Steven R. Dudgeon
Department of Biology
California State University
Northridge, CA 91330-8303
Clonal life cycles are widespread in each eukaryotic kingdom. In many of these organisms, morphological development is continuous with growth, there is no pre-determined colony size or lifespan, and no known senescence. It is unlikely, therefore, that the genome can pre-program every morphogenetic event during a colony's life. Rather, morphogenesis results from the interaction between the physiological state of a colony (i.e., the integration of environmental conditions with the underlying metabolic supply and demand of the organism) and simple rules established by the genome. We have been investigating the physiological control of morphogenesis in the hydractiniid hydrozoans, Podocoryne carnea and Hydractinia symbiolongicarpus. Hydractiniid hydrozoans serve as useful models for studying morphogenesis and its plasticity in clonal taxa because morphological variation within some species is representative of much of the morphological variation observed across clonal taxa. A colony is composed of two elements; polyps (pumps) and stolons (pipes).Colonies grow by elongation of stolon tips, branching of new stolon tips, anastomosis of tips and the budding of polyps on stolons. Polyps are physiologically coupled to one another in a common gastrovascular system. This is a system of fluid-filled canals that runs throughout the stolonal network and joins the gastric cavities of polyps. In these hydrozoans, it is the only physiological system whose behavior is known to be manifested colonywide. In hydrozoans, the layout of the gastrovascular system in space is the morphology of the colony. Thus, colony form and gastrovascular fluid transport are inextricably linked. We have shown that the architecture of stolons (the relative size and arrangement) in the mat of Hydractinia spp. is correlated with colony morphology. Runner colonies, that show widely spaced polyps along sparsely branched stolons, are characterized by highly variable diameters of stolons in the mat, whereas sheet colonies, that have closely packed polyps on more highly branched and anastomosed stolons forming and encrusting sheet, show little variation amog stolon diameters. Moreover, surgically manipulating stolon architecture in order to effect a change in patterns of gastrovascular fluid transport within colonies, subsequently changes the morphological trajectory of colonies after ceasing surgery. Runner colonies can be transformed into sheets and vice-versa. The limits of plasticity are set by the degree to which flow patterns within colonies can be altered.
Flow patterns are a function of the dimensions of the stolons through which fluid flows and the behavior of polyps whose oscillations drive the flow. Experimental evidence suggests that the volumetric rate of flow regulates rates of polyp production and stolon branching. Increased branching and polyp production are associated with lower rates of flow. The characteristic(s) of flow that trigger these morphogenetic changes are not yet known. However, we have shown that polyp production is enhanced relative to stolon growth when colonies are grown in seawater with experimentally increased viscosity suggesting that shear forces may provide information to cells lining the lumen of stolons to differentiate polyp buds at critical levels of shear stress. Rates of stolon branching, however, were insensitive to variation in seawater viscosity implying that a polyp formation and stolon branching are achieved via different mechanisms.
Identifying the relevant hydromechanical characteristics of gastrovascular flow that signal morphogenetic events is complicated by the dynamic nature of circulation under the control of polyps. Colonywide patterns of gastrovascular circulation emerge from the collective behavior of polyps interacting with one another. Colonies may be comprised of one, several, or thousands of polyps acting in concert to generate a time- and space-varying distribution of metabolites and hydrodynamic signals. Our approach has been to characterize the behavioral dynamics of a single polyp, in the hope that the behavior of an isolated polyp is simple enough to allow development of a mathematical model. Polyps can be modelled as simple non-linear oscillators. Our model suggests that polyp oscillations are triggered by the presence of nutrients in the digestive cavity and that the release of nutrients into the colonial gastrovascular system induces unfed polyps to oscillate, thereby generating a colonywide transport of fluid and metabolites. A spatially distributed system of coupled non-linear oscillators appears to be a reasonable abstraction of a hydrozoan colony.