The Origin and Evolution of Cellular Differentiation in the Volvocine Green Algae

Abstract

During the evolution of multicellularity, the unit of selection transitions from that of the single cell to that of the integrated multicellular organism. Cellular specialization mediates this transition, as the evolution of differentiated cell types leads to fitness becoming a property of the multicellular organism. How does cellular specialization evolve? While we know that genetic changes result in the development of new cell types, it remains unclear whether the development of a new cell type can be ancestrally plastic prior to coming under developmental-genetic control via genetic assimilation. We use the volvocine green algae as a model system to address the overarching question of whether the plastic development of a new cell type preceded its fixation via genetic assimilation. Previous research on the evolution of cellular differentiation in this clade has determined that a gene necessary for somatic cell development is present in species with and without soma and that an ancestral stress response was co-opted during the evolution of somatic differentiation. This raises the possibility that somatic cells may have originated as a plastic trait prior to coming under developmental-genetic control. Here, I show that Eudorina species previously characterized as undifferentiated develop a small proportion of cells resembling soma following exposure to cold shock, an environmental stressor. We also find that the offspring of cold-shocked colonies (but not the grand-offspring) also develop somatic-like cells. We show that these cells are morphologically consistent with the somatic cells seen in closely related species that are obligately differentiated. We find that somatic-like cells in cold-shocked colonies are controlled by cell-level, temporal regulation while the production of somatic-like cells in the offspring of cold-shocked colonies are controlled by group-level, developmental regulation induced by the maternal environment. We propose that cell-level control of cellular differentiation, a cross-level byproduct, could be an intermediate step in the evolution of a group-level trait. We then repeatedly exposed a different Eudorina species that has been classified as undifferentiated to two repeated rounds of cold shock to determine if obligate somatic cells can evolve by genetic assimilation. We assessed the lines dozens of generations after treatment and found that repeatedly cold-shocked lines evolved an increased proportion of differentiated colonies. Moreover, we found that the proportion of differentiated cells also increased over the course of the study. These results provide evidence that plasticity followed by genetic assimilation likely played an important role in the evolution of somatic differentiation in the volvocine green algae.