Spermatogenesis and ultrastructure of the spermatozoa of Seison nebaliae (Syndermata)

 The spermatozoa of Seison nebaliae are characterized by an elongated sperm body, a filiform nucleus, and an anteriorly inserting external cilium with a 9×2+2 axoneme pattern. In the sperm body a frontal, middle, and hind region can be distinguished. The frontal region contains an acrosomal vesicle, a perforatorium, a basal body, and a pair of apical dense bodies; an accessory centriole is absent. The middle region is characterized by several so-called filamental plates. One large mitochondrion and one pair of accessory tubular structures are located in the middle and hind region. The hind region also contains two rows of dense bodies. Accessory tubular structures and filamental plates are autapomorphies of S. nebaliae. The shared appearance of the dense bodies in spermatozoa of species of the taxa Seison and the Acanthocephala founds their sister-group relationship, while the anterior insertion of the cilium in the spermatozoa of these taxa and in the Rotifera confirms the monophylum Syndermata Ahlrichs, 1995. Accepted: 5 August 1998     

Musculature of Seison nebaliae Grube, 1861 and Paraseison annulatus (Claus, 1876) revealed with CLSM: a comparative study of the gnathiferan key taxon Seisonacea (Rotifera)

The somatic muscular systems of two species of Seisonacea (Rotifera), Seison nebaliae and Paraseison annulatus, are described using fluorescently labelled phalloidin in combination with confocal laser scanning microscopy. Their overall muscular arrangement is similar and consists of segmentally organised longitudinal fibres that extend the length of the body and are surrounded by semi-circular (= incomplete) bands. However, differences in the musculature between the two species are present and possibly reflect specific adaptations in feeding strategy and locomotion related to the occupation of individual niches on their host, the leptostracan crustacean N. bipes. For example, S. nebaliae has semi-circular muscles in the head region only, while P. annulatus possesses incomplete circular muscles also in the trunk region; furthermore, there are also differences in the arrangements and number of longitudinal muscles. The muscular systems of all rotifer species examined so far are compared in order to establish the ground pattern of the last putative ancestor as well as to seek for traits of systematic importance. Results from both species corroborate earlier hypotheses on the arrangement of muscles in the putative common ancestor of Rotifera, which suggested an orthogonal arrangement consisting of a series of probably continuous (not segmental) inner longitudinal muscles, surrounded by semi-circular fibres, ventrally opened. However, significant morphological and ecological variations among taxa investigated so far show that a consistent correlation between muscular traits and specific ecological features and/or phylogeny is still far from being clear. Hence, musculature of additional taxa, representing the systematic width and occupying a diverse range of habitats, should be investigated.     

Old and new data on Seisonidea (Rotifera)

Class Seisonidea consists of one marine genus, Seison, with two species (S. nebaliae and S. annulatus) which are epizoic on the crustacean Nebalia. Seisonidea are the only rotifers whose reproduction is strictly bisexual. They also possess the unusual feature of having well-developed males. In this paper we review the literature concerning biogeographical distribution, relationships with their host, and morphology, and present new information obtained with SEM and optical microscopy of both living animals and serial sections.Some seisonid characters, such as the paired retrocerebral organ, nervous system, and trophi, suggest that they hold a primitive position within phylum Rotifera. However, they do share features with other rotifers: paired gonads and an unusual locomotory behavior with Bdelloidea; lateral antennae, cellular stomach wall, arrangement of intracytoplasmic lamina, and other characters with Monogononta. Some features are peculiar to Seison: obligatory amphimixis, endolecythal eggs, encysted spermatozoa, unique mastax, and absence of copulatory organ in males and of vitellaria in females. Reduction of the corona and absence of resistant stages in Seisonidea may be related to their habitat and to their life style. We propose a closer relationship of Seisonidea to Monogononta than previously asserted.     

Epidermal ultrastructure of Seison nebaliae and Seison annulatus, and a comparison of epidermal structures within the Gnathifera

 The epidermis of both species of Seison is syncytial and has a characteristic internal layer divided into two distinct sublayers. Sublayer I is very thin (0.03 μm) and bounded to the outer cell membrane of the epidermis. Sublayer II is 0.5 μm thick and separated from sublayer I by a thin layer of cytoplasm. Intrusions of the outer cell membrane of the epidermis perforate the internal layer, before terminating within the cytoplasm. The intrusions of the cell membrane of S. annulatus are coated by an electron-dense material, the annulus, when passing through the internal layer. Bundles of filaments are present in the epidermis of S. nebaliae. A comparison of epidermal structures within the Gnathifera Ahlrichs, 1995, confirms phylogenetic relationships earlier proposed by the author. Accepted: 19 December 1996     

Ultrastructure of the protonephridia of Seison annulatus (Rotifera)

Summary Each of the two protonephridial systems of Seison annulatus consists of three sections which are separated by cell borders with septate junctions: (a) a terminal syncytium with eight terminal organs and a capillary canal, (b) a canal syncytium which is divided into a multiciliary canal region and a main canal region, and (c) a nephroporus cell. The terminal syncytium is branched and linked twice to the canal syncytium. The supporting structure of each filtration barrier is a hollow cylinder which is perforated by pores and lacks microvilli (pillars). A protonephridial spine is situated in the multiciliary canal region and stabilizes the neck region. The ored, hollow cylinder and the protonephridial spine are new characteristics for the Rotifera.     

Spermiogenesis in a Scutariellid (Platyhelminthes)

Spermiogenesis and spermatozoa were studied by transmission and scanning electron microscopy in Troglocaridicolasp., a scutariellid epizoic on a cavernicolous freshwater shrimp. Spermiogenesis involves elongation of the spermatid in which the nucleus elongates, but remains close to the common cytoplasmic mass. Flagella first grow in opposite direction and at a right angle to the cytoplasmic shaft, and centrioles show associate structures. Later, the two centrioles rotate and the flagella emerge parallel, but still perpendicular to the shaft. An apical process elongates at the extremity of the spermatid shaft. The spermatozoon shows active flagellar beating and undulations of the sperm body. The spermatozoon comprises an anterior ‘corkscrew’ region, the flagellar insertion region, a cytoplasmic region and a posterior nuclear region. The corkscrew contains an electron dense structure, not membrane-bound, originating from the apical process of the spermatid. The flagella show the 9+‘1’ pattern, usual in Platyhelminthes. The cytoplasmic and nuclear regions show a cortical row of about 50 twisted longitudinal microtubules surrounding a row of electron dense, and not membrane-bound, 25-nm granules. These granules are original structures and seem to be known only in a few Platyhelminthes species in which a non-flagellar movement of the spermatozoon occurs. Thus, it is hypothesised that the 25-nm granules play a role in cellular motility. Sperm ultrastructure in Troglocaridicolashows major differences to that in the temnocephalids. It is therefore concluded that the phylogenetic position of the scutariellids within the Temnocephalidea should be reinvestigated.     

Rotifera from Burundi: the Lepadellidae (Rotifera: Monogononta)

We studied the distribution of Lepadellidae (Rotifera) in freshwater habitats in the floodplain of the River Rusizi in northwest Burundi. Twenty-three species belonging to ColurellaBory de St. Vincent, 1824 (3 species), Lepadella Bory de St. Vincent, 1826 (18 species) and Squatinella Bory de St. Vincent, 1826 (2 species) are recorded, 22 of them are new to Burundi. One of the taxa encountered probably represents an unnamed species. Lepadella arabicaSegers & Dumont, 1993 is recognised as junior subjective synonym of Lepadella eurysterna Myers, 1942 (syn. nov.). Most of the taxa recorded are cosmopolitan or tropicopolitan, two are restricted to the tropical regions of the Old World and Australia, and one, Squatinella lunata Segers, 1993 is an Ethiopian endemic.     

Spermiogenesis in Psilochorus simoni (Berland, 1911) (Pholcidae, Araneae): evidence for considerable within-family variation in sperm structure and development

A large number of characters and considerable variation among taxa make animal sperm cells promising objects for phylogenetic studies. However, our knowledge about sperm structure and development in spiders is still rudimentary. In pholcids, previous studies of two species representing different subfamily level taxa have revealed conspicuous differences. Here, we report on a representative of a third subfamily level taxon, confirming substantial variation in sperm structure and development within the family. The male genital system in Psilochorus simoni (Berland, 1911) consists of paired testes and deferent ducts which lead into a common ejaculatory duct. The somatic cells of the testes show a high secretory activity, and produce at least two different kinds of secretion. The spermatozoa show features already known from other Pholcidae as well as unique characters. The acrosomal vacuole is tube-like with a narrow subacrosomal space. The axoneme migrates deep into the nucleus and is finally located near the acrosomal vacuole. Thus, the postcentriolar elongation of the nucleus is very long. A centriolar adjunct is not present and after the coiling process the implantation fossa is completely filled with glycogen which is also found in larger amounts within the cytoplasm of the sperm cell. After the coiling process, a vesicular area is present that becomes most prominent in the periphery of the sperm cell and surrounds the axoneme and parts of the nucleus. The secretion sheath surrounding the mature spermatozoon is already formed in the lumen of the testis, possibly by a secretion present in the testis but absent in the deferent duct. Sperm are transferred as cleistospermia. Results are compared with previous studies on pholcid spermiogenesis and sperm structure.     

Rhinoglena frontalis (Rotifera,Monogononta): a scanning electron microscopic study

Females and males of Rhinoglena frontalis (Monogononta, Epiphanidae) are observed by SEM and their external morphologies are compared. The two sexes differ in size and shape of the body. The female body is fusiform with a short, conical foot, while the male body is more slender and has a rather long foot. The rotatory apparatus (or corona) of both sexes is similar with only minor differences and consists of rows and tufts of cilia arranged around the mouth opening. The corona is made of two paired lobes lateral to the mouth and of a third prominent dorsal lobe, usually called proboscis. The three lobes are lined externally by dense rows of cilia, which constitute the cingulum, used for swimming. The central surface of the proboscis is covered with numerous longitudinal rows of cilia bent towards the mouth. The lateral lobes show, on their central surfaces, two concentric arcs of cirri (made of tightly packed cilia) bent towards the mouth. The similar organization of the rotatory apparatus of both sexes is related to the fact that the male, in this species, is able to feed and has a developed mastax and digestive system. The trophi of both sexes are illustrated and compared.     

The Philodinavidae (Rotifera Bdelloidea): a special family

Here we focus on the fine morphology and present observations on the biology of representatives of family Philodinavidae. Philodinavus paradoxus and Henoceros falcatus were collected and cultured under laboratory conditions. Rotifers of both species are tiny, about 200 μm long, have protrudable trophi and creep with leech-like movements. A very specific feature of these rotifers is their corona; a V-shaped lower lip contours the mouth opening, bilaterally bordered by two arched cuticular structures (‘cheeks’). The presence of the cheeks is a feature shared by the third genus, Abrochtha. On the basis of the morphology and biology of the three genera, we advance the hypothesis that Philodinavus is a primitive bdelloid, and that it can have originated Henoceros and Abrochtha, from which the other bdelloids could have stemmed. This revised version was published online in September 2006 with corrections to the Cover Date.     

Spermiogenesis in Anaspides tasmaniae (Thomson) (Crustacea,Malacostraca, Syncarida)

Spermiogenesis of the syncarid Anaspides tasmaniae (subclass Eumalacostraca) was investigated by transmission electron microscopy. The spermatozoan of Anaspides is an ovoid cell with an acrosome covering the anterior pole and a lobulated nucleus and mitochondria occupying the rest of the cell. A long subacrosomal filament bypasses the nucleus and forms a spiral that supports a thin extension of the posterior cytoplasm, giving the spermatozoan a bell-shaped appearance. No flagellum is present at any stage. The immobile spermatozoans are embedded in a hard capsule, secreted by the cells of the wall of the vas deferens.     

Oogenesis in Macrotrachela quadricornifera (Rotifera,Bdelloidea)

Bdelloids reproduce via obligate apomictic parthenogenesis. Oogenesis occurs through two subsequent equational divisions, with the extrusion of two polar bodies. Although the morphology of the bdelloid reproductive apparatus has been previously described, the eutely of the germarium has never been investigated. We studied oogenesis in Macrotrachela quadricornifera by assessing: (1) the constancy of oocyte number, (2) chromosome number and size, and (3) the DNA content of oocytes and blastomeres. Oocyte number at birth is constant and determines maximal fertility. We found a chromosome number of 5, in which two homologous pairs can be recognized. The genome size of the species is 0.75 picograms.     

Ultrastructure of Spermiogenesis in Hyla japonica (Anura,Amphibia)

Spermiogenesis in Hyla japonica was examined using transmission electron microscopy. Features which have not been reported previously during spermiogenesis of anurans include: (1) the neck of pericentriolar material is well developed, (2) the perforatorium contains many microtubules, (3) the tail is composed of axoneme and axial rod, but has no undulating membrane. Such a structure has not been described in amphibians, although it occurs in fish and mammals, and (4) the modified microtubules have one to two long projections. So far they have not been observed in any species except Gerris and Aphyosemion. With the exception of the above characteristics, the spermatozoa of Hyla japonica are remarkably similar to those of Bufo sp.     

Spermiogenesis in Three Species of Whitefly (Homoptera, Aleyrodidae)

Aflagellate and immotile spermatozoa of three species of whitefly, Bemisia tabaci, Dialeroudes citri and Trialeroudes vaporariorum (Aleyrodidae), are described. In these three species, axoneme and mitochondria are present in the early spermatid, but degenerate in the later stages. The acrosome has arborescent appendages that almost completely surround the spermatozoan. In D. citri the acrosomal projections are more elongated and branched than in T. vaporariorum and B. tabaci . Nuclear and cell elongation appear to occur in the absence of microtubules.     

Molecular evidence for Acanthocephala as a subtaxon of Rotifera

Rotifers are free-living animals usually smaller than 1 mm that possess a characteristic wheel organ. Acanthocephalans (thorny-headed worms) are larger endoparasitic animals that use vertebrates and arthropods to complete their life cycle. The taxa Acanthocephala and Rotifera are considered separate phyla, often within the taxon Aschelminthes. We have reexamined the relationship between Rotifera and Acanthocephala using 18S rRNA gene sequences. Our results conclusively show that Acanthocephala is the sister group of the rotifer class Bdelloidea. Rotifera was nonmonophyletic in all molecular analyses, which supports the hypothesis that the Acanthocephala represent a taxon within the phylum Rotifera and not a separate phylum. These results agree with a previous cladistic study of morphological characters. Correspondence to: J.R. Garey     

Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera)

Continental lake-dwelling zooplanktonic organisms have long been considered cosmopolitan species with little geographic variation in spite of the isolation of their habitats. Evidence of morphological cohesiveness and high dispersal capabilities support this interpretation. However, this view has been challenged recently as many such species have been shown either to comprise cryptic species complexes or to exhibit marked population genetic differentiation and strong phylogeographic structuring at a regional scale. Here we investigate the molecular phylogeny of the cosmopolitan passively dispersing rotifer Brachionus plicatilis (Rotifera: Monogononta) species complex using nucleotide sequence variation from both nuclear (ribosomal internal transcribed spacer 1, ITS1) and mitochondrial (cytochrome c oxidase subunit I, COI) genes. Analysis of rotifer resting eggs from 27 salt lakes in the Iberian Peninsula plus lakes from four continents revealed nine genetically divergent lineages. The high level of sequence divergence, absence of hybridization, and extensive sympatry observed support the specific status of these lineages. Sequence divergence estimates indicate that the B. plicatilis complex began diversifying many millions of years ago, yet has showed relatively high levels of morphological stasis. We discuss these results in relation to the ecology and genetics of aquatic invertebrates possessing dispersive resting propagules and address the apparent contradiction between zooplanktonic population structure and their morphological stasis.     

Spermiogenesis in the Oligochaetoid Polychaete Questa (Annelida, Questidae)

The spermatids are connected to a central cytophore by cytoplasmic bridges and are polarized in the sequence: "empty cytoplasm"; uncondensed nucleus; mitochondria which surround the distal region of the nucleus and the centrioles; axoneme; posterolateral to the base of the axoneme, the Golgi apparatus and (when secreted) the acrosomal rudiment. The dome-shaped acrosome vesicle elongates progressively as it migrates to the tip of the elongating and condensing nucleus; subacrosomal material gives rise to an almost equally long, tubular, thick-walled perforatorium. After the acrosome has greatly elongated, the mitochondria are reduced to two, which lose their rounded form and invest the growing axoneme to give a very elongate midpiece. Transfer of materials from nucleus to mitochondria is discussed. Microtubules surrounding the acrosome and nucleus disappear by maturity, but those internal to the mitochrondria apparently persist as the accessory microtubules, unique in the Annelida, which surround the 9 + 2 axoneme. Microvilli of the egg envelope, which have tetrads of terminal branches (epivitelline projections) resembling epicuticular projections, are less than 1 μm long, whereas the mature acrosome exceeds 5 μm. This suggests that the correlation seen in oligochaetes is absent.     

Spermiogenesis in three species of cicadas (Hemiptera: Cicadidae)

Spermiogenesis in three species of cicadas representing one cicadettine (Monomatapa matoposa Boulard) and two cicadines (Diceroprocta biconica [Walker] and Kongota punctigera [Walker]) was investigated by light and electron microscopy. Although spermiogenesis was occurring in the testis of adult males of all species, earlier spermiogenic stages were observed in D. biconica only. While spermiogenesis was similar to that described for other insects, some differences were noted. For example granular material did not assemble around the centriole to form a centriolar adjunct but did accumulate in the cytoplasm of early spermatids adjacent to a region of the nuclear membrane where nuclear pores were aggregated. In late spermatids this material accumulated anterior to the mitochondrial derivatives in a developing postero‐lateral nuclear groove. While this material has been named the ‘centriolar adjunct’ by previous authors, its formation away from the centriole raises questions about its true identity. Second, during acrosome maturation an ante‐acrosomal region of cytoplasm develops. Although present in later spermatids, this region is lost in spermatozoa. Interspecific variations in chromatin condensation patterns and the number of microtubule layers encircling the spermatid nucleus during spermiogenesis were noted.