Multicellularity and increasing Reynolds number impact on the evolutionary shift in photo-induced ciliary response in Volvocales

ABSTRACT Volvocales include species with different cell numbers and sizes, reflecting a history of gradual size increase evolution. Unicellular species live in low Reynolds-number ( Re ) environments where viscous forces dominate, whereas multicellular species live in higher Re environments with nonnegligible inertial forces. Despite significant changes in the physical environment, during the evolution of multicellularity they maintained photobehaviors (i.e., photoshock and phototactic responses), which allows them to survive under changing light conditions. In this study, we classified photo-induced ciliary responses in Volvocales into four patterns: temporal waveform conversion, no obvious response, pause in ciliary beating, temporal changes in ciliary beating directions. We found that which species exhibit which pattern depends on Re associated with the individual size of each species rather than phylogenetic relationships. These results suggest that species with increased cell numbers acquired their responses adapted to higher Re fluid environments. Significance Statement Volvocales green algae include species with various cell numbers and are excellent organisms for studying the evolution of multicellularity. They exhibit photobehaviors by changing the pattern of ciliary beating, which could be categorized into four patterns. We found that the difference in patterns among the organisms is due to the Reynolds number, the ratio of viscous and inertia forces, rather than their phylogenetic relationships. This study indicates that the fluid environment was an important factor in natural selection for behavioral changes in microalgae during evolution. The results link evolution and physics while contributing to the design of micromachines.