The germarium of panoistic ovarioles of Bacillus rossius (Insecta Phasmatodea): Structure and function during imaginal life

Summary

In adult females of Bacillus rossius (Insecta Phasmatodea) the germarium, localized at the ovariole tip just below the terminal filament and above the vitellarium, progressively reduces in size and eventually disappears at the end of the ovulatory period. The observations with light and electron microscopes show that in the end-chamber most germ cells are arrested in a post-pachytenic diffuse stage, which just precedes diplotenic oocyte growth. These observations also indicate that the reduction in size of the germarium of ovulating females should probably be ascribed to a progressive and extensive activation of the resting germ cells. The average number of ovulated eggs per ovariole (6.7±0.9) is consistent with this view. However, occasional findings of lepto-zygotenic germ cells in some preovulatory ovarioles of adult females do not completely rule out the persistence of scarce undifferentiated germ elements (oogonia) in the larval germarium at the onset of adult life. Furthermore, the reduction of the germarium in ovulating females and its subsequent disappearance in post-ovulating ones also includes the somatic cells, which are always present among the germ cells in previous stages. Since each early growing oocyte becomes surrounded by a thin monolayer of follicle cells, the diminution of end-chamber somatic cells supports the view that they actually represent prefollicular cells, which are progressively utilized from the onset of imaginal life onwards.     

Structure of the ovary in Nannochorista neotropica Navás (Insecta: Mecoptera: Nannochoristidae) with remarks on mecopteran phylogeny

Preliminary histological analysis showed that the ovaries in Nannochorista neotropica are composed of numerous ovarioles of panoistic type. In the ovaries of adult females each ovariole consists of a terminal filament, vitellarium and pedicle while a germarium is absent. Morphological observations supported by simple histochemical tests revealed the presence of multiple nucleoli in the oocyte nucleus. The appearance of multiple nucleoli suggests that the extrachromosomal amplification of ribosomal DNA may take place in the oocytes of Nannochorista. The results show that in the structure of the ovariole and the course of oogenesis nannochoristids share noteworthy derived features with boreids, but differ significantly from all other mecopterans. These findings indicate the possible monophyly of an assemblage comprising the Nannomecoptera, Neomecoptera and Siphonaptera.     

Distribution of cytoskeletal elements in the ovarioles of Mutilla sp. (Insecta,Hymenoptera)

The ovaries of Mutilla sp., as those of other hymenopterans, consist of meroistic-polytrophic ovarioles. Within each ovariole, a terminal filament, a germarium, and a vitellarium can be distinguished. The germaria contain numerous dividing and/or differentiating groups (clusters) of germ cells. The vitellaria are composed of several, linearly arranged, ovarian follicles; each follicle consists of an oocyte and a group of nurse cells. Distribution of cytoskeletal elements (microfilaments and microtubules) throughout the ovarioles of Mutilla sp. has been studied on whole mount preparations stained with rhodamine-conjugated phalloidin and FITC-labelled anti-tubulin.     

The ovaries of Mecoptera: basic similarities and one exception to the rule

Two entirely different types of ovaries (ovarioles) have been described in mecopterans. In the representatives of Meropeidae, Bittacidae, Panorpodidae and Panorpidae the ovarioles are of the polytrophic-meroistic type. Four regions: a terminal filament, germarium, vitellarium and ovariole stalk can be distinguished in the ovarioles. The germaria house numerous germ cell clusters. Each cluster arises as a result of 2 consecutive mitoses of a cystoblast and consists of 4 sibling cells. The oocyte always differentiates from one of the central cells of the cluster, whereas the remaining 3 cells develop into large, polyploid nurse cells. The vitellaria contain 7-12 growing egg chambers (= oocyte-nurse cell complexes). In contrast, the ovaries of the snow flea, Boreus hyemalis, are devoid of nurse cells and therefore panoistic (secondary panoistic). The ovarioles are composed of terminal filaments, vitellaria and ovariole stalks only; in adult females functional germaria are absent. Histochemical tests suggest that amplification of rDNA takes place in the oocyte nuclei. Resulting dense nucleolar masses undergo fragmentation into multiple polymorphic nucleoli. The classification of extant mecopterans as well as the phylogenetic relationships between Mecoptera and Siphonaptera are discussed in the context of presented data.     

Reproductive investment and the inter-ovariole differences in embryo development and size in virginoparae of the vetch aphid, Megoura viciae

Apterous virginoparae of the vetch aphid, Megoura viciae Buckton, contain between 13 and 22 ovarioles, and show an interovariole gradation in embryonic development, which is a consequence of anterior ovarioles ovulating first. It persists throughout development and is a consequence of a delay in the onset of ovulation in the posterior ovarioles, rather than a loss of reproductive potential. Up to eight embryos are present in the ovarioles of adults, and there are interovariole differences in size of up to two times between the largest and smallest terminal embryos within individuals. Maternal weight and size of embryos were not significantly associated with the number of ovarioles. Embryos of a particular developmental stage were larger in big (heavy) than small aphids.

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Résumé Le nombre d'ovarioles des M. viciae Buckton virginipares aptères varie de 13 à 22, quel que soit le poids de l'adulte. La taille de l'embryon ne dépend pas du nombre d'ovarioles. Des différences de taille et de développement des embryons comparables existent entre les ovarioles depuis le début de l'activité du termarium jusqu'au début de la reproduction. Les petits pucerons ont de plus petits embryons que les gros pucerons et le nombre d'embryons par ovariole augmente avec la taille jusqu'à un poids maximal. Les ovarioles antérieurs contiennent plus d'embryons bien développés que les ovarioles les plus postérieurs, par suite de l'ovulation plus précoce du germarium le plus antérieur.

     

Female reproductive system of the first-instar nymphs of Machilis helleri (verh.) (Thysanura : Machilidae) with special reference to the segmental arrangement of ovarioles in arthropods

The anatomy, histology and ultrastructure of immature ovarioles of the 1st-instar nymphs of Machilis helleri (Thysanura : Machilidae) are described. The nymphs have 7 pairs of segmentally arranged panoistic ovariole primordia in which the germarium and previtellarium can be distinguished. The germarium contains oogonia, young oocytes, and prefollicular cells. The previtellarium is filled with previtellogenic oocytes, prefollicular cells, and a pyramid-like group of somatic cells representing the primordium of the pedicel and oviduct. The ultrastructure of individual types of cells correlates to a great extent with the respective cells of ovarioles of adult machilids. Oogonia undergo mitosis in the germarium and transform into young oocytes. These grow and develop into previtellogenic oocytes characterized by changes in the nucleolus and by emission of ribonucleoproteinaceous bodies from the nucleus into cytoplasm. Segmental arrangement of ovarioles in Archaeognatha is discussed in view of contemporary hypotheses on the anagenesis of the reproductive system of Articulata.     

Morphology of the ovaries of Sphaerodema (Diplonychus) rusticum (Heteroptera,Belostomatidae)

The female reproductive system of Sphaerodema rusticum consists of a pair of ovaries, two lateral oviducts, a median common oviduct, and a median spermatheca. Accessory glands are absent. Each ovary has five free ovarioles branching from the oviduct. Each ovariole consists of a terminal filament, germarium, vitellarium, brown mass, and an exceptionally long pedicel. The terminal filament consists of a central core, interstitial cells, and an outer sheath. In the germarium, which consists of trophic and prefollicular regions, the trophic region or nurse cell chamber is divided into four histologically differentiated zones, distinguished as zones I–IV. Nutritive cords, originating from the posterior end of the trophic core in zone IV extend centrally and join the developing oocytes in the prefollicular chamber and the vitellarium. The compact prefollicular tissue at the base of the trophic core gives rise to prefollicular cells which, after encircling the young oocytes, become modified into follicular epithelial cells, the interfollicular plug, and epithelial plug. The young oocytes descend into the vitellarium and gradually develop into mature oocytes. A compound corpus luteum is observed simultaneously in all the ovarioles of both ovaries after ovulation. Below the epithelial plug there is an accumulation of material, the “brown mass,” which develops cyclically in correlation with the ovulation cycle. Each pedicel stores five mature chorionated eggs ready for oviposition. The epithelium of the anterior region of the pedicel secretes a PAS-positive material. General morphology and histology of the subdivisions of the ovarioles are described.     

Structure of the ovaries of the primitive aphids Phylloxera coccinea and Phylloxera glabra (Hemiptera,Aphidinea: Phylloxeridae)

Ovaries of phylloxerids consist of short telotrophic ovarioles. Ovaries of wingless morphs contain four ovarioles whereas those of winged morphs contain one or two ovarioles. The individual ovariole of the adult female is differentiated into a terminal filament, trophic chamber (tropharium), vitellarium and short ovariole stalk (pedicel). The number of germ cells constituting ovarioles is not stable and ranges between 49 and 64. The tropharia enclose individual trophocytes and arrested oocytes. The vitellaria contain usually two oocytes, which develop through three stages: previtellogenesis, vitellogenesis and choriogenesis. Endosymbiotic microorganisms do not occur in the germ cells. In the light of the obtained results, the phylogenetic relationships between aphid families are discussed.     

Development of terminal filaments and ovariole envelopes in Thermobia domestica (Insecta, Zygentoma) larvae

The 3rd instar female larvae of Thermobia domestica have five pairs of gonad primordia, each enclosed within a basal lamina (tunica propria). At the end of the 3rd instar some somatic cells scattered on the outer surface of the lamina are seen. During the 4th larval instar the gonad primordia start to form the ovarioles. Each ovariole is elongated and polarized, having anterior and posterior ends. The anterior group of outer somatic cells proliferate to form the terminal filament. At the 6th larval stage the ovarioles are already formed. The terminal filament is separated from the germarium by a thick basal lamina (transverse septum). There are three types of cell building the terminal filament. 1/Basal cells with numerous fingerlike projections; 2/Cells with electron lucent cytoplasm and large nuclei, and 3/Cells with darker cytoplasm containing bundles of fibers and more compact nuclei. The outer surface of the filament is covered by a thick, fibrous basal lamina. The somatic cells that in the previous stages were scattered on the tunica propria as distinct cells, in the 6th larval stage form a cellular envelope (tunica externa). This envelope is formed by a layer of flat cells, and contains numerous tracheae.     

Cyst geometry in the egg chambers of Calliphora erythrocephala Mg. (Diptera: Calliphoridae) ovaries

In the germarium of polytrophic ovarioles of Calliphora erythrocephala (Mg.) fly, four mitotic divisions of cystoblasts give rise to 16-cell germ-line cysts. One cell differentiates into an oocyte, while the remaining 15 cells become nurse cells. Concomitantly actin-rich ring canals are formed at the intercellular junctions. The present study considers a mutual arrangement of the ring canals formed after the second to fourth mitoses relative to the ring canal formed after the first mitotic division in different regions of the germarium and egg chambers. During the cyst formation and its movement to the posterior end of the germarium, the ring canals are displaced relative to one another, thereby giving different branching variants of the cyst. The pattern of cell interconnections becomes stable in germarium region 2b and does not change during the cyst movement along the ovariole despite the cyst polarizes and increases in size.     

Structure of the ovary and the differentiation of follicular epithelium in the pig louse, Haematopinus suis (Insecta: Phthiraptera)

The female reproductive system of the pig louse, Haematopinus suis (Insecta: Phthiraptera) is composed of paired ovaries, lateral oviducts, and a common oviduct that leads into a vagina. Clusters of mycetocytes (= cells filled with symbiotic organisms) are associated with lateral oviducts. Each ovary is composed of five loosely arranged ovarioles of the polytrophic-meroistic type. An individual ovariole is covered by a basal lamina and is composed of a terminal filament, germarium, and vitellarium. The terminal filament is composed of large, disc-shaped cells that are orientated perpendicularly to the long axis ofthe ovariole. The basal part of the terminal filament is separated from the germarium by a well-developed transverse septum. The germarium is short and filled with clusters of oogonial cells. In each cluster the cells arejoined by intercellular bridges, filled with fusomal material. Within the cluster, only one cell, the future oocyte, enters the prophase of the first meiotic division; the other cells differentiate into nurse cells. The basal part ofthe germarium is filled with the somatic prefollicular cells. The boundary between the germarium and the vitellarium is not distinct. The vitellarium contains linearly arranged ovarian follicles in subsequent stages of oogenesis (previtellogenesis, vitellogenesis and choriogenesis). Each follicle consists of an oocyte and 7 nurse cells and is surrounded by follicular cells. During oogenesis the follicular cells diversify, so that ultimately, five morphologically distinct subpopulations of these cells can be distinguished: (1) cells in contact with the nurse cells, (2) anterior cells, (3) mainbody cells, (4) posterior cells, and (5) interfollicular cells. Interestingly, the follicular cells associated with the anterior part of the oocyte, i.e. located in space at the oocyte/nurse cell border (fold cells) are mitotically active throughout previtellogenesis. It might be suggested, in this context, that the separation of the oocyte from the nurse cell compartment is brought about by mitotic divisions, consequent multiplication and centripetal migration of these cells.     

Cell death in ovarioles causes permanent sterility in Frieseomelitta varia worker bees

Frieseomelitta varia worker bees do not lay eggs even when living in queenless colonies, a condition that favors ovary development and oviposition in the majority of highly social bees. The permanent sterility of these worker bees was initially attributed to a failure in ovary morphogenesis and differentiation. Using transmission electron microscopy we found that at the beginning of the pupal phase the ovaries of F. varia workers are formed by four ovarioles, each of them composed of 1) a terminal filament at the apex of the ovarioles, containing juxtaposed and irregularly shaped cells, 2) a germarium with clusters of cystocytes and prefollicular cells showing long cytoplasmic projections that envelop the cystocyte clusters, 3) fusiform interfollicular and basal stalk precursor cells, and 4) globular, irregularly contoured basal cells with large nuclei. However, during the pupal phase an accentuated and progressive process of cell death takes place in the ovarioles. The dying cells are characterized by large membrane bodies, electron-dense apoptotic bodies, vacuoles, vesiculation, secondary lysosomes, enlarged rough endoplasmic reticulum cisternae, swollen mitochondria, pycnotic nuclei, masses of chromatin adjacent to the convoluted nuclear envelope, and nucleoli showing signs of fragmentation. Cell death continues in ovarioles even after the emergence of the workers. Once they become nurse bees, the ovaries have become transformed into a cell mass in which structurally organized ovarioles can no longer be identified. In F. varia workers, ovariole cell death most certainly is part of the program of caste differentiation.     

The trophic tissue of telotrophic ovarioles in polyphage coleoptera

Summary The trophic tissue of ovarioles of 32 species of polyphage Coleoptera was investigated by light and electron microscopy. Ovaries were compared according to the number of ovarioles, length, width, and volume of the terminal chambers, to the number, diameter, and volume of nurse cell nuclei, as well as to the structure of nurse cell cytoplasm and to the structure of interstitial cells. Mitosis of nurse cells or interstitial cells in fully developed ovarioles was never observed, but there is strong evidence for endomitosis in nurse cells. According to the different extent of reduction of nurse cell membranes in ovarioles of diverse species, three basic types of nurse cell organization could be established, representing tissues of a primary stage, transition stage, or secondary stage, respectively. These different forms of nurse cell organization are family-specific and correspond to ontogenetic stages of ovariole development ofBruchidius, which is a highly developed polyphage beetle. The distribution among the investigated families is consistent with the phylogenetic relationships among polyphage Coleoptera as far as they are known today. There is evidence that more highly organized nurse cell tissues have evolved independently from primary stage tissues in at least two cases. This investigation was supported in part by the Stiftung Volkswagenwerk     

Ultrastructural studies of the ovary of Palaeococcus fuscipennis (Burmeister) (Insecta, Hemiptera, Coccinea: Monophlebidae)

Ovaries of Palaeocoocus fuscipennis are composed of about 100 telotrophic ovarioles that are devoid of terminal filaments. In the ovariole a tropharium ( = trophic chamber) and vitellarium can be distinguished. The tropharium contains 7 trophocytes. A single oocyte develops in the vitellarium. The oocyte is surrounded by follicular cells that do not undergo diversification into subpopulations. The obtained results are discussed in a phylogenetic context.     

A very simple mode of follicular cell diversification in Euborellia fulviceps (Dermaptera, Anisolabididae) involves actively migrating cells

The ovaries of Euborellia fulviceps are composed of five elongated ovarioles of meroistic-polytrophic type. The individual ovariole has three discernible regions: the terminal filament, germarium, and vitellarium. The terminal filament is a stalk of flattened, disc-shaped somatic cells. In the germarium, germline cells in subsequent stages of differentiation are located, and the vitellarium comprises numerous ovarian follicles arranged linearly. The individual ovarian follicles within the vitellarium are separated by prominent interfollicular stalks. The follicles are composed by two germline cells only: an oocyte and a single, polyploid nurse cell, which are surrounded by a monolayer of somatic follicular cells (FCs). During subsequent stages of oogenesis, initially uniform follicular epithelium begins to diversify into morphologically and physiologically distinct subpopulations. In E. fulviceps, the FC diversification mode is rather simple and leads to the formation of only three different FC subpopulations: (1) cuboidal FCs covering the oocyte, (2) stretched FCs surrounding the nurse cell and (3) FCs actively migrating between oocyte and a nurse cell. We found that FCs from the latter subpopulation send long and thin filopodium-like and microtubule-rich processes penetrating between the oocyte and nurse cell membranes. This suggests that, in E. fulviceps, cells from at least one FCs subpopulation show the ability to change position within an ovarian follicle by means of active migration.     

The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes

Neither the overall differences in ovariole number nor the caste-specifically modulated expression of vitellogenin can fully explain the striking caste differences in honey bee reproduction, in particular the mechanisms that block oogenesis in virgin queens and in workers kept in the presence of a queen. For this reason we investigated the initial stages of oogenesis in queens in relation to mating status and in workers exposed to different social conditions. A striking feature in ovarioles of both castes was a considerably elongated terminal filament which consisted not only of normal terminal filament cells but also contained apparently undifferentiated cells that were tentatively considered as stem cells. BrdU incorporation was detected in the upper germarium, as well as in the terminal filament. Cytoskeleton analysis by TRITC-phalloidin labeling for F-actin, and immunofluorescence detection for β-tubulin did not reveal structural differences in the early oogenesis steps between queens and queenless workers. In contrast, queenright workers showed signs of a disorganized microtubule and microfilament system that could explain the histological evidence for progressive cell death observed in the germaria. In addition to cytoplasmic tubulin we also detected marked intranuclear foci indicating the presence of nuclear β_II-tubulin.     

Structure of the female reproductive system of the lac insect,Kerria chinensis (Sternorrhyncha,Coccoidea: Kerridae)

The ovaries of female lac insects, Kerria chinensis Mahd (Sternorrhyncha: Coccoidea: Kerridae), at the last nymphal stage are composed of several balloon‐like clusters of cystocytes with different sizes. Each cluster consists of several clusters of cystocytes arranging in rosette forms. At the adult stage, the pair of ovaries consists of about 600 ovarioles of the telotrophic‐meroistic type. An unusual feature when considering most scale insects is that the lateral oviducts are highly branched, each with a number of short ovarioles. Each ovariole is subdivided into an anterior trophic chamber (tropharium) containing six or seven large trophocytes and a posterior vitellarium harbouring one oocyte which is connected with the trophic chamber via a nutritive cord. No terminal filament is present. Late‐stage adult females show synchronized development of the ovarioles, while in undernourished females, a small proportion of ovarioles proceed to maturity.     

Habitat quality and reproductive investment in aphids

ABSTRACT.

• 1 Genetically identical vetch aphids, Megoura viciae (Buckton), showed a weak but significant positive relationship between reproductive investment (number of ovarioles) and weight, here used as an indicator of habitat quality.
• 2 Apterae reared on poor quality plants showed the same range in numbers (twelve to twenty-two) but on average fewer ovarioles than those reared on high quality plants.
• 3 The variability in ovariole number was determined prior to birth.
• 4 Under constant conditions the age of a mother does not affect the range of ovariole numbers or the proportion of her offspring in each ovariole class.
• 5 Apterae reared on poor quality host plants gave birth to proportionately fewer offspring with a high ovariole number than apterae reared on high quality plants.
• 6 Winged individuals gave birth to proportionately more offspring with a high number of ovarioles than apterae.
• 7 The control and ecological significance of the intramorph variation in reproductive tactics shown by many species of aphids is discussed in the light of these results.

     

Inhibition of reproduction and embryogenesis in the firebrat, Thermobia domestica, by juvenile hormone analogues

Application of compounds with juvenile hormone (JH) activity to reproducing females may result in shortening of the ovipositor and occasionally in some other changes in appearance. Severe defects occur in the ovaries: the differentiation of oögonia and prefollicular cells seems to be hindered and the mature oöcytes are resorbed. The affected ovarioles diminish and in extreme cases tear into the germarium, which remains attached to the terminal filament, and the rest of the ovariole, which shrinks into a small rudiment adjacent to the oviduct. The development of eggs deposited by treated females is often lethally affected. Disorders in embryogenesis also occur in the eggs contaminated with active substances at any time between deposition and 2 days before hatching. The substances interrupt the normal course of embryogenesis but the embryos survive for some time and may develop into strange creatures; in one case, two embryos were found within a single egg shell. One out of 27 tested substances was active in amounts lower than 1 ng/egg.