Abstract
Concerning the evolution of deuterostomes, enteropneusts (acorn worms) occupy a pivotal role as they share some characteristics with chordates (e.g., tunicates and vertebrates) but are also closely related to echinoderms (e.g., sea urchin). The nervous system in particular can be a highly informative organ system for evolutionary inferences, and advances in fluorescent microscopy have revealed overwhelming data sets on neurogenesis in various clades. However, immunocytochemical descriptions of neurogenesis of juvenile enteropneusts are particularly scarce, impeding the reconstruction of nervous system evolution in this group. We followed morphogenesis of the nervous system in two enteropneust species, one with direct (Saccoglossus kowalevskii) and the other with indirect development (Balanoglossus misakiensis), using an antibody against serotonin and electron microscopy. We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells. Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring. Comparative analysis of both species shows that the projections of the serotonin-LIR somata initially form a basiepidermal plexus throughout the body that disappears within the trunk region soon after settlement before the concentrated dorsal and ventral neurite bundles emerge. Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta. Moreover, all detected serotonin-LIR neurons are presumably receptor cells, and the absence of serotonin-LIR interneurons from the enteropneust nervous system, which are otherwise common in various bilaterian central nervous systems, is interpreted as a loss that might have occurred already in the last common ancestor of Ambulacraria.
Highlights
Numerous comparative studies on the nervous system have revealed highly variable neural anatomies in multicellular animals, ranging from a simple nerve net in cnidarians to highly complex central nervous systems (CNS) in vertebrates (Nieuwenhuys et al 1998) and some protostomes (Bullock and Horridge 1965; Nixon and Young 2003; Strausfeld 2012)
Portions (Fig. 1) (Bullock 1946; Cavey and Märkel 1994; Chia and Koss 1994; Knight-Jones 1952; Stach et al 2012). It is still debated whether a plexus-like nervous system or a concentrated CNS was present in the last common ancestor of deuterostomes (LCAD)
The nervous system of the tornaria larva features a prominent apical organ comprising a paired cluster of serotoninLIR somata connected by a median neuropil, a ciliary apical tuft (Fig. 2b, f), as well as neurite bundles along the ciliary bands (Nielsen and Hay-Schmidt 2007; Miyamoto et al 2010), which are distinct below the opisthotroch
Summary
Numerous comparative studies on the nervous system have revealed highly variable neural anatomies in multicellular animals, ranging from a simple nerve net in cnidarians to highly complex central nervous systems (CNS) in vertebrates (Nieuwenhuys et al 1998) and some protostomes (e.g., arthropods and cephalopods) (Bullock and Horridge 1965; Nixon and Young 2003; Strausfeld 2012). Similarities in the anteroposterior and mediolateral patterning including presence and position of specific neuronal types between the ventral CNS of some protostomes (annelids and arthropods) and the dorsal CNS of chordates lead some authors to propose a CNS in the LCAD (Denes et al 2007; Arendt et al 2008; Nomaksteinsky et al 2009; Holland et al 2013; Miyamoto and Wada 2013) Both contradicting hypotheses are mainly based on molecular genetic analyses, whereas potentially informative neuro-anatomical data has barely been integrated. This is because data on neural morphogenesis in juvenile enteropneusts still remain scarce (e.g., Kaul and Stach 2010; Miyamoto et al 2010) and precise anatomical descriptions of the nervous system are mainly based on histological analyses of adult specimens (Bullock 1946; Knight-Jones 1952)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Free) 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
