The order of trait emergence in the evolution of cyanobacterial multicellularity

Abstract

The transition from unicellular to multicellular organisms is one of the most significant events in the history of life. Key to this process is the emergence of Darwinian individuality at the higher level: groups must become single entities capable of reproduction for selection to shape their evolution. Evolutionary transitions in individuality are characterized by cooperation between the lower level entities and by division of labor. Theory suggests that division of labor may drive the transition to multicellularity by eliminating the trade-off between two incompatible processes that cannot be performed simultaneously in one cell. Here we examine the evolution of the most ancient multicellular transition known today, that of cyanobacteria, where we reconstruct the sequence of ecological and phenotypic trait evolution. Our results show that the prime driver of multicellularity in cyanobacteria was the expansion in metabolic capacity offered by nitrogen fixation, which was accompanied by the emergence of the filamentous morphology and succeeded by a reproductive life cycle. This was followed by the progression of multicellularity into higher complexity in the form of differentiated cells and patterned multicellularity. Significance StatementThe emergence of multicellularity is a major evolutionary transition. The oldest transition, that of cyanobacteria, happened more than 3 to 3.5 billion years ago. We find N2 fixation to be the prime driver of multicellularity in cyanobacteria. This innovation faced the challenge of incompatible metabolic processes since the N2 fixing enzyme (nitrogenase) is sensitive to oxygen, which is abundantly found in cyanobacteria cells performing photosynthesis. At the same time, N2-fixation conferred an adaptive benefit to the filamentous morphology as cells could divide their labour into performing either N2-fixation or photosynthesis. This was followed by the culmination of complex multicellularity in the form of differentiated cells and patterned multicellularity.