Coelomogenesis during the abbreviated development of the echinoid Heliocidaris erythrogramma and the developmental origin of the echinoderm pentameral body plan

The development of the coeloms is described in an echinoid with an abbreviated larval development and shows the early morphogenesis of the coeloms of the adult stage. The development is described from images obtained by laser scanning confocal microscopy. The development in Heliocidaris erythrogramma is asymmetric with a larger left coelom forming on the larval-left side and a smaller right coelom forming on the larval-right side. The right coelom forms after the development of the left coelom is well advanced. The hydrocoele forms from the anterior part of the left coelom. The five lobes of the hydrocoele from which the pentamery of the adult derives take shape on the outer, distal wall of the anterior part of the left coelom. The hydrocoele separates from the more posterior part of the left coelom, which becomes the left posterior coelom. The lobes of the hydrocoele are named, based on the site of the connexion of the stone canal to the hydrocoele. The mouth is assumed to form by penetration through only the outer, distal wall of the hydrocoele and the ectoderm. Both larval and adult polarities are evident in this larva. A comparison with coelomogenesis in the asteroid Parvulastra exigua, which also has an abbreviated development, leads to predictions of homology between the echinoderm and chordate phyla that do not require the hypothesis of a dorsoventral inversion event in chordates.     

The Development of the Brachiopod Crania (Neocrania) anomala (O. F. Müller)and its Phylogenetic Significance

The freely spawned eggs of Crania go through radial cleavage, embolic gastrulation, and the posteroventral part of the archenteron forms mesoderm through modified enterocoely. The blastopore closes in the posterior end of the larva. The ciliated, lecithotrophic larva has four pairs of coelomic pouches and three pairs of dorsal setal bundles. At metamorphosis, the larva curls ventrally by contraction of a pair of midventral muscles, which are extensions of the first pair of coelomic sacs; the larva attaches by the epithelium just behind the closed blastopore. The brachial valve is secreted by the middle part of the dorsal epithelium and the pedicle valve is secreted by the attachment epithelium. The second pair of coelomic sacs develop small attachment areas at the edge of the dorsal valve and become the lophophore coelom (mesocoel); the third pair of coelomic sacs become the body coelom (metacoel) with the adductor muscles. The posterior position of the closing blastopore is characteristic of deuterostomes. The ventral curving of the settling larva and the formation of both valves from dorsal epithelial areas indicate that the brachiopods have a very short ventral side as opposed to the phoronids. It is concluded that both groups have originated from a creeping ancestor with a straight gut.     

Early development of coelomic structures in an echinoderm larva and a similarity with coelomic structures in a chordate embryo

Early coelomic development in the abbreviated development of the sea urchin Holopneustes purpurescens is described and then used in a comparison with coelomic development in chordate embryos to support homology between a single arm of the five-armed radial body plan of an echinoderm and the single bilateral axis of a chordate. The homology depends on a positional similarity between the origin of the hydrocoele in echinoderm development and the origin of the notochord in chordate development, and a positional similarity between the respective origins of the coelomic mesoderm and chordate mesoderm in echinoderm and chordate development. The hydrocoele is homologous with the notochord and the secondary podia are homologous with the somites. The homology between a single echinoderm arm and the chordate axis becomes clear when the aboral to oral growth from the archenteron in the echinoderm larva is turned anteriorly, more in line with the anterior–posterior axis of the early zygote. A dorsoventral axis inversion in chordates is not required in the proposed homology.     

From larval bodies to adult body plans: patterning the development of the presumptive adult ectoderm in the sea urchin larva

Echinoderms are unique among bilaterians for their derived, nonbilateral adult body plan. Their radial symmetry emerges from the bilateral larval body plan by the establishment of a new axis, the adult oral–aboral axis, involving local mesoderm–ectoderm interactions. We examine the mechanisms underlying this transition in the direct-developing sea urchin Heliocidaris erythrogramma. Adult ectoderm arises from vestibular ectoderm in the left vegetal quadrant. Inductive signals from the left coelom are required for adult ectodermal development but not for initial vestibule formation. We surgically removed gastrula archenteron, making whole-ectoderm explants, left-, right-, and animal-half ectoderm explants, and recombinants of these explants with left coelom. Vestibule formation was analyzed morphologically and with radioactive in situ hybridization with HeET-1, an ectodermal marker. Whole ectodermal explants in the absence of coelom developed vestibules on the left side or ventrally but not on the right side, indicating that left–right polarity is ectoderm autonomous by the gastrula stage. However, right-half ectodermal explants robustly formed vestibules that went on to form adult structures when recombined with the left coelom, indicating that the right side retains vestibule-forming potential that is normally suppressed by signals from the left-side ectoderm. Animal-half explants formed vestibules only about half the time, demonstrating that animal–vegetal axis determination occurs earlier. However, when combined with the left coelom, animal-half ectoderm always formed a vestibule, indicating that the left coelom can induce vestibule formation. This suggests that although coelomic signals are not required for vestibule formation, they may play a role in coordinating the coelom–vestibule interaction that establishes the adult oral–aboral axis.     

Ultrastructure and formation of the body cavity lining in Phoronis muelleri (Phoronida, Lophophorata)

Among other characteristics a trimeric coelomic compartmentation consisting of an anterior protocoel, followed by a mesocoel and a posterior metacoel is traditionally believed to substantiate the sister-group relationship between Lophophorata and Deuterostomia, together forming the Radialia. As molecular data cannot support this hypothesis a reanalysis of the coelomic cavities in Phoronida is undertaken, because corresponding coelomic compartmentation is widely accepted to support the Radialia hypothesis. A coelomic cavity can be recognized on the ultrastructural level because its lining is a true epithelium with polarized cells interconnected by apical adherens junctions. This study reveals that neither in larval nor adult Phoronis muelleri (Phoronida) an anterior cavity with such a lining is present. What on the light microscopic level leads to the impression of a cavity inside the larval episphere, actually is an enlarged subepidermal extracellular matrix with an amorphous, presumably gel-like filling, into which several muscle cells are embedded. Larvae, thus, possess only one coelomic cavity, the large trunk coelom of the larva which is adopted in the adult organization. The second coelomic cavity of adult P. muelleri, the lophophore coelom, develops as a double-layer of epithelialized mesodermal cells at the base of the adult tentacle buds and becomes fluid filled during metamorphosis. Like the larval episphere, larval tentacles and most parts of the blastocoel are filled by an amorphous matrix. Reanalysis of the literature and comparison with Brachiopoda and Bryozoa allows the hypothesis that a protocoel is lacking in all Lophophorata, and that merely two unpaired coelomic cavities, one tentacle and one trunk coelom, can be assumed for the ground pattern of this taxon. These results do not provide further evidence for the Radialia hypothesis, but also do not contradict it. Accepted: 28 August 2000     

Expression of Hox4 during development of the pentamerous juvenile sea star, Parvulastra exigua

Expression of Hox4 during development of the bilateral larva and pentameral juvenile sea star was investigated in Parvulastra exigua. The role of Hox4, possibly the anterior-most gene in the echinoderm Hox cluster, in the formation of the echinoderm adult body plan has not been examined previously. In the larva of P. exigua, PeHox4 is expressed in the developing coeloms—the anterior and the right and left coeloms that generate the aboral and oral coeloms of the juvenile. At the rudiment stage, PeHox4 was expressed in the five primary lobes of the hydrocoel that give rise to primary podia, the foundation of the adult body plan. This suggests a role for this gene in the development of the echinoderm body plan. In contrast to other bilaterians, Hox4 was not expressed in the developing asteroid central nervous system.     

Development of the coelomic cavities in larvae of the living isocrinid sea lily Metacrinus rotundus

Coelomogenesis in the isocrinid sea lily, Metacrinus rotundus, is described through the swimming larval stages. After the late gastrula stage, the archenteron separates from the ectoderm to form an archenteral sac, which develops into a dumbbell shape consisting of anterior and posterior lobes, and a middle part connecting both lobes. The anterior and posterior lobes, and the middle part, become separated into an axo-hydrocoel, the left and right somatocoels and an enteric sac, respectively. The hydrocoel forms from the left lower edge of the axo-hydrocoel and becomes separated from the axocoel by the late dipleurula stage, when chambered organs and coelom X bud off from the anterior tip of the right and left somatocoels, respectively. Coelom X does not occur in comatulid crinoids (feather stars), and its fate is unclear. The pore canal extends from the axocoel. The hydrocoel differentiates into a crescent shape at the overtime semidoliolaria stage, a few days after the semidoliolaria becomes competent to settle. Coelomogenesis in M. rotundus is much simpler than in the comatulids and probably represents the ancestral mode of the crinoids. As each portion of the dumbbell sac differentiates almost in situ into each coelom, presumptive fates in the sac are easily followed in M. rotundus.     

Evolution of pelagic direct development in the starfish Pteraster tesselatus (Asteroidea: Velatida)

Despite a diversity of larval forms, remarkably conservative features of asteroid development define a larval body plan that occurs throughout the class. However, recent work on the starfish Pteraster tesselatus has documented a highly derived pattern of development. Several features, including radial symmetry, parallel embryonic and adult axes of symmetry, absence of a preoral lobe, and formation of coeloms in the adult orientation from seven separate enterocoels, have not been reported in asteroids before. The complete absence of the larval body plan features that are found in other asteroids, indicates that P. tesselatus develops directly from the embryo to the juvenile and has a pelagic, nonfeeding (lecithotrophic), but nonlarval mode of development. I postulate that direct development evolved over an extended period in a lineage of brooding, deep-sea velatid (probably pterastcrid) ancestors of P. tesselatus. Selection for increased developmental efficiency (loss of nonfunctional larval features) in the brooded offspring, could explain the lack of larval settlement structures, the nonlarval arrangement of coeloms, the lack of a preoral lobe, the transverse orientation of the juvenile disc, and the lack of bilateral symmetry. The pattern of coclomogenesis could have been derived from that of other velatids (e.g. solasterids) by relatively simple changes in timing and orientation of entcroeoel formation. Rotation and posterior translation of the coelomic fate map of the archenteron prior to enlerocoel formation would produce the coelomic compartments in the adult orientation that characterizes direct development in P. tesselatus. These unusual developmental features lead to a radically different interpretation for the evolution of the pelagic ‘larva’ of P. tesselatus: (1) evolution of benthie brooding, (2) extreme simplification of development involving the loss of all larval features from the life cycle, and (3) subsequent re-evolution of pelagic development. In the case of P. tesselatus, where all larval structures were lost, there do not seem to be functional constraints preventing the re-evolution of pelagic development. Analysis of pelagic and benthie larvae, in other asteroids, suggests that major ecological transitions in life histories need not be associated with substantia] changes in morphology. The loss of pelagic development should have occurred repeatedly and should be readily reversible. These findings have interesting implications for the loss and evolution of pelagic dispersal in the life histories of marine benthie invertebrates.     

The A/P axis in echinoderm ontogeny and evolution: evidence from fossils and molecules

SUMMARY Even though echinoderms are members of the Bilateria, the location of their anterior/posterior axis has remained enigmatic. Here we propose a novel solution to the problem employing three lines of evidence: the expression of a posterior class Hox gene in the coeloms of the nascent adult body plan within the larva; the anatomy of certain early fossil echinoderms; and finally the relation between endoskeletal plate morphology and the associated coelomic tissues. All three lines of evidence converge on the same answer, namely that the location of the adult mouth is anterior, and the anterior/posterior axis runs from the mouth through the adult coelomic compartments. This axis then orients the animal such that there is but a single plane of symmetry dividing the animal into left and right halves. We tentatively hypothesize that this plane of symmetry is positioned along the dorsal/ventral axis. These axis identifications lead to the conclusion that the five ambulacra are not primary body axes, but instead are outgrowths from the central anterior/posterior axis. These identifications also shed insight into several other evolutionary mysteries of various echinoderm clades such as the independent evolution of bilateral symmetry in irregular echinoids, but do not elucidate the underlying mechanisms of the adult coelomic architecture.     

A gastric-brooding asteroid, Smilasterias multipara

The gastric-brooding asterinid sea star, Smilasterias multipara, broods from late August to early November in the shallow sublittoral zone of southeastern Australia. We observed males and females spawning in the laboratory. They shed gametes through gonopores on the sides of the arms. The eggs were orange, about 1.0 mm in diameter, and heavier than seawater. They were externally fertilized by sperm, and placed into the stomach of the female by the tube feet. Twenty-four hours after fertilization, the first cleavage occurred. Cleavage was equal, total, and radial. Development via a non-feeding lecithotrophic brachiolaria was direct, there being no planktrotrophic bipinnaria or brachiolaria larva. Embryos developed, through wrinkled blastula and gastrula stages, into brachiolariae with arms. All of the surfaces of the brachiolaria were covered by cilia. At metamorphosis, a starfish rudiment appeared on the posterior portion of the larval body, while the anterior portion of the larval body was absorbed. Two months after fertilization, metamorphosis was complete. After metamorphosis, juveniles in the stomach grew six pairs of tube feet in each arm. Juveniles, 3 mm in diameter, emerged from the mouth of the mother in early November. Developmental evidence suggests that this asteroid has evolved mechanisms for the protection of larvae and juveniles from gastric digestion.     

Pattern formation in a pentameral animal: induction of early adult rudiment development in sea urchins

We investigated adult rudiment induction in the direct-developing sea urchin Heliocidaris erythrogramma microsurgically. After removal of the archenteron (which includes presumptive coelomic mesoderm as well as presumptive endoderm) from late gastrulae, larval ectoderm develops properly but obvious rudiments (tube feet, nervous system, and adult skeleton) fail to form, indicating that coelomic mesoderm, endoderm, or both are required for induction of adult development. Recombination of ectoderm and archenteron rescues development. Implanted endoderm alone or left coelom alone each regenerate the full complement of archenteron derivatives; thus, they are uninformative as to the relative inductive potential of the two regions. However, in isolated ectoderm, more limited regeneration gives rise to larvae containing no archenteron derivatives at all, endoderm only, or both endoderm and left coelom. Adult nervous system begins to develop only in the latter, indicating that left coelom is required for the inductive signal. Isolated ectoderm develops a vestibule (the precursor of adult ectoderm) and correctly regulates vestibular expression of the ectodermal territory marker HeET-1, indicating that the early phase of vestibule development occurs autonomously; only later development requires the inductive signal. Another ectodermal marker, HeARS, is regulated properly in the larval ectoderm region, but not in the vestibule. HeARS regulation thus represents an early response to the inducing signal. We compare HeARS expression in H. erythrogramma with that in indirect developers and discuss its implications for modularity in the evolution of developmental mode.     

Inverse larval development in a Devonian edrioasteroid from Spain and the phylogeny of Agelacrinitinae

The first edrioasteroid to be discovered from the Iberian Peninsula is reported from the Emsian (late Lower Devonian) of the north Spanish coast. It belongs to the species Krama devonica (Bassler) but is unusual in being a mirror image form. This is interpreted as the product of situs inversus during larval development whereby the coeloms on the right side rather than the left side of the bilateral larva have given rise to the definitive adult structures. Thus the hydropore lies in its mirror image position vis-à-vis the anterior/posterior axis and this axis must be homologous with Lovén's symmetry plane in echinoids. The phylogenetic position of Krama is analysed cladistically and, by combining this with available stratigraphical information, the most parsimonious phylogenetic tree is produced for the subfamily Agelacrinitinae.     

The physiological function of the coelom in starfish larvae and its evolutionary implications

The coelom in the bipinnaria larva of Asterias acts as a buoyancy tank. The concentrations of magnesium and sulphate in the coelomic fluid are lower than in seawater, reducing the density. The coelomic epithelium is a secretory epithelium, probably secreting sodium or chloride ions that then draw in the counter ion and water. The rate of urine production is very high for an isotonic marine animal, compensating for the large surface/volume ratio of the coelom. This function would account for the precocious development of the coelom and its association with an excretory duct. It is proposed that the coeloms of other pelagic larvae such as the actinotroch of Phoronis and of echiuran larvae have a similar function and that this may have been an original function of the coelom, although in many phyla this function has been modified or lost.     

Ultrastructure of the Coelomocytes in the Tentacular Coelom of Thysanocardia nigra Ikeda, 1904 (Sipuncula)

Free-floating coelomocytes in the tentacular coelomic cavity of the sipunculan Thysanocardia nigra Ikeda, 1904, were studied using light interference contrast microscopy and scanning and transmission electron microscopy. The following coelomocyte types were distinguished: hemerythrocytes, amoebocytes, and two morphological types of granular cells. No clusters of specialized cells that had been reported to occur in the trunk coelom of Th. nigra were found in the tentacular coelom. The corresponding types of coelomocytes from the tentacular and trunk coelomic cavities were shown to differ in size. These two coeloms are completely separated in sipunculans.     

Morphogenesis and organogenesis in the regenerating planktotrophic larvae of asteroids and echinoids

In a previous study, we described complete body regeneration (with organogenesis) following surgical bisection in the planktotrophic larvae of the asteroids Luidia foliolata and Pisaster ochraceus. Here we present further detailed observations of these unique regenerative processes not presented in the previous paper. Furthermore, we describe for the first time complete regeneration following surgical bisection of planktotrophic larvae of the regular echinoid Lytechinus variegatus and the irregular echinoid Dendraster excentricus. Larvae of both asteroids and echinoids displayed a capacity for rapid regeneration regardless of their developmental stage. Within 48 h after bisection, aggregations of mesenchyme cells with pseudopodia were observed at the site of surgical bisection. These cellular aggregations were similar in appearance to the mesenchymal blastemas that form in adult echinoderms prior to their arm regeneration, and to those described in other deuterostomes that undergo regeneration. When asteroid larvae were surgically bisected in the early stages of their development, clusters of mesenchyme cells developed into completely new pairs of coelomic pouches located anterior to the newly regenerated digestive tract. This indicates that cell fate in regenerating asteroid larvae remains indeterminate during early development. In the larvae of P. ochraceus, regardless of the developmental stage at the time of bisection, both the anterior and posterior portions regenerated all their missing organs and tissues. However, the larvae of L. foliolata displayed differential regenerative capacity in bisected larval halves at the late bipinnaria stage. The differences observed may be due to differences in larval development (L. foliolata has no brachiolaria stage), and may have evolutionary implications. In the regular echinoid L. variegatus, both larval portions regenerated into morphologically and functionally normal larvae that were indistinguishable from non-bisected control larvae. The regenerative processes were similar to those we observed in planktotrophic asteroid larvae. Regenerating larvae readily metamorphosed into normal juveniles. In the irregular echinoid D. excentricus, posterior portions of larvae completed regeneration and metamorphosis, but anterior portions regenerated only partially during the 2-week study. Our observations confirm that asteroid and echinoid larvae provide excellent models for studies of regeneration in deuterostomes.     

The Morphology of the Phoronid Phoronopsis harmeri

We studied the morphology and gross anatomy of the phoronid Phoronopsis harmeriusing light microscopy and scanning electron microscopy. The body of Ph. harmeriis subdivided into several regions: a lophophore, a head, anterior, and posterior parts of the body, and an ampulla. The lophophore is spiral and comprises 0.5 turns. In males, there are lophophoral organs in the tentacular crown; under the lophophore, there is an epithelial fold or collar. The internal organization shows partitioning into three coeloms: the coelom of the epistome, the tentacular coelom, and the trunk coelom. The trunk coelom is divided into a series of chambers by a complex system of mesenteries. The intestine is U-shaped, and the epistome is located above the mouth opening. The circulatory system is closed and consists of the following vessels: the efferent and afferent circular, left and right lateral (efferent), and medial (afferent) vessels. In Ph. harmeri, there is a dorsolateral (afferent) vessel running through the ampulla and the lower part of the posterior trunk region. The excretory system is composed of paired metanephridia that resemble asymmetrical U-shaped tubes. Sexual dimorphism is characteristic of the structure of the distal part of the nephridium, which opens into the body cavity. The nervous system consists of a dorsal nervous field, a circular nerve plexus, and a giant left nerve fiber. Ph. harmeriis a dioecious species; the gametes develop in a vasoperitoneal tissue that envelops the intestine in the posterior part of the trunk region.     

Ultrastructure of the body cavities in Phylactolaemata (Bryozoa)

Only species belonging to the bryozoan subtaxon Phylactolaemata possess an epistome. To test whether there is a specific coelomic cavity inside the epistome, Fredericella sultana, Plumatella emarginata, and Lophopus crystallinus were studied on the ultrastructural level. In F. sultana and P. emarginata, the epistome contains a coelomic cavity. The cavity is confluent with the trunk coelom and lined by peritoneal and myoepithelial cells. The lophophore coelom extends into the tentacles and is connected to the trunk coelom by two weakly ciliated coelomic ducts on either side of the rectum. The lophophore coelom passes the epistome coelom on its anterior side. This region has traditionally been called the forked canal and hypothesized to represent the site of excretion. L. crystallinus lacks an epistome. It has a simple ciliated field where an epistome is situated in the other species. Underneath this field, the forked canal is situated. Compared with the other species, it is pronounced and exhibits a dense ciliation. Despite the occurrence of podocytes, which are prerequisites for a selected fluid transfer, there is no indication for an excretory function of the forked canal, especially as no excretory porus was found. J. Morphol. 2009. © 2008 Wiley‐Liss, Inc.     

Organization of the epistome in <Emphasis Type="Italic">Phoronopsis harmeri</Emphasis> (Phoronida) and consideration of the coelomic organization in Phoronida

Results provided by modern TEM methods indicate the existence of the lophophoral and trunk coelomes but not of the preoral coelom in Phoronida. In the present work, the epistome in Phoronopsis harmeri was studied by histological and ultrastructural methods. Two kinds of cells were found in the frontal epidermis: supporting and glandular. The coelomic compartment is shown to be inside the epistome. This compartment has a complex shape, consists of a central part and two lateral branches, and contacts the lophophoral coelom, forming two complete dissepiments on the lateral sides and a partition with many holes in the center. TEM reveals that some portions of the incomplete partition are organized like a mesentery, with the two layers of cells separated by ECM. The myoepithelial cells of the coelomic lining form the circular and radial musculature of the epistome. Numerous amoebocytes occur in the coelom lumen. The tip of the epistome and its dorso-lateral parts lack a coelomic cavity and are occupied by ECM and muscle cells. The fine structure of the T-shaped vessel is described, and its localization inside lophophoral coelom is demonstrated. We assert that the cavity inside the epistome is the preoral coelom corresponding to the true preoral coelom of the larva of this species. Proving this assertion will require additional study of metamorphosis in this species. To clarify the patterns of coelom organization in phoronids, we discuss the bipartite coelomic system in Phoronis and the tripartite coelomic system in Phoronopsis.