BACKGROUND: The majority of annelid neuromorphological studies addresses macroscopic forms such as the well-studied Platynereis dumerilii; microscopic annelids are generally neglected. Several of these animals have remarkably smaller, compact brains composed of significantly fewer cells and having less complex sensory structures. Yet, very little is still known on how these small brains are organized to fulfil basic functions. This study addresses the structure, evolution and development of neuromuscular systems within two exclusively meiofaunal lineages Lobatocerebridae and Dinophilidae.
RESULTS: Both families were shown to be nested within annelids in phylogenomic analyses based on transcriptomic data, which also suggest the Spiralian ancestor to be meiofaunal (Manuscript 4). The annelid affinity of the enigmatic Lobatocerebridae was further tested by detailed morphological examinations showing a simple muscular, but complex nervous system (Manuscript 5). Although the exact position of Dinophilidae is still not settled, its annelid affinity is no longer questioned. Dinophilidae is the focus of a range of immunohistochemical and gene expression analyses in this study yielding 1) a detailed atlas of neuro-, myo- and ciliogenesis in Dinophilus gyrociliatus and D. taeniatus showing high complexity and predicting a progenetic origin of D. gyrociliatus (Manuscript 1); 2) the distribution of 14 neuropeptides in the nervous system of three representatives of Dinophilidae showing high interspecific variation contrary to the conserved patterns observed in previous neurotransmitter studies (Manuscript 2); 3) In situ mapping of 11 neural patterning genes in D. gyrociliatus indicating a molecular regionalization of the brain not recognized from gross anatomical studies (Manuscript 3). The adult female brain of D. gyrociliatus was found to resemble the anterior neural region in larvae of P. dumerilii and C. teleta as described in previous studies, with most overlap of individual patterns in the anterior region of the brain.
CONCLUSION: Meiofaunal annelids such as Lobatocerebridae and Dinophilidae show highly diverse body plans, with even the assumedly conserved nervous system showing different arrangements such as uniform, compact brains in Dinophilidae and comparably large lobular complexes in Lobatocerebridae. Seemingly uniform brains do not reveal signs of gross morphological regionalization (yet molecular), but comparison of closely related species revealed unexpected plasticity in the distribution of specific neuropeptidergic cells. The relatively similar molecular profile of the microscopic and macroscopic annelid brain suggests the presence of a common annelid pattern, though warranting further studies to uncover how the genetic domains influence the configuration of the brain.