Structure and development of ovaries in the weevil, Anthonomus pomorum (Coleoptera, Polyphaga). I. Somatic tissues of the trophic chamber

In developing ovarioles of Anthonomus pomorum (Coleoptera, Polyphaga, Curculionidae) the trophic chambers (tropharia) are relatively large and consist of clusters (clones) of germ cells and various somatic tissues. Each ovariole is enclosed within an outer epithelial sheath (tunica externa). Throughout the pupal phase, the growth of this sheath is accelerated and precedes the development of the rest of the ovariole. As a result, the epithelial sheath proliferates anteriorly and forms an elongated "sleeve" that during the later stages of development becomes gradually filled by the growing tropharium. In the early pupal stage, a few terminal filament cells are observed in contact with the anterior end of the tropharium. These cells are separated from the rest of the trophic chamber by a transverse septum, which maintains continuity with the basal lamina. Beneath the basal lamina there is a layer of inner sheath cells, whereas inside the tropharium there are interstitial cells. These two types of cell differ morphologically in a mature ovary but they retain, until the end of the imago-B stage, a similar ultrastructure testifying to their common origin. At the posterior end of the tropharium, from the imago-B stage on, many young oocytes, surrounded by prefollicular cells, are observed. This is the so-called neck region of the tropharium. Extraction with Triton X-100 detergent showed that in a mature trophic chamber there are only individual microtubules arranged along the projections of interstitial cells. This indicates that the cytoskeleton elements (microfilaments and microtubules) participate only to a very limited extent in the spatial organisation of the tropharium in A. pomorum.     

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.     

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.     

Structure of ovaries of scale insects: ii. margarodidae (INSECTA,hemiptera, COCCINEA)

The paired, spindle-shaped ovaries of the second instar of the Polish cochineal, Porphyrophora polonica (L.) (Hemiptera: Coccinea) are filled with cystocytes that are arranged into rosettes. In the centre of each rosette, there is a polyfusome. During the third instar, cystocytes differentiate into oocytes and trophocytes (nurse cells) and ovarioles are formed. Ovaries of adult females are composed of about 300 ovarioles of the telotrophic type. Each of them is subdivided into a tropharium (trophic chamber) and vitellarium. The tropharium consists of trophocytes and arrested oocytes that may develop. The number of germ cells in the trophic chambers varies from 11 to 18 even between the ovarioles of the same ovary. The obtained results seem to confirm the concept of a monophyletic origin of the primitive scale insects (Archaeococcoidea).     

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.     

The ovaries of aphids (Hemiptera,Sternorrhyncha, Aphidoidea): morphology and phylogenetic implications

The ovaries of aphids belonging to the families Eriosomatidae, Anoeciidae, Drepanosiphidae, Thelaxidae, Aphididae, and Lachnidae were examined at the ultrastructural level. The ovaries of these aphids are composed of several telotrophic ovarioles. The individual ovariole is differentiated into a terminal filament, tropharium, vitellarium, and pedicel (ovariolar stalk). Terminal filaments of all ovarioles join together into the suspensory ligament, which attaches the ovary to the lobe of the fat body. The tropharium houses individual trophocytes and early previtellogenic oocytes termed arrested oocytes. Trophocytes are connected with the central part of the tropharium, the trophic core, by means of broad cytoplasmic processes. One or more oocytes develop in the vitellarium. Oocytes are surrounded by a single layer of follicular cells, which do not diversify into distinct subpopulations. The general organization of the ovaries in oviparous females is similar to that of the ovaries in viviparous females, but there are significant differences in their functioning: (1) in viviparous females, all ovarioles develop, whereas in oviparous females, some of them degenerate; (2) the number of germ cells per ovariole is usually greater in females of the oviparous generation than in females of viviparous generations; (3) in oviparous females, oocytes in the vitellarium develop through three stages (previtellogenesis, vitellogenesis, and choriogenesis), whereas in viviparous females, the development of oocytes stops after previtellogenesis; and (4) in the oocyte cytoplasm of oviparous females, lipid droplets and yolk granules accumulate, whereas in viviparous females, oocytes accrue only lipid droplets. Our results indicate that a large number of germ cells per ovariole represent the ancestral state within aphids. This trait may be helpful in inferring the phylogeny of Aphidoidea.     

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.     

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.     

Morphology of female reproductive system of Mediterranean flatheaded peachborer,Capnodis tenebrionis (Linnaeus, 1761) (Coleoptera: Buprestidae)

Capnodis tenebrionis causes damage in many species of Rosaceae. The present study investigates on the morphology of the female reproductive system of C. tenebrionis. The female reproductive system of C. tenebrionis has a pair of ovaries, lateral oviducts, a common oviduct, spermatheca, and bursa copulatrix. Each ovary in C. tenebrionis consists of approximately 24 telotrophic meroistic type ovarioles. The ovarioles of C. tenebrionis have four regions (terminal filament, tropharium, vitellarium, and pedicel). Tropharium have trophocytes, young oocytes, and prefollicular cells. Vitellarium consists of previtellogenic, vitellogenic, and choriogenic oocytes. Previtellogenic oocyte is surrounded by cylindrical epithelial cells. Its ooplasm is homogeneous and basophilic. In vitellogenic oocyte, there are intercellular spaces between monolayered follicle cells. Its ooplasm has yolk granules and lipid droplets. Choriogenic oocyte are surrounded by chorion and single-layered cylindrical cells. There are yolk granules and lipid droplets in its ooplasm which is asidophilic. In C. tenebrionis female, spermatheca and bursa copulatrix wall is surrounded by thin cuticular intima, monolayer epithelial, glandular cells, and muscle layer. Spermatheca lumen contains a large number of spermatozoa. Bursa copulatrix lumen is filled with secretory material. This study may be useful in terms of the morphology of mature female reproductive organs of Buprestidae and other coleopteran species.     

Ultra- and microstructure of the female reproductive system of Matsucoccus matsumurae

The ultra- and microstructure of the female reproductive system of Matsucoccus matsumurae was studied using light microscopy, scanning and transmission electron microscopy. The results revealed that the female reproductive system of M. matsumurae is composed of a pair of ovaries, a common oviduct, a pair of lateral oviducts, a spermatheca and two pairs of accessory glands. Each ovary is composed of approximately 50 telotrophic ovarioles that are devoid of terminal filaments. Each ovariole is subdivided into an apical tropharium, a vitellarium and a short pedicel connected to a lateral oviduct. The tropharium contains 8–10 trophocytes and two early previtellogenic oocytes termed arrested oocytes. The trophocytes degenerate after egg maturation, and the arrested oocytes are capable of further development. The vitellarium contains 3–6 oocytes of different developmental stages: previtellogenesis, vitellogenesis and choriogenesis. The surface of the vitellarium is rough and composed of a pattern of polygonal reticular formations with a center protuberance. The oocyte possesses numerous yolk spheres and lipid droplets, and is surrounded by a mono-layered follicular epithelium that becomes binucleate at the beginning of vitellogenesis. Accessory nuclei are observed in the peripheral ooplasm during vitellogenesis.     

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.     

The ovaries of Cicadomorpha: distribution of microfilaments and microtubules in terminal filament cells

The ovaries of the investigated homopterans are telotrophicmeroistic and consist of several (7-21 ) ovarioles. Each ovariole is composed of three elements: an anteriorly localized terminal filament, a tropharium, and a posterior vitellarium. The latter comprises several developing ovarian follicles in a linear arrangement. The terminal filaments are relatively solid and composed of two distinct types of cells: the apical cells (ApCs) and the basal cells (BaCs). The BaCs are disc-shaped and oriented perpendicularly to the long axis of the ovariole, whereas the ApCs are strongly elongated and arranged parallel to this axis. The distribution of cytoskeletal elements has been studied with the use of electron microscope and histochemical methods. We show that the ApCs house prominent bundles of highly ordered microfilaments and/or parallel arranged microtubules. In contrast, BaCs contain only individual microtubules that are predominantly located in peripheral regions of the cells. It is suggested that microfilaments and microtubules present in the ApCs are responsible for the mechanical rigidity of the terminal filaments.     

The telotrophic ovary known from Neuropterida exists also in the myxophagan beetle <Emphasis Type="Italic">Hydroscapha natans</Emphasis>

The ovary structure of the myxophagan beetle, Hycdoscapha natans, was investigated by means of light and electron microscopy for the first time. Each of the two ovaries consists of three ovarioles, the functional units of insect oogenesis. The ovary type is telotrophic meroistic but differs strongly from the telotrophic ovary found among all polyphagous beetles investigated so far. All characters found here are typical of telotrophic ovaries of Sialidae and Raphidioptera. Both taxa belong to the Neuropterida. As in all telotrophic ovaries, all nurse cells are combined in an anterior chamber, the tropharium. The tropharium houses two subsets of germ cells: numerous nurse cell nuclei are combined in a central syncytium without any cell membranes in between, surrounded by a monolayer of single-germ cells, the tapetum cells. Each tapetum cell is connected to the central syncytium via an intercellular bridge. Tapetum cells of the posterior zone, which sufficiently contact prefollicular cells, are able to grow into the vitellarium and develop as oocytes. During previtellogenic and early vitellogenic growth, oocytes remain connected with the central syncytium of the tropharium via their anterior elongations, the nutritive cords. The morphological data are discussed in the light of those derived from ovaries of other Coleoptera and from the proposed sister group, the Neuropterida. The data strongly support a sister group relationship between Coleoptera and Neuropterida. Furthermore, several switches between polytrophic and telotrophic ovaries must have occurred during the radiation of ancient insect taxa.     

Ovary structure in a presocial insect,Elasmucha grisea (Heteroptera,Acanthosomatidae)

First generation egg clusters of Elasmucha grisea are more closely guarded than second generation clusters. The ovaries of this species are structured to enhance this behavior. The population of E. grisea from S-W Poland breeds in the spring (May–June) and late summer (July–August). The second generation clutches contain fewer eggs and are destroyed 3–4 days after oviposition by predators and parasitoids.The ovary structure in the studied species differs from that found in other Heteroptera. The average number of ovarioles per ovary is 24 while in the other investigated species the number of ovarioles per ovary is 6–7. Lateral oviducts are elongated and the ovarioles are arranged in a pennate pattern. Each ovariole contains only one growing ovarian follicle. Differentiation of the ovarioles and ovarian follicles is synchronised thus enabling simultaneous oviposition. A comparative analysis of the ovary structure during the life cycle, particularly the presence of atresive ovarian follicles in the ovarioles of egg- and nymph guarding females, as well as the shape and structure of the apical part of the tropharium all support the hypothesis of cooperation between females in E. grisea. A similar ovary structure has been observed in the Coccoidea (Hemiptera, Homoptera) which indicates presocial behavior.     

The larval development of the telotrophic meroistic ovary in the bug Dysdercus intermedius (Heteroptera, Pyrrhocoridae)

Bug ovaries are of the telotrophic meroistic type. Nurse cells are restricted to the anterior tropharium and are in syncytial connection with the oocytes via the acellular trophic core region into which cytoplasmic projections of oocytes and nurse cells open. The origin of intercellular connections in bug ovaries is not well understood. In order to elucidate the cellular processes underlying the emergence of the syncytium, we analysed the development of the ovary of Dysdercus intermedius throughout the five larval instars. Up to the third instar, the germ cell population of an ovariole anlage forms a single, tight rosette. In the center of the rosette, phosphotyrosine containing proteins and f-actin accumulate. This center is filled with fusomal cytoplasm and closely interdigitating cell membranes known as the membrane labyrinth. With the molt to the fourth instar germ cells enhance their mitotic activity considerably. As a rule, germ cells divide asynchronously. Simultaneously, the membrane labyrinth expands and establishes a central column within the growing tropharium. In the fifth instar the membrane labyrinth retracts to an apical position, where it is maintained even in ovarioles of adult females. The former membrane labyrinth in middle and posterior regions of the tropharium is replaced by the central core to which nurse cells and oocytes are syncytially connected. Germ cells in the most anterior part of the tropharium, i.e. those in close proximity to the membrane labyrinth remain proliferative. The posterior-most germ cells enter meiosis and become oocytes. The majority of the ovarioles' germ cells, located in between these two populations, endopolyploidize and function as nurse cells. We conclude that the extensive multiplication of germ cells and their syncytial assembly during larval development is achieved by incomplete cytokineses followed by massive membrane production. Membranes are degraded as soon as the trophic core develops. For comparative reasons, we also undertook a cursory examination of early germ cell development in Dysdercus intermedius males. All results were compatible with the known basic patterns of early insect spermatogenesis. Germ cells run through mitotic and meiotic divisions in synchronous clusters emerging from incomplete cytokineses. During the division phase, the germ cells of an individual cluster are connected by a polyfusome rich in f-actin.     

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.     

Organization of the tropharia in the telotrophic ovaries of the dipsocoromorphan bugs Cryptostemma alienum Herrich-Schaeffer and C. carpaticum Josifov (Heteroptera : Dipsocoridae)

The tropharia of the dipsocoromorphan bugs, Cryptostemma alienum and Cryptostemma carpaticum (Heteroptera : Dipsocoridae) are composed of 30–50 mononucleate nurse cells that are connected with centrally located trophic cores by means of broad cytoplasmic strands. The anteriormost nurse cells are markedly smaller and often reveal signs of degeneration. The trophic core is surrounded and penetrated by elaborate F-actin meshwork. Arrested oocytes and prefollicular cells are localized at the base of the tropharium. Anagenesis of heteropteran ovarioles is discussed in relation to the findings presented.     

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.     

Ultrastructure of the ovary of Dermatobia hominis (Diptera: Cuterebridae). III. Gonial cell degeneration.

We studied the ultrastructural aspects of pre-pupae and pupae ovaries of Dermatobia hominis. Physiological degeneration of gonial cells was observed: (a) after the ovarioles differentiation, in the oogonia residing in the apical region of the ovary; (b) at the beginning of vitellogenesis, in the cystoblasts close to the terminal filament. The significance of gonial cell degeneration was correlated with the physiological changes which occur in the ovary during development.     

The telotrophic-meroistic ovary of megaloptera. I. The ontogenetic development

Sialis flavilatera L. (Sialidae, Megaloptera) has telotrophic-meroistic ovarioles. The germ cells of the tropharium are organized into two distinct tissues, the central syncytium and the germ cell tapetum. The central syncytium consists of nurse cell nuclei embedded in a common cytoplasm which is rich in ribosomes and mitochondria. Cell membranes are totally absent. The germ cell tapetum surrounds the syncytium and consists of a monolayer of cells, each of which is connected with the central syncytium by an intercellular bridge. The oocytes differentiate from basal tapetum cells by previtellogenic growth. Their nutritive cords remain connected to the central syncytium by the intercellular bridge. Ovariole development starts soon after hatching with the immigration of germ cells into the ovariole-anlagen and is finished during pupal stages 23 months later. In apical regions of each tropharium, mitoses occur throughout larval life. The descendants enter the prophase of meiosis which lasts until pre-vitellogenesis; thus, a differential gradient of position and time is established. About 12 months after hatching, the central syncytium arises at the base of the tropharium from a membrane labyrinth in which intercellular bridges are entangled. Evidence is presented that endopolyploidization does not occur during germ cell differentiation. Finally, the results are compared with those found in Hemiptera and polyphage Coleoptera. The great diversities are interpreted as an indication for a polyphyletic origin of the telotrophic ovary.