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1 Department of Anatomy and Histology, F13, University of Sydney, NSW 2006, Australia
2 School of Biological Sciences, University of Auckland, New Zealand
* To whom correspondence should be addressed. E-mail: mbyrne{at}anatomy.usyd.edu.au
Within the deuterostomes, the similarity of the dipleurula-type larvae of echinoderms (auricularia, bipinnaria) and hemichordates (tornaria) is striking. Here we describe the serotonergic system of the auricularia larvae of the apodid sea cucumber Chiridota gigas to broaden the comparison of the dipleurula-type larval nervous system in the Holothuroidea. This larva has a simple serotonergic nervous system largely composed of the apical organ. The apical organ is a concentration of cells and fibers along, and spanning between, the portions of the ciliary band that traverse the larval apex. Bipolar and multipolar cells give rise to fibers that connect the bands. In contrast to other echinoderm larvae, this larva does not develop serotonergic cells around the mouth. The similar topology and structure of the apical organ of the auricularia and the tornaria suggests that the serotonergic apical organ of the Ambulacraria (Echinodermata + Hemichordata) may have originated as a group of nerve cell bodies and fibers that developed in association with ciliary band sectors at the larval apex.
The long-standing hypothesis, based on synapomorphic features of development and morphology (1), on the close phylogenetic relationships between echinoderms and hemichordates is strongly supported by molecular phylogeny (2,3). It thus appears that a dipleurula-type larva with single ciliary band topology, as seen in the holothuroid auricularia and the hemichordate tornaria, is a basal feature of the Ambulacraria. In consideration of this link, we investigated the serotonergic nervous system of the auricularia larvae of the apodid holothuroid Chiridota gigas and compared it with that described for other dipleurula-type larvae (4–11). This is the first modern developmental study of the planktotrophic larva of the order Apodida (12). Previous studies on the auricularia serotonergic system involved the larvae of Parastichopus californicus and Stichopus japonicus, members of the order Aspidochirotida (4,7,11).
The nervous system of the auricularia, bipinnaria, and tornaria develops in association with the ciliary bands (4–11). Serotonin immunoreactivity is conspicuous in the anterior region of these larvae, with an accumulation of cells and fibers at the larval apex forming the apical organ. Anterior serotonergic structures in these larvae have attracted interest because of their potential role as sensory structures (13,14). In C. gigas, the dominance of the serotonergic system at the larval apex was particularly interesting from both a functional and a phylogenetic perspective.
The auricularia of C. gigas has a single ciliary band that loops around the larval body, with the dorsal and ventral portions converging at the apex on the larval midline (Fig. 1A–GA–G; 2A; 3A). In early larvae (20 day) the ciliary band sections at the larval apex have a short region where they are aligned in parallel, and this carries over to the dorsal side (Fig. 1B, C). In older larvae (40–80 day) the ciliary band sections meet at the apex (Fig. 1D–G), although they may retain a short parallel alignment on the dorsal side. A thin fiber crosses between the bands (Fig. 1D, E, G), and this forms part of the apical organ.
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= 13; SE = 3.2, n = 10) in the apical organ; these were mostly bipolar, with a few multipolar cells present (Fig. 2G). The cells ( = 5.9 µm diam, SE = 0.5 µm; n = 22 cells from 6 larvae) had a strongly immunoreactive cytoplasm and gave rise to fibers that extended posteriorly along the ciliary band nerve (Fig. 2E, F). Lone immunoreactive cells and fibers present in the oral hood connected with the ciliary band plexus (Fig. 2A, B). One to two serotonergic cells were present in the esophagus.
In older auricularia (49-day-old) an immunoreactive fiber dotted by a few cell bodies developed in the mid and posterior regions of the larva. The nervous system was more complex, with the addition of more cells and fibers (Fig. 3A, B). These larvae had 23–32 serotonergic cells ( = 28; SE = 2.2, n = 6) in the apical organ. Fibers connecting the two ciliary band regions crossed directly or at an angle between the bands (Fig. 3C–E). The cells that formed the connections between the bands were mostly tripolar. They had a mean diameter of 4.8 µm (SE = 0.4 µm, n = 10 cells from 2 larvae) and were similar to the nerve cells in the apical organ of the auricularia of P. californicus and S. japonicus (4,7,15). No immunoreactive cells were seen between the bands. The ciliary band nerve had up to 5 fibers across its width at the larval apex and 2–3 fibers in the lateral region (Fig. 3F, G). Immunoreactive cytoplasm extended from the soma into the proximal portion of the fibers (Fig. 3F, G). Elsewhere around the larval body a thin fiber was present in the ciliary band nerve and appeared to be continuous (Fig. 3A, B).
Throughout the development of C. gigas, serotonin immunoreactivity was largely restricted to the apical and anterolateral ciliary band regions and had a right-left bilateral symmetry. The serotonergic system of the auricularia is morphologically simpler than in the other dipleurula-type echinoderm larva, the asteroid bipinnaria. Bipinnariae have a complex serotonergic system of processes and neuropil and have lateral and oral ganglia and postoral immunoreactivity (5,6,8). As in the auricularia, the anterior ciliary band sectors of the bipinnaria are joined by processes that span between them (6). The asteroid apical organ also has prominent lateral ganglia (5,6,8) that are suggested to have arisen through a split of the single apical organ (13).
The location and cellular organization of the echinoid apical organ differs from that seen in dipleurula-type larvae, and this is likely due to evolution of the echinopluteus. In echinoplutei, the apical organ is a single structure positioned on the oral hood and is made up of two ganglionic groups of cells joined by a thick nerve commissure (8,16). The cell bodies of the echinoid apical organ do not reside within the ciliary nerve, but processes from the apical organ connect with the ciliary band nerve of the arms.
Apical serotonin immunoreactivity in C. gigas larvae parallels the location of catecholaminergic cells in the auricularia of Actinopyga miliaris and P. californicus, which also form a nerve connecting the apical ciliary band sections (4,17). In contrast to the serotonergic system, the catecholaminergic system traces the entire ciliary band and is conspicuous in the oral region (5,17). Clearly we have identified only a subset of neurons that compose the apical organ of C. gigas. Use of other neuronal markers (5,8,11,18) may reveal greater complexity of the holothuroid larval nervous system and apical organ.
Serotonergic immunoreactivity was conspicuously absent in the oral region of C. gigas larvae, and this is also the case for aspidochirotid auriculariae and the tornaria (4,9–11). The presence of serotonergic adoral ganglia along the posterior rim of the mouth of asteroid, ophiuroid, and echinoid larvae is likely to be a convergent feature, given our current understanding of echinoderm class interrelationships (3). This structure is suggested to have a gustatory function in feeding (5,6,16,19). It seems likely that the auricularia of C. gigas have the ability to discriminate food particles, as do other echinoderm feeding larvae (20). This ability may involve nonserotonergic cells such as the catecholaminergic cells seen in the adoral region of P. californicus and A. miliaris (4,17). The shared absence of serotonergic adoral ganglia in the auricularia and tornaria suggests that the ancestral dipleurula larva also lacked this structure and may have employed other neurochemicals to modulate feeding behavior. We have a very poor understanding of what larval nervous systems do, and it would be useful to apply current detailed knowledge of their cellular organization to functional studies.
The larval form and topology of the single ciliary band of auricularia with parallel ciliary band segments traversing the right and left portions of the oral hood (Fig. 1A, B) is most similar to that seen in the tornaria (9,10). Asteroid bipinnaria differ from these larvae in having two ciliary bands that follow a dorsoventral path. The serotonergic system of the auricularia is largely restricted to the anterior region where the apical organ develops (Fig. 2A, B; 3A, B). In the tornaria, the serotonergic system is restricted to the apical organ and does not give rise to posteriorly directed fibers (9,10).
Comparison of the auricularia and tornaria indicates that the ancestral-type apical organ may have originated as an accumulation of nerve cells and processes at the larval apex that differentiated in association with two ciliary band sectors. In its anterior location, the ancestral apical organ may have had a sensory role in feeding and settlement.
For some time, interest in the echinoderm and hemichordate larval nervous system and the apical organ has focused on the proposed evolutionary link between the dipleurula larva and the chordate nervous system (21), a hypothesis that now has little support (see discussion in 22). Insights into similarities between the echinoderm and hemichordate nervous systems and that of the chordates appear best generated by investigation of the developing juvenile nervous system (232425). Comparison of echinoderm and hemichordate larval nervous systems remain, however, of great interest with respect to larval evolution (26).
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