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.     

Ultrastructural study of spermiogenesis and the spermatozoon in Catenotaenia pusilla, an intestinal parasite of Mus musculus

The ultrastructure of spermiogenesis and the mature spermatozoon in Catenotaenia pusilla (Cestoda: Catenotaeniidae) is described. Spermiogenesis is characterized by the presence of a single axoneme which grows on the outside of a cytoplasmic extension at an angle of 45 degrees. Flagellar rotation and proximodistal fusion are produced in this process. The centrioles lack striated roots and an intercentriolar body. In the mature spermatozoon four different regions are described. The anterior extremity is capped by an apical cone and presents two helical crest-like bodies of unequal length. The axoneme, of the 9 + '1' pattern of the Trepaxonemata, presents a periaxonemal sheath. The cortical microtubules form a spiral pattern at an angle of about 40 degrees to the hypothetical spermatozoon axis. The nucleus is kidney- to horseshoe-shaped in cross section. Granules and proteinaceus walls are not observed in the spermatozoon of C. pusilla.     

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.     

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.     

Spermiogenesis and spermatozoa in Acanthodasys aculeatus (Gastrotricha, Macrodasyida): an ultrastructural study

The spermatogenesis, the spermiogenetic process and the structure of the mature spermatozoon of Acanthodasys aculeatus (Gastrotricha, Macrodasyida) are described from an ultrastructural point of view. Several spermatogonia in mitotic divisions were seen, proving that euthely of gastrotrichs does not concern gonads. Spermiogenesis is characterized by the early formation of both the acrosome and the axoneme, by the subsequent appearances of a perinuclear helix and of a complex axial tubular structure in the acrosome and by the late development of the peraxonemal striated cylinder. The mature spermatozoon is filiform, and composed of a spiralized acrosome, a helical nuclear–mitochondrial complex and a long flagellum. The acrosome contains an axial tubular structure and the spring-shaped nucleus delimits a single, long mitochondrion. A perinuclear helix formed by the pro-acrosome surrounds the nuclear–mitochondrial complex extending for its whole length. A monolayered, obliquely striated cylinder encloses the 9 × 2 + 2 axoneme; its terminal part is empty because of the shortness of the axoneme.     

Ultrastructural study of spermiogenesis and the spermatozoon of the proteocephalidean cestode Barsonella lafoni de Chambrier et al., 2009, a parasite of the catfish Clarias gariepinus (Burchell, 1822) (Siluriformes, Clariidae)

Spermiogenesis in the proteocephalidean cestode Barsonella lafoni de Chambrier et al., 2009 shows typical characteristics of the type I spermiogenesis. These include the formation of distal cytoplasmic protrusions forming the differentiation zones, lined by cortical microtubules and containing two centrioles. An electron-dense material is present in the apical region of the differentiation zone during the early stages of spermiogenesis. Each centriole is associated to a striated rootlet, being separated by an intercentriolar body. Two free and unequal flagella originate from the centrioles and develop on the lateral sides of the differentiation zone. A median cytoplasmic process is formed between the flagella. Later these flagella rotate, become parallel to the median cytoplasmic process and finally fuse proximodistally with the latter. It is interesting to note that both flagellar growth and rotation are asynchronous. Later, the nucleus enlarges and penetrates into the spermatid body. Finally, the ring of arching membranes is strangled and the young spermatozoon is detached from the residual cytoplasm.The mature spermatozoon presents two axonemes of the 9 + ‘1’ trepaxonematan pattern, crested body, parallel nucleus and cortical microtubules, and glycogen granules. Thus, it corresponds to the type II spermatozoon, described in almost all Proteocephalidea. The anterior extremity of the gamete is characterized by the presence of an apical cone surrounded by the lateral projections of the crested body. An arc formed by some thick and parallel cortical microtubules appears at the level of the centriole. They surround the centriole and later the first axoneme. This arc of electron-dense microtubules disorganizes when the second axoneme appears, and then two parallel rows of thin cortical microtubules are observed. The posterior extremity of the male gamete exhibits some cortical microtubules. This type of posterior extremity has never been described in proteocephalidean cestodes. The ultrastructural features of the spermatozoon/spermiogenesis of the Proteocephalidea species are analyzed and compared.     

Spermiogenesis and spermatozoon ultrastructure of Nicolla wisniewskii (Digenea: Opecoelidae), an intestinal parasite of brown trout Salmo trutta (Pisces: Teleostei)

Spermiogenesis and ultrastructure of spermatozoon of Nicolla wisniewskii (Digenea, Opecoelidae), an intestinal parasite of Salmo trutta, were studied by electron microscopy. Spermiogenesis follows the general pattern found in the Digenea. It begins with the formation of a differentiation zone, including striated rootlets associated with 2 centrioles and an intercentriolar body. The flagella undergo a rotation of greater than 90 degrees. Then, their fusion with the median cytoplasmic process is proximodistal and asynchronous. A peculiarity was observed before the fusion of flagella, i.e., the attachment zones joined as 2 pairs by an electron-dense bridge. The mature spermatozoon is characterized by 2 axonemes, cortical microtubules, a nucleus, 2 mitochondria, external ornamentation, and spinelike bodies. At the posterior end of flagella, the spermatozoon is also characterized by the presence of a central element of the axoneme and without the 9 microtubule doublets. These results were compared with those of the other digeneans and, in particular, with other species of Opecoelidae. It appears that the number of cortical microtubules and their localization in the spermatozoon may be an interesting feature of their phylogeny.     

Ultrastructure of the spermatozoon of Anomotaenia quelea (Mettrick, 1961) (Cestoda,Cyclophyllidea, Dilepididae), an intestinal parasite of Quelea quelea (Aves,Ploceidae) in Senegal

The mature spermatozoon of Anomotaenia quelea exhibits an apical cone of electron-dense material and two helicoidal crest-like bodies. The apical cone near its base is surrounded by a lucent cytoplasm and a spiraled layer of cortical microtubules. The crest-like bodies are of different lengths, spiraled and make an angle of 30–40° to the hypothetical spermatozoon axis. The axoneme is of the 9 + ‘1’ trepaxonematan pattern and is surrounded by a periaxonemal sheath of electron-dense material. The cytoplasm contains in regions III and IV numerous electron-dense granules situated between the periaxonemal sheath and the cortical microtubules. The posterior extremity of the spermatozoon of A. quelea exhibits a nucleus and a disorganized axoneme and cortical microtubules. This type of posterior extremity of the mature spermatozoon has never been described previously in a Dilepididae. Similarly, two crest-like bodies have not been observed before in a dilepidid cestode.     

Ultrastructure of the spermatozoon of Anomotaenia quelea (Mettrick, 1961) (Cestoda,Cyclophyllidea, Dilepididae), an intestinal parasite of Quelea quelea (Aves,Ploceidae) in Senegal

The mature spermatozoon of Anomotaenia quelea exhibits an apical cone of electron-dense material and two helicoidal crest-like bodies. The apical cone near its base is surrounded by a lucent cytoplasm and a spiraled layer of cortical microtubules. The crest-like bodies are of different lengths, spiraled and make an angle of 30–40° to the hypothetical spermatozoon axis. The axoneme is of the 9 + ‘1’ trepaxonematan pattern and is surrounded by a periaxonemal sheath of electron-dense material. The cytoplasm contains in regions III and IV numerous electron-dense granules situated between the periaxonemal sheath and the cortical microtubules. The posterior extremity of the spermatozoon of A. quelea exhibits a nucleus and a disorganized axoneme and cortical microtubules. This type of posterior extremity of the mature spermatozoon has never been described previously in a Dilepididae. Similarly, two crest-like bodies have not been observed before in a dilepidid cestode.     

Ultrastructural study of the male gamete of Glossobothrium sp. (Cestoda: Bothriocephalidea: Triaenophoridae) a parasite of Schedophilus velaini (Perciformes: Centrolophidae) in Senegal

This paper describes the ultrastructure of the male gamete of Glossobothrium sp. (Bothriocephalidea: Triaenophoridae). The mature spermatozoon of Glossobothrium sp. is filiform and possesses two axonemes, a single helicoidal crested body, a parallel nucleus, parallel cortical microtubules and granules of glycogen. In Glossobothrium sp. we describe for first time a 200-250 nm thick crest-like body in the Bothriocephalidean. The anterior part of the spermatozoon exhibits a ring of 27 electron-dense cortical microtubules encircling the first axoneme. This structure persists until the appearance of the second axoneme. When the ring of electron-dense cortical microtubules disappears, the spermatozoon exhibits two bundles of thin cortical microtubules. The posterior part of the spermatozoon contains the posterior extremity of the second axoneme, the posterior extremity of the nucleus and few cortical microtubules. Soon nucleus disappears and the axoneme is disorganized. Thus the posterior extremity of the spermatozoon of Glossobothrium sp. exhibits only singlets produced by the disorganization of the doublets of the second axoneme and few cortical microtubules. This type of posterior extremity of the mature spermatozoon has never been described previously in the Triaenophoridae.     

Spermiogenesis and the spermatozoon ultrastructure of Robphildollfusium fractum (Digenea: Gyliauchenidae), an intestinal parasite of Sarpa salpa (Pisces: Teleostei)

Spermiogenesis in Robphildollfusium fractum begins with the formation of a differentiation zone containing: two centrioles, each bearing striated rootlets, nucleus, several mitochondria and an intercentriolar body constituted by seven electron-dense layers. The two centrioles originate two free flagella growing orthogonally to the median cytoplasmic process. Later, the free flagella rotate and undergo proximodistal fusion with the median cytoplasmic process. Nuclear and mitochondrial migrations occur before this proximodistal fusion. Finally, the young spermatozoon detaches from the residual cytoplasm after the constriction of the ring of arched membranes. The spermatozoon of R. fractum exhibits two axonemes of different length of the 9 + ‘1’ trepaxonematan pattern, nucleus, two mitochondria, two bundles of parallel cortical microtubules, external ornamentation of the plasma membrane, spine-like bodies and granules of glycogen. Additionally, a shorter axoneme, which does not reach the nuclear region, the presence of an electron-dense material in the anterior spermatozoon extremity and the morphologies of both spermatozoon extremities characterize the mature sperm of R. fractum.     

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.     

Ultrastructure of the spermatozoon of Bothriocotyle sp. (Cestoda: Bothriocephalidea), a parasite of Schedophilus velaini (Sauvage, 1879) (Perciformes: Centrolophidae) in Senegal

The mature spermatozoon of Bothriocotyle sp. is filiform and tapered at both extremities. It possesses 2 axonemes of unequal length, showing the 9 + "1" pattern of Trepaxonemata. The anterior extremity exhibits a crest-like body. Thereafter, the crest-like body disappears, and the first axoneme is surrounded by a ring of cortical microtubules (about 27 units) that persist until the appearance of the second axoneme. This ring of cortical microtubules is characteristic only for species of Bothriocephalidea and represents a very useful phylogenetic character. The spermatozoon cytoplasm is slightly electron-dense and contains numerous electron-dense granules of glycogen in several regions. The anterior and posterior extremities of the spermatozoon lack cortical microtubules. The posterior extremity of the spermatozoon of Bothriocotyle sp. possesses a nucleus and a disorganized axoneme, which also characterizes spermatozoa of the Echinophallidae studied to date.     

Spermiogenesis and spermatozoon ultrastructure of the digenean Neoapocreadium chabaudi (Apocreadiidae), a parasite of Balistes capriscus (Pisces,Teleostei)

Spermiogenesis and the ultrastructural organization of the spermatozoon of the digenean Neoapocreadium chabaudi are described by means of transmission electron microscopy.Spermiogenesis follows the usual pattern found in the digeneans. It begins with the formation of a zone of differentiation bordered by cortical microtubules, characterized by the presence of an intercentriolar body composed of seven electron-dense plates situated between two striated rootlets and two centrioles. These centrioles give rise to two free flagella. Later, both flagella undergo a rotation of 90° and fuse with the median cytoplasmic process. Spermiogenesis finishes when the ring of arched membranes constricts. The mature spermatozoon of N. chabaudi 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. Nevertheless, several characters such as the morphology of sperm extremities and the presence of spinelike bodies allow us to distinguish N. chabaudi from other digenetic trematodes. The present paper provides the first ultrastructural results of a digenean belonging to the family Apocreadiidae that may be useful for the understanding of digenean relationships and phylogenetic studies.     

The ultrastructure of spermiogenesis and spermatozoa in Diplomystes mesembrinus

Spermiogenesis in Diplomystes mesembrinus , one of the most primitive species from the Siluriformes, occurs in cysts. Differentiation of spermatids is characterized by chromatin compaction, flagellum development, nuclear fossa formation, rotation of the nucleus, and excess cytoplasm elimination. The spermatozoon head is round, the nucleus contains highly condensed chromatin clusters, the midpiece is short, the axoneme shows a 9 +2 pattern with two discrete lateral projections, and the acrosome is absent. The nuclear fossa penetrates deeply into the nucleus, including the centriolar complex and the start of the axoneme. The single large C-shaped mitochondrion surrounds the initial segment of the axoneme. The structural features of D. mesembrinus spermatozoon are similar to the Clupeiformes.     

Ultrastructure of the Spermatozoon of an Opisthobranch, Tornatina sp. (Mollusca, Gastropoda, Retusidae)

The spermatozoon of Tornatina sp. has been studied with phase-contrast light microscopy and transmission electron microscopy. The head of the spermatozoon consists of an elongate acrosome which caps the apex of an unusually complex, helical nucleus. This elaborate nuclear morphology has not been previously reported, but possibly is found in other opisthobranch gastropod spermatozoa. An axoneme is inserted deeply into the base of the nucleus whilst posterior from the nucleus, the axoneme is ensheathed successively by the mitochondrial derivative (midpiece) and 'glycogen' granules (glycogen piece). The midpiece exhibits fine structure similar to that observed in other euthyneuran spermatozoa (paracrystalline and matrix materials) and possesses a single helical compartment filled with what are probably glycogen granules. A dense ring structure occurs at the junction of the midpiece and glycogen piece. The spermatozoon of Tornatina and other gastropods (prosobranch and euthyneuran) are compared.     

Ultrastructural study of spermiogenesis and the spermatozoon of Crepidostomum metoecus (Digenea: Allocreadiidae), a parasite of Salmo trutta (Pisces: Teleostei)

Spermiogenesis and the spermatozoon of Crepidostomum metoecus, an intestinal parasite of brown trout Salmo trutta, were studied by transmission electron microscopy. Spermiogenesis begins with the formation of a differentiation zone in front of 2 centrioles associated by an intercentriolar body. Each centriole is linked to a striated rootlet, and gives rise to a flagellum. The rotation of flagella is greater than 90 degrees; their fusion with the median cytoplasmic extension is proximodistal and asynchronous. The spermatozoon is formed after constriction of arched membranes. The spermatozoon possesses 2 axonemes of the 9 + "1" pattern, a nucleus, mitochondria, and glycogen. A major feature is the presence, in the anterior part, of external ornamentation and a lateral expansion associated with spinelike bodies. Another attribute is the presence of 2 mitochondria rather than just 1, as in most of the digenean spermatozoa. To our knowledge, this study is the first undertaken with a species of the Allocreadiidae.     

Ultrastructure of the spermatozoon of Parachristianella trygonis Dollfus, 1946 (Trypanorhyncha: Eutetrarhynchidae)

The ultrastructural organization of the mature spermatozoon of the trypanorhynch cestode Parachristianella trygonis is described by transmission electron microscopy. The spermatozoon is a long and filiform cell, tapered at both ends, lacking both mitochondrion and crested bodies. Its cytoplasm contains 2 axonemes of the 9+'1' pattern of the Trepaxonemata longitudinally displaced, parallel cortical microtubules, the nucleus and glycogen in form of both alpha-glycogen rosettes and beta-glycogen particles. The anterior extremity of the spermatozoon is characterized by the presence of an arclike row of up to 10 parallel cortical microtubules that partially surround the first axoneme. The present study emphasizes the ultrastructural similarity between mature spermatozoa of all 4 trypanorhynchs that have been studied to date. Nevertheless, several features, i.e., the characteristics of spermatozoa extremities, the absence of crested bodies, and the possible presence of an arclike layer of cortical microtubules, need a more thorough analysis or confirmation in some of these species.     

ULTRASTRUCTURE OF THE MATURE SPERMATOZOA OF THE LAND SNAIL EPIPHRAGMOPHORA TUCUMANENSIS (DOERING, 1874) (GASTROPODA: HELICOIDEA)

The ultrastructure of the sperm of Epiphragmophora tucumanensis(Doering), a pulmonate land snail belonging to the family Xanthonychidae,was examined. The results showed that this spermatozoon presents a similarmorphology to the other advanced stylommatophoran sperm described.The most peculiar characteristic is the form of the nucleus,which is straight instead of helically coiled. An acrosome ispresent, composed of an apical vesicle and an acrosomal pedestal.The connecting piece or neck region is formed by a basal bodyplus a centriolar derivative. It is also the point of originof coarse fibres that accompany the axoneme. Thus, the axonemalcomplex exhibits a 9+9+2 pattern. The midpiece is an elongatedregion composed of paracrystalline and matrix materials (collectively,the mitochondrial derivative) enclosing a single glycogen helixand the axoneme. The mitochondrial derivative extends to theposterior tip of the spermatozoon. As observed in other stylommatophorans,both an annulus and a glycogen piece are absent. (Received 25 October 1993; accepted 4 February 1994)     

Ultrastructural study of spermatogenesis and the spermatozoon in Postorchigenes gymnesicus (Trematoda,Lecithodendriidae)

An ultrastructural study of spermatogenesis, spermiogenesis, and spermatozoa in Postorchigenes gymnesicus is presented. Cytoplasmic projections originating in nurse cells surround the spermatogonia, which are located at the periphery of the testes. Primary spermatocytes attached to a cytophore show synaptonemal complexes and a pair of centrioles. Spermiogenesis begins with the appearance of a cytoskeletal structure formed by an intercentriolar body and two perpendicular centrioles. An axoneme and a striated rootlet emerge from each centriole. The progressive rotation and fusion of both flagella with the median process occurs simultaneously with the migration of nucleus to the distal tip of the forming spermatozoon. The mature spermatozoon consists of three regions: (1) the nuclear region, containing the nucleus, one mitochondrion, two 9+1 axonemes, and cortical microtubules; (2) the intermitochondrial region, containing two axonemes; and (3) the mitochondrial region with another mitochondrion, two axonemes, cortical microtubules, and external ornamentation symmetrically and asymmetrically arranged coincidental with the cortical microtubules. Glycogen particles, absent in testicular cells, are abundant in the spermatozoon. Ultrastructural features of the non-nuclear region of the spermatozoon are specific for P. gymnesicus and are proposed to characterize the spermatozoon of digenean species. J. Morphol. 234:223–232, 1997. © 1997 Wiley-Liss, Inc.