Evolutionary paths towards multicellularity and cellular differentiation : a study of developmental strategies in cyanobacteria

Abstract

This thesis, developed at the interface between biology and applied mathematics, explores fundamental steps in the evolution of life, namely the evolution of multicellularity and cellular differentiation. Cyanobacteria, the main model organism for this work, were present on Earth billions of years ago and are a living image of the primordial emergence of multicellular organisms. The three themes of this work aim to study the evolutionary and ecological conditions governing this emergence. In chapter 2, we developed a theoretical model and tested it against experiments, showing that multicellular life cycles can emerge as a result of birth/death processes in an ecological context. When cell birth and death rates of multicellular filamentous bacteria are dependent on the density of cells in a population, a predictable cycle between short and long filament lengths is produced. Changes in generation time in bacterial populations can alter length distributions, and even when fitnesses do not differ, average filament lengths can differ drastically. This shows that differences in fitness are not the sole explanation for the evolution of multicellular life cycles. Chapter 3 is devoted to investigate how differentiation would evolve in a unicellular context. This would require collaborative consortia of single cells that survive through the exchange of common goods. Our mathematical model of cyanobacterial species shows that in such a configuration, deleterious mutations producing cheater cells would lead to the collapse of the system. Moreover, an optimal ratio between cell types that ensures an optimal growth can be achieved only in multicellular organisms. These findings indicate multicellularity as a necessary condition for the stability and the optimization of division of labor in cyanobacteria. Through terminal differentiation, cyanobacteria achieve a spatial separation of photosynthesis and nitrogen fixation, that are chemically incompatible. Undifferentiated species separate the tasks in time according to a circadian rhythm. In chapter 4, we use a theoretical model to compare the biomass production of the two species types at different latitudes. We find that an optimal resource investment into reproduction and nitrogen fixation can enhance the biomass production of terminally differentiated species as if there were no constraints. The results in this thesis offer new perspectives on the evolution of multicellularity and cellular differentiation in bacteria and higher organisms.