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Abstract: Collective behaviors, in which many individuals exhibit some degree of behavioral coordination, are frequent in nature and observed across a continuum of scales, from microbial aggregates to ungulate migrations. Intriguingly, however, such coordination is sometimes imperfect, and “out-of-sync” individuals exist in many of these systems. For example, in the model social amoeba Dictyostelium discoideum, free-living cells aggregate in a multicellular fruiting body upon starvation, while others remain in the unicellular phase. In several ungulate species, hundreds of thousands of individuals coordinate with each other to migrate across seasonal ranges, but resident populations that do not follow the migration also exist. The roots of such imperfect coordination, and hence the mechanisms underlying the emergence of out-of-sync individuals, will undoubtedly differ across systems. Nevertheless, the occurrence of imperfect coordination across such different systems and scales raises fundamental questions about its causes and consequences. Are “out-of-sync” individuals merely inevitable byproducts of large-scale coordination attempts, or can they, at least in some systems, be a variable trait that selection can shape with potential ecological consequences?
I will address this question by combining empirical data on D.discoideum imperfect aggregation and observed patterns of partial migration observed within three ungulate species. In each of these systems, we find that the number of individuals that do not engage in the collective behavior is unrelated to the total population size, suggesting that a complex individual decision-making process underlies the onset of the collective behavior. Using a minimalistic modeling framework, we propose that imperfectly synchronized collective behaviors are, in fact, a dynamic population partition process that originates from each individual making a stochastic signal-based decision. The parallelisms between these two seemingly different systems suggest that imperfectly synchronized collective behaviors could be critical to understanding social behaviors and ecological dynamics across scales. More broadly, these results suggest that, across taxa, imperfect coordination of collective behaviors might be adaptive by enabling the diversification of life-history strategies.