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.
Macromere cell fates during sea urchin development