Prototroch structure and innervation in the trochophore larva of Phyllodoce (Polychaeta)

The prototroch and prototroch nerve in trochophores of two Phyllodoce species are described at the ultrastructural level and interpreted with reference to the observed normal behavior of larvae during swimming. The prototroch is a complex structure consisting of four tiers of cells of which the second bears the main locomotory cilia. Cells in the other tiers also have cilia but are notable chiefly for the slender processes they send to the prototroch nerve and which evidently contribute to the sheath that surrounds the nerve. Neurociliary synapses were not observed, but the prototroch arrests when the frontal organ is touched and in response to cholinergic drugs. The arrests are only partial in that the cilia continue to beat, but in a restricted register. The mechanism responsible was not identified, but several possibilities are discussed. While the capacity to arrest could be intrinsic to the main trochal cells (i.e., tier 2), the absence of obvious regions of contact between these cells and the prototroch nerve increases the likelihood that the other tiers are also involved. The arrests could in fact result simply from physical interference between the cilia of adjacent tiers. The arrest response in Phyllodoce is compared with that seen in trochal bands in other spiralian larvae.

Structure and organization of the nervous system in the trochophore larva of spirobranchus

The trochophore larva of the polychaete Spirobranchus polycerus is described, based on ultrastructural surveys and three dimensional reconstructions, with emphasis on the structure and organization of the nervous system. A complete and detailed description is provided of the larval parts of the nervous system at the cellular level for the 48 h stage, by which time the larval system is fully developed in most respects. The adult nervous system, whose rudiments form a largely separate system of nerves and nerve cells, appears progressively during later development. Its principal structures, the brain, commissures and ventral cords, are briefly described based on an examination of the metatrochophore. The larval nervous system is entirely presegmental and is divisible into two parts: (1) a system of pretrochal cells and nerves arising from them that innervates the prototroch, linking it to the apical organ and the single larval eye, and (2) a system of intratrochal and intraepithelial nerves supplying the feeding apparatus of the larva. The latter consists of two nerves that encircle the pharynx and join basally beneath the cluster of cells that make up the basal pharyngeal complex. The pharyngeal nerves are then linked by means of a suboral complex of four sensory cells and their nerves to the nerves supplying the metatroch and neurotroch. The two parts of the larval system are anatomically separate and develop separately, each in association with its own organizational centres. These are: the apical organ and its central plexus in the case of the pretrochal system, and the suboral and pharyngeal complexes in the case of the oral and pharyngeal nerves. Like the larva itself, the larval nervous system is specialized and highly reduced. There are comparatively few cells, but a number of distinctive cell types. At 48 h, the larval system comprises 36 cells, including among these between 16 and 18 recognizably different types of sensory and non-sensory nerve cells and non-neural accessory cells. The majority of the cells are individually identifiable by morphology, ultrastructure and location, and are invariant or nearly so from larva to larva. The development of the system as a whole involves production of fibres by certain of these followed by fibre growth either along preestablished pathways, for example along the trochal bands or cells derived from these, or towards identifiable targets, for example, the apical plexus or pharyngeal complex. The resulting system varies little from larva to larva, and neurogenesis appears therefore to be a very precisely controlled developmental process. However, the individual cellular events that occur as parts of this process, do exhibit considerable diversity, both in terms of the cell types involved and of the types of interactions that occur between them, which raises the question of how the degree of developmental precision required by Spirobranchus is achieved. Cell lineage and lineage-dependent phenomena are clearly important, but it is not clear how concepts arising from linage studies in other organisms, e.g. in nematodes or other spiralia, should be applied in dealing with this particular case. Besides being anatomically separate, the two main parts of the larval nervous system evidently also have different evolutionary origins. Comparison of the Spirobranchus trochophore with the closely related M uller’s larva of polyclads supports the idea that the pretrochal system of the former is derived secondarily from the adult nervous system of some ancestral form despite the fact that it innervates a strictly larval organ, the protrotroch. Conversely, the nerves supplying the trochophore oral apparatus, which includes secondarily-derived adult structures like the pharynx, are of larval origin, probably derived by rearrangement from the nerves of a series of primitive trochal bands. The basic features of the oral apparatus in both Muller’s larva and the trochophore can be accounted for by assuming the existence of an ancestral larva with three circumferential trochal bands. Two of these would then be incorporated into the stomodeum as it evolved, with their nerves being retained as stomodeal structures in modern forms. This interpretation emphasizes (1) the evolutionary conservatism of the larval nervous system, i.e. larval nerves change less in organization and arrangement than the structures they innervate, which makes them important phylogenetic indicators, and (2) the importance of the evolutionary continuity of the mouth in protosomes as a justification for comparative studies of the oral apparatus in spiralian larvae that seek to establish homologies between them. In the case at hand, it is concluded that the oral apparatus of M uller’s larva and the trochopore, excluding the anus of the latter, are homologous. The functional operation of the larval nervous system in Spirobranchus is discussed briefly and in general terms. The larval nerve cells show a low degree of morphological differentiation, and specialized cell junctions (e.g., synapses) are largely absent, so only a rudimentary understanding of the circuitry of the larval system is possible. Further, it is not clear to what extent the morphological and ultrastructural differences between the various larval cell types and between larval and adult nerve cells reflect significant functional and physiological differences. It would be most interesting if such differences did exist: the trochophore would then have to be accorded independent status as an organism physiologically quite different from the adult polychaete with, in particular, a far more primitive nervous system.

Autoradiographic patterns of [3H]uridine incorporation during the development of the mollusc, Acmaea scutum

Autoradiographic experiments on eggs and embryos of the gastropod mollusc, Acmaea scutum, have provided information on the time of initiation of [3H]uridine incorporation into RNA, the relative degree to which different embryonic regions are participating, and the relative rates of incorporation at different times of development. The unfertilized egg does not incorporate exogenous [3H]uridine. After fertilization the first indication of incorporation in the stages examined was at the beginning of the sixth cleavage. There is a marked increase in the level of incorporation during the sixth cleavage which marks the beginning of gastrulation in these embryos. After this stage there is a gradual increase in incorporation per embryo, throughout development to the mid-veliger. Very little indication of significant differences in the level of incorporation among the cells of any embryo was found. The most pronounced exception was the lower activity of the anterior ectodermal cells of the trochophore larva. At later stages the derivatives of these cells were as active as the cells of other regions.

The effect of removing the polar lobe in centrifuged eggs of Dentalium

Classical evidence for the existence of morphogenetic substances was provided by experiments with spiralian eggs possessing a polar lobe: Ilyanassa (Crampton, 1896; Clement, 1952, 1956, 1962); Dentalium (Wilson, 1904); Chaetopterus (Tyler, 1930); Sabellaria (Hatt, 1932; Novikoff, 1938); and Mytilus (Rattenbury & Berg, 1954). Eggs from which the polar lobe had been removed developed into embryos with specific abnormalities. In Dentalium, after removal of the polar lobe at the trefoil stage, a trochophore larva is formed without post-trochal region and apical tuft. Removal of the polar lobe at second cleavage causes a larva without post-trochal region, but with an apical tuft. Wilson concluded that specific cytoplasmic materials essential to the formation of the apical tuft are contained in the first but no longer in the second polar lobe. Centrifuging the uncleaved egg just before first cleavage will disturb the normal distribution of substances.