Origin of the epidermis in parasitic platyhelminths

The epidermis of members of the major parasitic taxon Neodermata is distinctive among flatworms, being a syncytial, insunk, non-ciliated epidermis that develops through a wholesale replacement of larval epidermis at metamorphosis when the larva attacks a host. How it arose in evolution from what must have been a turbellarian-like ancestor is not immediately evident. While many turbellarian flatworms have also adopted a symbiotic way of life, the literature on ultrastructure of epidermis in these symbionts shows quite a variety of morphologies, many not so different from that of their free-living relatives. Various turbellarians do have syncytial or insunk epidermises or reduction of epidermal ciliation as is characteristic of the Neodermata, but co-occurrence in a single turbellarian of all features common to neodermatans has not been reported. Urastoma cyprinae, for example, which is ectosymbiotic on bivalves, has a ciliated cellular epidermis that is little different from what is known of epidermises of its free-living relatives. The endoparasitic Anoplodium hymanae, from the coelom of sea cucumbers, also bears a ciliated cellular epidermis, as is typical of many other rhabdocoels, but it shows marked phagocytic activity as well as incorporation of endosymbiotic bacteria. The closest similarity to neodermatan epidermis is that of the turbellarian Genostoma kozloffi, an ectosymbiont of the crustacean Nebalia: covering the bulk of the body is a non-ciliated syncytium with multiple branching connections to insunk nucleated portions, much as in epidermis of adult neodermatans and, on its ventral surface, is a field of ciliated cellular insunk epidermis resembling the epidermis of some larval neodermatans. Developmental clues to the origin of the neodermatan epidermis can be seen in turbellarian embryos. Before hatching, embryos of proseriate and triclad embryos go through 3 generations of epidermis, each replacing the next; 2 generations of epidermis are reported in the literature on rhabdocoel embryos. This process of replacement parallels the epidermal replacement that larval neodermatans undergo at metamorphosis. Ultrastructural study of developing acoel, polyclad and macrostomid embryos shows that they, too, have epidermal replacement and growth through immigration of deeper-lying cells, comparable to the processes seen in higher flatworms. Succession of distinct generations of epidermis in such animals as the proseriates, triclads and rhabdocoels is probably an adaptation to development of ectolecithal eggs, providing the means for the embryo to use yolk that resides in vitellocytes, outside its blastomeres. We propose that the Neodermata has taken advantage of this developmental mechanism, producing successive generations of epidermal cells even in its larval stages, to counter the defenses of hosts.