The non-brain anterior nerve center and tentacle crown structure of Owenia borealis (Annelida, Oweniidae): the evolution of the nervous system and tentacles in Bilateria

Abstract

The Oweniidae are marine annelids with many unusual features of organ system, development, morphology, and ultrastructure. Together with magelionds, oweniids have been placed within the Palaeoannelida, a sister group to all remaining annelids. The study of this group may increase our understanding of the early evolution of annelids (including their radiation and diversification) and of the morphology of the last common bilaterian ancestor. In the current research, scanning electron microscopy revealed that the tentacle apparatus consists of 10 branched arms. The tentacles are covered by monociliary cells that form a ciliar groove that extends along the oral side of the arm base. Light, confocal, and transmission electron microscopy revealed that head region contains two circular intraepidermal nerves (outer and inner) that give rise to the neurites of each tentacle, i.e., intertentacular neurites are absent. Each tentacle contains a coelomic cavity with a network of blood capillaries. Monociliar myoepithelial cells of the tentacle coelomic cavity form both the longitudinal and the circular muscles. The structure of this myoepithelium is intermediate between simple and pseudo-stratified myepithelium. Overall, tentacles lack prominent zonality, i.e., co-localization of ciliary zones, neurite bundles, and muscles. This organization, which indicates a non-specialized tentacle crown in O. borealis and other oweniids with tentacles, is probably ancestral for annelids and for all Bilateria. The outer circular nerve of O. borealis is a dorsal medullary commissure that apparently functions as an anterior nerve center and is organized at the ultrastructural level as a stratified neuroepithelium. Given the hypothesis that the anterior nerve center of the last bilateral ancestor might be a diffuse neural plexus network, these results suggest that the ultra anatomy of that plexus brain might be a stratified neuroepithelium. Alternatively, the results could reflect the simplification of structure of the anterior nerve center in some bilaterian lineages.