Ultrastructure of the spermatid and spermatozoon of Macracanthorhynchus hirudinaceus.

The ultrastructure of the spermatid and spermatozoon of Macracanthorhynchus hirudinaceus (Archiacanthocephala) was studied by means of transmission electron microscopy. The flagellum and nucleus in the spermatid gradually expanded simultaneously. The karyoplasma of the spermatid transformed into dense inclusions and a multibarrel structure, which were also found in the spermatozoan body. The multibarrel structure was located close to the flagellum and consisted of many irregular microtubes. The flagellum of the developing spermatozoon was observed in a concavity of the spermatid nucleus. The microtubule arrangement of the flagellum was "9 + 2". No mitochondria or acrosome were observed in spermatozoa.     

Fine structure of spermatozoa and spermatogenesis ofSchizomus palaciosi,Reddell and Cokendolpher, 1986 (Arachnida: Uropygi,Schizomida)

Summary Spermatogenesis ofSchizomus palaciosi occurs in cysts in paired tubular testes located ventrally in the opisthosoma. Only few germ cells comprise one cyst. In early spermiogenesis an acrosomal complex composed of a spherical vacuole and a short acrosomal filament is established opposite of which a 9×2+3 flagellum emerges from a flagellar tunnel. The latter, however, is only a short-lasting structure. A manchette of microtubules surrounds nucleus and part of the acrosomal vacuole. The alterations in the arrangement of the microtubules during spermiogenesis are described. The spermatid finally is an elongate cell with a slender acrosomal vacuole on top of the helical nucleus. A deep implantation fossa filled with dense material is encountered. The acrosomal vacuole is accompanied by an intricate paracrosomal lattice structure not known at present of otherArachnida. This structure disappears during final spermiogenesis. The acrosomal filament (perforatorium) reveals filamentous subunits arranged in a regular pattern. Large ovoid mitochondria do not establish a distinct middle piece. Finally the elongate spermatid is coiled to form the mature spherical spermatozoon.The results are discussed under functional and taxonomical aspects.     

Ultrastructure of spermiogenesis and the mature spermatozoon of Tetrabothrius erostris loennberg, 1896 (Cestoda, Tetrabothriidae)

The spermiogenesis of Tetrabothrius erostris is characterized by the following events: formation of a differentiation zone containing 2 basal bodies and a pair of rootlets; one of the basal bodies gives rise to a free flagellum, the other induces formation of a flagellar bud; rotation at 90° of the flagellum prior to its fusion with the middle cytoplasmic process of the differentiation zone and partial rotation of the flagellar bud; penetration of the nucleus between the rootlets and appearance of a spur-like protrusion in the differentiation zone; elongation and twisting of the differentiation zone, resulting in twisting of the peripheral microtubules and migration of the nucleus; formation of a crested body; proximal densification of the spermatozoon prior to its detachment from the spermatid rosette. The mature spermatozoon has a single axoneme of 9+“1” type and twisted peripheral microtubules. It consists of 3 portions: a proximal part with a crested body, a middle region rich in β-glycogen, and a distal part containing the nucleus. The pattern of spermiogenesis resembles most closely that in phyllobothriid tetraphyllideans, and probably reflects a relationship of the family Tetrabothriidae with this group.     

Ultrastructure of spermiogenesis and the spermatozoon of Mesocestoides litteratus (Cestoda, Mesocestoididae).

This paper constitutes the first ultrastructural study of spermiogenesis and the spermatozoon of a cestode belonging to the family Mesocestoididae, Mesocestoides litteratus. Spermiogenesis in M. litteratus is characterised by a flagellar rotation and a proximodistal fusion. The zone of differentiation presents striated roots associated with the centrioles and also an intercentriolar body. The most interesting ultrastructural feature found in the mature spermatozoon of M. litteratus is the presence of parallel cortical microtubules. The spermatozoon also exhibits a single crest-like body and granules of glycogen. The pattern of spermiogenesis and the parallel position of cortical microtubules reveal the lack of concordance between M. litteratus and cyclophyllidean species studied to date in spermiogenesis and in the ultrastructural organisation of spermatozoon. This study provides new spermatological data and calls into question the validity of the current systematic position of mesocestoidids.     

Spermiogenesis and spermatozoon ultrastructure of the davaineid cestode Raillietina micracantha (Fuhrmann, 1909)

Miquel, J., Torres, J., Foronda, P. and Feliu, C. 2010. Spermiogenesis and spermatozoon ultrastructure of the davaineid cestode Raillietina micracantha. — Acta Zoologica (Stockholm) 91 : 212–221 The spermiogenesis and the ultrastructural organization of the spermatozoon of the davaineid cestode Raillietina micracantha are described by means of transmission electron microscopy. Spermiogenesis begins with the formation of a zone of differentiation containing two centrioles. One of the centrioles develops a free flagellum that later fuses with a cytoplasmic extension. The nucleus migrates along the spermatid body after the proximodistal fusion of the flagellum and the cytoplasmic extension. During advanced stages of spermiogenesis a periaxonemal sheath and intracytoplasmic walls appear in the spermatids. Spermiogenesis finishes with the appearance of two helicoidal crested bodies at the base of spermatids and, finally, the narrowing of the ring of arched membranes detaches the fully formed spermatozoon. The mature spermatozoon of R. micracantha is a long and filiform cell, tapered at both ends, which lacks mitochondria. It exhibits two crested bodies of different lengths, one axoneme of the 9 + ‘1’ pattern of trepaxonematan Platyhelminthes, twisted cortical microtubules, a periaxonemal sheath, intracytoplasmic walls, granules of glycogen and a spiralled nucleus. The anterior extremity of the spermatozoon is characterized by the presence of an electron‐dense apical cone and two spiralled crested bodies while the posterior extremity of the male gamete exhibits only the axoneme and an electron‐dense posterior tip.     

Phylogenetic relationships between the families Capsalidae and Dionchidae (Platyhelminthes, Monogenea, Monopisthocotylea) indicated by the comparative ultrastructural study of spermiogenesis

Comparative ultrastructural observations were carried out on the spermiogenesis of the capsalid Caballerocotyla manteri Price and the dionchid Dionchus remorae MacCallum. At the beginning of spermiogenesis the zones of differentiation (ZD) jut out in all directions. A large mitochondrion shaped like a perforated bead, and through which the elongated nucleus passes, is found facing each ZD. Later the ZD become parallel and are embedded within the common cytoplasmic mass. Cortical longitudinal microtubules are present in the ZD at the outset of spermiogenesis, but they later disappear. The spermatozoon is long and filiform. It shows two parallel axonemes of the 9 +"1" flatworm pattern, the nucleus and mitochondrion, and no cortical microtubule. The ultrastructure of spermiogenesis and spermatozoon is remarkably similar in the two species studied, as in other capsalids previously described. Two characteristics, the perforated bead shape of the spermatid mitochondrion and the progressive disappearance of the microtubules of the ZD, may be considered as synapomorphies which indicate close phylogenetic relationships between the families Dionchidae and Capsalidae. This interpretation coincides with Llewellyn's (1971) scheme of the evolution of the monogeneans.     

Spermiogenesis and spermatozoon ultrastructure of the cestode Mosgovoyia ctenoides (Cyclophyllidea: Anoplocephalidae), an intestinal parasite of Oryctolagus cuniculus (Lagomorpha: Leporidae)

Ultrastructural characters in spermiogenesis and spermatozoa are considered important tools to elucidate the phylogenetic relationships within the Platyhelminthes. In the Anoplocephalidae, ultrastructural data refer to the spermatozoon of 14 species, whereas data on spermiogenesis refer to only 7 species. The present study focused on the spermiogenesis and spermatozoon of the anoplocephalid cestode Mosgovoyia ctenoides, as revealed by transmission electron microscopy. Type IV spermiogenesis was detected, beginning with the formation of a differentiation zone containing 2 centrioles, with a centriolar adjunct and vestigial striated rootlets. Different forms of the latter character have been described in other anoplocephalids. This study supports spermiogenesis of type IV as the most frequent in the Anoplocephalidae and confirms the presence of a centriolar adjunct in yet another type IV spermiogenesis species. The spermatozoon of M. ctenoides possesses 1 axoneme of the 9+ '1' trepaxonematan type, 2 crestlike bodies, dense plates, and granules of electron-dense cytoplasmic material, nucleus, and twisted cortical microtubules. It was again confirmed that the presence of granular material and the absence of both a periaxonemal sheath and intracytoplasmic walls are constant characters in the spermatozoa of all the Anoplocephalinae.     

Is the sperm type of the Nemertodermatida close to that of the ancestral Platyhelminthes?

Results from a transmission electron microscope study of the spermiogenesis and spermatozoon of Meara stichopi (Nemertodermatida, Platyhelminthes) indicate that the sperm type of the Nemertodermatida has evolved from the primitive metazoan sperm type rather than from an aberrant biflagellar sperm type as found in many other flatworms. The spirally coiled mitochondrial derivative in the mature spermatozoon develops from two large oval mitochondria in the early spermatid stages. A single flagellum grows out from a peripheral basal body adjacent to a perpendicularly placed accessory centriole. The basal body moves to a distal depression of the nucleus, and becomes equipped with an anchoring fibre apparatus. Most of the flagellum becomes axially incorporated into the developing spermatid. No trace of a second flagellum was found in any stage of the spermiogenesis. Rounded vesicles appear around the proximal, tapering end of the elongating nucleus. Most probably these vesicles form a thin acrosomal structure in the mature spermatozoon. No dense bodies, characteristic of many other ‘turbellarian’ flatworm sperm types, were found. This revised version was published online in July 2006 with corrections to the Cover Date.     

Ultrastructure of spermiogenesis and spermatozoa in Mesocastrada fuhrmanni Voltz, 1898 (Platyhelminthes, Rhabdocoela, Typhloplanoida)

Electron microscopy of the testes of the free-living flatworm Mesocastrada fuhrmanni collected from temporary freshwater ponds shows stages of spermiogenesis that are like other species of the Typhloplanidae. Spermiogenesis in Mesocastrada fuhrmanni is characterized by the presence, in the spermatid, of a differentiation zone underlain by peripheral microtubules and centered on two centrioles with an intercentriolar body. Two flagella of the 9+“1” pattern of the Trepaxonemata grow out in opposite directions from the centrioles. The flagella undergo a latero-ventral rotation, and a subsequent disto-proximal rotation of centrioles occurs in the spermatid. The former rotation involves the compression and the detachment of a row of cortical microtubules, and allows us to recognize a ventral from a dorsal side. Two features are of special interest at the end of differentiation: peripheral cortical microtubules lie parallel to the sperm axis near the anterior tip, but microtubules become twisted (about 40° with reference to the gamete axis) near the posterior extremity; in the same way, the posterior tip of the nucleus is spiralled. As far as we know, these features are observed for the first time in the Typhloplanidae. The pattern of spermiogenesis and the ultrastructural organization of the spermatozoon are compared with the available data on Typhloplanoida and in particular, species of the Typhloplanidae family.     

Ultrastructural study of spermiogenesis and the spermatozoon of Microcotyle pancerii (Monogenea: Polyopisthocotylea: Microcotylidae), parasite of meagre Argyrosomus regius (Pisces: Teleostei)

The present work deals with the ultrastructure of spermiogenesis and the spermatozoon of Microcotyle pancerii, a gill parasite of meagre Argyrosomus regius collected in Corsican fish farms. Spermiogenesis was rather similar to that observed in other polyopisthocotylean Monogenea. The intercentriolar body was different from that described in digeneans. The nuclear condensation occurred in 2 successive stages. First, during the nuclear migration in the median cytoplasmic process, the nucleus developed a honeycomb-like appearance. Then, after the flagellar fusion, a discontinuous twisting of the chromatin appeared along the nucleus, with this process ending in total nuclear condensation. The structure of the spermatozoon is characterized by 2 axonemes (9 + "1" pattern), a single and continuous field of cortical microtubules, a mitochondrion, and a nucleus. Our findings were compared with various ultrastructural features in order to highlight variability within the group.     

Spermiogenesis and spermatozoon of the tapeworm Ligula intestinalis (Diphyllobothriidea): phylogenetic implications

Using transmission electron microscopy, spermiogenesis and the spermatozoon ultrastructural organization are described in Ligula intestinalis (Linnaeus, 1758) (Diphyllobothriidea), a parasite of the great crested grebe Podiceps cristatus (Linnaeus, 1758). Spermiogenesis starts with the differentiation zone of 2 striated rootlets, 2 centrioles giving rise to 2 flagella, and an intercentriolar body. The latter is composed of 5 electron-dense layers separating 4 electron-lucent layers. In the early stages of spermiogenesis, an electron-dense material is present in the apical region of the differentiation zone. Later, the flagella undergo a rotation and fuse with the cytoplasmic extension in a proximo-distal process. The spermatozoon contains 2 axonemes with a 9 + "1" trepaxonematan pattern, the nucleus, the cortical microtubules, and an electron-dense zone. The spermatozoon anterior extremity in L. intestinalis is characterized by the absence of crested bodies and a ring of electron-dense cortical microtubules. Some characters of spermiogenesis and spermatozoon in L. intestinalis confirm the recent splitting of "Pseudophyllidea" into 2 new orders, i.e., Bothriocephalidea and Diphyllobothriidea. The process of spermiogenesis is similar in both orders for the "type I" of spermiogenesis and the presence of electron-dense material. However, the intercentriolar body is clearly more developed in the Diphyllobothriidea than in the Bothriocephalidea. Moreover, these 2 orders seem to differ in the presence or absence of a ring of electron-dense cortical microtubules in the anterior extremity of the spermatozoon.     

埃及尼罗河鲶的精子发生和精子的超微结构

用扫描和透射电子显微镜研究了尼罗河鲶——盾头歧须鮠(Synodontis schall)的精子发生和精子的超微结构。精巢中含有无数肾形的生精小叶,我们将其称为"精原无限型"。尽管其精子发生的大体过程与同类鱼无异。但是,在细节上仍具其独特之处。这些特点未见在其他硬骨鱼中报道过。其特点主要是:生精过程中不发生细胞核的旋转,中心粒复合体和轴丝起始段直接发生在核的基底面垂直线上,有无数的粗的固定纤维将近端中心粒和远端中心粒的近侧部连接到细胞核上。另外,精子发生过程中还包括染色质浓缩,细胞质和线粒体向细胞核的尾端迁移,在核的后端中轴位置上形成中等大小的核后凹,近端中心粒和远端中心粒的一部分嵌在核后凹之内,短的胞质内陷管将线粒体与鞭毛分隔开。精子头部接近圆形,无顶体或顶体泡,鞭毛的中段及胞质内陷管均较短,整个鞭毛却很长,鞭毛侧面无翼膜,轴丝呈典型的9 2结构。上述结果显示,盾头歧须鮠的精子发生具有类型Ⅰ和类型Ⅱ的共同派生特征,这种特征在常见的其他硬骨鱼中也是常有的。但是,正如文献所报道过的另两种尼罗河鲶——金鯵(Chrysichthys auratus)和电鲶(Malapterurus electricus)中的情况一样,盾头歧须的精子发生与类型Ⅲ的精子发生过程更为相似。     

Spermiogenesis and spermatozoon ultrastructure of the dilepidid cestode Molluscotaenia crassiscolex (von Linstow, 1890), an intestinal parasite of the common shrew Sorex araneus

Marigo, A.M., Bâ, C.T. and Miquel, J. 2011. Spermiogenesis and spermatozoon ultrastructure of the dilepidid cestode Molluscotaenia crassiscolex (von Linstow, 1890), an intestinal parasite of the common shrew Sorex araneus. —Acta Zoologica (Stockholm) 92 : 116–125. Spermiogenesis in Molluscotaenia crassiscolex begins with the formation of a differentiation zone containing two centrioles. One of the centrioles develops a flagellum directly into the cytoplasmic extension. The nucleus elongates and later migrates along the spermatid body. During advanced stages of spermiogenesis, a periaxonemal sheath appears in the spermatid. Spermiogenesis finishes with the appearance of a single helicoidal crested body at the base of the spermatid and, finally, the narrowing of the ring of arched membranes causes the detachment of the fully formed spermatozoon. The mature spermatozoon of M. crassiscolex exhibits a partially detached crested body in the anterior region of the spermatozoon, one axoneme, twisted cortical microtubules, a periaxonemal sheath, and a spiralled nucleus. The anterior spermatozoon extremity is characterized by the presence of an electron‐dense apical cone and a single spiralled crested body, which is attached to the sperm cell in the anterior and posterior areas of region I, whereas in the middle area it is partially detached from the cell. This crested body is described for the first time in cestodes. The posterior extremity of the male gamete exhibits only the disorganizing axoneme. Results are discussed and compared particularly with the available ultrastructural data on dilepidids sensu lato.     

The ultrastructure of amberjack (Seriola dumerilii) sperm

Scanning and transmission electron microscopy were used to investigate the fine structure of sperm of the Mediterranean amberjack Seriola dumerilii. Each spermatozoon has an ovoid head which lacks an acrosome, a short, irregularly-shaped midpiece and a long flagellar tail. The midpiece houses eight spherical mitochondria, which are separated from the axoneme by the cytoplasmic canal. The centrioles are arranged approximately at right angles to each other. The proximal centriole lies inside, and the distal centriole outside, the nuclear fossa. The flagellum is inserted eccentrically into the head and is tangential to the nucleus, so that the spermatozoon is asymmetrical. It contains the conventional 9 + 2 axoneme, shows intratubular differentiations in the A microtubules of doublets 1, 2, 5 and 6, and possesses one pair of lateral fins. On the basis of its ultrastructural organization, the amberjack sperm resembles type II sperm as defined previously, except for the presence of the proximal centriole inside the nuclear fossa. This could result from a partial rotation of the nucleus during spermiogenesis.     

Spermiogenesis in the Nile tilapia Oreochromis niloticus with notes on a unique pattern of nuclear chromatin condensation

Spermiogenesis in the Nile tilapia, Oreochromis niloticus, was observed ultrastructurally. The process of spermatid differentiation can be divided into six distinct stages based mainly on changes in the nucleus of spermatids. During the latter half of the process, nuclear chromatin condenses progressively to form many dense globules, which ultimately adhere tightly to pack the head of mature spermatozoa. During chromatin condensation the nucleus diminishes in size, and part of the nuclear envelope and nucleoplasm forms a vesicular structure that is finally discarded from the cells together with an associated thin layer of cytoplasm. The spermatozoon comprises a roundish head, a relatively small midpiece, and a relatively short flagellum consisting of the usual 9+2 axoneme. No acrosomal structure is developed during spermiogenesis.     

Semicystic spermatogenesis and biflagellate spermatozoon ultrastructure in the Nile electric catfish Malapterurus electricus (Teleostei: Siluriformes: Malapteruridae)

Spermatogenesis and spermatozoon ultrastructure in the Nile electric catfish Malapterurus electricus are described using scanning and transmission electron microscopy. Although the testis organization conforms to the ‘unrestricted’ spermatogonial type, the species has a rare type of spermatogenesis not previously described among catfishes, ‘semicystic’, in which the cyst ruptures before the spermatozoon stage. Spermiogenesis also involves some peculiar features such as condensation of the chromatin in the posterior part of the nucleus to form a compact electron‐dense mass with some irregular electron‐lucent lacunae, while the uppermost part of the nucleus is a loose electron‐lucent area, absence of the nuclear rotation and, as a consequence, the centriolar complex and the initial segment of each flagellum arise directly in a position perpendicular to the basal pole of the nucleus, and occurrence of numerous vesicles in the midpiece. In addition, spermiogenesis includes migration of the diplosome and mitochondria to the basal pole of the nucleus, formation of two moderate nuclear fossae, each of which contains the centriolar complex, development of two independent flagella and elimination of the excess cytoplasm. The mature spermatozoon has a more or less round head with no acrosome or acrosomal vesicle, a long midpiece with numerous mitochondria and vesicles and two long tails or flagella having the classical axoneme structure of 9 + 2 microtubular doublet pattern and with no lateral fins and membranous compartment. These findings suggest that the ultrastructural features of spermiogenesis and spermatozoa of M. electricus are synapomorphies of types I and II spermiogenesis and spermiogenesis is closely similar to the type described in the Nile catfish Chrysichthys auratus.     

Spermiogenesis and spermatozoon ultrastructure of the cranial digenean Troglotrema acutum (Leuckart, 1842)

Ultrastructure of spermiogenesis and the main characters of the mature spermatozoon of Troglotrema acutum are described by means of transmission electron microscopy. Specimens were obtained from the nasolacrimal sinuses of an American mink (Mustela vison). Spermiogenesis in T. acutum follows the general pattern of digeneans. The zone of differentiation is a conical-shaped area bordered by cortical microtubules and delimited at its base by a ring of arched membranes. This area contains 2 centrioles associated with striated rootlets and an intercentriolar body between them. The centrioles develop 2 free flagella that grow ortogonally to the median cytoplasmic process. The posterior flagellar rotation and proximodistal fusion of the free flagella with the median cytoplasmic process originate the spermatozoon. The mature spermatozoon of T. acutum is characterized by the presence of 2 axonemes of different lengths presenting the 9+'1' trepaxonematan pattern, 2 bundles of parallel cortical microtubules, 2 mitochondria, a nucleus, and granules of glycogen. These ultrastructural characters are compared with other digenean species previously studied and the importance of different spermatological features is discussed.     

Ultrastructural analysis of the aberrant axoneme morphogenesis in thrips (Thysanoptera, Insecta)

Thrips spermiogenesis is characterized by unusual features in the differentiating spermatid cells. Three centrioles from which three individual short flagella are initially assembled, make the early spermatid a tri-flagellated cell. Successively, during spermatid maturation, the three basal bodies maintain a position close to the most anterior end of the elongating nucleus, so that the three axonemes are progressively incorporated in the spermatid cytoplasm, where they run in parallel to the main nuclear axis. Finally, the three axonemes amalgamate to form a microtubular bundle. The process starts with the formation of rifts at three specific points in each axonemal circumference, corresponding to sites 1,3,7 and leads to the formation of 9 microtubular rows of different length, i.e. 3 "dyads", 3 "triads" and 3 "tetrads". In the spermatozoon, the nucleus, the mitochondrion and the bundle of microtubules are arranged in a helicoidal pattern. The elongation of the spermatozoon is allowed by the deep anchorage of the spermatid to the cyst cell through a dense mass of material which, at the end of spermiogenesis, becomes a long anterior cylindrical structure. This bizarre "axoneme" does not show any trace of progressive movement but it is able to beat. According to the presence of dynein arms, sliding can take place only within each row and not between the rows. The possible molecular basis underlying the peculiar instability of thrips axonemes is discussed in light of the present knowledge on the organization of the axoneme in mutant organisms carrying alterations of the tubulin molecule.     

Spermiogenesis and structure of spermatozoa in the oribatid mite,Hafenrefferia gilvipes (C.L. Koch) (Acari,Oribatida)

The process of spermiogenesis and the structure of spermatozoa in the mite, Hafenrefferia gilvipes (Koch) were studied ultrastructurally. Spermiogenesis was divided into six stages. The spermatids at stage 1 have the usual structure. At stage 2 the structure of the mitochondria and their distribution in the spermatid start to change, leading to the formation of specific mitochondrial derivatives which are subsequently incorporated into the nucleus of the spermatozoon. Parallel to the transformation of mitochondria occurs a reorganization of the nuclear material. The fully formed spermatozoon has a tadpole-like shape, with the cell nucleus located in the distended part of the cell, and containing mitochondrial derivatives in its karyoplasm. Acrosome, flagellum and centrioles are absent. The participation of peripherally distributed microtubules, present in spermatids at stages 4 to 6, in the shaping of the spermatozoon has been suggested.     

Fine structure of spermatozoa in the common pandora (Pagellus erythrinus Linnaeus, 1758) (Perciformes, Sparidae)

Scanning and transmission electron microscopy were used to investigate the fine structure of the sperm of the Sparid fish Pagellus erythrinus L. The spermatozoon of pandora has a spherical head lacking an acrosome, a cone-shaped midpiece and a long tail. The midpiece houses a single mitochondrion. The centriolar complex lies inside the nuclear fossa and is composed of a proximal and a distal centriole which are arranged at right angles to each other. The flagellum is inserted medio-laterally into the head, contains the conventional 9+2 axoneme and possesses one pair of lateral fins. On the basis of its ultrastructural organization, the pandora sperm can be regarded as an evolved form of the primitive spermatozoon found in Teleosts. According to the morphological classification proposed by Mattei (1970), the sperm of pandora belongs to a "type I" designation, like that of the other Sparid fish.