Myoanatomy and serotonergic nervous system of the ctenostome Hislopia malayensis: evolutionary trends in bodyplan patterning of ectoprocta

Background

Near the end of the nineteenth century the hypothesis was presented for the homology of book lungs in arachnids and book gills in the horseshoe crab. Early studies with the light microscope showed that book gill lamellae are formed by outgrowth and possibly some invagination (infolding) of hypodermis (epithelium) from the posterior surface of opisthosomal limb buds. Scorpion book lungs are formed near the bilateral sites of earlier limb buds. Hypodermal invaginations in the ventral opisthosoma result in spiracles and sac-like cavities (atria). In early histological sections of embryo book lungs, widening of the atrial entrance of some lamellae (air channels, air sacs, saccules) was interpreted as an indication of invagination as hypothesized for book gill lamellae. The hypodermal infolding was thought to produce the many rows of lamellar precursor cells anterior to the atrium. The ultrastructure of scorpion book lung development is compared herein with earlier investigations of book gill formation.

Results

In scorpion embryos, there is ingression (inward migration) of atrial hypodermal cells rather than invagination or infolding of the atrial hypodermal layer. The ingressing cells proliferate and align in rows anterior to the atrium. Their apical-basal polarity results in primordial air channels among double rows of cells. The cuticular walls of the air channels are produced by secretion from the apical surfaces of the aligned cells. Since the precursor cells are in rows, their secreted product is also in rows (i.e., primordial air channels, saccules). For each double row of cells, their opposed basal surfaces are gradually separated by a hemolymph channel of increasing width.

Conclusions

The results from this and earlier studies show there are differences and similarities in the formation of book lung and book gill lamellae. The homology hypothesis for these respiratory organs is thus supported or not supported depending on which developmental features are emphasized. For both organs, when the epithelial cells are in position, their apical-basal polarity results in alternate page-like channels of hemolymph and air or water with outward directed hemolymph saccules for book gills and inward directed air saccules for book lungs.     

The placental analogue and the pattern of sexual reproduction in the cheilostome bryozoan Bicellariella ciliata (Gymnolaemata)

Background

Matrotrophy or extraembryonic nutrition ?C transfer of nutrients from mother to embryo during gestation ?C is well known and thoroughly studied among vertebrates, but still poorly understood in invertebrates. The current paper focuses on the anatomy and ultrastructure of the oogenesis and placentotrophy as well as formation of the brood chamber (ovicell) in the cheilostome bryozoan Bicellariella ciliata (Linnaeus, 1758). Our research aimed to combine these aspects of the sexual reproduction into an integral picture, highlighting the role of the primitive placenta-like system in the evolution of bryozoan reproductive patterns.

Results

Follicular and nutrimentary provisioning of the oocyte occur during oogenesis. Small macrolecithal oocytes are produced, and embryos are nourished in the ovicell via a simple placental analogue (embryophore). Every brooding episode is accompanied by the hypertrophy of the embryophore, which collapses after larval release. Nutrients are released and uptaken by exocytosis (embryophore) and endocytosis (embryo). Embryos lack specialized area for nutrient uptake, which occurs through the whole epidermal surface. The volume increase between the ripe oocyte and the larva is ca. 10-fold.

Conclusions

The ovicell is a complex organ (not a special polymorph as often thought) consisting of an ooecium (protective capsule) and an ooecial vesicle (plugging the entrance to the brooding cavity) that develop from the distal and the fertile zooid correspondingly. Combination of macrolecithal oogenesis and extraembryonic nutrition allows attributing B. ciliata to species with reproductive pattern IV. However, since its oocytes are small, this species represents a previously undescribed variant of this pattern, which appears to represent a transitional state from the insipient matrotrophy (with large macrolecithal eggs) to substantial one (with small microlecithal ones). Altogether, our results substantially added and corrected the data obtained by the previous authors, providing a new insight in our understanding of the evolution of matrotrophy in invertebrates.     

Developmental dynamics of myogenesis in the shipworm <Emphasis Type="Italic">Lyrodus pedicellatus</Emphasis> (Mollusca: Bivalvia)

Background

The shipworm Lyrodus pedicellatus is a wood-boring bivalve with an unusual vermiform body. Although its larvae are brooded, they retain the general appearance of a typical bivalve veliger-type larva. Here, we describe myogenesis of L. pedicellatus revealed by filamentous actin labelling and discuss the data in a comparative framework in order to test for homologous structures that might be part of the bivalve (larval) muscular ground pattern.

Results

Five major muscle systems were identified: a velum retractor, foot retractor, larval retractor, a distinct mantle musculature and an adductor system. For a short period of larval life, an additional ventral larval retractor is present. Early in development, a velum muscle ring and an oral velum musculature emerge. In late stages the lateral and dorsal mantle musculature, paired finger-shaped muscles, an accessory adductor and a pedal plexus are formed. Similar to other bivalve larvae, L. pedicellatus exhibits three velum retractor muscles, but in contrast to other species, one of them disappears in early stages of L. pedicellatus. The remaining two velum retractors are considerably remodelled during late larval development and are most likely incorporated into the elaborate mantle musculature of the adult.

Conclusions

To our knowledge, this is the first account of any larval retractor system that might contribute to the adult bodyplan of a (conchiferan) mollusk. A comparative analysis shows that a pedal plexus, adductors, a larval velum ring, velum retractors and a ventral larval retractor are commonly found among bivalve larvae, and thus most likely belong to the ground pattern of the bivalve larval musculature.

     

Ontogenetic development of weberian ossicles and hearing abilities in the African bullhead catfish

Background

The Weberian apparatus of otophysine fishes facilitates sound transmission from the swimbladder to the inner ear to increase hearing sensitivity. It has been of great interest to biologists since the 19^th century. No studies, however, are available on the development of the Weberian ossicles and its effect on the development of hearing in catfishes.

Methodology/Principal Findings

We investigated the development of the Weberian apparatus and auditory sensitivity in the catfish Lophiobagrus cyclurus. Specimens from 11.3 mm to 85.5 mm in standard length were studied. Morphology was assessed using sectioning, histology, and X-ray computed tomography, along with 3D reconstruction. Hearing thresholds were measured utilizing the auditory evoked potentials recording technique. Weberian ossicles and interossicular ligaments were fully developed in all stages investigated except in the smallest size group. In the smallest catfish, the intercalarium and the interossicular ligaments were still missing and the tripus was not yet fully developed. Smallest juveniles revealed lowest auditory sensitivity and were unable to detect frequencies higher than 2 or 3 kHz; sensitivity increased in larger specimens by up to 40 dB, and frequency detection up to 6 kHz. In the size groups capable of perceiving frequencies up to 6 kHz, larger individuals had better hearing abilities at low frequencies (0.05–2 kHz), whereas smaller individuals showed better hearing at the highest frequencies (4–6 kHz).

Conclusions/Significance

Our data indicate that the ability of otophysine fish to detect sounds at low levels and high frequencies largely depends on the development of the Weberian apparatus. A significant increase in auditory sensitivity was observed as soon as all Weberian ossicles and interossicular ligaments are present and the chain for transmitting sounds from the swimbladder to the inner ear is complete. This contrasts with findings in another otophysine, the zebrafish, where no threshold changes have been observed.     

Myoanatomy and serotonergic nervous system of plumatellid and fredericellid phylactolaemata (lophotrochozoa,ectoprocta)

The phylogenetic position of the Ectoprocta within the Lophotrochozoa is discussed controversially. For gaining more insight into ectoproct relationships and comparing it with other potentially related phyla, we analysed the myoanatomy and serotonergic nervous system of adult representatives of the Phylactolaemata (Plumatella emarginata, Plumatellavaihiriae, Plumatella fungosa, Fredericella sultana). The bodywall contains a mesh of circular and longitudinal muscles. On its distal end, the orifice possesses a prominent sphincter and continues into the vestibular wall, which has longitudinal and circular musculature. The tentacle sheath carries mostly longitudinal muscle fibres in Plumatella sp., whereas F. sultana also possesses regular circular muscle fibres. Three groups of muscles are associated with the lophophore: 1) Lophophoral arm muscles (missing in Fredericella), 2) epistome musculature and 3) tentacle musculature. The epistome flap is encompassed by smooth muscle fibres. A few fibres extend medially over the ganglion to its proximal floor. Abfrontal tentacle muscles have diagonally arranged muscle fibres in their proximal region, whereas the distal region is formed by a stack of muscles that resemble an inverted ‘V’. Frontal tentacle muscles show more variation and either possess one or two bases. The digestive tract possesses circular musculature which is striated except at the intestine where it is composed of smooth muscle fibres. The serotonergic nervous system is concentrated in the cerebral ganglion. From the latter a serotonergic nerve extends to each tentacle base. In Plumatella the inner row of tentacles at the lophophoral concavity lacks serotonergic nerves. Bodywall musculature is a common feature in many lophotrochozoan phyla, but among other filter feeders like the Ectoprocta is only present in the ‘lophophorate’ Phoronida. The longitudinal tentacle musculature is reminiscent of the condition found in phoronids and brachiopods, but differs to entoproct tentacles. Although this study shows some support for the ‘Lophophorata’, more comparative analyses of possibly related phyla are required. J. Morphol., 2011. © 2011 Wiley Periodicals, Inc.     

Trapped in freshwater: the internal anatomy of the entoproct Loxosomatoides sirindhornae

Background

The identification of vast numbers of unknown organisms using DNA sequences becomes more and more important in ecological and biodiversity studies. In this context, a fragment of the mitochondrial cytochrome c oxidase I (COI) gene has been proposed as standard DNA barcoding marker for the identification of organisms. Limitations of the COI barcoding approach can arise from its single-locus identification system, the effect of introgression events, incomplete lineage sorting, numts, heteroplasmy and maternal inheritance of intracellular endosymbionts. Consequently, the analysis of a supplementary nuclear marker system could be advantageous.

Results

We tested the effectiveness of the COI barcoding region and of three nuclear ribosomal expansion segments in discriminating ground beetles of Central Europe, a diverse and well-studied invertebrate taxon. As nuclear markers we determined the 18S rDNA: V4, 18S rDNA: V7 and 28S rDNA: D3 expansion segments for 344 specimens of 75 species. Seventy-three species (97%) of the analysed species could be accurately identified using COI, while the combined approach of all three nuclear markers provided resolution among 71 (95%) of the studied Carabidae.

Conclusion

Our results confirm that the analysed nuclear ribosomal expansion segments in combination constitute a valuable and efficient supplement for classical DNA barcoding to avoid potential pitfalls when only mitochondrial data are being used. We also demonstrate the high potential of COI barcodes for the identification of even closely related carabid species.     

Three phyla—Two type specimens—One shell: History of a snail shell revealed by modern imaging technology

In a recent revision of the gastropod genus Bellardiella, it became evident that the neotype of B. crassilabris had numerous borings over its entire shell surface. Superficial and light microscopical observation of the shell showed that the borings were made by a bryozoan belonging to the genus Penetrantia. Conventional techniques such as endocasting with the dissolution of the shell are impossible for type material. The application of non‐destructive micro‐CT‐scanning of the shell revealed the three‐dimensional arrangement of the entire colony within the shell. Careful analysis of the structure of the autozooids of the colony revealed that the species could not be assigned to any known species; we accordingly describe it as Penetrantia bellardiellae Schwaha, n. sp. The application of micro‐CT not only allowed the depiction of the new bryozoan species but also revealed the remains of a hermit crab located within the shell. The shell of Bellardiella crassilabris thus represents the type specimen of two species and contains a member of a third phylum inside. To our knowledge, this is a unique case, which also emphasizes the usefulness of micro‐CT imaging for precious specimens as well as the importance of historical museum collections.     

Organogenesis during budding and lophophoral morphology of Hislopia malayensis Annandale, 1916 (Bryozoa, Ctenostomata)

Background  

Bryozoans represent a large lophotrochozoan phylum with controversially discussed phylogenetic position and in group relationships. Developmental processes during the budding of bryozoans are in need for revision. Just recently a study on a phylactolaemate bryozoan gave a comprehensive basis for further comparisons among bryozoans. The aim of this study is to gain more insight into developmental patterns during polypide formation in the budding process of bryozoans. Particular focus is laid upon the lophophore, also its condition in adults. For this purpose we studied organogenesis during budding and lophophoral morphology of the ctenostome bryozoan Hislopia malayensis.     

O anus,where art thou? An investigation of ctenostome bryozoans

Ctenostome bryozoans are a small group of approximately 350 currently described species that remain inadequately investigated anatomically. Recently, the importance of soft body morphology of zooids including the digestive tract has become more evident for addressing various biological aspects such as systematic, functional, or phylogenetic analyses. Particularly, the position of the anus shows considerable variation in ctenostomes and in its extreme form can either be at the lophophoral base or at the vestibular wall. However, it has never been analysed in a broader systematic, phylogenetic, or functional context. Hence, the purpose of this study is to assess the distribution of anus position among ctenostomes, analyse whether zooidal or colonial morphology affects anus position, and draw first conclusions on its functional effects. The survey shows that a vestibular anus is ubiquitously present in alcyonidioideans and several, probably closely related, walkerioideans. In other groups such as boring forms, it appears more patchily distributed, or in some currently unassignable genera, such as Monobryozoon, supports a closer relationship to alcyonidioideans. Other zooidal or colonial characters such as tentacle number or zooidal density in the colony do not show a distinct correlation to the position of the anus. It appears that the shift of the anus into a vestibular area occurred once or twice among ctenostomes; the reasons and functional effects remain unknown. Future important aspects of defecation research in bryozoans are discussed.     

Towards a ground pattern reconstruction of bivalve nervous systems: neurogenesis in the zebra mussel <Emphasis Type="Italic">Dreissena polymorpha</Emphasis>

Bivalvia is a taxon of aquatic mollusks that includes clams, oysters, mussels, and scallops. Within heterodont bivalves, Dreissena polymorpha is a small, mytiliform, freshwater mussel that develops indirectly via a planktotrophic veliger larva. Currently, only a few studies on bivalve neurogenesis are available, impeding the reconstruction of a ground pattern in Bivalvia. In order to inject novel data into this discussion, we describe herein the development of the serotonin-like and α-tubulin-like immunoreactive (lir) neuronal components of D. polymorpha from the early trochophore to the late veliger stage. Neurogenesis starts in the early trochophore stage at the apical pole with the appearance of one flask-shaped serotonin-lir cell. When larvae reach the veliger stage, four flask-shaped serotonin-lir cells are present in the apical organ. At the same time, the anlagen of the cerebral ganglia start to form at the base of the apical organ. From the apical organ, one pair of cerebro-visceral connectives projects posteriorly and connects to a posterior larval sensory organ that contains serotonin- and α-tubulin-like flask-shaped cells. Additional, paired serotonin-lir neurites originate from the apical organ and project into the velum. One unpaired stomatogastric serotonin-lir cell develops ventrally to the stomach at the veliger stage. The low number of serotonin-lir cells in the apical organ of bivalve veligers is shared with larvae of basally branching gastropods and scaphopods and is thus considered a feature of the last common ancestor of Conchifera, while the overall simplicity of the larval neural architecture appears to be a specific trait of Bivalvia.