Heterogeneous individual motility biases group composition in a model of aggregating cells

Abstract

Aggregative life cycles are characterized by alternating phases of unicellular growth and multicellular development. Their multiple, independent evolutionary emergence suggests that they may have coopted pervasive properties of single-celled ancestors. Primitive multicellular aggregates, where coordination mechanisms were less efficient than in extant aggregative microbes, must have faced high levels of conflict between different co-aggregating populations. Such conflicts within a multicellular body manifest in the differential reproductive output of cells of different types. Here, we study how heterogeneity in cell motility affects the aggregation process and creates a mismatch between the composition of the population and that of self-organized groups of active adhesive particles. We model cells as self-propelled particles and describe aggregation in a plane starting from a dispersed configuration. Inspired by the life cycle of aggregative model organisms such as Dictyostelium discoideum or Myxococcus xanthus, whose cells interact for a fixed duration before the onset of chimeric multicellular development, we study finite-time configurations for identical particles and in binary mixes. We show that co-aggregation results in three different types of frequency-dependent biases, one of which is associated to evolutionarily stable coexistence of particles with different motility. We propose a heuristic explanation of such observations, based on the competition between delayed aggregation of slower particles and detachment of faster particles. Unexpectedly, despite the complexity and non-linearity of the system, biases can be largely predicted from the behavior of the two corresponding homogenous populations. This model points to differential motility as a possibly important factor in driving the evolutionary emergence of facultatively multicellular life-cycles.