A Hydrodynamics Approach to the Evolution of Multicellularity: Flagellar Motility and Germ‐Soma Differentiation in Volvocalean Green Algae

Abstract

During the unicellular-multicellular transition, there are opportunities and costs associated with larger size. We argue that germ-soma separation evolved to counteract the increasing costs and requirements of larger multicellular colonies. Volvocalean green algae are uniquely suited for studying this transition because they range from unicells to multicellular individuals with germ-soma separation. Because Volvocales need flagellar beating for movement and to avoid sinking, their motility is modeled and analyzed experimentally using standard hydrodynamics. We provide comparative hydrodynamic data of an algal lineage composed of organisms of different sizes and degrees of complexity. In agreement with and extending the insights of Koufopanou, we show that the increase in cell specialization as colony size increases can be explained in terms of increased motility requirements. First, as colony size increases, soma must evolve, the somatic-to-reproductive cell ratio increasing to keep colonies buoyant and motile. Second, increased germ-soma specialization in larger colonies increases motility capabilities because internalization of nonflagellated germ cells decreases colony drag. Third, our analysis yields a limiting maximum size of the volvocalean spheroid that agrees with the sizes of the largest species known. Finally, the different colony designs in Volvocales reflect the trade-offs between reproduction, colony size, and motility.

Evolution of individuality during the transition from unicellular to multicellular life

“…Consequently, the cell growth (dependent on photosynthesis) and division (dependent on cell growth) of somatic cells are suppressed. Because they cannot divide, they do not participate directly in the offspring but contribute to the survival and reproduction of the colony through flagellar action (14,15,18). In other words, the somatic cells express an altruistic behavior, and regA [whose expression is necessary and sufficient for this behavior (16)] is an altruistic gene.…”

“…As with all forms of cooperation, this altruistic behavior is also susceptible to defection and selfish mutants; indeed, mutations in regA result in the somatic cells regaining reproductive abilities, which in turn results in them losing their flagellar capabilities (20). Because motility is important for these algae (flagellar activity is required to maintain themselves in the water column at an optimum position relative to sunlight intensity), the survival and reproduction of V. carteri individuals in which such mutant somatic cells occur are negatively affected (14).…”

“…The flagellation constraint becomes critical at the 32-cell colony size, because a flagellum may beat for up to five cell divisions without the basal bodies attached. The second factor leading to a tradeoff between reproduction and motility is that the increasing mass of the reproductive cells and embryos during reproduction decreases motility by increasing drag (14). This increasing mass is especially noticeable in the larger species.…”

“…3 B and C). A central focus of Solari's hydrodynamic work (14,25) is to quantify this hypothesized increasing cost of reproduction.…”

“…Second, we ask why reproductive altruism arises only in the larger members of the volvocine group. Our answer is that the selective pressures leading to reproductive altruism stem from the increasing cost of reproduction with increasing group size (14,15).…”