Developmental analysis reveals labial and subradular ganglia and the primary framework of the nervous system in nudibranch gastropods

Abstract

Previous ultrastructural observations on late stage larvae of dorid nudibranchs (Gastropoda, Opisthobranchia) revealed two pairs of ganglia within the base of the foot that do not have obvious counterparts in existing descriptions of other gastropod larvae [Chia and Koss (1989). Cell Tiss. Res. 256:17-26.] One of these ganglionic pairs has been implicated in the initiation of settlement preceding metamorphosis [Arkett et al. (1989). Biol. Bull. 176:155-160.] By examining neurogenesis in sequential larval stages, I have found that the pattern of connectives and commissures associated with these enigmatic ganglia is comparable to patterns found in less consolidated adult nervous systems of chitons, monoplacophorans, and archaeogastropods. These comparative data suggest that the two pairs of ganglia in dorid nudibranch larvae are homologues of labial and subradular ganglia. The labial ganglia become incorporated into the cerebral ganglia at metamorphosis. In an attempt to integrate anatomical and developmental observations with behavioral and neurophysiological results, I suggest that receptor cells of the larval labial ganglia may become postmetamorphic primary mechanoreceptors of the oral tube, which have central cell bodies within the "cerebral" ganglia and which help coordinate feeding. Results of this study also address a larger evolutionary issue by questioning the traditional model of an ancestral molluscan nervous system that consists of four longitudinal nerve cords that arise from separate sites along a circumesophageal nerve ring. This pattern results from secondary connections in nudibranchs and possibly other molluscs. The primary condition of a single axon bundle emerging from each cerebral ganglion is more similar to the developing nervous system in polychaete annelids than what has been recognized previously.

Similarities in Form and Developmental Sequence for Three Larval Shell Muscles in Nudibranch Gastropods

“…Sections through progressively older larval stages (compare Figs 9, 10 with Figs 14-16) show this to be incorrect. These observations underscore the fact that the proximal portion of what is called the foot rudiment in young nudibranch larvae is actually presumptive ventral lip tissue (also see Page 1993).…”

Gangliogenesis in the prosobranch gastropod Ilyanassa obsoleta

“…In Ilyanassa (Lin and Leise, 1994;Leise, 1996) and in the sea hare Aplysia californica (Marois et al, 1993), a distinct apical ganglion has been identified that lies above the dorsal cerebral commissure. This apical ganglion is most likely a developmental outgrowth of the trochophore apical plate (Raven, 1966) and an evolutionary enlargement of an apical or cephalic sensory organ like the ones described in other gastropods (Conklin, 1897;Fretter and Graham, 1962;D'Asaro, 1969;Bonar, 1978a,b;Morse et al, 1980;Bickell and Kempf, 1983;Chia and Koss, 1984;Marois and Carew, 1990;Kempf et al, 1991;Page, 1992aPage, , 1993Page, , 1994. Both Aplysia and Ilyanassa have relatively long-lived planktotrophic veligers that are large at metamorphic competence in comparison to the non-feeding larvae of many of their opisthobranch relatives.…”

Histochemical localization of FMRFamide, serotonin and catecholamines in embryonic Crepidula fornicata (Gastropoda, Prosobranchia)

“…An apical organ has been reported in some of the Gastropoda (Bonar 1977(Bonar , 1978Chia and Koss 1984;Kempf et al 1991Kempf et al , 1997Lin and Leise 1996a, b;Marois and Carew 1997c;Moor 1983;Page 1993;Raineri 1995;Raineri and Ospovat 1994) and the Bivalvia (Raineri 1995;Raineri and Ospovat 1994) as well as many other swimming invertebrate larvae (see for example, Hay- Schmidt 1990a-c, 1995Lacalli 1981Lacalli , 1994. In many molluscs (Bonar 1978;Chia and Koss 1984;Kempf et al 1997;Leise 1996;Marois and Carew 1997a, b) and other invertebrates (see Lacalli 1994), the apical organ possesses flask-or vase-shaped cells with protruding cilia at the epithelial surface.…”