Redox control in development and evolution: Evidence from colonial hydroids

Redox chemistry, involving the transfer of electrons and hydrogen atoms, is central to energy conversion in respiration, and the control of gene expre ssion by redox state commonly occurs in bacteria, allowing rapid responses to environmental changes, for instance, in the food supply. Colonial metazo ans often encrust surfaces over which the food supply varies in time or spa ce; hence, in these organisms, redox control of the development of feeding structures and gastrovascular connections could be similarly adaptive, allo wing colonies to adjust the timing and spacing of structures in response to a variable food supply. To investigate the possibility of redox control of colony development, the redox states of hydractiniid hydroid colonies were manipulated experimentally. As in many colonial animals, hydractiniid hydr oids display a range of morphological variation from sheet-like forms (i.e. closely spaced polyps with high rates of stolen branching) to runner-like forms (i.e. widely spaced polyps with low rates of stolen branching). In th e runner-like Podocoryna carnea, azide, a blocker of the electron transport chain, and dinitrophenol, an uncoupler of oxidative phosphorylation, dimin ished the largely polyp-driven gastrovascular flow to a similar extent. Mea sures of the redox state of the polyp epitheliomuscular cells using the flu orescence of NAD(P)H suggest that azide shifts the redox state in the direc tion of reduction, while dinitrophenol shifts the redox state in the direct ion of oxidation. Colony development corresponds to redox state in that azi de-treated colonies were more runner-like, while dinitrophenol-treated colo nies were more sheet-like. Nevertheless, the functional role of polyps in f eeding and generating gastrovascular how probably contributed to a trade-of f between polyp number and size such that azide-treated colonies had few la rge polyps, while dinitrophenol-treated colonies had many small polyps. Reg ardless of the treatment, P. carnea colonies developed to maturity and prod uced swimming medusae in the normal fashion. In the sheet-like Hydractinia symbiolongicarpus, treatment with azide resulted in complete suppression of the development of both the stolonal mat and the blastostyles, the reprodu ctive polyps. Azide-treated H. symbiolongicarpus colonies therefore develop ed in a juvenilized, runner-like manner and much resembled colonies of P. c arnea. Following cessation of azide treatment in H. symbiolongicarpus, norm al colony development ensued, and both a stolonal mat and blastostyles form ed. In both hydroid species, relative oxidization favors sheet-like growth, while relative reduction favors runner-like growth. Since feeding triggers strong contractions of polyp epitheliomuscular cells and results in relati ve oxidation, this experimental evidence supports the hypothesis of adaptiv e redox control of colony development and evolution.