Initial morphological diversity as a criterion in deciphering turbellarian phylogeny

The most profound structural variety in morphofunctional systems and morphogenetic mechanisms, i.e. the highest morphological diversity, is observed in those groups where these systems and mechanisms are evolutionarily most primitive. Here, such variety can involve the basic body plan of a given phylum and the types of morphogenesis characteristic of it. This correlation provides a new criterion of evolutionary primitiveness, namely, the criterion of initial morphological diversity.The highest morphological diversity among turbellarian groups is observed in the order Acoela. Acoel turbellarians are archaic in most of their features, apparently being a group near the base of the turbellarian phylogenetic tree. Among other turbellarians there are a few groups that also are archaic in some few features (above all, the Catenulida), although on the whole they are more advanced than the Acoela. The Turbellaria as a whole is notable for its morphological diversity in comparison with other classes of the Scolecida.     

Comparative ultrastructure of the pharynx simplex in turbellaria

Summary The simple pharynges in thirteen species of Turbellaria in the orders Macrostomida, Haplopharyngida, Catenulida, and Acoela have been studied by electron microscopy. After consideration of the functional aspects of the pharynx simplex, the relationship of the pharynx simplex ultrastructure to the phylogeny of the above mentioned groups is analyzed.The Haplopharyngida and Macrostomida are united as a group by the following characters: a pharynx transition zone of 1–5 circles of insunk cells with modified ciliary rootlets or no cilia, pharynx sensory cells without stereocilia collars and with a variable number of cilia, a prominent nerve ring with more than 30 axons circling the pharynx at the level of the beginning of the pharynx proper distal to the gland ring, 2 or more gland cell types in the pharynx, with at least two layers of muscle present and the longitudinal muscles derived from regular and special body wall circular muscles and a prominent post-oral nerve commissure. This specific arrangement can be distinguished from the other pharynx simplex types and is called the pharynx simplex coronatus.The catenulid pharynx simplex is characterized by the lack of a prominent nerve ring, no prominent post-oral commissure, a transition zone with epidermal type ciliary rootlets, recessed monociliated sensory cells, and one or no type of pharynx gland cell. The Acoela are specialized because of the epidermal type rootlets in the pharynx proper. They also lack a transition zone and a prominent nerve ring and have monociliated sensory cells different from the catenulid type.Ultrastructural characters of the pharynx simplex support the view that the Haplopharyngida-Macrostomida are monophyletic. The more primitive catenulid pharynx probably arose from a common ancestral pool with the Haplopharyngida and Macrostomida, although it does not appear possible presently to establish a clear monophyletic line for these forms. The various pharynx types within the Acoela appear to indicate independent origins with no clear link to the basic pharynx simplex type in the three other orders.Abbreviations Used in Figures a nerve axon - ar accessory rootlet - bb basal body - bn brain-nerve ring commissure - c caudal rootlet - ce centriole - ci cilium - cm circular muscle - cp ciliary pit - cu cuticle - cw cell web - d dictyosome - dp proximal pharynx proper cell - e epidermis - er rough endoplasmic reticulum - f fibrous rod - g gastrodermis - gc gastrodermal gland cell - he heterochromatin - i intercellular matrix - lc lateral nerve cord - lm longitudinal muscle - m mitochondria - mo mouth - mt microtubules - mv microvilli - n nucleus - nr nerve ring - ns neurosecretory granules - p pharynx proper - ph pharynx - po post-oral commissure - r rostral rootlet - rm radial muscle - s sphincter - sc sensory cell - sj septate junction - sr sensory rootlet - t transition zone - u ultrarhabdite - v vertical rootlet - va food vacuole - za zonula adhaerens - 1 type I gland cell - 2 type II gland cell - 3 type III gland cell - 4 type IV gland cell - 5 type V gland cell - 6 type VI gland cell - 7 type VII gland cell     

The importance of turbellarians in the marine meiobenthos: a review

Recent data and opinions on meiofaunal ecology are briefly reviewed; and from scattered data, the place of turbellarians in the meiobenthic community is discussed. Turbellarian diversity, density, and biomass are higher in sandy habitats than in muddy bottoms. In sand, turbellarian diversity is of the same magnitude as that of other important meiofaunal taxa, while densities range between 7–25% of the total meiofauna. Mean individual turbellarian dry weight seems to be four times that of nematodes and in sandy habitats turbellarian biomass may be equal to or excede that of nematodes. Most turbellarian species may be considered as predators and in this respect may take the place occupied by macrofaunal species in muddy sediments. mens.

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A rhabdocoel turbellarian (Platyhelminthes, Typhloplanoida) in Baltic amber with a review of fossil and sub-fossil platyhelminths

Abstract. Palaeosoma balticus n. g., n. sp. (Rhabdocoela, Typhloplanoida), the oldest body fossil of a turbellarian and the first representative of the phylum Platyhelminthes found in fossilized resin, is described from Baltic amber 40 million years old. Characters of the fossil turbellarian are epidermal cilia, rhabdoids, a rosulate pharynx, adhesive papillae, and sensory bristles. The body cavity contains developing eggs or capsules. The fossil demonstrates that rhabdocoels had developed a terrestrial habit and were producing subitaneous eggs by the Eocene. A summary of the fossil and sub-fossil records of platyhelminths is presented.     

Monociliary receptors in interstitial Proseriata and Neorhabdocoela (Turbellaria Neoophora)

Summary The ultrastructure of monociliary receptors in 10 species of the Proseriata and Neorhabdocoela is described, with particular reference to the epidermal dendritic part.Sensory cells with a single kinocilium situated at the level of the distal epidermis membrane are considered as mechano- or chemoreceptors.There exist sensory cells with a dendrite penetrating one epidermis cell and bearing an embedded kinocilium and a collar of 8 stereocilia or ridges with a fribrillose substructure. These collared receptors probably function as mechanoreceptors.In comparison with collared sensory cells in species of other turbellarian orders, the embedded receptors in the Proseriata and Neorhabdocoela are more advanced and possess synapomorphous characteristics. With the embedded receptors a new evidence is given for the close phylogenetic relationship between the Proseriata and Neorhabdocoela.The distribution of collared cells in the animal system and their phylogenetic implication for a choanoflagellate origin of the Metazoa are briefly discussed.List of abbreviations ar annular rootlet - bm basement membrane - cb crystalline body - cc collar cell - cw cell web - cwt cell web-thickening - d dendrite - kc kinocilium - lm longitudinal musculature - mv microvilli - n nerve - nt neurotubuli - pb parenchymal branches - r rootlet - rd ridges - rh rhabdite - rm ring musculature - sc stereocilia - sd septate desmosomes - tm transversal musculature - u ultrarhabdites - za zonula adhaerens     

Distinctive features of cilia in metazoans and their significance for systematics.

A comparative study of epidermal cilia in the Turbellaria and Nemertea has revealed features in these organelles that are specific to certain taxonomic groups. Turbellarians of the order Acoela, in particular, have a characteristic pattern of axonemal filament termination in the distal tips of their cilia and a characteristic ciliary rootlet system that is not seen in other turbellarian orders nor in other metazoans. Each epidermal cilium in acoels has a typical 9 + 2 axonemal pattern through the main part of its length, but near its distal tip there is an abrupt shelf-life narrowing at which filaments 4-7 terminate; filaments 1, 2, 8 and 9 continue into the thinner distal-most part of the shaft along with singlet microtubules from the axonemal center. The rootlet system in acoel cilia involves an interconnecting pattern with lateral connectives. The unique structure of these cilia has systematic and phylogenetic significance for the Acoela, and it is argued that ultrastructural characters in general, including characters of organelles, can be validly applied to the phylogeny and systematics of the Metazoa.     

What studies of turbellarian embryos can tell us about the evolution of development mechanisms

In spiralian embryos determination of the axes of bilateral symmetry is associated with D quadrant specification. This can occur late through equal cleavage and cell interactions (conditional specification) or by the four-cell stage through unequal cleavage and cytoplasmic localization (autonomous specification). Freeman & Lundelius (1992) suggest that in spiralian coelomates the former method is ancestral and the latter derived, with evolutionary pressure to shorten metamorphosis resulting in early D quadrant determination through unequal cleavage and appearance of adult features in the larvae. Because of the key phylogenetic position of the turbellarian platyhelminthes, understanding the method of axis specification in this group is important in evaluating the hypothesis. Polyclad development, with equal quartet spiral cleavage, is believed to represent the most primitive condition among living turbellarians and has been examined experimentally in Hoploplana inquilina. Blastomere deletions at the two and four-cell stage produce larvae that are abnormal in morphology and symmetry, indicating that early development is not regulative, and also establish that the embryo does not have an invariant cell lineage. Deletions of micromeres and macromeres at the eight-cell stage indicate that cell interactions are involved in dorso-ventral axis determination, with cross-furrow macromeres playing a more significant role than non-cross-furrow cells. The results support the idea that conditional specification is the primitive developmental mode that characterized the common ancestor of the turbellarians and spiralian coelomates. Evolutionary trends in development in polyclads and other turbellarian orders are discussed.     

The ciliated epidermis of Xenoturbella bocki (Platyhelminthes, Xenoturbellida) with some phylogenetic considerations

The epidermis of Xenoturbella bocki Westblad was studied by scanning and transmission electron microscopy. Two cell types predominate in the epidermis: multiciliated epidermal cells and non-ciliated or monociliated gland cells. A conspicuous feature is the dense ciliary coverage and the numerous gland cell openings. Xenoturbella has a characteristic pattern of axonemal filament termination in the distal tips of their cilia. Each epidermal cilium has the typical 9 + 2 patten through the major part of its shaft. Near the tip there is a shelf at which doublets 4–7 terminate. Doublets 1, 2, 3, 8 and 9 continue into the thinner distal part of the cilium. A similar shelf in cilia is known only from the turbellarian orders Nemertodermatida and Acoela, and hence may be an apomorphic feature which indicates a close relationship between Xenoturbellida, Nemertoder-matida and Acoela. The basal body is provided with a so-called basal foot which has a cross-striated appearance and an expanded distal plate that seems to act as a microtubule organizing center. Approximately 15–25 microtubuli radiate from the endplate of the basal foot to the basal bodies caudally. The arrangement of basal foot and ciliary rootlets in Xenoturbella differs from that of Acoela and related orders in that there are two striated rootlets only (an anterior and a posterior one), rather than one main rootlet and two lateral rootlets.     

Ultrastructural features of the epidermis in turbellaria from the Lake Baikal Geocentrophora wagini (Lecithoepitheliata, Plathelminthes)

The epidermis of Geocentrophora wagini was studied using transmission electron microscopy. The turbellarian body was entirely covered by cilia, whose density was higher on the ventral surface compared with the dorsal one. In all regions examined, the epidermis was made up of a one-layered insunk epithelium. The basal matrix, underlying the epidermis, was a well developed basement membrane (BM) with bilayered structure, overlying the muscle network of circular and longitudinal fibers. The double plasma membranes, extending from the apical surface of epidermis to BM, were linked by specialized cell junctions. This suggested that epidermis had a cellular rather than a cyncytial arrangement. Each insunk epidermal cell was made of two unequal parts: a comparatively thin surface plate attached to BM by hemiadherens junctions, and a massive nucleated portion located below the body wall musculature in the parenchyma. A thin cytoplasmic bridge connected the epidermal plate with the nucleated cell body. The epidermal plates were joined by belt-like junctions along their adjacent surfaces. Inconspicuous zonula adherens (ZA) had a most apical position, and prominent septate junction was arrayed proximally to this zonula. Except ZA, cell boundaries in epidermis were frequently flanked by rows of light tubules and vesicles. In the basal half of the epithelial sheet, they were occassionally accompanied by single cisternae of rough endoplasmic reticulum (RER). The ultrastructure of the insunk cell body and that of the surface plate showed a considerable similarity. The common features were distinctive profiles of RER and GA, the presence of epitheliosomes, light tubules and vesicles, centrioles and fibrous granules. Thus, ultrastructural features allow a rather reliable identification of epidermal cells in the parenchyma, despite the absence of any visible morphological association between cell body and its epidermal plate.     

Ultrastructure of the eyes of the larva of Neoheterocotyle rhinobatidis (Platyhelminthes, Monopisthocotylea), and phylogenetic implications.

The oncomiracidium of Neoheterocotyle rhinobatidis (Monogenea, Monopisthocotylea, Monocotylidae) has two pairs of eyes, each eye with a lens and pigment cup. The anterior eyes have a single rhadomere; the posterior ones, two rhadomeres. Lenses are part of the pigment cup cells, as indicated by cytoplasmic connections between them and the pigment cups, and they are of mitochondrial origin because mitochondrial cristae are present in the periphery of the lenses. This is the first time that mitochondrial lenses have been shown to exist in a neodermatan. Such lenses may be a synapomorphy of a large taxon comprising the Neodermata and its turbellarian sister groups, or they may have evolved convergently in several not closely related groups as a result of strong selection pressure to find a suitable habitat or host.     

The Nervous System of Procerodes littoralis (Maricola,Tricladida). An Ultrastructural and Immunoelectron Microscopical Study

The ultrastructure of the nervous system of a planarian, Procerodes littoralis, belonging to the taxon Maricola is described for the first time. The study has revealed the presence of two neuronal cell types and a glia-like cell. Immunogold labelling with antibodies to two native flatworm neuropeptides—neuropeptide F and GNFFRFamide—has been localised to one neuronal cell type and associated processes and synapses, thus indicating its peptidergic nature. The ultrastructural features are compared to those of other investigated turbellarian species. The number of features shared by species from the Proseriata, Lecitoepitheliata and Tridadida show that in respect of the nervous system these taxa form a closely related group.     

Flagellar and cytoskeletal systems in amitochondrial flagellates: Archamoeba,Metamonada and Parabasala

Summary The hypothesis that protists without mitochondria, the so-called Archezoa of Cavalier-Smith, are primitive has received some support from rRNA sequence studies on Microsporidia and Diplomonadida. In spite of the lack of mitochondria the archezoan groups of protists show considerable differences in their organization: mastigont and cytoskeletal system, mitosis, Golgi apparatus, hydrogenosomes. This paper examines the characters of the flagellar apparatus and its associated cytoskeleton to obtain clues used for phylogenetic consideration on the three cited groups of flagellates. Archamoebae of the Pelobiontida order comprising families such as Pelomyxidae and Mastigamoebidae share common features: a rudimentary mastigont system composed of only one basal body giving rise to a poorly motile flagellum and a basal body associated microtubular cone capping the nucleus. No Golgi apparatus has been detected.Metamonada, comprising three orders: Retortamonadida, Diplomonadida, and Oxymonadida, have been tentatively assembled on the basis of the absence of mitochondria, Golgi apparatus, and basal body arrangement. They all have four basal bodies arranged in two pairs with always one recurrent flagellum generally included in a cytostomal depression. The recurrent basal body/flagellum is in relation to recurrent microtubular fibers. However, they display marked differences in their cytoskeletal system and fiber ultrastructure indicating a distant evolutionary relationship. The presence of a corset of microtubules in retortamonads and three microtubular fibers are distinguished in diplomonads, as well as a paracrystalline preaxostyle and axostyle in oxymonads are features that lend support to these groups being highly divergent.Parabasala, comprising the orders Trichomonadida and Hypermastigida, is a monophyletic group with a set of homologous features such as the presence of the same arrangement of four basic basal bodies, the parabasal apparatus (striated fibre supporting Golgi), the microtubular pelta-axostyle complex, the external mitotic apparatus (crypto-pleuro-mitosis), the hydrogenosomes. These three phyla appear distantly related, the Parabasala being a homogeneous group, perhaps also the Pelobiontida, while the Metamonada is heterogeneous and composed of three evolutionary lineages. Additional information such as rRNA and protein sequence data could contribute to a better understanding of the phylogenetic relationships among these groups.Abbreviations EM electron microscopy - MTOC microtubule organizing centre - PF parabasal fibre     

On the evolution of central nervous systems: Implications from polyclad turbellarian neurobiology

The nervous system of the polyclad turbellarian Notoplana acticola consists of a series of nerve plexuses and a central ganglion, the brain. The brain contains a variety of cell types including multipolar heteropolar and bipolar neurons. These cell types are rare in other invertebrate ganglia. Individual neurons also contain a variety of different ion channels. both spiking and nonspiking neurons are found. Some neurons are multimodal interneurons. Habituation appears to be a postsynaptic phenomenon. Sensitization and long-term potentiation have not been demonstrated. Polyclads appear to represent a stage in the evolution of centralized nervous systems where much of the neuronal machinery underlying behavior occurs in the peripheral nervous system and the brain's main functions are the coordination and sequencing of peripherally placed reflexes. Even at this stage, however, the brain already contains cells that seem as advanced as those found in higher organisms.     

Epidermal ultrastructure of the adult parasitic phase female and encapsulated larva of Kronborgia isopodicola (Platyhelminthes, Fecampiidae): Phylogenetic implications

The parasitic phase female K. isopodicola possesses a ciliated epidermis of polyhedral cells. Adjacent lateral plasma membranes are separated at intervals creating intercellular spaces. Epidermal cilia are anchored by a horizontal rootlet, opposite which a spur projects from the basal body, and a narrow vertical rootlet. The cytoplasm contains coated vesicles, and coated pits lie between microvilli. Large granular and vesicular bodies (rhabdoids) are scattered through the epidermal epithelium; in the epidermis of the encapsulated larva, granular rhabdoids are densely packed and slender, more compact bodies also occur. The compact, granular and vesicular bodies are probably morphological variants of the same epidermal structures, suggested to undergo sequential changes accomplished in later stages by lysosomal activity. Morphologically similar epidermal bodies are found in triclads. They are also characteristic of the parasitic genus Urastoma, which shares other ultrastructural features with K. isopodicola. The Neodermata may have arisen from parasitic turbellarian forms, at a more “primitive” level of organization than ancestors of the contemporary Rhabdocoela.     

Microanatomy of the trophosome region of <Emphasis Type="Italic">Paracatenula</Emphasis> cf. <Emphasis Type="Italic">polyhymnia</Emphasis> (Catenulida,Platyhelminthes) and its intracellular symbionts

Marine catenulid platyhelminths of the genus Paracatenula lack mouth, pharynx and gut. They live in a symbiosis with intracellular bacteria which are restricted to the body region posterior to the brain. The symbiont-housing cells (bacteriocytes) collectively form the trophosome tissue, which functionally replaces the digestive tract. It constitutes the largest part of the body and is the most important synapomorphy of this group. While some other features of the Paracatenula anatomy have already been analyzed, an in-depth analysis of the trophosome region was missing. Here, we identify and characterize the composition of the trophosome and its surrounding tissue by analyzing series of ultra-thin cross-sections of the species Paracatenula cf. polyhymnia. For the first time, a protonephridium is detected in a Paracatenula species, but it is morphologically reduced and most likely not functional. Cells containing needle-like inclusions in the reference species Paracatenula polyhymnia Sterrer and Rieger, 1974 were thought to be sperm, and the inclusions interpreted as the sperm nucleus. Our analysis of similar cells and their inclusions by EDX and Raman microspectroscopy documents an inorganic spicule consisting of a unique magnesium–phosphate compound. Furthermore, we identify the neoblast stem cells located underneath the epidermis. Except for the modifications due to the symbiotic lifestyle and the enigmatic spicule cells, the organization of Paracatenula cf. polyhymnia conforms to that of the Catenulida in all studied aspects. Therefore, this species represents an excellent model system for further studies of host adaptation to an obligate symbiotic lifestyle.     

Comparative study of the choanosome of porifera: II. The keratose sponges

The aquiferous system of representatives of the orders Dictyocer-atida, Dendroceratida, and Verongida has been studied to note its relevance to the systematics of the groups. The volume of the choanocyte chamber, the size and shape of the choanocytes, the number of choanocytes per chamber, the relative development of the mesohyl, and the features of endopinacocytes are estimated from scanning and transmission electron microscopic observations of representatives of most families of the three orders. Although the Dysideidae have a reticulate skeleton and were classified in the order Dictyoceratida, they are actually closer to the Aplysillidae (Dendroceratida) than to dictyoceratids. The anatomy and cytology of the Halisarcidae differ profoundly from those of these three orders and are clearly more closely related to nonkeratose sponges. Some changes in classification lead to a pattern with highly homogeneous orders that clearly differ in their anatomic and cytologic features, which does not support the hypothesis of a common origin of the “keratose” sponges.     

False Vertical Rootlets of Epidermal Cilia in the Oncomiracidia of Neoheterocotyle rhinobatidis and Monocotyle spiremae (Platyhelminthes,Monogenea, Monopisthocotylea)

Epidermal cilia of the oncomiracidium of Neoheterocotyle rhinobatidis (Monogenea, Monopisthocotylea, Monocotylidae) have long cross-striated vertical rootlets that are not extensions of the basal bodies as are the vertical rootlets in all catenulid and rhabditophoran turbellarians examined to date. Instead, they originate in the basal part of the horizontal rootlet a short distance from the basal bodies. In Monocotyle spiremae (Monocotylidae), the vertical rootlets are less distinct, with no apparent cross-striation, but they also originate from the basal part of the horizontal rootlets. Epidermal cilia of the oncomiracidium of Zeuxapta seriolae (Monogenea, Polyopisthocotylea, Axinidae) lack vertical rootlets like all other neodermatans examined, but bundles of fibres extend from the basal bodies a short distance into the cytoplasm of the epidermal cells. Monopisthocotylean Monogenea would be intermediate between rhabditophorans and the other neodermatans (in having weakly developed vertical rootles), if these structures were homologous in the two groups. However, in view of the different origin of vertical rootlets in turbellarians and monopisthocolylean oncomiracidia, it is suggested that they are not homologous, and vertical rootlets in the Monopisthocotylea are therefore named “false vertical rootlets”.