Aggregative cycles evolve as a solution to conflicts in social investment

Author summary In aggregative multicellular life cycles, cells come together in heterogenous aggregates, whose collective function benefits all the constituent cells. Current explanations for the evolutionary stability of such organization presume that alternating phases of aggregation and dispersal are already in place. Here we propose that, instead of being externally driven, the temporal arrangement of aggregative life cycles may emerge from the interplay between ecology and evolution in populations with differential motility. In our model, cell motility underpins group formation and allows cells to forage individually and collectively. Notably, slower cells can exploit the propulsion by faster cells within multicellular groups. When the level of such exploitation is let evolve, increasing social conflicts are associated to the evolutionary emergence of self-sustained oscillations. Akin to aggregative life cycles, resource exhaustion triggers group formation, whereas conflicts within multicellular groups restrain resource consumption, thus paving the way for the subsequent unicellular phase. The evolutionary transition from equilibrium coexistence to life cycles solves conflicts among heterogenous cell types by integrating them on a timescale longer than cell division, that comes to be associated to multicellular organization. Multicellular organization is particularly vulnerable to conflicts between different cell types when the body forms from initially isolated cells, as in aggregative multicellular microbes. Like other functions of the multicellular phase, coordinated collective movement can be undermined by conflicts between cells that spend energy in fuelling motion and 'cheaters' that get carried along. The evolutionary stability of collective behaviours against such conflicts is typically addressed in populations that undergo extrinsically imposed phases of aggregation and dispersal. Here, via a shift in perspective, we propose that aggregative multicellular cycles may have emerged as a way to temporally compartmentalize social conflicts. Through an eco-evolutionary mathematical model that accounts for individual and collective strategies of resource acquisition, we address regimes where different motility types coexist. Particularly interesting is the oscillatory regime that, similarly to life cycles of aggregative multicellular organisms, alternates on the timescale of several cell generations phases of prevalent solitary living and starvation-triggered aggregation. Crucially, such self-organized oscillations emerge as a result of evolution of cell traits associated to conflict escalation within multicellular aggregates.

Automated summary

In aggregative multicellular life cycles, the temporal arrangement of aggregation phases may emerge from the interplay between ecology and evolution in populations with differential motility. Cell motility underpins group formation and slower cells can exploit faster cells within groups. Resource exhaustion triggers group formation and conflicts within groups restrain resource consumption, leading to self-sustained oscillations.