Homology of echinoderm radial nerve cords and the chordate neural tube???

In a recent issue of Evolution & Development, Haag (2005) discussed the origin of the chordate central nervous system (CNS) in relation to some new and old papers on gene expression and embryology of echinoderms. One of the conclusions was that rather than comparing the ciliary bands of echinoderm larvae with the chordate neural tube ‘‘It would be better to . or to compare the development of the adult CNS of echinoderms with that of chordates. ’’ More explicitly he stated that ‘‘The sea urchin does indeed have a strong candidate for a homologue of the chordate CNS, but it is not the ciliary band, nor is it even present in the pluteus. Rather, it is comprised of the radial nerves and the circumoral nerve ring of the adult, which does not begin to form until the echinus rudiment (. . .) is well developed. ’’ This view is based on observations both from morphology and from gene expression, but in my opinion it completely disregards historical–morphological homology and modern phylogenetic results. Neurulation, that is the formation of a tubular nerve cord through a longitudinal invagination from the ectoderm, is a textbook favorite of chordate development, and similar processes are seen during the development of the ventral radial nerve cords in some echinoderm groups, and in the development of the collar cord of some enteropneusts. The chordate neural tube (spinal cord) is of course a very prominent feature of the vertebrates and amphioxus, but in urochordates its posterior, tubular part contains no nerve cells, and it is lost at metamorphosis (Burighel and Cloney 1997), except the appendicularians (Fenaux 1998). The phylogenetic significance of this is not clear. In some enteropneusts, the collar cord develops through a process very similar to the chordate neurulation (Dawydoff 1948). The resulting structure is poorly known, but it is clearly not a nerve cord with integrative functions like that of the chordate nerve cord (Cameron and Mackie 1996). The living adult echinoderms are almost all pentameric with five rays extending from a central mouth. Their ontogeny demonstrates that this type of symmetry develops from a bilateral symmetry in which the left side outgrows the right side. Especially, the left mesosome with the left mesocoel, which becomes the water vascular system, develops much stronger than the right side, in which the mesocoel becomes the tiny heart vesicle. The pentamery is also very pronounced in the nervous system, which comprises a number of subsystems. The ventral system develops around the new mouth of the adult rudiment in echinoids and asteroids, whereas it differentiates around the larval oesophagus in ophiuroids, which have a less complicated metamorphosis. It consists of a circumoral nerve ring without cell bodies and five radial nerve cords, each comprising an ectodermal (ectoneural) and a mesodermal (hyponeural) component (Ruppert et al. 2004). In ophiuroids, echinoids, and holothurians, the ectoneural nerve cords become internalized at metamorphosis through a neurulation process which forms the epineural canals, as nicely documented already by Ubisch (1913). Some authors (e.g., Smith 1988, Ax 2001, Ruppert et al. 2004) consider this character as a synapomorphy of these three classes, collectively called Cryptosyringida, and this implies that this character is not ancestral in the echinoderms. The development of the echinoderms clearly demonstrates that their radial nerve cords are outgrowths from the left side of a mesosomal nerve, which becomes ring shaped. They cannot be regarded as homologous to the chordate neural tube. As also stated by Haag, the same genes are probably found and expressed in nervous systems of all bilaterians, which indicates that all bilaterian nervous systems have evolved from an ancestral system applying these genes. However, it is well known that genes can be co-opted (see, e.g., True and Carroll 2002), and it appears that the same genes are often involved in the organization of similar structures. A good example could be the function of tinman/ceh-22/nkx2.5 in the organization of tubular contractile structures, viz. the mesodermal hearts of insects and vertebrates and the ectodermal myoepithelial pharynx of nematodes, respectively (Haun et al. 1998). However, this is clearly no proof of historical–morphological homology. Nielsen and Martinez (2003) proposed the term homocratic for such structures which are governed by identical genes, in order to distinguish them from structures which are morphologically homologous. EVOLUTION & DEVELOPMENT 8:1, 1–2 (2006)