Differential Adhesion between Moving Particles as a Mechanism for the Evolution of Social Groups

Author Summary Although pervasive in the living world, collective behavior is a puzzle for evolutionary biology. The genetic traits that sustain it are costly for their carriers and make them vulnerable to the exploitation of asocial free-riders that benefit from the group without contributing to its cohesion. This paradox has spawned an extensive literature mainly concerned with elaborate cooperative behaviors that might be inoperant for simple biological entities such as microbes. We model successive life cycles of aggregation, reproduction and dispersal in a biological population combining a statistical physics approach to mimic the group formation process and an evolutionary game theory approach to account for the conflict between individual competition and collective success. Our results show a parsimonious way to the advent of sociality based on differential physical adhesion in organisms deprived of complex cognitive abilities. We also stress the key role of ungrouped individuals and specify the conditions on motion properties that make sociality possible. In detailing a mechanism akin to promote social behavior in microbes in the absence of genealogical relatedness, our work might shed light on both the maintenance of facultative multicellular lifestyles and the evolutionary origins of multicellularity. The evolutionary stability of cooperative traits, that are beneficial to other individuals but costly to their carrier, is considered possible only through the establishment of a sufficient degree of assortment between cooperators. Chimeric microbial populations, characterized by simple interactions between unrelated individuals, restrain the applicability of standard mechanisms generating such assortment, in particular when cells disperse between successive reproductive events such as happens in Dicyostelids and Myxobacteria. In this paper, we address the evolutionary dynamics of a costly trait that enhances attachment to others as well as group cohesion. By modeling cells as self-propelled particles moving on a plane according to local interaction forces and undergoing cycles of aggregation, reproduction and dispersal, we show that blind differential adhesion provides a basis for assortment in the process of group formation. When reproductive performance depends on the social context of players, evolution by natural selection can lead to the success of the social trait, and to the concomitant emergence of sizeable groups. We point out the conditions on the microscopic properties of motion and interaction that make such evolutionary outcome possible, stressing that the advent of sociality by differential adhesion is restricted to specific ecological contexts. Moreover, we show that the aggregation process naturally implies the existence of non-aggregated particles, and highlight their crucial evolutionary role despite being largely neglected in theoretical models for the evolution of sociality.