Evolution of reproduction driven by ecology at the onset of multicellularity

During the transition to multicellularity, nascent multicellular organisms evolved reproductive strategies that relied on coordinating behaviour across cells in the group. Cell-cell interactions that once occurred between independent single-celled organisms in an ecological context were integrated into the developmental programs of emerging multicellular forms. To study this transition, we developed a spatially structured evolutionary model in which cells can migrate, divide, and adhere to neighbours --- behaviours common to most unicellular eukaryotes. When coupled to a selective pressure driven by food scarcity, the model reveals how ecological interactions between single cells can give rise to multicellular reproductive programs. We show that a life cycle alternating cohesive multicellular clusters and dispersive unicellular propagules --- the most prevalent reproductive strategy in multicellular life --- evolves spontaneously as a dispersal strategy in environments where food is concentrated in patches of intermediate size. More broadly, the spatial distribution of food strongly shaped evolutionary outcomes: environments where food was homogeneously distributed favoured unicellular life cycles, while those where food was heterogeneously distributed favoured multicellular life cycles. Furthermore, we show that ancestral unicellular and multicellular life cycles were co-opted and encapsulated as phases of the reproductive programs of propagule-forming lineages during evolution. Taken together, our results highlight how ecological interactions can be repurposed to organise development during the transition to multicellularity.