Larval Esophagus Research Articles

Foregut Development and Metamorphosis in a Pyramidellid Gastropod: Modularity and Constraint within a Complex Life Cycle.

Pyramidellids are tiny ectoparasitic gastropods with highly derived feeding structures for piercing and sucking. We attempted to resolve homology controversies about unique pyramidellid feeding structures by examining foregut development through larval and metamorphic stages, using sections for light and electron microscopy. We anticipated that, like many marine invertebrate larvae, post-metamorphic structures would differentiate extensively in late larvae to speed metamorphic transition. Previous studies of gastropods suggested that development of juvenile feeding structures in larvae was facilitated by foregut subdivision into dorsal and ventral developmental modules, and spatial uncoupling of these modules may have facilitated adaptive radiation in neogastropods. Observations of Odostomia tenuisculpta suggested that the stylet may be derived from cuticle-secreting buccal epithelium surrounding the proximal end of the salivary duct, whereas the stylet sheath could be either a derived jaw or a radular tooth. The anterior half of the remarkable buccal pump of these euthyneuran gastropods develops from the larval esophagus, which is unorthodox compared to caenogastropods, where extensive post-metamorphic specialization of a dorsal module component has not been previously described. The introvert tube develops from pouches of the distal larval esophagus and may actually be an eversible oral tube rather than an acrembolic proboscis. Minimal differentiation of presumptive juvenile foregut structures occurred during the larval stage of O. tenuisculpta, when compared to other gastropods. The stylet, stylet sheath, and buccal pump may be incompatible with functioning of the larval esophagus; thus, an explosive period of morphogenesis is necessary at metamorphosis. Although dorsal and ventral modules were recognizable during the development of O. tenuisculpta, we failed to find evidence that this modularity facilitated the extreme evolutionary remodeling of post-metamorphic feeding structures.

How did phytoplankton-feeding larvae re-evolve within muricid gastropods? A view from developmental morphology

Post-Paleozoic life history transitions in mollusks and echinoderms have been biased toward switches from feeding, planktonic larvae (planktotrophic), to one of the non-feeding developmental modes, such as maternally provisioned planktonic larvae, fully encapsulated larvae, or direct development. Nevertheless, rare resurrections of feeding larvae from fully encapsulated larvae have occurred within calyptraeid and muricid gastropods. The only previous study on the developing foregut of a muricid with encapsulated larvae (Nucella lapillus) indicated loss of the larval esophagus, a potential barrier to evolutionary re-emergence of larval planktotrophy. However, histological and ultrastructural examination of foregut development in two other nucellids, Nucella lamellosa and N. ostrina, both with fully encapsulated development, revealed a transient larval esophagus in both, as identified by anatomical position, tissue composition, interconnections to other structures, and fate at metamorphosis. The larval esophagus is difficult to recognize in nucellids without a comparative framework and a complete developmental series extending from early veliger stages through to juveniles. Both the larval mouth and distal larval esophagus are completely destroyed at metamorphosis. Surprisingly, encapsulated larvae of N. lamellosa also developed all three velar ciliary tracts needed for capture and ingestion of particles, despite absence of nurse egg feeding by encapsulated larvae of this species and despite apparent absence of phytoplankton-feeding larvae in this genus since its origin 20 million years ago. Retention of a larval esophagus and a full complement of velar ciliary tracts needed for particle capture and ingestion in encapsulated larvae of some muricids may help explain how larval planktotrophy re-emerged within this clade.

Immunocytochemical studies reveal novel neural structures in nemertean pilidium larvae and provide evidence for incorporation of larval components into the juvenile nervous system

IntroductionNemertea is one of the least studied lophotrochozoan phyla concerning neurogenesis. The sparse data available do not unambiguously allow for answering questions with respect to the neural groundplan of the phylum or the fate of larval neural structures during metamorphosis. In order to contribute to this issue, we studied neurotransmitter distribution during development of the pilidiophoran Lineus albocinctus Verrill, 1900.ResultsTwo serotonin-like immunoreactive (lir) neurons are present in the anterior part of the apical plate. They send numerous processes into the four lobes of the pilidium larva, where they form a complex subepithelial nerve net. All four larval lobes are underlain by a marginal neurite bundle, which is associated with numerous serotonin-lir monociliated perikarya. A serotonin-lir oral nerve ring encircles the stomach sphincter and is associated with few serotonin-lir conical cells. Two suboral neurites descend from the oral nerve ring and merge with the marginal neurite bundle. The oral nerve ring and the suboral neurites contain the mollusk-specific VD1/RPD2 α-neuropeptide. The lateral lobes of the larva have three and the anterior and the posterior lobes two VD1/RPD2-lir marginal neurite bundles. The lobar FMRFamide-lir plexus of Lineus albocinctus is much more complex than previously described for any pilidium larva. It includes a circumesophageal neurite that descends along each side of the larval esophagus and together with the inner marginal neurite bundle gives rise to the lobar plexus of the lateral lobes. An outer FMRFamide-lir marginal neurite bundle with numerous associated FMRFamide-lir marginal sensory cells surrounds all four lobes. FMRFamide-lir structures are absent in the larval apical region. The oral nerve ring and the two suboral serotonin-lir neurites are incorporated into the juvenile nervous system.ConclusionOur study confirms the presence of serotonin-lir components in the apical region of the pilidium larva of Lineus albocinctus and thus contradicts an earlier study on the same species. We show that the nervous system of pilidium larvae, especially the FMRFamide-lir components, is much more complex than previously assumed. The presence of the VD1/RPD2-α-neuropeptide indicates that this compound may have been part of the lophotrochozoan neural groundplan.

Changes in the Gut Microbiome of the Sea Lamprey during Metamorphosis

Vertebrate metamorphosis is often marked by dramatic morphological and physiological changes of the alimentary tract, along with major shifts in diet following development from larva to adult. Little is known about how these developmental changes impact the gut microbiome of the host organism. The metamorphosis of the sea lamprey (Petromyzon marinus) from a sedentary filter-feeding larva to a free-swimming sanguivorous parasite is characterized by major physiological and morphological changes to all organ systems. The transformation of the alimentary canal includes closure of the larval esophagus and the physical isolation of the pharynx from the remainder of the gut, which results in a nonfeeding period that can last up to 8 months. To determine how the gut microbiome is affected by metamorphosis, the microbial communities of feeding and nonfeeding larval and parasitic sea lamprey were surveyed using both culture-dependent and -independent methods. Our results show that the gut of the filter-feeding larva contains a greater diversity of bacteria than that of the blood-feeding parasite, with the parasite gut being dominated by Aeromonas and, to a lesser extent, Citrobacter and Shewanella. Phylogenetic analysis of the culturable Aeromonas from both the larval and parasitic gut revealed that at least five distinct species were represented. Phenotypic characterization of these isolates revealed that over half were capable of sheep red blood cell hemolysis, but all were capable of trout red blood cell hemolysis. This suggests that the enrichment of Aeromonas that accompanies metamorphosis is likely related to the sanguivorous lifestyle of the parasitic sea lamprey.

Development of foregut and proboscis in the buccinid neogastropod Nassarius mendicus: Evolutionary opportunity exploited by a developmental module

This article extends previous descriptions of foregut development and metamorphosis in neogastropods by providing data on the buccinid Nassarius mendicus, a species with a feeding larva. Histological sections showed that, like many other gastropods, the postmetamorphic buccal cavity and radular sac of N. mendicus differentiate during the larval stage from a ventral outpocketing of the distal larval esophagus. However, in N. mendicus the outpocketing also gives rise to the entire anterior esophagus and valve of Leiblein, suggesting that both these structures may be evolutionary derivatives of the gastropod buccal cavity. Scanning electron microscopy and three-dimensional reconstructions of section profiles revealed that the distal larval esophagus and larval mouth are completely destroyed at metamorphosis. The postmetamorphic mouth is formed as a new orifice. Furthermore, epithelia covering the proboscis and proboscis sac arise from preexisting epidermal epithelium of the larval head, an interpretation that contradicts an earlier suggestion on the origin of these epithelial elements in neogastropods with a feeding larval stage. These results, when compared to foregut development in other gastropods, lead me to propose that the gastropod buccal cavity and buccal mass is a developmental module. Canalized development of this module may have been important to the "evolvability" of the complex gastropod foregut, because it allowed a silent developmental novelty to arise (secondary formation of the postmetamorphic mouth) without disrupting development of the whole module. Nevertheless, this silent novelty might have subsequently facilitated dramatic evolutionary change by allowing the elaborate foregut structure of predatory, postmetamorphic neogastropods to arise in late stage larvae without compromising larval feeding.

Larval and metamorphic development of the foregut and proboscis in the caenogastropod Marsenina (Lamellaria) stearnsii.

The specialized, postmetamorphic feeding structures of predatory caenogastropods evolved by changes to an ancestral caenogastropod developmental program that generated a planktotrophic larval stage followed by a herbivorous postmetamorphic stage. As part of a program of comparative studies aimed at reconstructing these developmental changes, I studied the development of the postmetamorphic feeding system of Marsenina stearnsii using histological sections for light microscopy and scanning and transmission electron microscopy. The feeding system of this species has two very different designs during ontogeny. The larval system uses ciliary effectors to capture and ingest microalgae, whereas the juvenile/adult system includes a proboscis, jaws, and radular apparatus for predation on ascidian zooids. The postmetamorphic foregut begins to develop during the early larval phase, but the anlagen does not interfere with larval feeding because it develops as an increasingly elaborate outpocketing from the ventral wall of the larval esophagus. At metamorphosis, an opening is created in the anterior tip of the prospective, postmetamorphic buccal cavity and the margins of this opening anneal with the metamorphically remodeled lips of the larval mouth. This process exposes the jaws, which differentiate within the buccal cavity prior to metamorphosis. As a working hypothesis, I suggest that rupture of the buccal cavity to the outside at metamorphosis was selected as a mechanism to allow precocious development of jaws in species where jaws enhanced feeding performance by young juveniles. The larval esophagus of M. stearnsii appears to be completely destroyed at metamorphosis. Larval esophageal cells have distinctive apical characteristics (cilia, blebbed microvilli, stacks of lamellae within the glycocalyx) and no cells having this signature persist through metamorphosis. Development of the proboscis and proboscis sac, which begins prior to metamorphosis, conforms to previous descriptions of pleurembolic proboscis development, although an acrembolic proboscis has been ascribed to members of the Lamellaroidea.

Ultrastructure and differentiation of the larval esophageal muscle cells of the starfish Pisaster ochraceus.

The muscle cells that cause constriction of the starfish larval esophagus (esophageal muscle cells) are one of the first cell types to express their differentiated morphological characteristics during development. Ultrastructurally these muscle cells resemble vertebrate and invertebrate smooth muscles. They contain a nucleus, a Golgi apparatus, contractile myofilaments, hemidesmosome-like structures, and what appears to be a simple sarcoplasmic reticulum. In asteroid embryos, this muscle layer originates during mouth formation when mesenchyme cells migrate from the tips of the coeloms to the esophagus. Once there, they elongate, forming processes. Over the next few days, the processes become filled with arrays of longitudinally arranged thick and thin myofilaments and thin sacs of smooth endoplasmic reticulum. The latter appear between the bundles of contractile filaments and the cell membranes. Contractile activity begins at approximately this time. The cisternae may represent a sarcoplasmic reticulum that is required for contraction. The majority of the esophageal muscle cell processes extend around the circumference of the developing esophagus, but occasional cells may be oriented in other directions. The latter cells are always farther away from the basal lamina and probably have little or no contact with it. Contact with basal lamina may serve to direct the migration of the cells and the orientation of the processes. J. Morphol. 237:1-18, 1998. © 1998 Wiley-Liss, Inc.

Ultrastructure and differentiation of the larval esophageal muscle cells of the starfish Pisaster ochraceus

The muscle cells that cause constriction of the starfish larval esophagus (esophageal muscle cells) are one of the first cell types to express their differentiated morphological characteristics during development. Ultrastructurally these muscle cells resemble vertebrate and invertebrate smooth muscles. They contain a nucleus, a Golgi apparatus, contractile myofilaments, hemidesmosome-like structures, and what appears to be a simple sarcoplasmic reticulum. In asteroid embryos, this muscle layer originates during mouth formation when mesenchyme cells migrate from the tips of the coeloms to the esophagus. Once there, they elongate, forming processes. Over the next few days, the processes become filled with arrays of longitudinally arranged thick and thin myofilaments and thin sacs of smooth endoplasmic reticulum. The latter appear between the bundles of contractile filaments and the cell membranes. Contractile activity begins at approximately this time. The cisternae may represent a sarcoplasmic reticulum that is required for contraction. The majority of the esophageal muscle cell processes extend around the circumference of the developing esophagus, but occasional cells may be oriented in other directions. The latter cells are always farther away from the basal lamina and probably have little or no contact with it. Contact with basal lamina may serve to direct the migration of the cells and the orientation of the processes. J. Morphol. 237:1–18, 1998. © 1998 Wiley-Liss, Inc.

Transformation of Phytoplanktivorous Larvae into Predatory Carnivores during the Development of Polinices lewisii (Mollusca, Caenogastropoda)

We studied morphogenetic events that transform phytoplanktivorous larvae of a naticid gastropod into predatory juveniles that drill and ingest bivalves and ostracods within 3-5 days of metamorphic induction. Larvae of Polinices lewisii were cultured through meta- morphosis and histological sections were prepared of 9 larval and 2 post-metamorphic stages. Rapid, metamorphic transformation of feeding and gut structures is accomplished by destruction of larval tissues (velum, large areas of larval esophagus, and gastric shield of the stomach) and by prior formation during the larval stage of various juvenile/adult structures (accessory boring organ, esophageal gland, and buccal mass with jaws, cartilages, intrinsic musculature, salivary glands, and radula). Advanced differentiation of the post-metamorphic buccal mass during the larval stage is possible because the buccal cavity and radular sac develop from a semi-isolated outpocketing of the larval esophagus that does not interfere with the functioning of the larval esophagus. At metamorphosis, the buccal cavity punches out a new mouth opening in the ventral lip of the larval mouth, the larval mouth is sealed shut, and the distal part of the larval esophagus is destroyed. The epithelia forming the oral tube and buccal cavity in predatory adults of P. lewisii have a different developmental origin than the corresponding epithelia in many other adult gastropods.

Alterations to the subepithelial layers of the larval alimentary tract during metamorphosis in the sea lamprey Petromyzon marinus, with emphasis on tissue interactions

Light-microscopic histochemistry and conventional electron microscopy were used to study the changes to the subepithelial layers in the larval esophagus of the sea lamprey Petromyzon marinus during metamorphosis. During early stages of metamorphosis, smooth muscle cells of the muscularis mucosae and tunica muscularis dedifferentiate into myofibroblast-like cells, which make contact with the basal lamina of the overlying mucosal epithelium. During later stages, these myofibroblast-like cells redifferentiate into smooth muscle cells, reforming the muscularis mucosae and tunica muscularis. Alterations to the extracellular matrix occur concomitantly.

Filtration of microparticles from liquids ingested by the red imported fire antSolenopsis invicta Buren

The imported fire ant,Solenopsis invicta, has a highly efficient mechanism for filtering particles from food material. Latex microspheres as small as 0.88 μm were filtered and concentrated in the infrabuccal pocket. The compacted mass was then ejected as a pellet. The maximum size latex spheres swallowed by larvae were 45.8 μm, which approximately corresponds to the diameter of the larval esophagus. The efficient filtration of particles offers little hope for the success of controlled release insecticide formulations that require ingestion of solid particles.

Morphogenesis of the digestive system during metamorphosis of the nudibranch Doridella steinbergae (Gastropoda): Conversion from phytoplanktivore to carnivore

The structural changes undergone by the digestive system of a phytoplanktotrophic nudibranch larva during metamorphosis into a benthic carnivore are described using histological and electron microscopic techniques. The relative positions of the stomach, digestive gland, and distal end of the intestine are rearranged at metamorphosis by the actions of the larval retractor muscle and the accessory pedal retractor muscle. Although the anus and distal end of the intestine are secondarily displaced to the posterior end of the gastropod, the stomach undergoes further torsional displacement at metamorphosis. The tissues of the larval stomach and distal end of the larval esophagus undergo drastic alteration at metamorphosis. The larval stomach consists of a ciliated vestibule, which receives the openings of the esophagus and left digestive gland, a gastric shield, a style sac, and an intestinal groove. All of these areas, except the vestibule, are destroyed by cell dissociation at metamorphosis. The vestibule becomes the ventral stomach of the benthic stage and the proximal end of the intestine becomes enlarged and muscularized to form the dorsal ‘stomach’ of the benthic stage. The metamorphic changes involving the distal end of the esophagus include the continued development of the radula and oral lip glands, which both appear in rudimentary form during the larval stage, and differentiation of the buccal pump, salivary glands, and oral lips.

Strongyloides myopotomi: Fine structure of the body wall and alimentary tract of the adult and third-stage larva

The body wall of the adult and larval worms is composed of cuticle, hypodermis, and muscle layers. The cortex layer of the adult has an outer unit membrane; cortex and matrix layers are both amorphous. The matrix contains regularly spaced transverse bands surrounded by bundles of collagen fibers. The fiber layer consists of two rows of large collagen-like fibers and an outer layer of smaller unbanded fibers. In third-stage larvae the fiber layer is granular and the inner portion of the matrix is crystalloid. Nerves lie between the plasma membrane of the larval hypodermis and the sarcolemma of the muscle cells, which are similar in larvae and adults. Muscle structure resembles that of known nematode species. The striated border of the adult intestinal cells is composed of many microvilli, clothed in an extracellular tubular coat. The terminal web, directly beneath the apical plasma membrane, contains extensions of the cytoplasmic cores of the microvilli. Intestinal cells are separated by a terminal bar and contain pigment granules, dense foamy masses, endoplasmic reticulum, mitochondria, lipid, and a large nucleus. The larval intestine has widely spaced microvilli with dense central cores. A granular extracellular coat surrounding the microvilli may serve as a food reserve for the larva. The larval esophagus is a triradiate, cellular structure lined with cuticle. Posteriorly, the three esophageal glands contain many laminated secretory granules. The larval hindgut is also lined with cuticle and its cells contain vacuoles with membranous elements.