Convergent evolution of the ladder-like ventral nerve cord in Annelida

Abstract

BackgroundA median, segmented, annelid nerve cord has repeatedly been compared to the arthropod and vertebrate nerve cords and became the most used textbook representation of the annelid nervous system. Recent phylogenomic analyses, however, challenge the hypothesis that a subepidermal rope-ladder-like ventral nerve cord (VNC) composed of a paired serial chain of ganglia and somata-free connectives represents either a plesiomorphic or a typical condition in annelids.ResultsUsing a comparative approach by combining phylogenomic analyses with morphological methods (immunohistochemistry and CLSM, histology and TEM), we compiled a comprehensive dataset to reconstruct the evolution of the annelid VNC. Our phylogenomic analyses generally support previous topologies. However, the so far hard-to-place Apistobranchidae and Psammodrilidae are now incorporated among the basally branching annelids with high support. Based on this topology we reconstruct an intraepidermal VNC as the ancestral state in Annelida. Thus, a subepidermal ladder-like nerve cord clearly represents a derived condition.ConclusionsBased on the presented data, a ladder-like appearance of the ventral nerve cord evolved repeatedly, and independently of the transition from an intraepidermal to a subepidermal cord during annelid evolution. Our investigations thereby propose an alternative set of neuroanatomical characteristics for the last common ancestor of Annelida or perhaps even Spiralia.Electronic supplementary materialThe online version of this article (10.1186/s12983-018-0280-y) 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

“…Ganglia or somata-free connectives are not present. The same is true for the putative sister taxon Oweniidae [8,9], indicating that an intraepidermal cns with lateral medullary cords which fuse caudally might be the plesiomorphic condition for Annelida.…”

“…The same is true for Bryozoa, Brachiopoda and Phoronida [27][28][29]. Accordingly, the anatomy of the cns of spiralian relatives shows more similarities to the adult anatomy of Oweniidae and questions the sister-group relationship of oweniids and magelonids [8].…”

“…Clustered polymorphic neurons are also found in Amphinomidae and Sipuncula as well as in pleistoannelid taxa [1]. However, polymorphic neurons are not described for Chaetopteriformia [1], which form another basally-branching clade within the annelid tree and therefore hamper the explanation of the evolution of these neuron types [8].…”

“…In textbooks the central nervous system (cns) of Annelida is described as to consist of a dorsal brain with several commissures, in most taxa located in the prostomium, and nerves that encircle the mouth and connect the brain to the ventral ganglionic nervous system [1,2]. This statement, however, is challenged by the results of recent phylogenomic investigations to unravel the evolution of Annelida [3][4][5][6][7][8]. Hence, these studies lead to two important conclusions: 1: Most of our assumptions on the structure and primary organization of Annelida so far results from comparative analyses of different representatives of derived annelid ingroups, i.e.…”

Spaghetti to a Tree: A Robust Phylogeny for Terebelliformia (Annelida) Based on Transcriptomes, Molecular and Morphological Data

“…Terebelliforms show remarkable variation in palps, branchiae and chaetae (Figure 1). The combination of these features has traditionally been used to delineate the major lineages [8,9]: Terebellidae Grube, 1850 (including Terebellinae Hessle, 1917, Polycirrinae Malmgren, 1866, Thelepodinae Malmgren, 1866), Trichobranchidae Malmgren, 1866, Pectinariidae Quatrefages, 1866, Ampharetidae Malmgren, 1866 (including Ampharetinae Malmgren, 1866, Melinninae Chamberlin, 1919) and Alvinellidae Desbruyères and Laubier, 1986. Understanding how this diversity arose requires a phylogenetic hypothesis with robust support and, ideally, with broad taxonomic sampling.…”