Abstract

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.

Highlights

  • Multicellular life cycles have evolved multiple times during the history of life

  • Current explanations for the evolutionary stability of such organization presume that alternating phases of aggregation and dispersal are already in place

  • 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

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Summary

Introduction

Multicellular life cycles have evolved multiple times during the history of life. Their emergence is believed to follow from general mechanistic principles, rather than from rare fortuitous events that took place in a single lineage [1, 2]. For D. discoideum, several options have been proposed [12], that range from biasing the composition of the multicellular groups [4, 13], to modulating the individual investment in response to group composition [14, 15]. These game-theoretical explanations only focus on one specific phase of the life cycle, while they disregard the mechanisms that enable such phase to occur repeatedly. The time scale associated to the life cycle was extrinsically imposed and requires an appropriate source of environmental variation—for instance the day-night cycle—prior to the emergence of subsequent adaptations

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