Sperm ultrastructure and spermiogenesis in two Exogone species (Polychaeta, Syllidae, Exogoninae)

Abstract. The spermatozoa of Exogone naidina and E. dispar are characterized by a prominent bell-shaped acrosome, a spheroidal nucleus, and a conventional flagellum. During spermiogenesis, the acrosomal vesicle undergoes conspicuous modifications leading to its final bell shape with a posterior opening. The subacrosomal material initially shows radiating filaments but in mature sperms it appears as a meshwork of electron-opaque material. The acrosomal axis is oblique with respect to the main longitudinal sperm axis. The chromatin is arranged in electron-opaque strands in the early spermatids, then becomes amorphous, and is finally organized in filaments in mature sperms. Centrioles are orthogonally arranged beneath the nucleus and fibers radiate from the distal centriole to contact the plasma membrane and the single mitochondrion. The latter is located eccentrically on the side of the nucleus opposite the acrosome. A disk-shaped structure is evident beneath the distal centriole. The flagellar axoneme has a 9+2 microtubule pattern. A conspicuous glycocalyx surrounds the flagellar plasma membrane, and an electron-lucent space is present between these two structures at the distal tip of the flagellum. We compare the sperm morphology of these two species of Exogone with that described in other members of the subfamily Exogoninae. The fine structure of these two species supports the occurrence of an ent-aquasperm type within Exogoninae, in accordance with the brood strategy present within this subfamily. The mode of reproduction is of taxonomic importance for defining subfamilies within Syllidae, and is likely also of phylogenetic significance. Because epitoky is probably plesiomorphic, the ent-aquasperm type found in Exogoninae can be considered a derived feature within Syllidae.     

Spermatogenesis and sperm ultrastructure in the polychaete genusOphryotrocha (Dorvilleidae)

The details of spermatogenesis and spermiogenesis are described forOphryotrocha puerilis. The ultrastructure of mature sperm is shown forO. puerilis, O. hartmanni, O. gracilis, O. diadema, O. labronica, andO. notoglandulata. Clusters of sixteen cells each are proliferated by two stem cells in each setigerous segment ofO. puerilis representing the very early stages of both oogenesis and spermatogenesis. In each spermatocyte-I cluster, the cells are interconnected by cytoplasmic bridges. Early, clusters are enveloped by peritoneal sheath cells. These transient gonad walls break down prior to meiosis. The meiotic processes may start in the clusters with the cells still interconnected, or during breakdown of the original cluster, giving rise to smaller subclusters of both spermatocytes I and spermatocytes II with various numbers of cells. Finally, spermatid tetrads are present. As spermiogenesis progresses, the tetrads disintegrate. Golgi vesicles in both spermatocytes and spermatids contain electron-dense material, presumably preacrosomal. The acrosome is formed by such vesicles. In the six species studied here, the acrosomes appear to be of a similar overall structure but are of different shape. Centrioles are usually located beneath the acrosome. The distal centriole forms the basal body of a flagellum-like cytoplasmic process. The microtubules of these flagellar equivalents do not show a normal ciliar arrangement. The flagellar equivalent appears to be non-motile. InO. hartmanni and inO. notoglandulata, a flagellar equivalent is missing. Microtubules originating from the proximal end of the distal centriole stretch to the nuclear envelope. This feature appears to be especially conspicuous inO. puerilis and inO. labronica. InO. labronica and inO. notoglandulata, bundles of microtubules paralleling the cell perimeter appear to stabilise the sperm. Various numbers of mitochondria are either randomly distributed around the nucleus or accumulate on one side, often directly under the acrosome. Parts of the present paper were presented at the 2^nd International Polychaete Conference, Copenhagen 1986 and at the 3^rd International Polychaete Conference, Long Beach, Ca. 1989.     

Sperm ultrastructure and spermiogenesis in the relic species Tricholepidion gertschi Wygodzinsky (Insecta, Zygentoma)

The silverfish Tricholepidion gertschi is of interest in that it is the most basal representative of Zygentoma. An ultrastructural study of its spermiogenesis was performed to find out whether there are traits which resemble those of other, more advanced insects. This was found to be the case; spermiogenesis can be considered to be of a common insectan type, leading to the formation of elongated sperm cells with acrosome, nucleus, neck region and a tail with axoneme and two mitochondrial derivatives. Total cell length, 50 microm, is short for an insect. There are some specializations, which probably represent autapomorphies. The acrosome has a posterior canal or cleft that makes a U-turn. The centriole adjunct forms a prominent post-nuclear ring surrounding the centriole and have a posterior extension, and further originates nine intertubular fibers with a longitudinal periodicity and two accessory bodies. The mitochondrial derivatives have five rows of regularly spaced cristae within a crystalline matrix. The axoneme has accessory tubules consisting of 16 protofilaments, formed at the B-tubules of the doublets and placed at some distance from them in the posterior part of the sperm tail.     

Sperm structure and ultrastructure in the Hymenoptera (Insecta)

A light and electron microscopical survey of spermatozoan gross morphology and ultrastructure in the Hymenoptera is presented. Details are provided for the first time for members of the families Xyelidae, Argidae, Tenthredinidae, Diprionidae, Cephidae, Figitidae, Proctotrupidae, Diaprii- dae, Heloridae, Eurytomidae, Leucospidae, Perilampidae, Torymidae, Braconidae, Dryinidae, Sphecidae, Pompilidae and Vespidae. Spermatozoan length ranged from 8 μ m in some Braconidae to 500 μm in one chalcidoid. Considerable variation in gross morphology and ultrastructure were observed between taxa. Several phylogenetically informative characters were noted. Very small spermatozoa characterized most of the non-cyclostome subfamilies of Braconidae; spirally twisted axoneme and mitochondrial derivatives occur in the Eulophidae, Eurytomidae and Pteromalidae; spermatozoa with virtually indistinguishable head (nucleus and acrosome) regions characterized the Vespinae and Polistinae. The presence of well-developed spermatodesmata in the vas deferens and seminal vesicle characterize the Symphyta and were largely absent from other groups though they are occasionally present in some bees.     

Sperm ultrastructure of five species of the Neotropical ant genus Pseudomyrmex (Hymenoptera: Formicidae)

The seminal vesicles of adult males of five species of Pseudomyrmex were prepared for light and transmission electron microscopy. The Pseudomyrmex spermatozoa are long and slender with similar morphology. The head region has an acrosome and a nucleus. In all the studied species, two morphologically distinct types of acrosomal vesicles were observed, a long structure, as observed in all known ants, and a pear‐shaped one, never before observed in ants. The nucleus is elongated and both condensed and loose chromatin are present. The flagellum has an axoneme, a centriolar adjunct, two mitochondrial derivatives and two accessory bodies. The centriolar, the mitochondrial derivatives and the accessory bodies are similar to observations in most ant species that have been studied. The axoneme presents an uncommon 9 + 9 + 1 microtubule arrangement and the central microtubule has 13 protofilaments. The acrosomal dimorphism and the different levels of chromatin organization are exclusive characteristics of Pseudomyrmex. Furthermore, the 9 + 9 + 1 microtubule arrangement is different from all Hymenoptera, as well as from most insects, which present a 9 + 9 + 2 arrangement. These new morphological characters that are specific to Pseudomyrmex, are valuable synapomorphies of the genus and can be used in taxonomic characterization of the Pseudomyrmecinae subfamily and in phylogenetic analyses in Formicidae family.     

Sperm ultrastructure in Chironomoidea (Insecta, Diptera)

The fine structure of spermatozoa from several species of chironomids, of Culicoides sp. (Ceratopogonidae) and of Odagmia pontina (Simulidae) was studied. A synapomorphic feature, consisting of nine kidney-shaped structures forming the centriole adjunct, was found in the chironomid species. All members of Chironomoidea share a mono-layered acrosome and a flagellar axoneme, provided with accessory tubules with 15 protofilaments in their tubular wall. The axoneme has a 9+9+2 pattern, but in an unidentified species of chironomid, a 9+9+0 model was observed where the central complex and the spokes are missing. Sperm motility is, however, maintained in all the examined species. The spermatozoa of this taxon have the tendency to complete maturation during their progression along the deferent ducts. Thus, in the proximal region of these ducts, they often show remnants of the spermatid cytoplasm.     

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.     

Tri-oceanic connectivity of the supposedly cosmopolitan polychaete,Harmothoe imbricata (Annelida: Polynoidae): insights from the COI marker

ABSTRACT

In this study, we investigated the global population genetic structure of the polychaete, Harmothoe imbricata, to determine connectivity patterns within the species. We sequenced the mtDNA marker, cytochrome c oxidase I (COI) from 29 specimens sampled across three sites from the New England coast of the United States. These were supplemented with 145 archived sequences from GenBank and the Barcode of Life Database, representing 16 global populations, which encompassed three broadly defined marine biogeographic regions: the Atlantic, Pacific and Arctic. The resulting haplotype network and pairwise AMOVA results showed marked structure across all the major biogeographic regions and also provides evidence for cryptic diversity in the species. Haplotypes from Arctic populations were more closely related to each other than those from the northwestern and northeastern Atlantic. Two evolutionary divergent lineages were recovered from Los Angeles, California and Manitoba, Canada. The highest genetic diversity was observed in the Arctic populations, providing evidence for an Arctic origin for H. imbricata. While human-mediated introductions may have likely contributed to some of the genetic patterns observed in this study, future work should incorporate a nuclear DNA component which could shed more light on contemporary movement of this species across large spatial scales.     

A new species of Lepidasthenia (Polychaeta, Polynoidae) from Canary Islands

Lepidasthenia medanensis spn, is described from subtidal sandy bottom and beds of Cymodoceanodosa on the south west coast of Tenerife, Canary Islands.     

Sperm ultrastructure of an oviparous and an ovoviviparous onychophoran species (Peripatopsidae) with some phylogenetic considerations

The spermatozoa of the Australian oviparous Ooperipatellus insignis and the South African ovoviviparous Opisthopatus cinctipes (both: Onychophora, Peripatopsidae) were studied and compared with the spermatozoal patterns already described in the taxon. The spermatozoa of both species conform with the general plan described for the Onychophora: they are filiform cells formed, in sequence, by an elongated, fully condensed nucleus capped by an acrosome and surrounded by several spiral ridges; by a mitochondrial midpiece characteristically interpolated between the nucleus and a characteristic flagellum. Major differences between the spermatozoa of both species concern their acrosome organization. The correlation between the acrosomal pattern and the size and structure of the ovarial eggs (oocytes) in onychophorans has been investigated. A parsimony analysis was performed on 21 spermatozoal characters of the species considered. Its results are congruent with those of the traditional systematics. A new set of autapomorphies characterising onychophoran sperm is suggested and some of the spermatological homologies proposed between Onychophora and Euclitellata spermatozoa are critically discussed. Our analysis suggests that spermatozoal characters are good phylogenetic markers among onychophorans, also at low taxonomic level.     

Gamete ultrastructure in two species of the genus Upeneus (Mullidae) from the South China Sea

Ultrastructure of envelopes of ovulated oocytes and spermatozoon ultrastructure are described in two closely related species of the family Mullidae, Upeneus tragula and U. cf. margarethae. Oocyte envelope is represented by the thin zona radiata and weakly expressed chorion. The spermatozoon is characterized by the presence of elongated head with a pointed bend in its apical part and nuclear fossa reaching approximately 90% of the head length. The centriolar complex and basal part of the flagellum are located inside of the nuclear fossa.     

Sperm ultrastructure and spermiogenesis of Coniopterygidae (Neuroptera, Insecta)

The spermiogenesis and the sperm ultrastructure of several species of Coniopterygidae have been examined. The spermatozoa consist of a three-layered acrosome, an elongated elliptical nucleus, a long flagellum provided with a 9+9+3 axoneme and two mitochondrial derivatives. No accessory bodies were observed. The axoneme exhibits accessory microtubules provided with 13, rather than 16, protofilaments in their tubular wall; the intertubular material is reduced and distributed differently from that observed in other Neuropterida. Sperm axoneme organization supports the isolated position of the family previously proposed on the basis of morphological data.     

Sperm ultrastructure in Kellia suborbicularis (Bivalvia: Galeommatoidea: Kellidae)

The sperm cells of Kellia suborbicularis are narrow with a short bullet‐shaped acrosome, a 5.0–5.5 µm long and 0.4–0.6 µm broad nucleus, and a short midpiece with a ring of five mitochondria. The disposition of the subacrosomal substance into a coronet‐like formation is unique, and the sperm structure offers no clue to the relationship between Kellia and other galeommatoidean genera. The possible significance of narrow elongate sperm for their entry into the brood pouch is discussed.     

Sperm ultrastructure of the spider crab Maja brachydactyla (Decapoda: Brachyura)

This study describes the morphology of the sperm cell of Maja brachydactyla, with emphasis on localizing actin and tubulin. The spermatozoon of M. brachydactyla is similar in appearance and organization to other brachyuran spermatozoa. The spermatozoon is a globular cell composed of a central acrosome, which is surrounded by a thin layer of cytoplasm and a cup‐shaped nucleus with four radiating lateral arms. The acrosome is a subspheroidal vesicle composed of three concentric zones surrounded by a capsule. The acrosome is apically covered by an operculum. The perforatorium penetrates the center of the acrosome and has granular material partially composed of actin. The cytoplasm contains one centriole in the subacrosomal region. A cytoplasmic ring encircles the acrosome in the subapical region of the cell and contains the structures‐organelles complex (SO‐complex), which is composed of a membrane system, mitochondria with few cristae, and microtubules. In the nucleus, slightly condensed chromatin extends along the lateral arms, in which no microtubules have been observed. Chromatin fibers aggregate in certain areas and are often associated with the SO‐complex. During the acrosomal reaction, the acrosome could provide support for the penetration of the sperm nucleus, the SO‐complex could serve as an anchor point for chromatin, and the lateral arms could play an important role triggering the acrosomal reaction, while slightly decondensed chromatin may be necessary for the deformation of the nucleus. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

Ultrastructure of prostomial photoreceptors in four marine polychaete species (annelida)

The photoreceptors of four polychaete species were investigated by transmission electron microscopy: Eteone longa and Anaitides mucosa (Phyllodocidae), Scolelepis squamata (Spionidae), and Heteromastus filiformis (Capitellidae). Four different types of light-sensitive organs could be distinguished: 1) a simple, unpigmented rhabdomeric type; 2) a simple ocellus composed of a sensory and a pigmented cell; 3) complex eyes with a lens consisting of secretory granules; 4) a simple, unpigmented type with modified cilia. In spite of its simpler organization the fourth type is listed last, because its function as a photoreceptor seems dubious. The first type (unpigmented rhabdomeric receptor) occurs in all four species investigated. It is the only type of photoreceptor in Heteromastus. Additionally, the two phyllodocids Eteone and Anaitides possess another kind of receptor (type 4) in close proximity to the type 1 receptor. Simple ocelli (type 2) are found in Scolelepis. A pair of complex eyes (type 3) is present in both Eteone and Anaitides, but they show important differences in the two species. First, the eyes in Eteone exhibit ciliary rudiments within the sensory processes, but such rudiments are absent in the eyes of Anaitides. Secondly, the sensory cells in Anaitides possess pigment granules, whereas in Eteone they do not. Thirdly, the lens in Eteone is composed of secretion granules of equal electron density, whereas in Anaitides the lens granules show increased electron density centrally. Lens material appears to be secreted from a single corneal cell in Eteone, and from several corneal cells in Anaitides. In both species these corneal cells are located distally outside the lens.     

Sperm ultrastructure in the inseminating Macropsobrycon uruguayanae (Teleostei: Characidae: Cheirodontinae)

Macropsobrycon uruguayanae is a small, inseminating characid (tetra) of the tribe Compsurini. Although spermatozoa can be found within the ovarian cavity close to oocytes, the exact moment of fertilization has not yet been determined. Spermatozoa have moderately elongate nuclei with electron-dense chromatin. During spermiogenesis, nuclear rotation takes place. Elongate mitochondria with lamellar cristae are found posterior to the nucleus. Centrioles are parallel to one another with the proximal centriole slightly anterior to the longer distal one. The anterior tip of the proximal centriole is located within a shallow nuclear fossa. Electron-dense spurs are associated within the anterior and posterior ends of the distal centriole. Striated centriolar rootlets radiate both anteriorly and posteriorly from the distal centriole. Nine longitudinal accessory microtubules surround the axoneme in the proximal flagellum. The flagellum has a typical 9 + 2 axoneme with no intratubular differentiation. Atypical spermatozoa are also found in the testicular lumen. These cells resemble spermatozoa in most aspects, except that their nuclei are variable in shape, with the granular chromatin less electron-dense than that seen in spermatozoa. The origin and function of these cells could not be determined. The specializations seen in the spermatozoa are discussed as possible adaptations related to the habit of insemination.     

Sperm ultrastructure in Myxinidocotyle and Acanthocotyle (Platyhelminthes, Monogenea, Acanthocotylidae)

Spermatozoa of Myxinidocotyle californica from the hagfish Eptatretus stoutii and of Acanthocotyle lobianchi from the skate Raja clavata show a similar ultrastructure: two axoncmes of the 9 + 1 type in parallel with the nucleus-and one mitochondrion. In the released Acanthocotyle spermatozoa nucleus and mitochondrion both have a triangular cross-section. No cortical microtubules are present. The ultrastructure of these two acanthocotylid spermatozoa thus corresponds to sperm pattern 2 according to Justine et al. (1985). This pattern is derived from the more primitive pattern 1, which in the Monogenea is found only in the Oligonchoinea Bychowsky, 1937 or the Polyopisthocotylea sensu Justine et al.     

Zoospore ultrastructure in species ofTrebouxia andPseudotrebouxia (Chlorophyta)

Zoospore ultrastructure (incl. flagellar apparatus) has been investigated in three species ofTrebouxia (T. glomerata, T. erici, T. pyriformis) and one species ofPseudotrebouxia (P. impressa) using an absolute configuration analysis. Zoospores in all taxa studied are nearly identical in ultrastructure and exhibit a very distinctive disposition of cell organelles: cells are naked, biflagellate and considerably flattened along the plane of flagellar beat, the single contractile vacuole is located anteriorly in the ventral region of the cell, the nucleus is anteriorly to centrally located in the dorsal region of the cell. A single dictyosome is located close to the anterior, ventral edge of the nucleus. The chloroplast occupies a posterior position in the cell and usually has an anterior profile in the left region of the cell. There are two branched mitochondria per cell or a single mitochondrial reticulum with profiles anterior to the nucleus (in the dorsal region of the cell), and posterior to the nucleus. In zoospores ofTrebouxia spp. the posterior mitochondrial profile is associated with a microbody, inP. impressa zoospores the anterior mitochondrial profiles are associated with a microbody. The zoospores contain a distinctive system of three ER-cisternae: one system links to both basal bodies and extends to the nucleus, the other two systems subtend the plasmamembrane on the left and right broad cell surfaces and extend to the posterior region of the cell. The flagellar apparatus is structurally identical to that previously described for zoospores ofFriedmannia israelensis and exhibits basal body displacement by one basal body diameter into the 11/5 o'clock direction, a non-striated distal connecting fiber, a cruciate microtubular root system lacking system I fibers and presence of a single system II fiber which connects the basal bodies with the nucleus and runs parallel to one of the ER-strands. The left flagellar roots (X-roots) are subtended by a complex set of amorphous and striated material that connects each left root with both basal bodies.—This study demonstrates the close systematic relationship between the phycobiontsTrebouxia andPseudotrebouxia and the generaFriedmannia, Pleurastrum, andMicrothamnion and supports recent classification schemes which place all these taxa into a single order separate from otherChlorophyta. Dedicated to Prof. DrElisabeth Tschermak-Woess on the occasion of her 70th birthday.