Structure and formation of the unusual sperm of Patelloida latistrigata (Mollusca : Patellogastropoda): implications for fertilization biology.

The structure of the spermatozoa and spermatogenesis of the lottiid limpet Patelloida latistrigata is described by transmission electron microscopy. Although the lengths of the spermatozoa (about 60 µm) and their head region (about 12 µm) are similar to those of other patellogastropods, the structure of the sperm head and midpiece are very different. The head consists of an unusually large acrosome (about 11-µm long) with a broad posterior invagination that houses the relatively small nucleus. The midpiece mitochondria, which are rather elongate with large folded tubular cristae, are housed in a cytoplasmic sheath posterior to the nucleus. The proximal centriole is unusually elongate (about 2-µm long). The axoneme that emerges from the distal centriole is surrounded anteriorly by the cytoplasmic sheath in which the cytoplasmic side of the plasma membrane has electron-dense material. The flagellum is enlarged at its terminal end. Spermatogenesis is similar to that described for other patellogastropods. Patelloida latistrigata, therefore, has spermatozoa that seem to meet the morphological criteria of ent-aquasperm, which raises the question of whether fertilization is truly external in this limpet. However, it is also possible that the modifications to the sperm are linked to unknown specializations of the egg or egg envelope.

Spermiogenesis and modified sperm morphology in the "seepworm" Methanoaricia dendrobranchiata (Polychaeta: Orbiniidae) from a methane seep environment in the Gulf of Mexico: implications for fertilization biology.

Spermatogenesis and mature sperm morphology have been described along with limited observations of the ovary in Methanoaricia dendrobranchiata, an orbiniid polychaete associated with dense populations of the mussel Bathymodiolus childressi at brine pools on the Louisiana slope, Gulf of Mexico. The species is gonochoric with gonads serially repeated in numerous segments and each associated with a nexus of blood vessels at the base of the parapodia. In the female, synchronous, intraovarian egg development occurs with the release from the ovary of large, yolky eggs into the coelom at first meiotic metaphase. Sperm develop in the coelom as free-floating, plasmodial clones interconnected via an anuclear cytophore. At the end of spermiogenesis, mature spermatozoa float freely in the coelom. The mature spermatozoon differs significantly from that of shallow-water orbiniid species by possessing an elongated nucleus and a greatly elongated and curved acrosome reaching 19.5 microm in length. The spermatozoon resembles an ent-aquasperm and may not fertilize the eggs directly in seawater in the classical manner. We hypothesize that the unusual spermatozoon morphology in this species has evolved due to the hypoxic environment in which the adults live and that fertilization biology is likely modified in some way to minimize sperm exposure to high levels of hydrogen sulfide. An analysis of life-history features in shallow-water orbiniids is used to infer reproductive features in M. dendrobranchiata that could not be directly documented.

Ultrastructural study of the ovary of the sessile scyphozoan, Haliclystus octoradiatus (Cnidaria: Stauromedusae).

An ultrastructural study of the ovary of the sessible jellyfish, Haliclystus octoradiatus, indicates that it is fundamentally different from that of other scyphozoans and is the most structurally complex within the class. Oocytes develop within a series of spherical, sac-like ovarian follicles consisting of an enlarged intercellular space between two layers of subumbrellar gastrodermis. Developing oocytes are largely restricted to a thin germinal epithelium at the periphery of each follicle and gradually migrate toward the lumen as they mature. Individual oocytes are surrounded by early germ cells and follicle-like accessory cells of presumed somatic origin. Similar folliclelike cells have not been described in the Cnidaria previously. Vitellogenesis appears to involve the combined activity of the Golgi complex and associated rough endoplasmic reticulum. Ovarian morphology may be helpful in deciphering phylogeneitc relationships within the Cnidaria. © 1993 Wiley-Liss, Inc.

Ultrastructure of sperm development and mature sperm morphology in three species of commensal bivalves (Mollusca: Galeommatoidea).

Ultrastructural features of the ovotestes, spermatogenesis, and the mature sperm are described for three galeommatid bivalves, Divariscintilla yoyo, Divariscintilla troglodytes, and Scintilla sp., from stomatopod burrows in eastern Florida. All three species yielded similar results except with respect to mature sperm dimensions. The ovotestis contains three types of somatic cells within the testicular portion: flattened myoepithelial cells defining the outer acinal wall; underlying pleomorphic follicle cells containing abundant glycogen deposits; and scattered, amoeboid cells containing lysosomal-like inclusions which are closely associated with developing sperm. Early spermatogenesis is typical of that reported from other bivalves. In contrast, the late stages of spermiogenesis involve the migration and gradual rotation of the acrosomal vesicle, resulting in a mature acrosome tilted about 70° from the long axis of the cell. The mature sperm possesses an elongated, slightly curved nucleus; a subterminal, concave acrosome with a nipple-like central projection; five spherical mitochondria and two centnoles in the middlepiece; and a long flagellum. The rotational asymmetry and the presence of perimitochondrial glycogen deposits in these sperm are unusual in the Bivalvia and may be associated with fertilization specializations and larval brooding common among galeommatoideans.

Ultrastructure and Development of Dimorphic Sperm in the Abyssal Echinoid Phrissocystis multispina (Echinodermata: Echinoidea): Implications for Deep Sea Reproductive Biology.

Mature males of the abyssal echinoid Phrissocystis multispina produce two types of sperm including a euspermatozoon typical of echinoids, and a paraspermatozoon, which is bipolar-tailed. The structure of the testis and most features of spermatogenesis are similar to that of other echinoids. Development of both sperm types is identical until the spermatid stage when the nucleus of the paraspermatozoon undergoes chromatin reduction. Both sperm types have acrosomes typical of other echinoid sperm. However, we never observed a Golgi complex during any stage of sperm differentiation so the origin of the acrosome is unclear. Both the distal and proximal centrioles are involved in the formation of an anteriorly and posteriorly directed flagellum in the paraspermatozoon. Mixtures of both sperm types tend to clump due to the entanglement of sperm axonemes in the paraspermatozoon flagellum. Although the function of the paraspermatozoa is unknown, they may play a role in facilitating fertilization through the reduction of euspermatozoon diffusion during spawning. This study reports only one of several recently discovered reproductive adaptations associated with deep-sea habitats.

Structure of the ovotestis and evidence for heterosynthetic incorporation of yolk precursors in the oocytes of the nudibranch mollusc, Spurilla neapolitana.

The ovotestis of Spurilla neapolitana consists of a series of spherical lobes, each of which is composed of radially arranged, sac-like acini or follicles. The male and female portions of each acinus are separated by ovarian follicle cells and testicular accessory cells. A thick basal lamina serves as a barrier between adjacent acini. The surface of each ovotestis lobe is covered by several layers of myoepithelial cells resting on a connective tissue layer. Developing oocytes are intimately associated with follicle cells except in the last stages of vitellogenesis. Follicle cells are characterized by the presence of extensive arrays of rough endoplasmic reticulum (RER) and Golgi complexes and may play a role in vitellogenesis. An ultrastructural analysis of vitellogenesis suggests that oocytes utilize both auto- and heterosynthetic mechanisms of yolk formation. Autosynthetsis is suggested by the activity of the Golgi complex and RER, while heterosynthesis is indicated by high levels of endocytotic activity by the oocyte. Follicle cell development and high endocytotic activity in the oocytes may be a reproductive adaptation to accelerate yolk synthesis, resulting in more rapid egg production.

ULTRASTRUCTURAL DIFFERENCES IN THE EGGS AND OVARIAN FOLLICLE CELLS OF CAPITELLA (POLYCHAETA) SIBLING SPECIES.

Ultrastructural studies of ovarian follicle cells and mature eggs in four sibling species in the polychaete genus Capitella have revealed distinct and consistent morphological differences that parallel in some respects the differences between the species in egg size, and embryonic and larval development. Capitella spp. I and II are extremely similar in all respects: the follicle cells lack lipid and contain a modest amount of glycogen; the mature eggs are rich in lipid and glycogen and contain very similar proteid yolk granules. In both species mature eggs have a characteristic electron-dense band and a zone of mitochondria in the cortical ooplasm. These sympatric species have eggs that are similar in size and lecithotrophic larvae that are planktonic for only a short time. Capitella sp. III (Capitella jonesi) has ovarian follicle cells containing a small amount of lipid and no glycogen, while the mature eggs have a small amount of lipid, abundant glycogen, and large proteid yolk granules. These small eggs show no evidence of an electron-dense band or any concentration of mitochondria in the cortical ooplasm. This species has planktotrophic larvae that remain in the plankton for many weeks. Capitella sp. IIIa has ovarian follicle cells rich in both lipid and glycogen. The large mature eggs are rich in lipid, have relatively little glycogen, and have abundant proteid yolk granules. The cortical ooplasm contains electron-dense material similar to that observed in the eggs of species I and II but it is distributed in a discontinuous band. This species has direct development, and juvenile worms emerge from the parental brood tube after metamorphosis. The egg envelopes and microvilli of the eggs of all four sibling species undergo substantial morphological changes following release from the ovary into the coelom. The significance of these morphological and biochemical differences between the species is not known, but the lack of intraspecific variation in these characters suggests that their presence or absence reflects specific differences in the processes of yolk formation and utilization.

Ultrastructure of the ovary and oogenesis in the polychaete Capitella jonesi (Hartman, 1959).

Ultrastructural features of the ovary and oogenesis in the polychaete Capitella jonesi (Hartman, '59) have been described. The ovaries are paired, sac-like follicles suspended by mesenteries in the ventral coelom throughout the midbody region of the mature worm. Oogenesis is unsynchronized and occurs entirely within the ovary, where developing gametogenic stages are segregated spatially within a germinal and a growth zone. Multiplication of oogonia and differentiation of oocytes into the late stages of vitellogenesis occur in the germinal region of the ovary, whereas late-stage vitellogenic oocytes and mature eggs are located in a growth zone. Follicle cells envelop the oocytes in the germinal zone of the ovary and undergo hypertrophy and ultrastructural changes that correlate with the onset of vitellogenesis. These changes include the development of extensive arrays of rough ER and numerous Golgi complexes, formation of microvilli along the surface of the ovary, and the initiation of extensive endocytotic activity. Oocytes undergo similar, concomitant changes such as the differentiation of surface microvilli, the formation of abundant endocytotic pits and vesicles along the oolemma, and the appearance of numerous Golgi complexes, cisternae of rough ER, and yolk bodies. Yolk synthesis appears to occur by both autosynthetic and heterosynthetic processes involving the conjoined efforts of the Golgi complex and rough ER of the oocyte and the probable addition of extraovarian (heterosynthetic) yolk precursors. Evidence is presented that implicates the follicle cells in the synthesis of yolk precursors for transport to the oocytes. At ovulation, mature oocytes are released from the overy after the overlying follicle cells apparently withdraw. Bundles of microfilaments within the follicle cells may play a role in this withdrawal process.

An ultrastructural study of spermatogenesis in the nudibranch mollusc Spurilla neapolitana.

The ultrastructural features of spermatogenesis were investigated in the nudibranch mollusc Spurilla neapolitana. Sperm develop in the proximal half of numerous sac-like acini which are radially arranged within about ten ovotestis lobes. Accessory cells line the inner wall of the testicular portion of each acinus and are connected to developing sperm by numerous desmosomes. Stages of spermatid development have been divided into precup, cup, postcup, and elogate stages depending on the general shape of the nucleus. Nuclear differentiation includes the formation of anterior and posterior nuclear plaques, condensation of chromatin fibrils into nuclear lamellae, the insertion of the developing flagellar axoneme into a shallow, nuclear implantation fossa, and eventual formation of an elongated sperm head with a terminal twist. Spermiogenesis also includes the differentiation of an anterior, perinuclear structure having the characteristics of an acrosome, the appearance of peculiar arrays of ER cisternae, and the fusion of mitochondria into a large mitochondrial derivative which eventually encircles the axoneme, forming a crystalline-like periaxonemal sheath.