Convergent evolution of sensory palps in Scalibregmatidae (Annelida)

Abstract Scalibregmatidae are deposit feeders inhabiting muddy or sandy sea floors at considerable depths, and usually lack head appendages common in many other marine annelids. Surprisingly, one lineage within this family bears palp-like structures comparable to anterior head appendages in other Annelida. Nevertheless, a homology of the scalibregmatid appendages with those of other annelids is highly questionable. Using an integrative morphological approach including immunohistochemistry, azan-histology, and 3D reconstruction, we examined the neural innervation of the anterior head region in one travisiid and two scalibregmatid species: Travisia sp. (without appendages), Scalibregma celticum (lateral, prostomial horns), and Axiokebuita cavernicola (palp-like appendages). Scalibregma and Axiokebuita show an innervation pattern of their appendages different from that of palps in other annelids, while no prominent prostomial innervation is present in Travisia. The short, lateral horn-like appendages of S. celticum possess a quite diffuse neuronal scaffold extending from distinct neurite bundles originating from multiple regions of the brain. The elongated palp-like head appendages of A. cavernicola exhibit a neuronal innervation pattern comparable with that of thin sensory antennae known from other annelid groups. Thus, innervating neurites solely originate in the dorsal part of the brain, a pattern not observable for “true” feeding- or sensory palps of other taxa. We also shed new light on the mysterious “neck organ” in scalibregmatids, which are shown to be ventral dublications of the olfactory nuchal organs considering the level of external features and nervous innervation. These results, combined to previous phylogenetic studies, show that Scalibregmatidae are the only so far known annelids to have re-evolved palp-like sensory head structures after a secondary loss. Thus, this is the first example of convergent evolution of palps, a character complex hitherto showing similar overall innervation patterns and considered homologous across all annelids. Competing Interest Statement The authors have declared no competing interest.