Evolution of reproduction driven by ecology at the onset of multicellularity

Abstract

At the origin of multicellularity, genetic programs used by single-celled organisms to interact with their environment become organised into a developmental program. While previous work has clarified the selective advantages of simple multicellularity, the origin of development remains unclear. Here, we investigate the ecological origin of a fundamental developmental process -- multicellular reproduction -- using a computational model where cells forage in a structured environment, and evolve adhesion and regulated environmental responses. Multicellular modes of reproduction are not pre-specified in the model, but must emerge from the evolving dynamics under ecological selection. We find that distinct multicellular life cycles evolve depending on the spatial distribution of resources. Among these are life cycles with a single-celled propagule phase the most prevalent reproductive strategy in multicellular life that evolves as a dispersal strategy to reach new resources. These propagules form through the activation of molecular programs co-opted from the unicellular ancestor, where they mediated interactions with neighbours in its ecological context. Once propagules evolve, multicellular lineages can invade environments previously dominated by unicellular competitors, showing this strategy is adaptive beyond the conditions that permit its evolution. Altogether, our results show that developmental regulation evolves through co-option of ecological interactions during the transition to multicellularity. Significance statementReproduction is a universal feature of life. Yet, the evolution of multicellularity transformed it fundamentally: while single-celled organisms reproduce via cell division, reproduction in multicellular organisms is a complex process involving the coordination of many cells. How these new forms of multicellular reproduction first evolved is currently unknown. Using a computational model, we study how group reproduction emerges from the collective dynamics of individual cells. The model shows that unicellular ancestral life cycles can be repurposed as propagules used for reproduction in multicellular species, suggesting that genetic co-option is a key mechanism through which early development evolves.