Development and structure of the anterior nervous system and sense organs in the holopelagic annelid Tomopteris spp. (Phyllodocida, Errantia)

Abstract

Tomopteridae are transparent, predatory Annelida inhabiting pelagic ocean zones. Despite being well-known for their fast metachronal swimming and species-specific bioluminescence, our knowledge of morphological adaptations in these fascinating holopelagic worms remains extremely limited. In particular, the evolutionary scenarios and adaptive changes related to the transition from putative benthic ancestors to recent free-swimming groups remain poorly investigated and understood. Therefore, we investigated different taxa and developmental stages within the holopelagic Tomopteridae. We used a comparative morphological approach, including a range of microscopic methods, in our investigations focused on the anterior nervous system and prominent sensory structures, such as nuchal organs and tentacular cirri, in early developmental and adult stages of four tomopterid species. Our data show that Tomopteridae undergo heterochronic, lecithotrophic development with early visibility of adult-like features, which is consistent with earlier investigations. Furthermore, our ultrastructural examinations of the tomopterid nuchal organ highlight the conservativism in the fine structure and development of this prominent polychaete chemosensory organ. Nevertheless, our data indicate ultrastructural differences, such as an extraordinary number of supporting cell types and a bipartite olfactory chamber, potentially related to their pelagic lifestyle. In contrast to previous assumptions, it is shown that the supporting structures in the cirrus-like appendages of the first chaetiger contain prominent intracellular skeletal elements rather than annelid chaetae. These findings highlight the need for further investigations to understand Annelida’s immense morphological diversity of organ systems. Furthermore, our data demonstrate the necessity of functional analyses to understand Annelida’s adaptive radiation of sensory and neuronal structures.