Convergent evolution of the ladder-like ventral nerve cord in Annelida
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RESEARCH
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Convergent evolution of the ladder-like ventral nerve cord in Annelida Conrad Helm1*, Patrick Beckers2, Thomas Bartolomaeus2, Stephan H. Drukewitz3, Ioannis Kourtesis1, Anne Weigert4, Günter Purschke5, Katrine Worsaae6, Torsten H. Struck7 and Christoph Bleidorn1,8*
Abstract Background: A 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. Results: Using 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. Conclusions: Based 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. Keywords: Neuroanatomy, Lophotrochozoa, Central nervous system, Segmentation, Neurophylogeny, Spiralia
Background A rope-ladder-like organization of the ventral nerve cord (VNC) has often been regarded to represent the ancestral condition of annelids [1–6]. According to this traditional view, the VNC in Annelida consists of a chain of paired ganglia containing the neuronal somata, linked longitudinally by parallel somata-free connectives and transversely by segmental commissures. The organization, development and cell types of the annelid mid-ventral cord are best investigated in the annelid model organisms Capitella teleta Blake, Grassle & Eckelbarger, 2009, Helobdella robusta Shankland, Bissen & Weisblat, 1992 and Platynereis dumerilii (Audouin & Milne Edwards, 1834) [7–14]. Gene expression studies in these annelids inspired wide reaching comparisons of the annelid VNC * Correspondence: [email protected]; [email protected] 1 Animal Evolution and Biodiversity, Georg-August-University Göttingen, 37073 Göttingen, Germany Full list of author information is available at the end of the article
to that of arthropods and vertebrates (e.g., [15–17]). Nonetheless, the annelid VNC shows a great diversity in number and position of neurite bundles and localizatio
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