Despite multiple benefits of multicellularity, unicellular life forms are ubiquitous and there have been multiple cases of evolutionary reversal to unicellularity. These evolutionary reversals offer insights on the potential limits to multicellularity and the ecological conditions favoring each of these life forms. One hypothesis is that reversibility to unicellularity could result from conflicts between cells and between cells and the multicellular organism as a whole. The difficulties of cooperation, nevertheless, are not the only constraints faced by multicellular individuals: increases in size and group density, coupled with reduced cell dispersal can lead to less efficient nutrient uptake and higher local (within-group) competition. To evaluate these ideas we used a combination of computer simulations, growth rate measurements, competition assays and evolution experiments. For these experiments we capitalize on a recently developed system: multicellular phenotypes of the brewers yeast Saccharomyces cerevisiaethat recently evolved in the lab as a result of a selection experiment favoring larger sizes. This is a tractable system where we can address the importance of increased size, local competition and dispersal in the evolution of multicellularity and reversals to unicellularity.
Results/Conclusions
In this system, we demonstrated an increased fitness cost of multicellular isolates relative to their unicellular ancestor due to limitations in resource acquisition in mass-action environments (where resources are widely distributed and competition is mainly global). In contrast, in structured environments (i.e. resources localized and local competition) cells in multicellular and unicellular organisms are equally limited by nutrient availability because in this environment cells grow in high density colonies. Despite being equally limited by resources (in terms of per cell growth), in spatially structured environments, single-cells are better able to disperse across the environment, securing more resources per cell and minimizing local competition. Consistent higher costs of fitness for multicellular isolates in structured environments and rapid reversals to unicellularity after selection on agar plates (vs. shaken liquid media) highlight the importance of dispersal and local competition in the evolution of multicellular and unicellular life forms; these results suggest that dispersal might have been one of the main constraints in the evolution of early multicellular forms.