Ecological significance of imperfectly synchronized collective behaviors*

Loners, individuals out-of-sync with a coordinated majority, occur frequently in nature. But are loners incidental byproducts of the large-scale coordinated behavior or are they part of a mosaic of life-history strategies? To address this question, we provide empirical evidence of naturally occurring heritable variation in loner behavior in the model social amoeba Dictyostelium discoideum. We propose that Dictyostelium loners—cells that do not join the multicellular life stage— arise from a dynamic population-partitioning process, the result of each cell making a stochastic, signal-based decision. Finally, we predict theoretically that when a pair of Dictyostelium strains differing in their partitioning behavior co-aggregate, cross-signaling impacts slime-mold diversity across spatiotemporal scales. Our findings suggest that loners could be critical to understanding collective and social behaviors, multicellular development, and ecological dynamics in D. discoideum. More broadly, across taxa, imperfect coordination of collective behaviors might be adaptive by enabling diversification of life-history strategies.