Evolution of selfish multicellularity: collective organisation of individual spatio-temporal regulatory strategies

Abstract Background The unicellular ancestors of modern-day multicellular organisms were remarkably complex. They had an extensive set of regulatory and signalling genes, an intricate life cycle and could change their behaviour in response to environmental changes. At the transition to multicellularity, some of these behaviours were co-opted to organise the development of the nascent multicellular organism. Here, we focus on the transition to multicellularity before the evolution of stable cell differentiation, to reveal how the emergence of clusters affects the evolution of cell behaviour. Results We construct a computational model of a population of cells that can evolve the regulation of their behavioural state - either division or migration - and study both a unicellular and a multicellular context. Cells compete for reproduction and for resources to survive in a seasonally changing environment. We find that the evolution of multicellularity strongly determines the co-evolution of cell behaviour, by altering the competition dynamics between cells. When adhesion cannot evolve, cells compete for survival by rapidly migrating towards resources before dividing. When adhesion evolves, emergent collective migration alleviates the pressure on individual cells to reach resources. This allows individual cells to maximise their own replication. Migrating adhesive clusters display striking patterns of spatio-temporal cell state changes that visually resemble animal development. Conclusions Our model demonstrates how emergent selection pressures at the onset of multicellularity can drive the evolution of cellular behaviour to give rise to developmental patterns.