Development of the enteropneust Ptychodera flava: Ciliary bands and nervous system

Abstract

Ripe specimens of Ptychodera flava were collected at Paiko Peninsula, Oahu, Hawaii, USA, and the development from egg to tornaria larva was followed in the laboratory. To complete the series, large tornaria larvae were collected from the plankton off the nearby Ala Moana Beach, and followed through metamorphosis to a juvenile stage with four pairs of gill slits. Ciliary band development was examined by scanning electron microscopy, and the development of the serotonergic nervous system was followed by means of immunostaining. The development of the apical tuft and neotroch (circumoral/perioral ciliary band) and their subsequent degeneration accorded fully with previous descriptions. A perianal ciliary ring of separate cilia develops just after hatching. This later develops a midventral extension, the neurotroch, extending to the neotroch posterior to the mouth. The cilia of this ring apparently beat diaplectically, with the effective stroke in the clockwise direction when seen from behind. An additional ring of cilia develops several days later anterior to the perianal ring. This opisthotroch (called telotroch by previous authors) consists at first of separate cilia, but later they became organized as large compound cilia. The apical tuft disappears after about a week, the neotroch degenerates at the transition to the Agassiz stage, and the opisthotroch degenerates just after metamorphosis. The serotonergic nervous system of the fully grown tornaria consists of an apical ganglion with many perikarya, a paired lateral group of perikarya on the postoral ciliary band, and scattered perikarya along the opisthotroch. Serotonergic processes are found along the ciliary bands except for the ventral and perianal ciliary bands and are scattered along the epidermis. At the Spengel stage and at metamorphosis (Agassiz stage), the processes along the ciliary bands are concentrated in the three ciliated food grooves so as to form three separate nerves, and are retained on the proboscis at least until 2-3 gill slit stage. No serotonergic processes were found to extend from the proboscis to the collar region, and no serotonergic neurons were observed in the collar cord or in the ventral nerve cord. Our results therefore do not provide any clues as to the origin of the chordate neural tube relative to the dorsal-ventral orientation of the enteropneusts.

Hemichordata

“…For instance, the mesoand metacoels in Saccoglossus kowalevskii and Glandiceps hacksi (Urata et al 2014 ) develop from separate evaginations of the middle and posterior endodermal region (Bateson 1884 ;Kaul-Strehlow and Stach 2013 ), whereas in Balanoglossus clavigerus and B. misakiensis , they emerge from a single pair of evaginations that eventually subdivide into the more anterior mesocoels and posterior metacoels (Stiasny 1914b ;Spengel 1893 ;Urata and Yamaguchi 2004 ). A closer look at other enteropneust species and echinoderms reveals enormous intraphyletic variation of coelom formation (for review, see Nielsen 2011 ). Although an ancestral deuterostome pattern may be hard to reconstruct, it seems that at least in all cases, the mesoderm is formed from the endoderm.…”

“…Homology of this heart-glomerulus complex of hemichordates with the axial complex of echinoderms is widely accepted, because of a number of functional and structural similarities (Balser and Ruppert 1990 ;Mayer and Bartolomaeus 2003 ;Kaul-Strehlow and Stach 2011 ;Nielsen 2011 ;Merker et al 2013 ). These include a contractile pericardium (pulsatile vesicle in echinoderms), fi ltrating podocytes on the protocoelic (axocoelic) side, an excretory hydropore and a glomerulus.…”

“…Pterobranchia is a small taxon consisting of roughly 25 species, of which all are colonial and semi-sessile animals (Cameron 2005 ;Nielsen 2011 ). They are tube dwellers that secrete the socalled coenecium from the anterior mouth shield ( Fig.…”

Larval nervous systems: true larval and precocious adult

“…However, this must be interpreted as an example of homoplasy (Nielsen and Martinez, 2003;Nielsen, 2006). The tornaria larva has a posterior ring of large, compound cilia, which has often been called a telotroch, but its homology is uncertain (Nielsen and Hay-Schmidt, 2007). There is a nerve along this ciliary band (Lacalli and Gilmour, 2001), and both the ciliary band and the nerve begin to degenerate at metamorphosis.…”

Evolutionary crossroads in developmental biology: hemichordates

“…4L) prior to metamorphosis (Fig. 4M,N) (Hadfield, 1975;Tagawa et al, 1998b;Nielsen and Hay-Schmidt, 2007). Competent larvae are composed mainly of anterior structures and can be collected by…”