The spermiogenesis and the early spermatozoa of <Emphasis Type="Italic">Armorloricus elegans</Emphasis> (Loricifera,Nanaloricidae)

The spermiogenesis consisting of five spermatid stages and the early spermatozoon has been investigated in Armorloricus elegans (Loricifera) with the use of transmission electron microscopy. The male reproductive system consists of three parts; testes, vasa deferentia and seminal vesicles. Caudally, the two seminal vesicles merge together in a ciliated duct and the excretory/gonadal—and digestive systems continue through the recto-urogenital canal, which opens via the lateral gonopores and the temporarily closed anal system. Spermiogenesis mainly occurs in the testes, whereas further maturation of the late spermatids and early spermatozoa occurs in the vasa deferentia and seminal vesicles. A maturation gradient (from spermatocytes to spermatozoa) is found from the posterior peripheral part of the testes to the anterior periphery and then centrally. During spermiogenesis the round nucleus becomes more osmiophilic and condensation of chromatin occurs. Later the nucleus elongates until it becomes rod-shaped in the early spermatozoa. In the second spermatid stage, a large vesicle is formed by saccules developed from the Golgi complex. This vesicle develops further and consists of three different osmiophilic parts with some crystal-like structures inside and is on the outside almost entirely surrounded by thick striated filaments. In the mid-piece the flagellum has a typical 9 × 2 + 2 axoneme and the two mitochondria are fused into a single sheet surrounding the flagellum. In the early spermatozoon stage an acrosomal-like cap structure with an acrosome filament appears proximal to the protruded rod-shaped nucleus. This cap is not formed by the Golgi complex and therefore might not be a true acrosome. Comparing the early spermatozoa of A. elegans with other cycloneuralians has shown some similarities with especially Kinorhyncha and Priapulida. These similarities are thought to be plesiomorphic.     

Spermatogenesis inPlatynereis massiliensis (Polychaeta: Nereidae)

Stage 1 of spermatogenesis in the protandrous polychaetePlatynereis massiliensis is represented by clusters of about 60 spermatogonia which appear in the coelomic cavity. There are no testes inP. massiliensis. The origin of the spermatogonial clusters is not known. Subclusters of approximately 20 primary spermatocytes each represent stage 2. The appearance of synaptonemal figures in the spermatocyte nuclei marks the beginning of stage 3. Cells tend to lose their tight packing during stage 3 but interdigitate with cellular processes. Then very small subclusters of 4 to 8 spermatocytes appear. Meiosis is completed during stage 4, giving rise to secondary spermatocytes and then to spermatid tetrads. Spermatogonia and primary spermatocytes are interconnected by structurally specialized fusomes while secondary spermatocytes and spermatids, which are also in cytoplasmic continuity, show rather simple cell bridges. Synthesis of acrosomal material starts during stage 2. During spermiogenesis the proacrosomal vesicles of Golgi origin travel from the posterior part of the cell to its anterior part to form the acrosome proper. Acrosome formation, nuclear condensation, shaping of the long and slender sperm nucleus, and development of the sperm tail are the main events during spermiogenesis. Sperm morphology is briefly discussed wity respect to its phylogenetic bearings.     

Sperm ultrastructure and a new type of spermiogenesis in two species of Pimelodidae, with a comparative review of sperm ultrastructure in Siluriformes (Teleostei: Ostariophysi)

During spermiogenesis, the spermatids of the pimelodid species Pimelodus maculatus and Pseudoplatystoma fasciatum show a central flagellum development, no rotation of the nucleus, and no nuclear fossa formation, in contrast to all previously described spermatids of Teleostei. These characteristics are interpreted as belonging to a new type of spermiogenesis, named here type III, which is peculiar to the family Pimelodidae. In P. maculatus and P. fasciatum, spermatozoa possess a spherical head and no acrosome; their nucleus contains highly condensed, homogeneous chromatin with small electron-lucent areas; and a nuclear fossa is not present. The centriolar complex lies close to the nucleus. The midpiece is small, has no true cytoplasmic channel, and contains many elongate and interconnected vesicles. Several spherical to oblong mitochondria are located around the centriolar complex. The flagellum displays the classical axoneme (9+2) and no lateral fins. Only minor differences were observed among the pimelodid species and genera. Otherwise, spermiogenesis and spermatozoa in the two species of Pimelodidae studied exhibit many characteristics that are not found in other siluriform families, mainly the type III spermiogenesis.     

Ultrastructure of the spermatozoon and spermiogenesis in the interstitial annelid Potamodrilus fluviatilis

The ultrastructure of spermatozoa and its genesis (spermiogenesis) have been investigated in the interstitial annelid Potamodrilus fluviatilis. The mature spermatozoa are threadlike cells which are bent at the base of the flagellum, giving the cell a hairpinlike appearance. The acrosome consists of an unusual, long, flasklike vesicle with a granum in its basal part. The cylindrical nuclear region is characterized by a monolayer of vesicles enwrapping the posterior half of the nucleus. This region is endowed with a number of altered rodlike mitochondria. No middlepiece is present. The basal body of the flagellum is obliquely arranged with respect to the long axis, giving rise to a curved flagellum, which, along most of its length, exhibits a thick layer of vacuolized cytoplasm around the axoneme. During spermiogenesis, which occurs in the body fluid, spermatids develop at the surface of syncytial masses which have been formed during meiotic divisions. The acrosome protrudes in the distal part of the cell, while the basal body of the flagellum is shifted toward the proximal region, which connects the cell with the cytophore. These are unusual features in annelid spermiogenesis. As indicated in Discussion, the phylogenetic implications of these findings include the assumption that Potamodrilus is not related to any oligochaete or even any other clitellate group or species and, hence, has to be excluded from these taxa.     

An Electron Microscopic Study of Spermatogenesis in Marenzelleria viridis (Verrill, 1873) (Polychaeta; Spionidae)

Abstract Spermatogenesis in Marenzelleria viridis was studied by ultrastructural investigation. The testes are formed on the greatly ramified nephridial blood vessel and are enveloped by a thin layer of peritoneal cells. The spermatogonia vary in shape, are about 10 μm in diameter and are not linked by intercellular bridges. Pairs or tetrads of spermatocytes connected by intercellular bridges float freely in the coelomic cavity. A complex acrosome is produced by a Golgi complex. The acrosome consists of four to five different structures, forms cisternae and, in the mature spermatozoon, lies deep in an invagination of the nucleus. Two centrioles are also situated in a deep centriolar fossa, the proximal centriole being perpendicular to the distal one. The mature spermatozoon is an ect-aquasperm measuring about 5 μm in length and 2.5 μm in width. The midpiece consists of five spherical mitochondria arranged around the axoneme behind the nucleus. The axoneme is connected to the plasma membrane by a satellite complex. The microtubules of the flagellum are arranged in a typical 9 × 2 + 2 configuration. The spermatogenesis and the sperm morphology of M. viridis were compared with those of other members of the family Spionidae. Copyright © 1996 The Royal Swedish Academy of Sciences. Published by Elsevier Science Ltd.     

Ultrastructure of spermiogenesis in Plagioscion squamosissimus (Teleostei, Perciformes, Sciaenidae)

Spermiogenesis in Plagioscion squamosissimus occurs in cysts. It involves a gradual differentiation process of spermatids that is characterized mainly by chromatin compaction in the nucleus and formation of the flagellum, resulting in the spermatozoa, the smallest germ cells. At the end of spermiogenesis, the cysts open and release the newly formed spermatozoa into the lumen of the seminiferous tubules. The spermatozoa do not have an acrosome and are divided into head, midpiece, and tail or flagellum. The spermatozoa of P. squamosissimus are of perciform type with the flagellum parallel to the nucleus and the centrioles located outside the nuclear notch.     

Spermiogenesis in the imbricate alligator lizard,Barisia imbricata (Reptilia,Squamata, Anguidae)

Although the events of spermiogenesis are commonly studied in amniotes, the amount of research available for Squamata is lacking. Many studies have described the morphological characteristics of mature spermatozoa in squamates, but few detail the ultrastructural changes that occur during spermiogenesis. This study's purpose is to gain a better understanding of the subcellular events of spermatid development within the Imbricate Alligator Lizard, Barisia imbricata. The morphological data presented here represent the first complete ultrastructural study of spermiogenesis within the family Anguidae. Samples of testes from four specimens collected on the northwest side of the Nevado de Toluca, México, were prepared using standard techniques for transmission electron microscopy. Many of the ultrastructural changes occurring during spermiogenesis within B. imbricata are similar to that of other squamates (i.e., early acrosome formation, chromatin condensation, flagella formation, annulus present, and a prominent manchette). However, there are a few unique characteristics within B. imbricata spermatids that to date have not been described during spermiogenesis in other squamates. For example, penetration of the acrosomal granule into the subacrosomal space to form the basal plate of the perforatorium during round spermatid development, the clover‐shaped morphology of the developing nuclear fossa of the flagellum, and the bulbous shape to the perforatorium are all unique to the Imbricate Alligator Lizard. These anatomical character differences may be valuable nontraditional data that along with more traditional matrices (such as DNA sequences and gross morphological data) may help elucidate phylogenetic relationships, which are historically considered controversial within Squamata. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.     

Structure of the ellipsoid sheath in the spleen of the armadillo (Dasypus novemcinctus). A light and electron microscopic study

A seasonal study of the seminal vesicles in relation to that of the testes had been conducted in the catfish, H. fossilis. The annual reproductive cycle of the catfish has been divided into (i) Preparatory period (February–April), (ii) Prespawning period (May–June), (iii) Spawning period (July–August) and (iv) Postspawning period (September–January). Testes exhibit initiation of spermatogenesis in the mid-preparatory period, but significant increase in weight of the testes accompanied by active spermatogenesis occurs during the prespawning period. In the spawning period, the testes are maximally enlarged and their seminiferous tubules are packed with spermatozoa. Following spawning, the testes gradually regress in the postspawning period. The seminal vesicles show initiation of secretory activity during the preparatory period but their recrudescence lags behind that of the testes by about a month. The seminal vesicles attain maximum weight and secretory activity during the spawning period. Thereafter, the seminal vesicles regress precipitously and sooner than the testes. The histochemical and biochemical studies on the seminal vesicles indicate that the secretion contains mucoproteins, acid mucopolysaccharides, primary proteoses, besides traces of phospholipids and native proteins.     

Four lines of spermatid development and dimorphic spermatozoa in the sea urchin Anthocidaris crassispina (Echinodermata, Echinoida)

 The process of sperm development in the sea urchin Anthocidaris crassispina was studied by light and electron microscopy. Similar to other echinoids studied, a single flagellum, striated rootlet and nuage-like materials were present in spermatogonia of A. crassispina. Spermatocytes near the diplotene stage showed intracellular localization of the axoneme which appeared to be a retracted flagellum prior to cell division. Fibrous filaments were associated with a proximal centriole in spermatocytes and spermatids and might be involved in movement of the proximal centriole. An acrosomal vesicle was developed and a residual body was formed in spermatids. The special development patterns in A. crassispina attributed to the presence of two patterns of tail development and two patterns of mitochondrial development during spermiogenesis. These four lines of spermiogenesis resulted in the formation of four morphological types of sperm cell, i.e. sperms with: (1) a symmetrical midpiece and posterior tail, (2) an asymmetrical midpiece and posterior tail, (3) a symmetrical midpiece and bent tail and (4) an asymmetrical midpiece and bent tail. Sperm cells with bent tails (type 3+4) were probably still at the late spermatid stage because results of scanning electron microscopy demonstrated gradual detachment and eventual straightening of the bent tail, and their percentage occurrence in the sperm population decreased significantly (P<0.05) towards the spawning season of A. crassispina. Spermatozoa with a symmetrical midpiece were dominant (averaging 70% occurrence in the sperm population) over those with an asymmetrical midpiece. The dimorphic spermatozoa in A. crassispina (types 1, 2) are both considered to be euspermatozoa as their morphology is typical for Echinoida. Accepted: 4 May 1998     

Ultrastructure and histochemistry of the male reproductive system of the genus Callinectes Stimpson, 1860 (Brachyura: Portunidae)

We described the ultrastructure and histochemistry of the reproductive system of five Callinectes species, and evaluate the seasonal variation in weight of the reproductive system and hepatopancreas by comparing annual changes of somatic indices. The somatic indices changed little throughout the year. In Callinectes, spermatogenesis occurs inside the lobular testes and, within each lobule, the cells are at the same developmental stage. Spermatogenesis and spermiogenesis follow the same development pattern in all Callinectes studied. Mature spermatozoa are released into the seminiferous ducts through the collecting ducts. Cells of the vas deferens are secretory as evidenced by rough endoplasmic reticulum, Golgi complex, and secretory vesicles that produce the seminal fluid. The anterior vas deferens shows two portions: proximal and distal. In proximal portion (AVDp), spermatozoa are clustered and embedded in an electron-dense, basophilic glycoproteinaceous secretion Type I. In the distal portion (AVDd), the spermatophore wall is formed by incorporation of a less electron-dense glycoproteinaceous secretion Type II. The secretion Type I change to an acid polysaccharide-rich matrix that separates the spermatophores from each other. The median vas deferens (MVD) stores the spermatophores and produces the granular glycoproteinaceous seminal fluid. The posterior vas deferens (PVD) has few spermatophores. Its epithelium has many mitochondria and the PVD seminal fluid changes into a liquid and homogeneous glycoprotein. Many outpocketings in the PVD and MVD help to increase the fluid production. Overall, the reproductive pattern of Callinectes is similar to other species that produce sperm plugs. The secretions of AVD, MVD, and PVD are responsible for the polymerization that forms the solid, waxy plug in the seminal receptacle. The traits identified here are common to all Portunidae species studied so far.     

Ultrastuctural and cytochemical study of spermatogenesis in Scrobicularia plana (Mollusca,Bivalvia)

The ultrastructure of the mature spermatozoa and spermatogenesis of the bivalve Scrobicularia plana are described. Support cells extend from the basal lamina to the lumen of the testis and are laterally connected to the germinal epithelium. Germ cells present intercellular bridges and flagella since the spermatogonial stage. While spermatogonia and spermatocytes appear connected to support cells by desmosome-like junctions, elongated spermatids are held at the acrosomal region by support cell finger-like processes. During spermiogenesis, the acrosomal vesicle differentiates from a golgian saccule and then migrates to the nuclear apex. A microtubular manchette arising from centrioles surrounds the acrosomal vesicle, the nucleus, and the mitochondria at the time these three organelles start their elongation, disappearing after that. The mature spermatozoon of S. plana lacks a distinct midpiece because the mitochondria extend from the region of the pericentriolar complex along the nucleus anteriorly for approximately 1.4 μm. The features of this bivalve type of modified spermatozoon are compared with those of other animal groups having similar modifications.     

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.     

Gonadal maturation is dependent on body size in the sea urchin,Echinometra tsumajiroi

Summary

This study examined gonadal maturation in the sea urchin, Echinometra tsumajiroi, in relationship to body size. In the breeding season, E. tsumajiroi were collected and divided into six groups based on the length of the major axis (LM) as a measure of body size: Group 1 (6–10 mm in LM), Group 2 (11–15 mm in LM), Group 3 (16–20 mm in LM), Group 4 (21–25 mm in LM), Group 5 (26–30 mm in LM), and Group 6 (> 31 mm in LM). Although gonads were present in individuals larger than 8 mm in LM, the germ cells were undifferentiated in Group 1. Gonadal sex differentiation was first seen in Group 2: a few young oocytes appeared at the periphery of the ovary, and both spermatogonia and spermatocytes were also observed at the periphery of the testis. As size increased from Group 3 to Group 4, more mature germ cells such as ripe ova or spermatozoa were observed in ovaries and testes. In Group 5, the ovaries and testes were filled with a large number of mature eggs and spermatozoa, respectively. Spawning could be induced in this group by the injection of 0.5 M KCl into the coelomic cavity. In contrast, gonads of some of the biggest individuals, belonging to Group 6, appeared to be spent due to spawning, because few eggs were present in the ovary and relict spermatozoa were present in the testis. These results suggest that reproductive activity in the sea urchin, E. tsumajiroi, depends on body size.     

Morphology of the male system and spermatophores of the arrowworm Ferosagitta hispida (Chaetognatha)

Transmission electron microscopy reveals that the somatic testicular tissues and sperm ducts are elaborations of the epithelial lining of the tail coelom. The testes consist of closely packed spermatogonia embedded between specialized lateral field cells. These cells contain few organelles and appear to function mainly as a compartment boundary. Masses of spermatogenic cells are released into the tail coelom from the anterior end of the testes. The sperm ducts, lined by simple cuboidal ciliated epithelium, collect mature spermatozoa from the tail coelom and convey them to the blindly ending seminal vesicles. The sperm ducts also modify coelomic fluid entering them along with the spermatozoa. The seminal vesicles consist of a simple glandular lining epithelium embedded in the stratified epidermis. Secretions of the lining epithelium surround the enclosed sperm mass and correspond in position to a noncellular spermatophore coat visible by light microscopy around released sperm masses. Spermatophores leave the seminal vesicles through a temporary split that forms between microfilament-containing suture cells. Maturation of spermatozoa and filling of the seminal vesicles is cyclical, occurring late each day. © 1994 Wiley-Liss, Inc.     

Histomorphological studies of the testis and male genital ducts of Supachai's caecilian,Ichthyophis supachaii Taylor, 1960 (Amphibia: Gymnophiona)

We investigated the structure of the male reproductive system in Ichthyophis supachaii. The testis comprises a series of mulberry‐like lobes, each of which contains testis lobules occupied by germ cysts. A single cyst consists of synchronously developing germ cells. Six spermatogenic cell types, viz. primary spermatogonia, secondary spermatogonia, primary spermatocytes, secondary spermatocytes, spermatids and spermatozoa, have been identified and described. Notably, the testis of I. supachaii encompasses specific organization patterns of spermatids and spermatozoa during spermiogenesis. Spermiating cysts rupture and release spermatozoa to the collecting ducts, which are subsequently transported to the sperm duct, Wolffian duct and cloaca. We report for the first time ciliated cells in the epithelium of the caecilian Wolffian duct. The cloaca is divided into the urodeum and phallodeum. The urodeum has ciliated and glandular epithelia at its dorsolateral and ventral regions, respectively, as the lining of its internal surface. The muscular phallodeum is lined by ciliated epithelium. Paired Mullerian ducts lie parallel to the intestine and join the cloaca. The posterior portion of the duct is modified as the Mullerian gland. The most posterior region is non‐glandular and lined by ciliated epithelium. Our findings contribute further to information on the reproductive biology of caecilians in Thailand.     

Reproductive system of the Schrenckii salamander (Salamandrella schrenckii, Amphibia, Caudata, Hynobiidae) in spring and fall

The reproductive system of 319 individuals of the Schrenckii salamander (Salamandrella schrenckii Strauch 1870) (synonym S. tridactyla sensu (Kuz’min et al., 2008) from a Khabarovsk population has been studied before wintering and during the spawning of animals. In the fall, all adult males had enlarged testes filled with bundles of spermatozoa and no spermatozoa in the spermaducts. Females had large pigmented ova in the ovaries and empty expanded oviducts. In the spring, only mature S. schrenckii individuals were found in the water; the entire spectrum of physiological states from the preparation for breeding to its end was noted in them. The preovulatory stage, ovulation, pregnancy, and spawning were registered in females; the predominance of spermatozoa in the testes or in spermaducts, or almost complete absence of them in the reproductive system, and different degrees of hypertrophy of spermaducts were noted in males. These differences are related to the different times of arrival of individuals to the spawning pond. The material analyzed evidences the yearly breeding of S. schrenckii. S. schrenckii differs from S. keyserlingii in the type and duration of the reproductive cycle, sizes and morphology of spermatozoa, and structure and functioning of ovaries (Saveliev et al., 1993; Kuranova and Saveliev, 2006). The majority of the reviewed characteristics of S. schrenckii are similar to those of the allied genus representatives: Hynobius nigrescens and H. retardatus (Hasumi et al., 1990; Iwasawa et al., 1992; Hasumi, 1996a).     

Morphological evaluation of spermatogenesis in Lake Magadi tilapia (Alcolapia grahami): A fish living on the edge

Spermatogenesis in Lake Magadi tilapia (Alcolapia grahami), a cichlid fish endemic to the highly alkaline and saline Lake Magadi in Kenya, was evaluated using light and transmission electron microscopy. Spermatogenesis, typified by its three major phases (spermatocytogenesis, meiosis and spermiogenesis), was demonstrated by the presence of maturational spermatogenic cells namely spermatogonia, spermatocytes, spermatids and spermatozoa. Primary spermatogonia, the largest of all the germ cells, underwent a series of mitotic divisions producing primary spermatocytes, which then entered two consecutive meiotic divisions to produce secondary spermatocytes and spermatids. Spermatids, in turn, passed through three structurally distinct developmental stages typical of type-I spermiogenesis to yield typical primitive anacrosomal spermatozoa of the externally fertilizing type (aquasperm). The spermatozoon of this fish exhibited a spheroidal head with the nucleus containing highly electron-dense chromatin globules, a midpiece containing ten ovoid mitochondria arranged in two rows and a flagellum formed by the typical 9 + 2 microtubule axoneme. In addition, the midpiece, with no cytoplasmic sheath, appeared to end blindly distally in a lobe-like pattern around the flagellum; a feature that was unique and considered adaptive for the spermatozoon of this species to the harsh external environment. These observations show that the testis of A. grahami often undergoes active spermatogenesis despite the harsh environmental conditions to which it is exposed on a daily basis within the lake. Further, the spermiogenic features and spermatozoal ultrastructure appear to be characteristic of Cichlidae and, therefore, may be of phylogenetic significance.     

Ultrastructure of the spermatogenesis of the cockle Anadara granosa L. (Bivalvia: Arcidae)

In this paper spermatogenesis and sperm ultrastructure of the cockle Anadara granosa are studied using transmission electron microscopy. The spermatocyte presents electron-dense vesicles and the arising axoneme that begins to form the flagellum. During spermatid differentiation, proacrosomal vesicles appear to migrate towards the presumptive anterior pole of the nucleus; eventually these vesicles become acrosome. The spermatozoon of Anadara granosa is of the primitive type. The acrosome, situated at the apex of the nucleus, is cap-shaped and deeply invaginated at the inner side. The spherical nucleus of the spermatozoon contains dense granular chromatin and shows invagination at the posterior poles. The centriole shows the classic nine triplets of microtubules. The middle piece consists of the centriolar complex surrounded by five giant mitochondria. It is shown that the ultrastructure of spermatozoa and spermiogenesis of Anadara granosa reveals a number of features that are common among bivalves. Received: 29 September 1998 / Received in revised form: 20 May 1999 / Accepted: 14 June 1999