Hemichordate neurulation and the origin of the neural tube

Abstract

The origin of the body plan of our own phylum, Chordata, is one of the most fascinating questions in evolutionary biology. Yet, after more than a century of debate, the evolutionary origins of the neural tube and notochord remain unclear. Here we examine the development of the collar nerve cord in the hemichordate Balanoglossus simodensis and find shared gene expression patterns between hemichordate and chordate neurulation. Moreover, we show that the dorsal endoderm of the buccal tube and the stomochord expresses Hedgehog RNA, and it seems likely that collar cord cells can receive the signal. Our data suggest that the endoderm functions as an organizer to pattern the overlying collar cord, similar to the relationship between the notochord and neural tube in chordates. We propose that the origin of the core genetic mechanisms for the development of the notochord and the neural tube date back to the last common deuterostome ancestor.

Hemichordata

“…The collar cord within the collar region neurulates in a similar way as in Saccoglossus kowalevskii (Fig. 2.8 ) and eventually becomes situated subepidermally (Morgan 1894 ;Miyamoto and Wada 2013 ). From approx.…”

“…More condensed areas are present in the trunk region, where they constitute a dorsal and a ventral median longitudinal nerve cord, respectively (Bullock 1946 ;Knight-Jones 1952 ). Furthermore, the dorsal nerve cord continues anteriorly into the collar region to form the subepidermal, hollow collar cord that is reminiscent of the neural tube present in chordates (Morgan 1894 ;Kaul and Stach 2010 ;Miyamoto and Wada 2013 ). The collar cord links to the basiepidermal plexus at the base of the proboscis, that is, the proboscis stem.…”

“…This will provide an important resource to identify the genetic toolkit and regulatory elements of acorn worms. Protocols have been developed and optimised for whole mount or section in situ hybridisation or immunocytochemistry and are now routinely applied on several hemichordate species (Tagawa et al 1998b ;Okai et al 2000 ;Lowe et al 2003 ;Smith et al 2003 ;Sato et al 2009 ;Miyamoto et al 2010 ;Miyamoto and Wada 2013 ). In order to determine relative spatial gene expression for a set of genes, double fl uorescent in situ hybridisation has been developed in S. kowalevskii (Pani et al 2012 ).…”

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].…”

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

“…In another gene expression study, Cunningham & Casey [37] similarly proposed that a CNS was present and was composed of the trunk ventral nerve cord, trunk dorsal nerve cord and collar cord (figure 3f ); they likewise found that the peripheral nervous system included relatively few neurons at advanced developmental stages. Finally, Miyamoto & Wada [46] focused on the Hedgehog gene in developing enteropneusts and demonstrated its endodermal expression in the stomochord and roof of the buccal cavity, while the dorsal ectoderm was differentiating and invaginating to form the collar nerve cord. The situation was reminiscent of what happens in neurulating embryos of vertebrates when Hedgehog signalling from the notochord plays a key role in the genesis of the neural tube.…”