. Although focused on this cellular slime mold, our results are general and may be easily extended to other microbes.