No abstract

Evolution from unicellular organisms to larger multicellular ones requires matching their needs to the rate of exchange of molecular nutrients with the environment. This logistic problem poses a severe constraint on development. For organisms whose body plan is a spherical shell, such as the volvocine green algae, the current (molecules per second) of needed nutrients grows quadratically with radius, whereas the rate at which diffusion alone exchanges molecules grows linearly, leading to a bottleneck radius beyond which the diffusive current cannot meet metabolic demands. By using Volvox carteri, we examine the role that advection of fluid by the coordinated beating of surface-mounted flagella plays in enhancing nutrient uptake and show that it generates a boundary layer of concentration of the diffusing solute. That concentration gradient produces an exchange rate that is quadratic in the radius, as required, thus circumventing the bottleneck and facilitating evolutionary transitions to multicellularity and germ-soma differentiation in the volvocalean green algae.advection ͉ multicellularity ͉ Volvox

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.

Benefits, costs, and requirements accompany the transition from motile totipotent unicellular organisms to multicellular organisms having cells specialized into reproductive (germ) and vegetative (sterile soma) functions such as motility. In flagellated colonial organisms such as the volvocalean green algae, organized beating by the somatic cells' flagella yields propulsion important in phototaxis and chemotaxis. It has not been generally appreciated that for the larger colonies flagellar stirring of boundary layers and remote transport are fundamental for maintaining a sufficient rate of metabolite turnover, one not attainable by diffusive transport alone. Here, we describe experiments that quantify the role of advective dynamics in enhancing productivity in germ somadifferentiated colonies. First, experiments with suspended deflagellated colonies of Volvox carteri show that forced advection improves productivity. Second, particle imaging velocimetry of fluid motion around colonies immobilized by micropipette aspiration reveals flow fields with very large characteristic velocities U extending to length scales exceeding the colony radius R. For a typical metabolite diffusion constant D, the associated Peclet number Pe ‫؍‬ 2UR͞D Ͼ Ͼ 1, indicative of the dominance of advection over diffusion, with striking augmentation at the cell division stage. Near the colony surface, flows generated by flagella can be chaotic, exhibiting mixing due to stretching and folding. These results imply that hydrodynamic transport external to colonies provides a crucial boundary condition, a source for supplying internal diffusional dynamics.diffusion ͉ flagella ͉ Volvox T he efficient exchange of nutrients, metabolites, and wastes is among the most basic factors affecting the fitness of organisms. Understanding the effect of resource delivery and exchange on metabolic rate, as organisms increase in size, is leading to rapid advances across disparate fields of the life sciences, from comparative biology to ecosystem ecology (1-4). Yet, these insights have not been applied to the analysis of the evolutionary transitions which underlie the hierarchy of life (5, 6). Although cooperative endeavors provide substantial benefits, certain key problems must be solved for a group to emerge into a new complex individual. As lower level units (cells) associate to form groups, the constraints of surface to volume ratio, S͞V, and of spatial organization limit the type and extent of interactions with the environment, with profound effects on metabolism, growth rate, viability, and fecundity. We refer to this as the ''transport limitation'' and view it as a general aspect of evolutionary transitions in individuality.Nutrient consumption increases proportionally with the size of the organism, creating an increased boundary layer of nutrient depletion. In the absence of active mixing of the medium, this decreases the passive diffusion of nutrients. This transport limitation constraint as size increases can be circumvented in several ways. For example, d...