Breaking the ladder: Evolution of the ventral nerve cord in Annelida

Abstract

AbstractA 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 neither a plesiomorphic nor a typical condition in annelids.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 ancestral state in Annelida. Thus, a subepidermal ladder-like nerve cord clearly represents a derived condition.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 question a common origin of the bilaterian median ganglionated VNC and propose an alternative set of neuroanatomical characteristics of the last common ancestor of Annelida or perhaps even Spiralia.