Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords

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.

Hemichordate models

“…Kaul-Strehlow et al recently provided an immunocytochemical description of neurogenesis in directly and indirectly developing enteropneusts. Perhaps ancestral deuterostomes retained a CNS with an AP patterning gene network, which was secondarily lost or reduced in the lineage leading to hemichordates; nonetheless, it is too early to draw unambiguous conclusions [4,11 ].…”

“…At that time, only a few people worldwide were working on these rarely encountered animals. Currently at least four species of the Class Enteropneusta (Ptychodera flava, Saccoglossus kowalevskii, Balanoglossus misakiensis, and Balanoglossus shimodensis) and two species of the Class Pterobranchia (Rhabdopleura compacta and Cephalodiscus gracilis) are used for comparative developmental biology and/or phylogenetic studies by various laboratories in Japan, Taiwan, the U.S., Canada, and Europe [1][2][3][4][5][6][7][8].…”

The first brain: Species comparisons and evolutionary implications for the enteric and central nervous systems

“…Other invertebrates, including echinoderms, acorn worms, cephalopods, gastropod molluscs, and annelid worms have an ENS (Table ), some of which have architectures reminiscent of that of vertebrates, including human (Figure ). However, the ENS of insects has diverged from that of other invertebrates, in that enteric neurons are in ganglia and along nerve strands on the surface of the gut, rather than being embedded in its wall .…”

Nervous systems and scenarios for the invertebrate-to-vertebrate transition

“…Such problems should be largely resolved when more is learned about the developmental genetics, wiring diagrams and physiology of enteropneust nervous systems. A start in this direction has recently been made by Kaul-Strehlow et al [49], who mapped the distribution of serotonin-containing neurons in two species over several lifehistory stages. Even so, a better understanding of enteropneust neurobiology will still leave open the broader question of whether the Urbilaterian nervous system was simply a nerve net or also included a CNS.…”