Differences in Cell Division Rates Drive the Evolution of Terminal Differentiation in Microbes

Multicellular differentiated organisms are composed of cells that begin by developing from a single pluripotent germ cell. In many organisms, a proportion of cells differentiate into specialized somatic cells. Whether these cells lose their pluripotency or are able to reverse their differentiated state has important consequences. Reversibly differentiated cells can potentially regenerate parts of an organism and allow reproduction through fragmentation. In many organisms, however, somatic differentiation is terminal, thereby restricting the developmental paths to reproduction. The reason why terminal differentiation is a common developmental strategy remains unexplored. To understand the conditions that affect the evolution of terminal versus reversible differentiation, we developed a computational model inspired by differentiating cyanobacteria. We simulated the evolution of a population of two cell types –nitrogen fixing or photosynthetic– that exchange resources. The traits that control differentiation rates between cell types are allowed to evolve in the model. Although the topology of cell interactions and differentiation costs play a role in the evolution of terminal and reversible differentiation, the most important factor is the difference in division rates between cell types. Faster dividing cells always evolve to become the germ line. Our results explain why most multicellular differentiated cyanobacteria have terminally differentiated cells, while some have reversibly differentiated cells. We further observed that symbioses involving two cooperating lineages can evolve under conditions where aggregate size, connectivity, and differentiation costs are high. This may explain why plants engage in symbiotic interactions with diazotrophic bacteria.
Author Summary The evolution of multicellularity is one of the most fascinating topics of evolutionary biology. Without multicellularity the incredible diversity of extant life would not be possible. In many multicellular organisms with specialized cells, some cell types become terminally differentiated (somatic cells) and lose the ability to reproduce new organisms while other cells maintain this ability (germline). Little is known about the conditions that favor the evolution of terminal differentiation in multicellular organisms. To understand this problem we have developed a computational model, inspired by multicellular cyanobacteria, in which the cells in an organism composed of two cell types (photosynthetic and nitrogen fixing) are allowed to evolve from germline to soma cells. We find three striking results. First, faster dividing cell types always evolve to become the germline. Second, the conditions under which we find different outcomes from the model are in good agreement with the different forms of development observed in multicellular cyanobacteria. Third, some conditions lead to a symbiotic state in which the two cell types separate into different lineages evolving independently of one another. Remarkably, cyanobacteria are also known to engage in symbiotic relationships with plants, producing fixed nitrogen for the plant in exchange for carbohydrates.