The first data on the innervation of the lophophore in the rhynchonelliform brachiopod Hemithiris psittacea: what is the ground pattern of the lophophore in lophophorates?

BACKGROUND: The nervous system in brachiopods has seldom been studied with modern methods. An understanding of lophophore innervation in adult brachiopods is useful for comparing the innervation of the same lophophore type among different brachiopods and can also help answer questions about the monophyly of the lophophorates. Although some brachiopods are studied with modern methods, rhynchonelliform brachiopods still require investigation. The current study used transmission electron microscopy, immunocytochemistry, and confocal laser scanning microscopy to investigate the nerve system of the lophophore and tentacles in the rhynchonelliform Hemithiris psittacea. RESULTS: Four longitudinal nerves pass along each brachium of the lophophore: the main, accessory, second accessory, and lower. The main brachial nerve extends at the base of the dorsal side of the brachial fold and gives rise to the cross nerves, passing through the extracellular matrix to the tentacles. Cross nerves skirt the accessory brachial nerve, branch, and penetrate into adjacent outer and inner tentacles, where they are referred to as the frontal tentacular nerves. The second accessory nerve passes along the base of the inner tentacles. This nerve consists of Ʊ-like parts, which repetitively skirt the frontal and lateral sides of the inner tentacle and the frontal sides of the outer tentacles. The second accessory nerve gives rise to the latero-frontal nerves of the inner and outer tentacles. The abfrontal nerves of the inner tentacles also originate from the second accessory nerve, whereas the abfrontal nerves of the outer tentacles originate from the lower brachial nerve. The lower brachial nerve extends along the outer side of the lophophore brachia and gives rise to the intertentacular nerves, which form a T-like branch and penetrate the adjacent outer tentacles where they are referred to as abfrontal nerves. The paired outer radial nerves start from the lower brachial nerve, extend into the second accessory nerve, and give rise to the lateroabfrontal tentacular nerves of the outer tentacles. CONCLUSIONS: The innervation of the lophophore in the rhynchonelliform Hemithiris psittacea differs from that in the inarticulate Lingula anatina in several ways. The accessory brachial nerve does not participate in the innervation of the tentacles in H. psittacea as it does in L. anatina. The second accessory nerve is present in H. psittacea but not in L. anatina. There are six tentacular nerves in the outer tentacles of H. psittacea but only four in all other brachiopods studied to date. The reduced contribution of the accessory brachial nerve to tentacle innervation may reflect the general pattern of reduction of the inner lophophoral nerve in both phoronids and brachiopods. Bryozoan lophophores, in contrast, have a weakened outer nerve and a strengthened inner nerve. Our results suggest that the ancestral lophophore of all lophophorates had a simple shape but many nerve elements.

The nervous system of the most complex lophophore provides new insights into the evolution of Brachiopoda.

The lophophore is a tentacle organ unique to the lophophorates. Recent research has revealed that the organization of the nervous and muscular systems of the lophophore is similar in phoronids, brachiopods, and bryozoans. At the same time, the evolution of the lophophore in certain lophophorates is still being debated. Innervation of the adult lophophore has been studied by immunocytochemistry and confocal laser scanning microscopy for only two brachiopod species belonging to two subphyla: Linguliformea and Rhynchonelliformea. Species from both groups have the spirolophe, which is the most common type of the lophophore among brachiopods. In this study, we used transmission electron microscopy, immunocytochemistry, and confocal laser scanning microscopy to describe the innervation of the most complex lophophore (the plectolophe) of the rhynchonelliform species Coptothyris grayi. The C. grayi lophophore (the plectolophe) is innervated by three brachial nerves: the main, second accessory, and lower. Thus, the plectolophe lacks the accessory brachial nerve, which is typically present in other studied brachiopods. All C. grayi brachial nerves contain two types of perikarya. Because the accessory nerve is absent, the cross nerves, which pass into the connective tissue, have a complex morphology: each nerve consists of two ascending and one descending branches. The outer and inner tentacles are innervated by several groups of neurite bundles: one frontal, two lateral, two abfrontal, and two latero-abfrontal (the latter is present in only the outer tentacles). Tentacle nerves originate from the second accessory and lower brachial nerves. The inner and outer tentacles are also innervated by numerous peritoneal neurites, which exhibit acetylated alpha-tubulin-like immunoreactivity. The nervous system of the lophophore of C. grayi manifests several evolutionary trends. On the one hand, it has undergone simplification, i.e., the absence of the accessory brachial nerve, which is apparently correlated with a reduction in the complexity of the lophophore's musculature. On the other hand, C. grayi has a prominent second accessory nerve, which contains large groups of frontal perikarya, and also has additional nerves extending from the both ganglia to the medial arm; these features are consistent with the complex morphology of the C. grayi plectolophe. In brachiopods, the evolution of the lophophore nervous system apparently involved two main modifications. The first modification was the appearance and further strengthening of the second accessory brachial nerve, which apparently arose because of the formation of a double row of tentacles instead of the single row of the brachiopod ancestor. The second modification was the partial or complete reduction of some brachial nerves, which was correlated with the reduced complexity of the lophophore musculature and the appearance of skeletal structures that support the lophophore.

Spermatogenesis in the deep-sea brachiopod Pelagodiscus atlanticus and the phylogenetic significance of spermatozoon structure.

Details of spermatogenesis and sperm organization are often useful for reconstructing the phylogeny of closely related groups of invertebrates. Development in general and gametogenesis in particular usually differ in shallow water and deep-sea invertebrates. Here, the spermatogenesis and ultrastructure of sperm were studied in the deep-sea brachiopod Pelagodiscus atlanticus. The testes of P. atlanticus are voluminous sacs located along the lateral sides of the body. Germ cells develop around the blood capillaries, contact the basal lamina, and contain germ plasm, numerous mitochondria, Golgi apparatus, lipid droplets, and centrioles of the rudimentary cilium. During spermatogenesis, several proacrosomal vesicles appear at the posterior pole of the cell; these vesicles then fuse and migrate to the anterior pole. The spermatozoon has a head with an acrosome, nucleus, eight mitochondria, proximal and distal centrioles orthogonally arranged, and a long tail. Comparative analysis suggests that the spermatozoon of P. atlanticus can be considered the most ancestral among all brachiopods. Such an organization indicates that fertilization is external in this deep-sea species. Spermatozoa of other brachiopods should be regarded as derived from this ancestral type. The transformation of brachiopod spermatozoa might have occurred in three different ways that correspond to the three main clades of recent brachiopods: Linguliformea, Craniiformea, and Rhynchonelliformea.

The periesophageal celom of the articulate brachiopod Hemithyris psittacea (Rhynchonelliformea, Brachiopoda).

The celomic system of the articulate brachiopod Hemithyris psittacea is composed of the perivisceral cavity, the canal system of the lophophore, and the periesophageal celom. We study the microscopic anatomy and ultrastructure of the periesophageal celom using scanning and transmission electron microscopy. The periesophageal celom surrounds the esophagus, is isolated from the perivisceral cavity, and is divided by septa. The lining of the periesophageal celom includes two types of cells, epithelial cells and myoepithelial cells, both are monociliary. Some epithelial cells have long processes extending along the basal lamina, suggesting that these cells might function as podocytes. The myoepithelial cells have basal myofilaments and may be overlapped by the apical processes of the adjacent epithelial cells. The periesophageal celom forms protrusions that penetrate the extracellular matrix (ECM) of the body wall above the mouth and the ECM that surrounds the esophagus. The canals of the esophageal ECM form a complicated system. The celomic lining of the external circumferential canals consists of the epithelial cells and the podocyte-like cells. The deepest canals lack a lumen; they are filled with the muscle cells surrounded by basal lamina. These branched canals might perform dual functions. First, they increase the surface area and might therefore facilitate ultrafiltration through the podocyte-like cells. Second, the deepest canals form the thickened muscle wall of the esophagus and could be necessary for antiperistalsis of the gut.