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).     

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.     

Germ cell cluster formation in insect ovaries

Three different ovariole types exist in insects: panoistic, polytrophic- and telotrophic-meroistic. Their ontogenetic development is comparable to all insect orders. Each ovariole is composed of somatic tissues and germ cells.Panoistic ovarioles can be developed: (1) by totally blocking germ cell cluster division (e.g. in “primitive” insect orders; and (2) after germ cell cluster formation by final cleavage of cystocytes, which develop as oocytes (e.g. in stoneflies or thrips).Polytrophic-meroistic ovaries, showing a set of identical characters, are found among hemirnetabolous and holometabolous insects, indicating a “basic type” of common origin. One characteristic feature is the differentiation of only one oocyte, which is derived from one central cell of the cluster, whereas all other siblings are transformed into nurse cells.Telotrophic ovaries differ from polytrophic ovaries by retention of all nurse cells in the anterior trophic chamber. In addition, oocyte-nurse cell determination can be shifted towards more oocytes in a cluster, and clusters or subclusters can fuse by cell membrane reduction among nurse cells. This type of ovary developed independently 3 times from polytrophic ancestors and once in mayflies directly from panoistic ancestors.     

Structure of ovaries in scale insects. i. pseudococcidae,kermesidae, eriococcidae,and cryptococcidae (INSECTA,hemiptera, COCCINEA)

Developing ovaries of scale insects (Hemiptera : Coccinea) Nipaecoccus nipae (Pseudococcidae) and Cryptococcus fagisuga (Cryptococcidae) contain clusters of interconnected cells (cystocytes) that are arranged into rosettes; polyfusomes occur in the centres of the rosettes. Ovaries of the investigated adult scale insects are composed of numerous short telotrophic ovarioles. Tropharia (trophic chambers) of Dysmicoccus newsteadi (Pseudococcidae), Eriococcus buxi (Eriococcidae), Cryptococcus fagisuga and Pseudochermes fraxini (Cryptococcidae) comprise only trophocytes (nurse cells), whereas those of Kermes quercus (Kermesidae) and Gossyparia spuria (Eriococcidae) also contain arrested oocytes. The latter probably degenerate. It is suggested that during evolution of scale insects a gradual reduction of germ cells to 4 per cluster (3 trophocytes and 1 oocyte) took place. In light of the obtained results, anagenesis of scale insects ovarioles is discussed.     

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.     

Oogenesis and ovarian morphology in pollinating and non-pollinating fig wasps: evidence from adult and immature stages

Hymenopteran insects have meroistic polytrophic ovaries characterised by trophocytes associated with oocytes inside the follicles. In pro-ovigenic species, all oocytes mature before emergence and no trace of oogenesis is visible in adult females. Pro-ovigeny is a rare condition among Hymenoptera, but common in pollinating fig wasps. In the present investigation, we studied adult and pupa females of three fig wasp species with different trophic strategies. We demonstrated that females of Pegoscapus aerumnosus and Idarnes spp. have an unusual ovarian organisation (i.e. each ovariole has only one mature egg and no oocyte) that has led to misleading interpretation of fig wasp reproductive anatomy. The ovaries of these studied species have several ovarioles, recognisable by the presence of nuclei of tunica propria cells surrounding them. Each adult wasp ovariole had one mature egg. None of the pupae had mature eggs, but all of them had follicles with oocytes in different developmental stages. The studied fig wasps are pro-ovigenic, irrespective of their trophic strategy, since there were no signs of ovigeny in adult females. We discuss ecological and phylogenetic factors that could play a role in fig wasps reproductive strategies.     

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 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.     

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.     

Structure and development of ovaries in the weevil,Anthonomus pomorum (Coleoptera,Polyphaga). II. Germ cells of the trophic chamber

The analysis of the germ cell cluster formation in Anthonomus pomorum (Coleoptera, Polyphaga, Curculionidae) has revealed that both linear and branched clones of cystocytes occur in the pupa stage. In the branched clones a poorly developed polyfusome is formed and cystocytes with maximally 3 intercellular bridges were found. In the linear clones the polyfusomes are absent. Further divisions of cystocytes produce exclusively linearly arranged cells. Just after metamorphosis (Imago-A stage), the process of the germ cell membrane reduction starts. Only 2 groups of cells retain cell membranes: i.e the most anteriorly localized group of cystocytes and the posteriorly located presumptive oocytes. The former cells divide mitotically during the summer. As a result an anterior-posterior gradient of the syncytialization process arises in the Imago-B stage (females preparing for hibernation). In the sexually mature females (Imago-C) the trophic chamber consists of a huge syncytial area with numerous nurse cell nuclei embedded in a common cytoplasm, and posteriorly located young oocytes surrounded by prefollicular cells. In the light of recent hypothesis concerning the germ cell cluster formation and telotrophy anagenesis in Polyphaga the significance of the presented results is discussed.     

Morphological Oogenesis in the out1 Mutant of Drosophila melanogaster Meigen (Diptera: Drosophilidae)

ABSTRACT The sex-linked, recessive otu¹ mutant of Drosophila melanogaster was studied cytologically to reveal the effect of the otu gene mutation on oogenesis. Consequently, the germarium of the otu¹ mutant was found to be larger as compared to the normal fertile one and contains many undifferentiated tumor cells resembling cystocytes. Each ovary consists of three types of ovarioles; ovarioles with only a germarium, ovarioles with a germarium and one tumor chamber, and ovarioles with a germarium and two tumor chambers. In the otu¹ germarium, the mesodermal follicle cells invade the clusters of different number of tumor cells at the posterior region of the germarium in order to make the tumor chamber and the dividing frequency of the tumor cells in the first tumor chamber was six times more than in the second tumor chamber. Follicle cells surrounding the tumor chamber are morphologically normal, but the number of the follicle cells becomes less as the tumor chambers move down contrary to the fertile one. The otu¹ mutant female never lays the egg and the formation of the vitelline membrane is incomplete. The otu¹ mutant tumor cells also showed characteristics of certain rapidly dividing cells and its nucleus is lobulated.     

Effect of Microwave Exposure on the Ovarian Development of Drosophila melanogaster

In the present experiments the effect of GSM radiation on ovarian development of virgin Drosophila melanogaster female insects was studied. Newly emerged adult female flies were collected and divided into separate identical groups. After the a lapse of certain number of hours-different for each group-the insects (exposed and sham-exposed) were dissected and their intact ovaries were collected and photographed under an optical microscope with the same magnification. The size of the ovaries was compared between exposed and sham-exposed virgin female insects, during the time needed for the completion of oogenesis and maturation of the first eggs in the ovarioles. Immediately after the intact ovaries were photographed, they were further dissected into individual ovarioles and treated for TUNEL and acridine-orange assays to determine the degree of DNA damage in the egg chamber cells. The study showed that the ovarian size of the exposed insects is significantly smaller than that of the corresponding sham-exposed insects, due to destruction of egg chambers by the GSM radiation, after DNA damage and consequent cell death induction in the egg chamber cells of the virgin females as shown in previous experiments on inseminated females. The difference in ovarian size between sham-exposed and exposed virgin female flies becomes most evident 39-45 h after eclosion when the first eggs within the ovaries are at the late vitellogenic and post-vitellogenic stages (mid-late oogenesis). More than 45 h after eclosion, the difference in ovarian size decreases, as the first mature eggs of the sham-exposed insects are leaving the ovaries and are laid.     

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.     

Structure of the trophic chamber (germarium) in virginoparae of the vetch aphid,Megoura viciae Buckton (Homoptera : Aphididae)

The structure of the germaria in the ovaries of the viginoparous morph of the vetch aphid, Megoura viciae Buckton (Homoptera : Aphididae) is described and compared to other insects, including aphids. Each consists of a syncytium of trophocytes and resting oocytes arranged around a trophic core. Trophocytes contain mitochondria, ribosomes, vacuoles and some membrane-bounded material. Golgi complexes were not found. Each trophocyte has a single spherical nucleus with “nuage-like” material confluent between nucleoplasm and cytoplasm via numerous nucleopores. The surrounding monolayer of somatic epithelial sheath cells are bounded externally by an acellular tunica propria. These cells continue into the prefollicular tissue in the base of each germarium. Cells from the prefollicular tissue envelop each oocyte as it is released from a germarium. The “previtellogenic” growth phase of oocytes is relatively short, and vitellogenesis is absent. Virginoparae are reproductively precocious, and newly born larvae have up to 3 oocytes undergoing development in their anterior ovarioles. Interovariole ovulation is asynchronous within, and partially synchronous between, the 2 ovaries.     

Temperature-dependent ovariole and testis maturation in the yellow dung fly

Temperature is one of the abiotic environmental factors most strongly affecting animal behaviour, physiology, and life history. In insects, lower temperatures generally slow down most physiological processes, reducing growth rate and prolonging the juvenile period. Here, we investigate temperature‐dependent ovariole and testis maturation in the anautogenous yellow dung fly, Scathophaga stercoraria L. (Diptera: Scathophagidae), and relate it to corresponding temperature effects on pre‐adult development time and the adult pre‐reproductive period. Flies were reared in the laboratory at three constant temperatures (18, 22, and 26 °C), and the size of the developing ovarioles and testes (reflecting sperm production) was measured over time (i.e., age). Ovariole size increased asymptotically over the first 12 days of adult life, while the testes continued to fill after day 10. In accordance with the temperature‐size rule, warmer temperatures resulted in smaller ovarioles (eggs) and smaller testes, independent of body size. Warmer temperatures also greatly reduced pre‐adult development time by more than half, from 12 to 25 °C, the larger males always taking 1–3 days longer than the females. Corresponding temperature effects on the adult pre‐reproductive period were small (<1 day between 15 and 25 °C), with males taking 5–6 days and females 10–13 days to first reproduction. Time lost by males during the pre‐adult stage, when ovaries and testes are produced, can thus be more than compensated‐for by time gained during the pre‐reproductive period, when eggs and sperm are produced, so males can nevertheless start reproducing sooner than females.     

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.     

Germ cell cluster formation and cell death are alternatives in caste-specific differentiation of the larval honey bee ovary

Summary

Caste-specific differentiation of the female honey bee gonad takes place in the fifth larval instar. In queen larvae most ovarioles exhibit almost simultaneous formation of numerous germ cell clusters within the first 20 h after the last larval molt. Ultrastructurally distinctive fusomal cytoplasm connects these cystocytes. Germ cell differentiation is accompanied by morphological changes in somatic components of the ovarioles, the follicle and the terminal filament cells. Subsequently, queen ovarioles elongate and differentiate basal stalks that coalesce in a basal calyx. A second round of mitotic activity was found to occur in the late prepupal and early pupal queen ovary. This round may elevate germ cell numbers composing each cluster to levels observed in follicles of adult honey bee queens. In contrast, germ cell cluster formation does not occur in most of the 120–160 ovarioles of the larval worker ovary, but instead many cells in such ovarioles show signs of impending degeneration, such as large autophagic bodies. DNA extracted from worker ovaries did not reveal nucleosomal laddering, and ultrastructurally, chromatin in germ cell nuclei appeared intact. In the 4–7 surviving ovarioles of the small worker ovary, germ cell clusters were found with ultrastructural characteristics identical to those in queen ovarioles. The temporal window during which divergence in developmental pathways of the larval ovaries initiates shortly after the last larval molt coincides with caste-specific differences in juvenile hormone titer which have long been considered critical to caste-specific morphogenesis.     

Ontogenesis of the ovary in a moth midge,Tinearia alternata Say (Diptera: Psychodidae)

In a psychodid, Tinearia alternata, the initial differentiation of the polytrophic ovary occurs during the early larval stages. Early in development, each ovary anlage is a solid organ subdivided into three distinct zones: the cortex houses germ cells and somatic interstitial tissue, while two other somatic regions will give rise to the oviduct calyx and anterior part of the lateral oviduct. Germ cell cluster formation precedes the development of ovarioles. Each ovariole houses only one functional egg chamber. All ovarioles within paired ovaries are developmentally synchronized. In the larval ovaries, the newly formed egg chambers and then the ovarioles are intermingeled with and surrounded by the somatic interstitial tissue of the ovary cortex. The interstitial cells give rise to all the somatic elements of the ovarioles. In the pupal ovaries, the remaining interstitial tissue degenerates; thus, the ovarioles protrude into the body cavity. The ovaries in psychodids develop relatively large and swollen oviduct calyxes that are equivalent to receptaculum seminis (spermatheca). The morphological differentiation of germ cells within the egg chambers starts during late larval/early pupal stages. Nurse cell nuclei contain prominent nucleoli and polytene chromosomes. Oocyte growth results from accumulation of yolk and then, in the final stages of oogenesis, from an inflow of cytoplasm from the nurse cells. J. Morphol. 236:167–177, 1998. © 1998 Wiley-Liss, Inc.     

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.