Nervous system evolution in early deuterostomes

The majority of known animals belong to the Bilateria, which comprises the sister groups Protostomia (e.g. molluscs, annelids and arthropods) and Deuterostomia (e.g. echinoderms, sea squirts and vertebrates). Within the higher deuterostome taxon, Chordata (including lancelets, sea squirts and vertebrates), a complex centralised nervous system (CNS) is present, constituted by a dorsal neural tube and an anterior brain, while the nervous system in basal metazoans (e.g. cnidarians) consists of a simple nerve-net plexus around the body. In protostomes, such as annelids and arthropods, the nervous system features a ventral CNS with an anterior brain. However, it is still controversially discussed if the dorsal CNS of chordates and the ventral CNS of protostomes are homologous and thus a CNS has already been present in the last common ancestor of Deuterostomia (LCAD), or if the nervous system of the LCAD rather resembled a nerve-net as found in basal metazoans. In this respect, the specific architecture of the nervous system in enteropneusts (acorn worms), a supposedly basal group of deuterostome animals, is of special interest and may play a crucial role in unravelling the evolution of nervous systems in Deuterostomia. The nervous system of enteropneusts comprises a basiepidermal nerve-net around the body and additional centralised parts in the form of a dorsal as well as a ventral nerve cord. In order to clarify now whether the centralised ventral and dorsal nerve cords in enteropneusts represent (i) secondary centralisations that evolved in Enteropneusta or (ii) represent remnants of an ancient CNS of the LCAD, data on the development of the nervous system in enteropneusts are needed. Following Haeckel`s theory of recapitulation (at least in partem), enteropneusts possibly undergo a stage of development featuring a centralised nervous system prior to the formation of the basiepidermal nerve-net or vice versa. Indeed, developmental data are present on the molecular genetic level, though only from a derived species undergoing a direct mode of development without a tornaria larva. Furthermore, data on the neurogenesis of the adult nervous system in enteropneusts from a cytological level are completely missing for direct developers or still fragmentary for indirect developers (tornaria larva). Therefore, the ancestral condition of neurogenesis for Enteropneusta remains ambiguous. In order to contribute new data on this problem, this project will use a combined methodological approach, applying a set of modern morphological as well as molecular techniques (immunocytochemistry + confocal laser scanning microscopy, histology + 3D- reconstructions, and in situ hybridisation) to generate an accurate description of the neurogenesis in two enteropneust species. From the data obtained herein, a potential ground pattern for Enteropneusta will be hypothesized, further contributing significantly to the reconstruction of the nervous system of the LCAD.

The evolutionary origin of a central nervous system (CNS) as present in vertebrates is still debated and remains unclear in many points. In basal metazoans such as cnidarians, a nerve plexus is present while chordate deuterostomes (including tunicates, lancelets and vertebrates) feature a dorsal central nervous system. In protostomes such as annelids and arthropods, a ventral CNS is present. It is currently discussed, if a CNS was already present in in the last common ancestor of Deuterostomia (LCAD) or if the nervous system of the LCAD rather constituted a diffuse nerve plexus. In order to elucidate the evolution of the CNS in Deuterostomia (e.g. echinoderms, tunicates, vertebrates), this project studies the development of the nervous system in acorn worms (enteropneusts) by means of morphological as well as molecular genetic methods. Enteropneusta, a group of basal deuterostomes feature both a basiepidermal nerve plexus as well as a dorsal and ventral nerve cord, which is why they are supposed to reveal insights into nervous system evolution. The data obtained during this project show that the nervous system of hemichordates passes through a transitory nerve plexus stage before the centralized cords are established. This neurogenetic pathway is highly conserved among enteropneust species and independent from the developing mode (indirect vs. direct). In contrast, the CNS of vertebrates and protostomes forms a priori without a plexus-like stage. Furthermore, our molecular genetic analyses of mediolateral patterning genes (dlx, pax6, nkx 2.1/2.2) in the dorsal and ventral cord in enteropneusts do not support homology of the chordate neural tube to either of the enteropneust cords. Apart from that, the absence of a typical apical organ as well as an opisthotroch nerve ring in the direct developer S. kowalevskii are interpreted as secondary losses that support a derived phylogenetic position within Enteropneusta for this species. Taken together, the differences in formation of a CNS in enteropneusts and other bilaterians as well as the lack of mediolateral columns in both nerve cords indicates an independent centralization of neurite bundles in Enteropneusta. Our data reveal that the enteropneust nervous system only barely shows similarities to the CNS of chordates and protostomes and thus is not likely to represent the ancestral condition in Deuterostomia. Its neuronal architecture and genetic characteristics are interpreted as derived features for Enteropneusta. As a consequence, our data do not contradict the hypothesis that a CNS evolved already in the stem group of Bilateria and thus was present in the LCAD.