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.

Keywords: N2 fixation; complexity; division of labor; filament; transition in individuality.

Fig. 1

Support for three possible basal/ancestral cyanobacterial groups in 273 rooted gene trees. The number of gene families supporting each type of rooted topology is given (median alignment length is shown in parenthesis).

Fig. 2

Order of trait emergence. Left: traits and their inferred origin node from the rooted species tree. Colors mark traits with a common origin node (note that the order of traits within the colored blocks is arbitrary). Colored boxes are nested, that is, earlier traits are present also in the nested colors. Right: Frequency of gene trees in agreement with the relative order of pairs of traits. Cells in the matrix are shaded according to the color bar on the right.