The central nervous system of Oweniidae (Annelida) and its implications for the structure of the ancestral annelid brain

Abstract

BackgroundRecent phylogenomic analyses congruently reveal a basal clade which consists of Oweniidae and Mageloniidae as sister group to the remaining Annelida. These results indicate that the last common ancestor of Annelida was a tube-dwelling organism. They also challenge traditional evolutionary hypotheses of different organ systems, among them the nervous system. In textbooks the central nervous system is described as consisting of a ganglionic ventral nervous system and a dorsally located brain with different tracts that connect certain parts of the brain to each other. Only limited information on the fine structure, however, is available for Oweniidae, which constitute the sister group (possibly together with Magelonidae) to all remaining annelids.ResultsThe brain of Oweniidae is ring- shaped and basiepidermal. Ganglia, higher brain centers or complex sensory organs do not exist; instead the central nervous system is medullary. Posterior to the brain the ventral medullary cord arises directly from the ventral region of the brain in Myriowenia sp. while in Owenia fusiformis two medullary cords arise perpendicular to the brain ring, extend caudally and fuse posterior. The central nervous system is composed of a central neuropil and surrounding somata of the neurons. According to ultrastructural and histological data only one type of neuron is present in the central nervous system.ConclusionThe central nervous system of Oweniidae is the simplest in terms of enlargement of the dorsal part of the brain and neuron distribution found among Annelida. Our investigation suggests that neither ganglia nor commissures inside the brain neuropil or clusters of polymorphic neurons were present in the annelid stem species. These structures evolved later within Annelida, most likely in the stem lineage of Amphinomidae, Sipuncula and Pleistoannelida. Palps were supposedly present in the last common ancestor of annelids and innervated by two nerves originating in the dorsal part of the brain. A broader comparison with species of each major spiralian clade shows the medullary nervous system to be a common feature and thus possibly representing the ancestral state of the spiralian nervous system. Moreover, ganglia and clusters of polymorphic neurons seemingly evolved independently in the compared taxa of Spiralia and Annelida.Electronic supplementary materialThe online version of this article (10.1186/s12983-019-0305-1) contains supplementary material, which is available to authorized users.

The anatomy and development of the nervous system in Magelonidae (Annelida) – insights into the evolution of the annelid brain

“…The latter especially applies to the presumable sister groups Oweniidae and Magelonidae, which putatively form a monophylum that is the sister group to all remaining annelids. Additionally, recent neuroanatomical studies of Oweniidae show that the anatomy of the nervous system of these worms differs tremendously from the textbook annelid's nervous system [9]. Thus, the brain of Oweniidae is ring shaped, encircles the mouth and is confluent with the ventral nervous system.…”

“…Thus, the brain of Oweniidae is ring shaped, encircles the mouth and is confluent with the ventral nervous system. Concentrations of neurites (tracts) and neurons (ganglia) are not present, the nervous system is medullary [9][10][11]. These differences either result from transformations in the stem lineage of Oweniidae or show ancestral annelid conditions or a mixture of both.…”

“…The so-called shovel-head worms inhabit sandy or muddy bottoms and possess ventro-laterally located palps which are used for the transport of food particles (detritus) into the mouth opening and may have a sensory function [12,13]. Different tracts or commissures that are absent in the brain neuropil of Oweniidae, are described in Magelonidae as well as in pleistoannelid taxa [1,2,9]. Tracts or commissures are regions inside the neuropil of the brain, where neurites are differentially arranged compared to the neurites of the surrounding neuropil and thus can be discriminated.…”

“…Among the prostomial ones, eyes and nuchal organs are the most prominent sensory structures [1,16]. Nuchal organs are absent in Oweniidae and Magelonidae [9,15,17]. While larval eyes are described for Owenia fusiformis [18] and Magelona mirabilis [17], pigmented eye spots are only present in certain adult oweniids [9,11] and are not present in adult Magelonidae.…”

“…Nuchal organs are absent in Oweniidae and Magelonidae [9,15,17]. While larval eyes are described for Owenia fusiformis [18] and Magelona mirabilis [17], pigmented eye spots are only present in certain adult oweniids [9,11] and are not present in adult Magelonidae. Despite these organs another sensory structure may be present in setigers of the trunk of Annelida.…”