Nervous system development of the sea cucumber Stichopus japonicus

The nervous system development of the sea cucumber Stichopus japonicus was investigated to explore the development of the bilateral larval nervous system into the pentaradial adult form typical of echinoderms. The first nerve cells were detected in the apical region of epidermis in the late gastrula. In the auricularia larvae, nerve tracts were seen along the ciliary band. There was a pair of bilateral apical ganglia consisted of serotonergic nerve cells lined along the ciliary bands. During the transition to the doliolaria larvae, the nerve tracts rearranged together with the ciliary bands, but they were not segmented and remained continuous. The doliolaria larvae possessed nerves along the ciliary rings but strongly retained the features of auricularia larvae nerve pattern. The adult nervous system began to develop inside the doliolaria larvae before the larval nervous system disappears. None of the larval nervous system was observed to be incorporated into the adult nervous system with immunohistochemistry. Since S. japonicus are known to possess an ancestral mode of development for echinoderms, these results suggest that the larval nervous system and the adult nervous system were probably formed independently in the last common ancestor of echinoderms.     

The structure of the nervous system of the pluteus larva of Strongylocentrotus purpuratus

Summary Tissues that have the ultrastructural characteristics of nervous tissues are associated with ciliary and muscular elements of the pluteus larva of Strongylocentrotus purpuratus. The nerve cells are found along the margins of the ciliary bands, which are composed predominantly of spindle-shaped ciliated cells. The nerve cells contribute axonal processes to a tract of axons, which runs at the base of the ciliary band throughout its length. Axonal tracts, in the esophagus, lie beneath the circumesophageal muscles. Branched microvilli, which have been interpreted as sensory receptors, are located on the oral side of the main ciliary band and connect with the nerve cells in the ciliary band. The nervous structures described here, and other tissues of the pluteus that have been previously described as nervous, are compared on the basis of their association with receptor and effector organs, and their ultrastructural characteristics.     

Development and neural organization of the tornaria larva of the Hawaiian hemichordate, Ptychodera flava

We report scanning and transmission electron microscopic studies of the early development of the Hawaiian acorn worm, Ptychodera flava. In addition, we provide an immunohistochemical identification of the larval nervous system. Development occurs and is constrained within the stout chorion and fertilization envelope that forms upon the release of the cortical granules in the cytoplasm of the egg. The blastula consists of tall columnar blastomeres encircling a small blastocoel. Typical gastrulation occurs and a definitive tornaria is formed compressed within the fertilization envelope. The young tornaria hatches at 44 hr and begins to expand. The major circumoral ciliary band that crosses the dorsal surface and passes preorally and postorally is well developed. In addition, we find a nascent telotroch, as well as a midventral ciliary band that is already clearly developed. The epithelium of tornaria is a mosaic of monociliated and multiciliated cells. Immunohistochemistry with a novel neural marker, monoclonal antibody 1E11, first detects nerve cells at the gastrula stage. In tornaria, 1E11 staining nerve cells occur throughout the length of the ciliary bands, in the apical organ, in a circle around the mouth, in the esophageal epithelium and in circumpylorus regions. Axon(s) and apical processes extend from the nerve cell bodies and run in tracks along the ciliary bands. Axons extending from the preoral and postoral bands extend into the oral field and form a network. The tornaria nervous system with ciliary bands and an apical organ is rather similar to the echinoderm bipinnaria larvae.     

Divergent patterns of neural development in larval echinoids and asteroids

The development and organization of the nervous systems of echinoderm larvae are incompletely described. We describe the development and organization of the larval nervous systems of Strongylocentrotus purpuratus and Asterina pectinifera using a novel antibody, 1E11, that appears to be neuron specific. In the early pluteus, the antibody reveals all known neural structures: apical ganglion, oral ganglia, lateral ganglia, and an array of neurons and neurites in the ciliary band, the esophagus, and the intestine. The antibody also reveals several novel features, such as neurites that extend to the posterior end of the larva and additional neurons in the apical ganglion. Similarly, in asteroid larvae the antibody binds to all known neural structures and identifies novel features, including large numbers of neurons in the ciliary bands, a network of neurites under the oral epidermis, cell bodies in the esophagus, and a network of neurites in the intestine. The 1E11 antigen is expressed during gastrulation and can be used to trace the ontogenies of the nervous systems. In S. purpuratus, a small number of neuroblasts arise in the oral ectoderm in late gastrulae. The cells are adjacent to the presumptive ciliary bands, where they project neurites with growth cone-like endings that interconnect the neurons. In A. pectinifera, a large number of neuroblasts appear scattered throughout the ectoderm of gastrulae. The cells aggregate in the developing ciliary bands and then project neurites under the oral epidermis. Although there are several shared features of the larval nervous systems of echinoids and asteroids, the patterns of development reveal fundamental differences in neural ontogeny.     

On the morphology of the central nervous system in larval stages ofCarcinus maenas L. (Decapoda,Brachyura)

We investigated the morphology of the central nervous system throughout the larval development ofCarcinus maenas. For that purpose single larvae were reared in the laboratory from hatching through metamorphosis. Complete series of whole mout semithin sections were obtained from individuals of all successive larval stages and analysed with a light microscope. Morphological feature and spatial arrangement of discernable neural cell clusters, fibre tracts and neuropile are described and compared with the adult pattern. We found that most of the morphological features characterizing the adult nervous system are already present in the zoea-1. Nevertheless, there are marked differences with respect to the arrangement of nerve cell bodies, organization of cerebral neuropile, and disposition of ganglia in the ventral nerve cord. It appears that complexity of the central nervous neuropile is selectively altered during postmetamorphotic development, probably reflecting adaptive changes of sensory-motor integration in response to behavioural maturation. In contrast, during larval development there was little change in the overall structural organization of the central nervous system despite some considerable growth. However, the transition from zoea-4 to megalopa brings about multiple fundamental changes in larval morphology and behavioural pattern. Since central nervous integration should properly adapt to the altered behavioural repertoire of the megalopa, it seems necessary to ask in which respect synaptic rearrangement might characterize development of the central nervous system.     

Development of the Nervous System of Sea Urchin Embryos: Formation of Ciliary Bands and the Appearance of Two Types of Ectoneural Cells in the Pluteus

An ultrastructural study of the larval integument of the sea urchin, Hemicentrotus pulcherrimus , was conducted with special emphasis on the development of the nervous system in relation to the formation of ciliary bands. In the integument of 4-armed pluteus larvae, cells associated with the ciliary band, which have 200 nm-thick projections at their apices, and cells in the squamous epithelium, which have a cilium and long, fine radiating processes in the apical region, were observed. Both cell types have axons at their basal ends that form nerve bundles beneath the ciliary bands, where the axons make contact with ectodermal effector cells with motile cilia. The cilia and other apical projections of these ectoneural cells run parallel to the surface of the cells, and are under the hyaline layer. The axoneme of the cilium has a typical "9 + 2" microtubular arrangement, but generally has no dynein arms. These ectoneural cells are more frequent on the oral surface than on the antioral surface.     

A developmental study of serotonin-immunoreactive neurons in the larval central nervous system of the spider crabHyas araneus (Decapoda,Brachyura)

Larval development in crabs is characterized by a striking double metamorphosis in the course of which the animals change from a pelagic to a benthic life style. The larval central nervous system has to provide an adequate behavioural repertoire during this transition. Thus, processes of neuronal reorganization and refinement of the early larval nervous system could be expected to occur in the metamorphosing animal. In order to follow identified sets of neurons throughout metamorphosis, whole mount preparations of the brain and ventral nerve cord of laboratory reared spider crab larvae (Hyas araneus) were labelled with an antibody against the neurotransmitter serotonin. The system of serotonin-immunoreactive cell bodies, fibres and neuropils is well-developed in newly hatched larvae. Most immunoreative structures are located in the protocerebrum, with fewer in the suboesophaegeal ganglia, while the thoracic and abdominal ganglia initially comprise only a small number of serotonergic neurons and fibres. However, there are significant alterations in the staining pattern through larval development, some of which are correlated to metamorphic events. Accordingly, new serotonin-immunoreactive cells are added to the early larval set and the system of immunoreactive fibres is refined. These results are compared to the serotonergic innervation in other decapod crustaceans.     

A Distinctive Nerve Cell Type Common to Diverse Deuterostome Larvae: Comparative Data from Echinoderms,Hemichordates and Amphioxus

Abstract The larval ciliary bands of echinoderm bipinnaria and pluteus larvae and the hemichordate tornaria contain similar multipolar or bipolar nerve cells with unusual apical processes that run across the surface of the band between the bases of its cilia. We report on some distinctive ultrastructural features of these cells. Among these are specialized junctions that occur between the cells' apical processes and adjacent ciliary band cells near the base of each cilium. Such structures are best developed in pluteus larvae. Many nerve cells in the larval spinal cord of amphioxus also have large apical processes that cross the central lumen of the cord. We interpret our observations on these cells in terms of Garstang's hypothesis, which derives the chordate neural tube from a larval ciliary band, and suggest that multipolar cells like those in echinoderm and tornaria bands may be the antecedents of some categories of neurons in the chordate spinal cord.     

Peptidergic and serotonergic immunoreactivity in the metamorphosing ophiopluteus of Ophiactis resiliens (Echinodermata, Ophiuroidea)

Abstract. Antibodies against the echinoderm-specific neuropeptide S1 and against 5HT were used to examine the fate of the larval nervous system during metamorphosis in the ophiuroid Ophiactis resiliens . In contrast to most echinoderms, the onset of peptidergic and serotonergic expression was delayed to the advanced ophiopluteus stage, in particular for 5HT. In advanced ophioplutei, peptidergic immunoreactivity was located in simple fibres associated with the ciliated bands, a stomach nerve ring, and cells along the antero-lateral arms. 5HT immunoreactivity was concentrated in 2 oral ganglia in the adoral projections, located at the posterior rim of the mouth. Clusters of 5HT-positive cells were also found along the antero-lateral arms. The ophiopluteus lacked a serotonergic (or peptidergic) anterior ganglion. In echinoids, holothuroids, and crinoids, anterior ganglia are thought to have a sensory role in settlement and metamorphosis. Given that ophioplutei metamorphose in the plankton and that larval structures degenerate before settlement, the absence of apical ganglia correlates with the lack of a functional role for larval structures in substrate selection and settlement. Although most of the larval nervous system degenerated during metamorphosis, the adoral projections and associated oral ganglia appeared to be incorporated into the juvenile mouth, suggesting a potential role for larval neurons in contributing to oral neuronal structures in the adult. S1-positive neurons and fibres in the rudiment developed de novo and in parallel with development of the epineural canal. This structure gives rise to the primordia of the adult circumoral nerve ring and radial nerves, indicating that differentiation of the adult nervous system begins in the early stages of metamorphosis.     

Fine structure of the doliolaria larva of the feather star Florometra serratissima (Echinodermata: Crinoidea), with special emphasis on the nervous system

The epidermis of the doliolaria larva of the Florometra serratissima is differentiated into distinct structures including an apical organ, adhesive pit, ganglion, ciliary bands, nerve plexus, and vestibular invagination. All these structures possess unique cell-types, suggesting that they are functionally specialized in the larva, except the vestibular invagination that becomes the postmetamorphic stomodeum. The epidermis also contains yellow cells, amoeboid-like cells, and secretory cells. The enteric sac, hydrocoel, axocoel, and somatocoels have differentiated but are probably not functional in the doliolaria stage. Mesenchymal cells, around the enteric sac and coeloms, appear to be actively secreting the endoskeleton and connective tissue fibers. The nervous system is composed of a nerve plexus, ganglion, and sensory receptor cells in the apical organ. The apical organ is a larval specialization of the anterior end; the ganglion is located in the base of the epidermis at the anterior dorsal end of the larva. The nerve plexus underlies most of the epidermis, although it is more prominent in the anterior region. Here, processes from sensory receptor cells of the apical organ, as well as those from nerve cells, contribute to the plexus. These processes contain one or a combination of organelles including vesicles, vacuoles, microtubules, and mitochondria. The configuration of glyoxylic acid-induced fluorescence, revealing catecholamine activity, correlates to the apical organ, nerve cells, and nerve plexus. Morphological evidence suggests that the nervous system may function in initiation and control of settlement, attachment, and metamorphosis. The crinoid larval nervous system is discussed and compared to that found in other larval echinoderms.     

Organization of the Nervous System and Sensory Organs in the Larva of the Marine Bryozoan Bowerbankia gracilis (Ctenostomata: Vesiculariidae): Functional Significance of the Apical Disc and Pyriform Organ

The organization of the nervous system and the histology and ultrastructure of the apical disc and the pyriform organ have been investigated by serial sections with light and electron microscopy for the larva of the vesiculariid ctenostome bryozoan Bowerbankia gracilis Leidy 1855. The nervous system consists of four major internal components: (1) a median-anterior nerve nodule; (2) an equatorial, subcoronal nerve ring; (3) paired aboral nerve cords; (4) paired antero-lateral nerve tracts. The nervous system is associated with the ciliated larval surface at the apical disc, the pyriform organ, the corona and the intercoronal cells. The paired aboral nerve cords extend from the apical disc to the nerve nodule, which gives rise to the paired antero-lateral nerve tracts to the pyriform organ and to paired lateral tracts that form the equatorial nerve ring. Ultrastructural evidence is provided for the designation of primary sensory cells in the neural plate of the apical disc and in the juxtapapillary regions of the pyriform organ. Efferent synapses are described between the equatorial nerve ring and the overlying coronal cells, which constitute the primary locomotory organ of the larva. The repertoire of potential functions of the apical disc and pyriform organ are discussed. It is concluded that the apical disc and pyriform organ constitute larval sensory organs involved in orientation and substrate selection, respectively. Their association with the major effector organs of the larva (the corona and the musculature) via the nervous system supports this interpretation.     

Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria

The anatomy and cellular organization of serotonergic neurons in the echinoderm apical organ exhibits class-specific features in dipleurula-type (auricularia, bipinnaria) and pluteus-type (ophiopluteus, echinopluteus) larvae. The apical organ forms in association with anterior ciliary structures. Apical organs in dipleurula-type larvae are more similar to each other than to those in either of the pluteus forms. In asteroid bipinnaria and holothuroid auricularia the apical organ spans ciliary band sectors that traverse the anterior-most end of the larvae. The asteroid apical organ also has prominent bilateral ganglia that connect with an apical network of neurites. The simple apical organ of the auricularia is similar to that in the hemichordate tornaria larva. Apical organs in pluteus forms differ markedly. The echinopluteus apical organ is a single structure on the oral hood between the larval arms comprised of two groups of cells joined by a commissure and its cell bodies do not reside in the ciliary band. Ophioplutei have a pair of lateral ganglia associated with the ciliary band of larval arms that may be the ophiuroid apical organ. Comparative anatomy of the serotonergic nervous systems in the dipleurula-type larvae of the Ambulacraria (Echinodermata+Hemichordata) suggests that the apical organ of this deuterostome clade originated as a simple bilaterally symmetric nerve plexus spanning ciliary band sectors at the anterior end of the larva. From this structure, the apical organ has been independently modified in association with the evolution of class-specific larval forms.     

Development of the larval nervous system of the sand dollar,Dendraster excentricus

Transformation of the gastrula to the pluteus includes development of the ability of the larva to control the direction of ciliary beat and coordinate activities of the ciliary band with activities of the esophageal muscles (48-60 h, 15 degrees C). Glyoxylic acid-induced fluorescence shows several cells of the animal plate to contain catecholamines in the 36-h gastrula. As the ectoderm thickens to form the ciliary band (36 48 h), the catecholamine-containing cells increase in number and occur dispersed throughout the band. Tissues with the ultrastructural characteristics of nerves first became apparent associated with the ciliary band in 60-h larvae. The coincident development of coordinated behaviour and the appearance of cells with ultrastructural and histochemical characteristics of nerves suggests that the larval nervous system is derived at least in part from cells of the animal plate and develops in association with the ciliary bands.     

Structure of the caudal neural tube in an ascidian larva: Vestiges of its possible evolutionary origin from a ciliated band

Ultrastructural analysis and differential immunocytochemical staining with two antitubulin monoclonal antibodies were used to reexamine the organization and development of the neural tube in the larva of an ascidian, Ciona intestinalis, in appraisal of a theory that the dorsal tubular nervous system of the chordates evolved from two halves of a ciliated band in an auricularia-like larva of the kind found in echinoderms and hemichordates. One of the antibodies stained cilia in the nervous system and elsewhere; the other reacted primarily with neuronal axons. The caudal neural tube consists of four rows of large ciliated ependymal-glial cells enclosing an axial neural canal into which their single cilia extend. Two ventrolateral nerve tracts, containing axons, arise in the posterior brain region and extend along the length of the caudal tube, partially surrounded by the ependymal cells. The nonnervous, ciliated, ependymal neural tube of the ascidian larva with its two associated nerve tracts survives as a primitive early condition that could result from a ciliated band transformation. Tissues in the distal-most part of the ascidian larval tail have cell lineage origins that indicate an evolutionary history different from those in the proximal majority of the tail. The ependymal cells in this presumed later addition to the tail are not ciliated, although all of the others in the caudal ependymal tube appear to be.     

Nervous system development of two crinoid species, the sea lily Metacrinus rotundus and the feather star Oxycomanthus japonicus

Nervous system development in echinoderms has been well documented, especially for sea urchins and starfish. However, that of crinoids, the most basal group of extant echinoderms, has been poorly studied due to difficulties in obtaining their larvae. In this paper, we report nervous system development from two species of crinoids, from hatching to late doliolaria larvae in the sea lily Metacrinus rotundus and from hatching to cystidean stages after settlement in the feather star Oxycomanthus japonicus. The two species showed a similar larval nervous system pattern with an extensive anterior larval ganglion. The ganglion was similar to that in sea urchins which is generally regarded as derived. In contrast with other echinoderm and hemichordate larvae, synaptotagmin antibody 1E11 failed to reveal ciliary band nerve tracts. Basiepithelial nerve cells formed a net-like structure in the M. rotundus doliolaria larvae. In O. japonicus, the larval ganglion was still present 1 day after settlement when the adult nervous system began to appear inside the crown. Stalk nerves originated from the crown and extended down the stalk, but had no connections with the remaining larval ganglion at the base of the stalk. The larval nervous system was not incorporated into the adult nervous system, and the larval ganglion later disappeared. The aboral nerve center, the dominant nervous system in adult crinoids, was formed at the early cystidean stage, considerably earlier than previously suggested. Through comparisons with nervous system development in other ambulacraria, we suggest the possible nervous system development pattern of the echinoderm ancestor and provide new implications on the evolutionary history of echinoderm life cycles.     

The Sense Organs and Ventral Ganglion of Sagitta (Chaetognatha)

This paper describes some features of the chaetognath nervous system from ultrastructural observations and observations on material stained with specific techniques for nervous tissue, and from records of the activity of the locomotor muscles and ventral ganglion. Sensory cells grouped on the ventral surface of the head bear ciliary processes (some with multiple tubules), and are probably in connexion with the central nervous system by their own axons, unlike the sensory cells of the hair fan vibration receptors of head and body. The ventral ganglion is motor to the locomotor muscles of the body, and controls the rhythmic locomotor activity of the animal. Electrical events associated with contraction of these muscles are compound non-overshooting spike-like potentials. The ventral ganglion contains several large nerve fibres constant in position and connexions in different individuals. Some of these arise from cells in the ganglia of the head, and pass to the ventral ganglion, others from cells within the ventral ganglion, and probably supply the ciliary hair fan receptors of the body, whilst the motor axons issuing from the ventral ganglion are smaller in diameter. The ganglion is arranged on a ladder-like plan, and axons of the lateral cell bodies cross the central neuropil transversely before they contribute to the longitudinal tracts or pass out in the radial nerves. Synapses in the neuropil contain 30–40 nm electron lucent vesicles; the transmitter is unknown, but is unlikely to be either acetylcholine or l -glutamate. Occasional larger electron dense vesicles up to 70 nm in diameter are also found within nerve fibres of the neuropil. It is concluded that the arrangement of the peripheral nervous system is unlike that of several groups which have been suggested as related to chaetognaths.     

Embryonic and post-embryonic development of the polyclad flatworm Maritigrella crozieri; implications for the evolution of spiralian life history traits

Background

Planktonic life history stages of spiralians share some muscular, nervous and ciliary system characters in common. The distribution of these characters is patchy and can be interpreted either as the result of convergent evolution, or as the retention of primitive spiralian larval features. To understand the evolution of these characters adequate taxon sampling across the Spiralia is necessary. Polyclad flatworms are the only free-living Platyhelminthes that exhibit a continuum of developmental modes, with direct development at one extreme, and indirect development via a trochophore-like larval stage at the other. Here I present embryological and larval anatomical data from the indirect developing polyclad Maritrigrella crozieri, and consider these data within a comparative spiralian context.

Results

After 196 h hours of embryonic development, M. crozieri hatches as a swimming, planktotrophic larva. Larval myoanatomy consists of an orthogonal grid of circular and longitudinal body wall muscles plus parenchymal muscles. Diagonal body wall muscles develop over the planktonic period. Larval neuroanatomy consists of an apical plate, neuropile, paired nerve cords, a peri-oral nerve ring, a medial nerve, a ciliary band nerve net and putative ciliary photoreceptors. Apical neural elements develop first followed by posterior perikarya and later pharyngeal neural elements. The ciliated larva is encircled by a continuous, pre-oral band of longer cilia, which follows the distal margins of the lobes; it also possesses distinct apical and caudal cilia.

Conclusions

Within polyclads heterochronic shifts in the development of diagonal bodywall and pharyngeal muscles are correlated with life history strategies and feeding requirements. In contrast to many spiralians, M. crozieri hatch with well developed nervous and muscular systems. Comparisons of the ciliary bands and apical organs amongst spiralian planktonic life-stages reveal differences; M. crozieri lack a distinct ciliary band muscle and flask-shaped epidermal serotonergic cells of the apical organ. Based on current phylogenies, the distribution of ciliary bands and apical organs between polyclads and other spiralians is not congruent with a hypothesis of homology. However, some similarities exist, and this study sets an anatomical framework from which to investigate cellular and molecular mechanisms that will help to distinguish between parallelism, convergence and homology of these features.     

Ontogeny of the holothurian larval nervous system: evolution of larval forms

Echinoderm larvae share numerous features of neuroanatomy. However, there are substantial differences in specific aspects of neural structure and ontogeny between the dipleurula-like larvae of asteroids and the pluteus larvae of echinoids. To help identify apomorphic features, we have examined the ontogeny of the dipleurula-like auricularia larva of the sea cucumber, Holothuria atra. Neural precursors arise in the apical ectoderm of gastrulae and appear to originate in bilateral clusters of cells. The cells differentiate without extensive migration, and they align with the developing ciliary bands and begin neurogenesis. Neurites project along the ciliary bands and do not appear to extend beneath either the oral or aboral epidermis. Apical serotonergic cells are associated with the preoral loops of the ciliary bands and do not form a substantial commissure. Paired, tripartite connectives form on either side of the larval mouth that connect the pre-oral, post-oral, and lateral ciliary bands. Holothurian larvae share with hemichordates and bipinnariae a similar organization of the apical organ, suggesting that the more highly structured apical organ of the pluteus is a derived feature. However, the auricularia larva shares with the pluteus larva of echinoids several features of neural ontogeny. Both have a bilateral origin of neural precursors in ectoderm adjacent to presumptive ciliary bands, and the presumptive neurons move only a few cell diameters before undergoing neurogenesis. The development of the holothurian nervous systems suggests that the extensive migration of neural precursors in asteroids is a derived feature. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Development of the nervous system in the acorn worm Balanoglossus simodensis: insights into nervous system evolution

SUMMARY To examine the evolutionary origin of the chordate nervous system, an outgroup comparison with hemichordates is needed. When the nervous systems of chordates and hemichordates are compared, two possibilities have been proposed, one of which is that the chordate nervous system has evolved from the nervous system of hemichordate‐like larva and the other that it is comparable to the adult nervous system of hemichordates. To address this issue, we investigated the entire developmental process of the nervous system in the acorn worm Balanoglossus simodensis. In tornaria larvae, the nervous system developed along the longitudinal ciliary band and the telotroch, but no neurons were observed in the ventral band or the perianal ciliary ring throughout the developmental stages. The adult nervous system began to develop at the dorsal midline at the Krohn stage, considerably earlier than metamorphosis. During metamorphosis, the larval nervous system was not incorporated into the adult nervous system. These observations strongly suggest that the hemichordate larval nervous system contributes little to the newly formed adult nervous system.