A hydrodynamics approach to the evolution of multicellularity: Flagellar motility and the evolution of germ-soma differentiation in Volvocalean green algae

The fitness of any evolutionary unit can be understood in terms of its two basic components: fecundity and viability. The trade-offs between these fitness components drive the evolution of a variety of life-history traits in extant multicellular lineages. Here, I show evidence that the evolution of germ-soma separation and the emergence of individuality at a higher level during the unicellular-multicellular transition are also consequences of these trade-offs. The transition from unicellular to larger multicellular organisms has benefits, costs, and requirements. I argue that germ-soma separation evolved as a means to counteract the increasing costs and requirements of larger multicellular colonies. Volvocalean green algae are uniquely suited for studying this transition since they range from unicells to undifferentiated colonies, to multicellular individuals with complete germ-soma separation. In these flagellated organisms, the increase in cell specialization observed as colony size increases can be explained in terms of increased requirements for self-propulsion and to avoid sinking. The collective flagellar beating also serves to enhance molecular transport of nutrients and wastes. Standard hydrodynamic measurements and concepts are used to analyze motility (self-propulsion) and its consequences for different degrees of cell specialization in the Volvocales as colony size increases. This approach is used to calculate the physical hydrodynamic limits on motility to the spheroid colony design. To test the importance of collective flagellar beating on nutrient uptake, the effect of advective dynamics on the productivity of large colonies is quantified. I conclude first, that when colony size exceeds a threshold, a specialized and sterile soma must evolve, and the somatic to reproductive cell ratio must increase as colony size increases to keep colonies buoyant and motile. Second, larger colonies have higher motility capabilities with increased germsoma specialization due to an enhancement of colony design. Third, advection has a significant effect on the productivity of large colonies. And fourth, there are clear trade-offs between investing in reproduction, increasing colony size (i.e. colony radius), and motility. This work shows that the evolution of cell specialization is the expected outcome of reducing the cost of reproduction in order to realize the benefits associated with increasing size.