Structure of ovarioles in Adelges laricis, a representative of the primitive aphid family Adelgidae

The structure of ovaries has been analysed in advanced aphids only. In this paper we report the results of ultrastructural studies on the ovarioles of Adelges laricis, a representative of the primitive aphid family, Adelgidae. The ovaries of the studied species are composed of five telotrophic‐meroistic ovarioles that are subdivided into a terminal filament, tropharium (= trophic chamber) and vitellarium. The tropharium houses trophocytes (= nurse cells) and arrested oocytes. The vitellarium consists of one or two ovarian follicles. The total number of germ cells (trophocytes + oocytes) in the ovarioles analysed varies from 50 to 92 and is substantially higher than in previously studied aphids. The centre of the tropharium is occupied by a cell‐free region, termed a trophic core, which is connected both with trophocytes and oocytes. Trophocytes are connected to the core by means of cytoplasmic strands, whereas oocytes by nutritive cords. Both trophic core and nutritive cords are filled with parallel arranged microtubules. In the light of obtained results the anagenesis of hemipteran ovaries is discussed.     

Ovary structure and transovarial transmission of endosymbiotic microorganisms in Marchalina hellenica (Insecta,Hemiptera, Coccomorpha: Marchalinidae)

Szklarzewicz, T., Kalandyk‐Kolodziejczyk, M., Kot, M. and Michalik, A. 2011. Ovary structure and transovarial transmission of endosymbiotic microorganisms in Marchalina hellenica (Insecta, Hemiptera, Coccomorpha: Marchalinidae). —Acta Zoologica (Stockholm) 00 :1–9. The paired ovaries of Marchalina hellenica are composed of about 200 ovarioles of telotrophic type. In each ovariole, a trophic chamber, vitellarium and ovariolar stalk can be distinguished. The tropharia comprise trophocytes and early previtellogenic oocytes (termed arrested oocytes) or trophocytes only. The arrested oocytes are not capable of further development. In the vitellaria, single oocytes develop that are connected to the tropharium by means of broad nutritive cords. The number of germ cells (trophocytes and oocytes) constituting ovarioles is not constant and may range between 25 and 32. Numerous endosymbiotic bacteria occur in the cytoplasm of trophocytes. The endosymbionts are transported via nutritive cords to the developing oocyte. The obtained results are discussed in a phylogenetic context.     

Effects of pyrimidine-2-thiol on the ovarian histology of Epilachna vigintioctopunctata (Fabr.) (Coleoptera: Coccinellidae)

The telotrophic ovary of Epilachna vigintioctopunctata is composed of 32-40 ovarioles, each with an apical germarium and a basal vitellarium. The germarium encloses mononucleate and binucleate trophocytes, prefollicular tissue and oogonia, while the vitellarium contains 2-5 oocytes arranged in order of maturity. Definite nutritive cords are absent. When females are exposed to 75 mg 4,4,6-trimethyl-1h, 4H-pyrimidine-2-thiol by contact, the trophocytes and the follicular epithelial cells disintegrate to form dark-staining clumps and thus fail to supply nourishment to the developing oocytes, which consequently remain yolk-less and are ultimately reduced to shrunken masses.     

Microsporidia infect the Liophloeus lentus (Insecta, Colepotera) ovarioles, developing oocytes and eggs

In the ovarioles of Liophloeus lentus (Insecta, Coleoptera, Curculionidae) two types of bacteria and parasitic microorganisms belonging to Microsporidia have been found. This study shows that the different microsporidian life stages (meronts, sporonts, sporoblasts and spores) infect the outer ovariole sheath, trophic chambers, follicular cells, late previtellogenic and vitellogenic oocytes and eggs. In trophic chambers the parasites are very abundant and are distributed unevenly, i.e. their large mass occupies the syncytial cytoplasm between the nurse cell nuclei, whereas the neck region of the trophic chamber (which houses young oocytes, prefollicular cells and trophic cords) is almost free of parasites. The developing oocytes and eggs contain a lower number of parasites which are usually distributed in the cortical ooplasm. The gross morphology of the ovaries is similar in infected and non-infected specimens. Similarly, the presence of a parasite seems to not disturb the course of oogensis. The only difference was found in the ultrastructure of mitochondria in young previtellogenic oocytes. In the infected females they are unusual i.e. bigger and spherical with tubullar cristae, whereas in the non-infected insects they are elongated and have lamellar cristae. As oogenesis progresses the unusual mitochondria rapidly change their morphology and become similar to the mitochondria in non-infected females. Taking into account the distribution of parasites within the ovarioles, it is suggested that they infect growing oocytes via outer ovariole sheath and follicular epithelium rather than via trophic cords.     

Heteropteran ovaries: variations on the theme

Ovaries of heteropterans consist of telotrophic meroistic ovarioles that are composed of apically located tropharium and basal vitellarium, containing developing oocytes. The tropharium (trophic chamber) houses trophocytes (nurse cells) that are connected with the centrally located trophic core. The organization of the heteropteran tropharia is highly variable and differs in representatives of primitive versus advanced families. The differences concern the mitotic activity of the apical nurse cells, organization of the trophocytes (individual cells or "syncytial lobes"), their connection with the trophic core and the development of F-actin meshwork around the trophic core. In members of primitive taxa of the Heteroptera, tropharia are composed of individual, usually mononucleate trophocytes. On the contrary, tropharia in advanced heteropterans are built of large "cytoplasmic lobes" that contain several trophocyte nuclei. Mitotic divisions of the trophocytes in the apical part of the trophic chamber are observed in most bugs (except Dipsocoridae, Miridae and Cimicidae). Tropharia of Miridae represent an entirely different organization (they are built of one type of highly polyploid trophocytes). Anagenesis of heteropteran trophic chamber is discussed in the context of presented data.     

Structure of the ovaries and oogenesis in Cixius nervosus (Cixiidae), Javesella pellucida and Conomelus anceps (Delphacidae) (Insecta, Hemiptera, Fulgoromorpha)

Ovary organization in representatives of two families of Fulgoromorpha, Cixiidae (Cixius nervosus) and Delphacidae (Javesella pellucida and Conomelus anceps), was examined by light and transmission electron microscopy. Ovaries of studied fulgoromorphans consist of telotrophic ovarioles. From apex to base individual ovarioles have four well defined regions: a terminal filament, tropharium (trophic chamber), vitellarium and pedicel (ovariolar stalk). Tropharia are not differentiated into distinct zones and consist of syncytial lobes containing multiple trophocyte nuclei embedded in a common cytoplasm. Lobes are radially arranged around a branched, cell-free trophic core. Early previtellogenic (arrested) oocytes and prefollicular cells are located at the base of the tropharium. The vitellarium houses linearly arranged developing oocytes each of which is connected to the trophic core by a broad nutritive cord. Each oocyte is surrounded by a single layer of follicular cells that become binucleate at the beginning of vitellogenesis.     

Vitellogenesis in the milkweed bug,Oncopeltus fasciatus Dallas (Hemiptera). A light and electron microscopic investigation

Histochemical and electron microscopic methods have revealed that there are four types of cell inclusions in the late vitellogenic oocytes of Oncopeltus. (a) Type 1 is a vacuole which seems to be contributed from the tropharium via the nutritive tubes. It is suggested that this type consists partly at least of nucleolus-like material (ribonucleoprotein) emitted from the nuclei of the Zone III trophocytes. (b) Type 2 is lipid yolk which in early stage oocytes seems to be produced in the “Balbiani body.” In the vitellogenic oocytes these lipid spheres are apparently imported by the oocyte from the haemolymph either through the follicle cells, or through the extracellular space in the follicular epithelium. (c) Type 3 is carbohydrate/protein yolk where at least part of the protein (“vitellogenic protein”) is taken up from the haemolymph, transported through the extracellular space in the follicular epithelium, and deposited into the oocyte by pinocytosis. (d) Glycogen is deposited from the early phases of vitellogenesis. The tropharium may contribute, besides Type 1 vacuoles, ribosomes, mitochondria, stacks of annulated lamellae, and “food vacuoles” to the oocytes. Specialized cells which line the tropharium and send projections toward the trophic core have been called “peripheral trophocytes.” Contrary to the regular trophocytes, they contain glycogen and an abundance of Golgi complexes.     

Morphological and histochemical studies on oogenesis in Callosobruchus analis Fabr. (Bruchidae-Coleoptera)

The ovary in Callosobruchus analis consists of telotrophic ovarioles with the so called nurse cells confined to one chamber at the anterior end of the ovariole. There are three types of lipids in the ovary: (1) L₁ bodies that are present in the early oocytes, in the posterior prefollicular tissue and in the follicular epithelium and contain unsaturated phospholipids; (2) L₂ bodies that have a complete or incomplete sheath of phospholipids and a triglyceride core; (3) L₃ bodies that are formed of highly saturated triglycerides. Lipids are absent from the trophic tissue. In a mature oocyte the L₁ and L₂ bodies are cortical in distribution while the L₃ bodies are centrally located. The mitochondria contain lipoproteins with RNA. The yolk spheres are acid mucopolysaccharides and protein in nature. The precursors of the yolk spheres appear first in the cortical coplasm and are absent from the follicular epithelium or the trophic tissue. The nucleolus of the oocyte shows evidence of extrusions that are believed to pass into the ooplasm. There are no nutritive cords connecting the trophic tissue to the oocytes; nor is there any evidence of any histochemically demonstrable nutritive material being contributed to the oocyte by the trophic tissue. The circumstantial evidence points towards a contribution of the raw materials to the oocyte by the haemolymph either through or in between the follicular epithelium in some soluble form or as submicroscopic particles.     

Structure and development of the telotrophic ovariole in ensign scale insects (Hemiptera, Coccomorpha: Ortheziidae)

The paired ovaries of young larva of the 3rd instar of Orthezia urticae are filled with numerous germ cell clusters that can be regarded as ovariole anlagen. Germ cells (cystocytes) belonging to one cluster form a rosette, in the centre of which a polyfusome occurs. Staining with rhodamine-phalloidin has revealed that polyfusomes contain numerous microfilaments. The number of cystocytes per cluster is not stable and varies considerably. The ovaries of older larva become elongated with numerous young ovarioles protruding into the body cavity. The ovarioles are not subdivided into the tropharium and vitellarium. In this stage germ cells differentiate into oocytes and trophocytes (nurse cells). The ovaries of adult females are composed of about 20 (Newsteadia floccosa) or 30 (O. urticae) ovarioles. Their trophic chambers contain trophocytes and arrested oocytes. In the vitellarium, at the given moment, only one oocyte develops. It has been observed that after maturation of the first egg the arrested oocytes may develop.     

Structure of ovaries in ensign scale insects,the most primitive representatives of Coccomorpha (Insecta,Hemiptera)

The ovaries of Orthezia urticae and Newsteadia floccosa are paired and composed of numerous short ovarioles. Each ovariole consists of an anterior trophic chamber and a posterior vitellarium that contains one developing oocyte. The trophic chamber contains large nurse cells (trophocytes) and arrested oocytes. The total number of germ cells per ovariole (i.e., cluster) is variable, but it is always higher than 32 and less than 64. This suggests that five successive mitotic cycles of a cystoblast plus additional divisions of individual cells are responsible for the generation of the cluster. Cells of the trophic chamber maintain contact with the oocyte via a relatively broad nutritive cord. The trophic chamber and oocyte are surrounded by somatic cells that constitute the inner epithelial sheath around the former and the follicular epithelium around the latter. Anagenesis of hemipteran ovarioles is discussed in relation to the findings presented. © 1995 Wiley-Liss, Inc.     

Formation and structure of nutritive cords in telotrophic ovarioles of snake flies (Insecta: Raphidioptera)

Telotrophic ovariole of Raphidia spp. is composed of the anteriorly located terminal filament, tube-shaped tropharium, the vitellarium and the ovariole stalk. The tropharium consists of a central syncytial core surrounded by one cell thick layer of tapetum cells. Early previtellogenic oocytes differentiate at the base of tropharium. Both the oocytes and the tapetum cells are connected with the central syncytium by delicate intercellular bridges. At the onset of previtellogenic growth, the anterior parts of the oocytes become extended and form long cytoplasmic projections--nutritive cords. Each nutritive cord contains numerous microtubules that show no preferential orientation within the cord but diminishing anterior-posterior gradient of distribution. Irregular arrangement of microtubules indicates that this cytoskeletal scaffold does not play any role in directed transport within the ovariole but instead constitutes one of the elements of the structural framework of the nutritive cord. Besides microtubules, the stability of the nutritive cords in Raphidia ovarioles is maintained by the rim-shaped membrane foldings lined with microfilaments.     

Germ cell cluster formation and ovariole structure in viviparous and oviparous generations of the aphid Stomaphis quercus

The developing ovaries of S. quercus contain a limited number of oogonial cells which undergo a series of incomplete mitotic divisions resulting in the formation of clusters of cystocytes. Ovaries of viviparous generations contain 6 to 9 clusters, containing 32 cystocytes each, whereas ovaries of oviparous generations contain 5 clusters containing 45-60 cystocytes. During further development, clusters become surrounded by a single layer of follicular cells, and within each cluster the cystocytes differentiate into oocytes and trophocytes (nurse cells). Concurrently, cysts transform into ovarioles. The anterior part of the ovariole containing the trophocytes becomes the tropharium, whereas its posterior part containing oocytes transforms into the vitellarium. The vitellaria of viviparous females are composed of one or two oocytes, which develop until previtellogenesis. The nuclei of previtellogenic oocytes enter cycles of mitotic divisions which lead to the formation of the embryo. Ovarioles of oviparous females contain a single oocyte which develops through three stages: previtellogenesis, vitellogenesis and choriogenesis. The ovaries are accompanied by large cells termed bacteriocytes which harbor endosymbiotic microorganisms.     

The telotrophic nature of ovarioles of polyphage coleoptera

Summary The ovarian type of 23 families of polyphage Coleoptera has been determined. The ovaries of all species belong to the telotrophic-meroistic type, indicated by nutritive cords connecting oocytes with the trophic tissue. These nutritive cords persist during previtellogenesis and the main part of vitellogenesis. The cytoplasm of the nutritive cords shows the same elements in similar frequencies as they were found in the nurse cell cytoplasm or in the ooplasm of oocytes during previtellogenesis. No indications are found supporting the idea that a reduction of nutritive cords early in ovarian development gives rise to a deviated panoistic ovary. The histological uniformity of nutritive cords among all investigated species as well as the fact that these species are scattered by chance among the polyphage Coleoptera seems to justify the conclusion that all Polyphaga s. str. have telotrophicmeroistic ovarioles. This investigation was supported in part by the Stiftung Volkswagenwerk     

The histology and histochemistry of oogenesis in the water strider, Gerris remigis Say

In each ovariole of Gerris remigis, nurse cells arise by mitotic divisions at the anterior end of the germarium. These cells enlarge as they move posteriorly. This size increase is possibly caused by fusion of cells, but probably by endopolyploidy as well. The nurse cells then establish connections with a central trophic core, which receives the products of subsequent nurse cell degradation. Two possible pathways of nuclear degradation are suggested: one involves the condensation of chromatin within the nucleus; the other, the release of DNA as fine granules into the cytoplasm. Cytoplasmic areas containing such DNA are also rich in proteinaceous granules, but have a meager content of RNA. The remainder of the cytoplasm of the mature nurse cells contains a high concentration of RNA, as do the nucleoli. Posteriorly the trophic core connects via nutritive cords with each developing oocyte in the prefollicular region and in the anterior vitellarium. RNA is apparently contributed to the ooplasm via the trophic stream. Patches of cytoplasmic DNA are present in the young oocytes; the origin and fate of this DNA is uncertain. During early oocyte maturation chromosomal stainability decreases, and the nucleolus enlarges. In previtellogenic stages, numerous proteinaceous bodies appear in association with the nucleolus-chromosome complex. These bodies, like the nucleolus, have only a low RNA content. They may pass to the cytoplasm, but cannot be traced with certainty. During the latter part of this period a complex population of small proteinaceous and lipid preyolk bodies accumulates peripherally in the oocyte. Definitive protein and lipid yolk are probably derived by the enlargement and inward migration of these bodies. The oocytes are each surrounded by a layer of follicle cells proliferated in the prefollicular region. These become binucleate and enlarge as the enclosed oocytes grow and elongate. RNA also increases in the nucleoli and cytoplasm of the follicle cells as they move posteriorly in the vitellarium. There is no evidence of transfer of nucleic acids or protein from the follicle cells to the oocyte. The nurse cells are therefore implicated as the major source of nucleic acids for the maturing oocyte.     

Electron microscopic study of the differentiation and development of trophocytes and oocytes in Gerris najas (Heteroptera).

The differentiation of oogonia and oocytes, and of trophocytes, from undifferentiated germ line cells has been studied in Gerris najas, a pond skater, from the fourth instar to the adult animal. For the first time criteria have been obtained which allow the distinction between poorly differentiated early oogonia and nurse cells. The most important criteria are the size, shape, and structure of nuclei and mucleoli. This is consistent with the different function of these cell types, which is primarily a different nuclear function: meiosis in the oocytes, and RNA synthesis to support the trophic core and the oocytes in the trophocytes.     

Cytochemical studies of oocyte development in Sarcophaga lineatocollis Macq. (Muscidae: Diptera)

The ovary of Sarcophaga lineatocollis is a typical polytrophic ovary. Each of its 25-30 ovarioles is composed of a small terminal filament, a small germarium and a vitellarium consisting of the egg follicle. The tunica propria is a noncellular, PAS-positive membrane. The ovarian follicle contains fifteen trophocytes and one oocyte. RNA is synthesized with the aid of the nuclei in the trophocyte cytoplasm, which are RNA- and PAS-positive. Protein is deposited intensively in the early stages of the trophocytes. The trophocytes of Sarcophaga lineatocollis synthesize RNA and protein more actively than the oocyte. In this fly, protein yolk precursor (PYP) bodies are supplied by the trophocyte cytoplasm to the ooplasm at an advanced stage of development. Nucleolar budding and vacuolation are observed in the trophocytes. RNA, DNA, protein and PYP bodies appear to be transported to the ooplasm from the trophocytes. Pyknotic trophocyte nuclei can be seen entering the ooplasm. The perinuclear Golgi bodies of the trophocytes help in the production and maturation of PYP bodies in the trophocytes before they are organized and passed on to the oocytes. Some RNA is contributed to the oocyte by the follicular epithelium. All these processes leading to maturation and development of the oocyte are discussed and interpreted.     

Structure of ovaries and oogenesis in the snow scorpionfly boreus hyemalis (LINNE)(MECOPTERA : BOREIDAE)

The ovaries of the snow scorpionfly, Boreus hyemalis (Mecoptera : Boreidae) are panoistic and comprise 7–8 ovarioles. Each ovariole consists of a terminal filament, elongated vitellarium, and ovariole stalk (=pedicel) only ; in adult specimens, functional germaria are absent. Five consecutive stages of oogenesis i.e., early, mid- and late previtellogenesis, vitellogenesis, and choriogenesis have been distinguished in imagines. Oocyte nuclei (=germinal vesicles) of previtellogenic oocytes contain numerous polymorphic multiple nucleoli (or nucleolar masses), endobodies, and chromatin aggregations. Next to the nuclear envelope, large accumulations of nuage material are localized. The ooplasm of late previtellogenic oocytes is differentiated into transparent (perinuclear) and opaque (peripheral) regions. Ultrastructural investigations have revealed that within the latter, abundant ribosomes as well as mitochondria, elements of endoplasmic reticulum, Golgi complexes, annulate lamellae, symbiotic bacteroids, lipid droplets and distinctive accumulations of membrane-free clathrin-like cages are present. Early- and mid previtellogenic oocytes are invested with flat somatic cells that gradually transform into a follicular epithelium. In the vicinity of 3-cell junctions, neighbouring follicular cells are joined by narrow intercellular bridges. During late previtellogenesis, numerous microvilli develop on the oocyte surface. They interdigitate with morphologically similar but less frequent microvilli of the follicular cells. Concurrently, first endocytotic vesicles appear in the cortical ooplasm. In the context of presented results, the phylogenetic relationships between mecopterans (boreids) and fleas are discussed.     

3NTPT: a newly discovered antifertility agent. V. Ovarian dysfunction in Dysdercus koenigii.

A 4 h exposure to a residual film of 15 mg 1-(3-nitrophenyl)-4,4,6-trimethyl-1H,4H-pyrimidine-2-thiol (3NTPT) dissolved in 5 ml acetone significantly inhibited ovarian growth in Dysdercus koenigii. The ovaries of treated females remained small and the trophocytes, the trophic core, the prefollicular tissue and the oogonia completely degenerated. This was followed by degenerative changes in the follicular epithelium, the interfollicular tissue and the developing oocytes. Resorption of the oocytes reduced the vitellarium to an empty tube. The follicular epithelium of the resorbed oocytes protruded into the lumen, while the interfollicular tissue completely degenerated. By day 7 after treatment, the ovaries were completely dystrophic, and this state was not reversible.     

Development of nurse cell-oocyte interactions in the insect telotrophic ovary (Rhodnius prolixus)

The establishment and reorganization of intercellular bridges during larval-adult ovarian differentiation is the basis of the syncytial nature of the adult hemipteran telotrophic ovary. The formation, in the late differentiation phase, of groups of closely arranged nurse cell nuclei occupying a common cytoplasm results from membrane fusions. Oocyte-oocyte intercellular bridge systems later are modified to form the trophic cords. The trophic core, which undergoes a restructuring during the late differentiation phase, mediates nurse cell-oocyte interactions in this system. Material, transported to and accumulated by late differentiation phase pre-vitellogenic oocytes, originates from trophic core restructuring and zone III nurse cell production.     

Ovary cord structure and oogenesis in Hirudo medicinalis and Haemopis sanguisuga (Clitellata, Annelida): remarks on different ovaries organization in Hirudinea

In Hirudo medicinalis and Haemopis sanguisuga, two convoluted ovary cords are found within each ovary. Each ovary cord is a polarized structure composed of germ cells (oogonia, developing oocytes, nurse cells) and somatic cells (apical cell, follicular cells). One end of the ovary cord is club-shaped and comprises one huge apical cell, numerous oogonia, and small cysts (clusters) of interconnected germ cells. The main part of the cord contains fully developed cysts composed of numerous nurse cells connected via intercellular bridges with the cytophore, which in turn is connected by a cytoplasmic bridge with the growing oocyte. The opposite end of the cord degenerates. Cord integrity is ensured by flattened follicular cells enveloping the cord; moreover, inside the cord, some follicular cells (internal follicular cells) are distributed among germ cells. As oogenesis progresses, the growing oocytes gradually protrude into the ovary lumen; as a result, fully developed oocytes arrested in meiotic metaphase I float freely in the ovary lumen. This paper describes the successive stages of oogenesis of H. medicinalis in detail. Ovary organization in Hirudinea was classified within four different types: non-polarized ovary cords were found in glossiphoniids, egg follicles were described in piscicolids, ovarian bodies were found characteristic for erpobdellids, and polarized ovary cords in hirudiniforms. Ovaries with polarized structures equipped with apical cell (i.e. polarized ovary cords and ovarian bodies) (as found in arhynchobdellids) are considered as primary for Hirudinea while non-polarized ovary cords and the occurrence of egg follicles (rhynchobdellids) represent derived condition.