Ontogeny of the collar cord: Neurulation in the hemichordateSaccoglossus kowalevskii

Abstract

The chordate body plan is characterized by a central notochord, a pharynx perforated by gill pores, and a dorsal central nervous system. Despite progress in recent years, the evolutionary origin of each of theses characters remains controversial. In the case of the nervous system, two contradictory hypotheses exist. In the first, the chordate nervous system is derived directly from a diffuse nerve net; whereas, the second proposes that a centralized nervous system is found in hemichordates and, therefore, predates chordate evolution. Here, we document the ontogeny of the collar cord of the enteropneust Saccoglossus kowalevskii using transmission electron microscopy and 3D-reconstruction based on completely serially sectioned stages. We demonstrate that the collar cord develops from a middorsal neural plate that is closed in a posterior to anterior direction. Transversely oriented ependymal cells possessing myofilaments mediate this morphogenetic process and surround the remnants of the neural canal in juveniles. A mid-dorsal glandular complex is present in the collar. The collar cord in juveniles is clearly separated into a dorsal saddle-like region of somata and a ventral neuropil. We characterize two cell types in the somata region, giant neurons and ependymal cells. Giant neurons connect via a peculiar cell junction that seems to function in intercellular communication. Synaptic junctions containing different vesicle types are present in the neuropil. These findings support the hypotheses that the collar cord constitutes a centralized element of the nervous system and that the morphogenetic process in the ontogeny of the collar cord is homologous to neurulation in chordates. Moreover, we suggest that these similarities are indicative of a close phylogenetic relationship between enteropneusts and chordates.

Hemichordate neurulation and the origin of the neural tube

“…1p-t). Note that although some enteropneust species lack an obvious tubular collar cord because the central lumen of the cord is filled with cells, their collar cord still forms via invagination of the neural plate 16 .…”

“…The ventral nerve cord exists only in the trunk region and is connected to the dorsal nerve cord via the prebranchial nerve ring. Among them, only the collar cord has tubular organization and thus proposed to be a homologous organ to the neural tube 4,8,[15][16][17] . However, this homology is still controversial 14,16 , because the enteropneust collar cord, unlike the much more extensive neural tubes of chordates, runs along only a relatively short stretch of the anteroposterior axis 18 .…”

“…Among them, only the collar cord has tubular organization and thus proposed to be a homologous organ to the neural tube 4,8,[15][16][17] . However, this homology is still controversial 14,16 , because the enteropneust collar cord, unlike the much more extensive neural tubes of chordates, runs along only a relatively short stretch of the anteroposterior axis 18 . In addition, the dorsal position of the collar cord is not consistent with the dorsoventral axis inversion in the chordate lineage 9,18 .…”

Chordate evolution and the three-phylum system

“…However, several studies demonstrate the formation of a dorsal, neural tube-like structure in acorn worm adults [65][66][67], which is reminiscent of dorsal, neural tube formation of chordate embryos. It should be noted that the inversion hypothesis cannot necessarily explain the occurrence of chordate-specific structures or the notochord [18,55].…”

The origin and evolution of chordate nervous systems

“…There is no evident brain in enteropneust hemichordates, although the proboscis ectoderm contains many neurons. The dorsal nerve cord does undergo a sort of neurulation in the region of the collar and has most often been proposed as homologous to the chordate nerve cord [58,59]. However, some authors could not decide which of the two nerve cords was homologous to the chordate one [60].…”