Evolution of multicellular reproduction through co-option of ecological interactions

During the transition to multicellularity, cells evolved novel regulatory mechanisms to coordinate cell division and differentiation, which enabled the emergence of group reproduction. These mechanisms were repurposed from molecular and cellular traits that once mediated interactions between single-celled organisms. However, it remains unclear how these traits were evolutionarily integrated to form the first developmental programs in multicellular life. To address this issue, we developed a spatially structured evolutionary model in which cells can migrate, divide, and adhere to their neighbors — behaviors common to most unicellular eukaryotes. When coupled to a selective pressure driven by food scarcity, the model reveals that the ecological context plays a central role in the evolution of multi-cellular reproduction. Depending on the spatial distribution of food in the environment, both unicellular and multicellular life cycles with diverse modes of reproduction could evolve. Among these were multicellular life cycles that reproduce through unicellular propagules, the most prevalent reproductive strategy in multicellular life, which emerged spontaneously as a dispersal strategy in some environments. We show that these propagules are genetically homologous to the lineage’s unicellular ancestors, which were co-opted and repurposed as reproductive structures during evolution. Furthermore, after multicellular lineages with propagules evolved, they could colonize environments that were previously dominated by unicellular life. Altogether, our results show how ecological interactions between single cells can transform into developmental processes during the evolutionary transition towards multicellularity.