May the palps be with you – new insights into the evolutionary origin of anterior appendages in Terebelliformia (Annelida)

BACKGROUND: Head appendages in Annelida contribute significantly to the immense morphological diversity in this spiralian taxon. Nevertheless, the evolutionary origin of annelid antennae, palps, cirri and tentacles are part of vast theories and debates that took place over decades. One of these heavily discussed groups are the Terebelliformia, which bear numerous anterior tentacles originating from different regions of the head. The question, whether these tentacles are homologous to feeding palps in other annelids or if these structures evolved convergently in terebellids and the remaining taxa, has been highly debated in the past. RESULTS: By using morphological methods including immunohistochemistry, confocal microscopy, Azan-stained serial sections and 3D-visualisation, we are able to shed new light and a fresh look on the old question of the evolutionary origin of the buccal tentacles and their associated head structures in Terebelliformia. Our investigations show that the brains of the ampharetid Hypania invalida and the aulophora larvae of Lanice conchilega (Terebellidae) consist of a dorsal, more prominent and a more slender, ventral brain region. Neurite bundles innervating the buccal tentacles split off from the ventral and dorsal root within the ventral brain region and thus originate from the dorsal and ventral root of the circumoesophageal connectives. Hence, the observed neurite bundles fulfil the morphological criteria for the innervating neurite bundles of feeding palps known from Paleoannelida. CONCLUSIONS: We disagree with former conclusions that buccal tentacles are part of the alimentary canal. Based on the presented data, the buccal tentacles of terebelliform taxa are innervated by neurite bundles and can be homologized with peristomial feeding palps of other Annelida. Our comparative investigations reveal important insights into morphological changes during the evolution of anterior head appendages in Terebelliformia and Annelida in general. Nevertheless, our analyses also illustrate the gaps in knowledge and that more investigations throughout the annelid tree are necessary to explain and understand the huge diversity of annelid anterior appendages.