Voltage gradients and microtubules both involved in intercellular protein and mitochondria transport in the telotrophic ovariole of Dysdercus intermedius

Summary In the telotrophic ovariole of Dysdercus intermedius the intercellular transport consists of different subsystems. Microinjection of FITC-labeled slowly diffusing proteins with opposite electrical net charges and of mitochondria was used to study the translocation of macromolecules and organelles. a) By intracellular measurements a voltage gradient of about 4 mV between the tropharium as the more negative side and the previtellogenic oocytes could be demonstrated. b) After injection into the tropharium negatively charged proteins migrated according to the electropotential gradient via the trophic cords into the oocytes. Positively charged proteins, however, were retained in the tropharium. c) After injection into previtellogenic oocytes both negatively and positively charged proteins moved into the trophic cords. Thus, the effectiveness of the electropotential gradient on the distribution of charged proteins is more pronounced from the tropharium side. d) Mitochondria microinjected into the trophic core were probably aligned along microtubules and translocated towards the trophic cords. — These results suggest that in the telotrophic bug ovariole a number of intercellular transport subsystems contribute to provide previtellogenic oocytes with nurse cells products. An electrophoretic transport mechanism for soluble proteins acting especially within the tropharium and a microtubule-associated transport for mitochondria could be evidenced.     

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.     

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.     

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.     

Cytoarchitecture of the ovarioles in scale insects (Hemiptera,Coccinea)

Telotrophic ovarioles of scale insects are subdivided into tropharia (=trophic chambers) and vitellaria that contain single developing oocytes. Tropharium encloses trophocytes (=nurse cells) and arrested oocytes. The central area of the tropharium, termed the trophic core, is devoid of cells. Both trophocytes and oocytes are connected to the trophic core: trophocytes by cytoplasmic processes, oocytes by means of nutritive cords. The trophic core, processes and nutritive cords are filled with bundles of microtubules. The trophocytes contain large lobated nuclei with giant nucleoli. Fluorescent labelling with DAPI has shown that trophocyte nuclei are characterized by high contents of DNA. In the cortical cytoplasm of trophocytes, numerous microfilaments are present. The developing oocyte is surrounded by a simple follicular epithelium. The cortical cytoplasm of follicular cells contains numerous microtubules and microfilaments.     

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.     

Heterologous gap junctions between oocytes and follicle cells of an insect,Dysdercus intermedius,and their potential role as ion current pathways

Summary In telotrophic insect ovaries, the oocytes develop in association with two kinds of supporting cells. Each ovary contains five to seven ovarioles. An ovariole consists of a single strand of several oocytes. At the apex of each ovariole is a syncytium of nurse cells (the tropharium), which connects by strands of cytoplasm (the trophic cords) to four or more previtellogenic oocytes. In addition, each oocyte is surrounded by an epithelium of follicle cells, with which it may form gap junctions. To study the temporal and spatial patterns of these associations, Lucifer yellow was microinjected into ovaries of the red cotton bug, Dysdercus intermedius. Freeze-fracture replicas were examined to analyze the distribution of gap junctions between the oocyte and the follicle cells. Dye-coupling between oocytes and follicle cells was detectable early in previtellogenesis and was maintained through late vitellogenesis. It was restricted to the lateral follicle cells. The anterior and posterior follicle cells were not dye-coupled. Freeze-fracture analysis showed microvilli formed by the oocyte during mid-previtellogenesis, and the gap junctions became located at the tips of these. As the microvilli continued to elongate until late vitellogenesis, gap junction particles between them and follicle cell membranes became arranged in long arrays. The morphological findings raise questions about pathways for the intrafollicular phase of the ion currents known to surround the previtellogenic and vitellogenic growth zones of the ovariole.Supported by the Deutsche Forschungsgemeinschaft (Schwerpunkt Differenzierung)     

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 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.     

Nurse cell-oocyte interaction in the telotrophic ovarioles of an insect, Rhodnius prolixus

Microinjection of intracellular tracers fluorescein, Procion Yellow, Lucifer Yellow and horseradish peroxidase unequivocally showed the syncytial structure of the tropharium and its interaction with the oocytes. The tropharium tip is a separate isolated compartment. Finger-like nurse cell projections comprising the syncytial tropharium interact via gap junctions along their abutting membranes and also via large cytoplasmic continuities at the central trophic core. The trophic cords connecting the tropharium to oocyte vary in diameter relative to oocyte stage. Continuity of the tropharium with the oocytes is lost at approximately 1000 μm oocyte length and the severed cords then regress from the oocyte to the tropharium base. Variation in cord diameters and timing of cord closure may account for the highly regulated sequential oocyte growth.     

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.     

Mayflies (ephemeroptera), the most “primitive” winged insects,have telotrophic meroistic ovaries

Germ line cell cluster formation in ovarioles of three different stages, each from a different mayfly species, was studied using ultra-thin serial sectioning. In the analysed ovariole of Cloeön sp., only one linear, zigzag germ line cell cluster was found, consisting of sibling cells connected by intercellular bridges which represent remnants of preceding synchronized mitotic cycles followed by incomplete cytokinesis. A polyfusome stretched through all sibling cells. At the tip of the ovariole, cytokinesis occurred without preceding division of nuclei; thus, intercellular bridges were lined up but the remaining cytoplasm between the bridges had no nuclei. The analysed Siphlonurus armatus vitellarium contained five oocytes at different stages of development. Each oocyte in the vitellarium was connected via a nutritive cord to the linear cluster of its sibling cells in the terminal trophic chamber. Each cluster had the same architecture as was found in Cloëon. The 3-dimensional arrangement and distribution of closed intercellular bridges strongly suggest that all five clusters are derived from a single primary clone. The position of oocytes within each cluster is random. However, each oocyte is embraced by follicular or prefollicular cells whilst all other sibling cells are enclosed by somatic inner sheath cells, clearly distinguishable from prefollicular cells. In the analysed ovariole of Ephemerella ignita, two small linear clusters were found in the tropharium beside two single cells, two isolated cytoplasmic bags with intercellular bridges but no nuclei, and some degenerating aggregates. One cluster was still connected to a growing oocyte via a nutritive cord. In all species the nurse cells remained small and no indications of polyploidization were found. We suggest that this ancient and previously unknown telotrophic meroistic ovary has evolved directly from panoistic ancestors.     

Structure of the ovary in Steingelia (Sternorrhyncha: Coccinea), and its phylogenetic implications

The paired ovaries of Steingelia gorodetskia are composed of about 100 telotrophic ovarioles devoid of terminal filaments (scale insect autapomorphy). In structure they resemble those of other scale insects, but differ in the following details: (a) all ovarioles develop synchronously, (b) they are suspended to the lateral oviducts by means of long stalks, (c) the tropharium is tubular (unique in scale insects) and (d) consists of 15-35, trophocytes, 2-4 previtellogenic oocytes that further develop, and numerous somatic prefollicular cells, (e) the vitellarium houses 2-4 linearly arranged vitellarial oocytes (versus one in most scale insects). Most of these features must be considered as plesiomorphic corresponding with the conditions in the most primitive Heteroptera. Bacterial endosymbionts have been found in some somatic cells, trophocytes, oocytes and in the nutritive cord. Present results support the opinion, based on external morphology, that the Steingeliidae are closely related to the Ortheziidae, Xylococcidae and Matsucoccidae.     

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.     

Independent regulation of microtubule spacing and microtubule stability following redundancy of nutritive tubes in telotrophic ovaries in hemiptera (insecta)

The nutritive tubes that act as conduits between the nutritive cells and the developing oocytes within the ovaries of hemipteran insects, contain vast aggregates of aligned microtubules. During the previtellogenic stages of oogenesis, components synthesised in the nutritive cells pass within the nutritive tubes and accumulate in the oocytes. Using polarised light and electron microscopy, we have monitored the changes in both the spacing and stability of the microtubules which occur when, at the onset of vitellogenesis, translocation within the nutritive tube ceases and the tube becomes redundant. Having investigated nutritive tube redundancy in the ovaries of 4 species of hemipterans, we have discovered the outcome to be similar in each case, with the microtubules losing their characteristic spacing and becoming closely packed prior to their depolymerisation. The feature that differs is the timing of these changes because, in certain species, microtubule depolymerisation closely follows the microtubule rearrangement, while in other species, depolymerisation of the microtubules occurs some considerable time after their change in pattern. This evidence demonstrates that microtubule spacing and stability are regulated independently following redundancy of nutritive tubes, and we speculate upon how this regulation might be achieved within the insect ovaries.     

Morphology,ultrastructure, and germ cell cluster formation in ovarioles of aphids

The structure of aphid ovaries, including ovipare and virginopare morphs of five species, was investigated by light and electron microscopy. Aphids contain telotrophic meroistic ovarioles. The amount and distribution of cytoplasmic components of nurse cells, nutritive cords, and young oocytes are nearly identical to those known from scale insects and heteropterans. Each ovariole has a constant number of nurse cells and oocytes. In ovaries of ovipare morphs, the nurse cell nuclei enlarge by endomitosis (n = 2⁸n?2¹⁰n), whereas in virginopare morphs the nurse cell nuclei remain small (n = 2²n?2⁴n). Furthermore, in virginoparae the previtellogenic growth of oocytes is highly reduced, and vitellogenesis and chorionogenesis are blocked totally. Embryogenesis starts immediately after the shortened previtellogenic growth. In each ovariole, all germ cell descendants belong to one germ cell cluster that follows the 2ⁿ rule. The cluster normally contains 2⁵ = (32) cells, but other mostly smaller numbers also occur. In contrast to polytrophic meroistic ovarioles, more than one cell of each cluster will develop into an oocyte. In Drepanosiphum platanoides, 16 (2^n?1) nurse cells and 16 (2^n?1) oocytes exist in each cluster, whereas, in Metopolophium dirhodum, 8 (2^n?2) oocytes and 24 (2^n?1 + 2^n?2) nurse cells are normally found. In many ovarioles of Macrosiphum rosae, 21 nurse cells nourish 11 oocytes. Models of germ cell cluster formation in aphid ovaries are discussed.     

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.     

A cytological study of the ovary of Rhodnius prolixus. III. Cytoarchitecture and development of the trophic chamber

The tropharium of the telotrophic ovarioles of Rhodnius is syncytial with the nurse cell nuclei located in tortuous finger-like projections arborizing from a common cytoplasmic area, the trophic core. The nurse cell nuclei exhibit prominent nucleoli. Located adjacent to the nuclear envelope are masses of granular material both within the nucleus and adjoining cytoplasm. The cytoplasm consists primarily of ribosomes and mitochondria. The trophic core and the trophic cords that connect the core to individual oocytes characteristically possess parallel arrays of microtubules with ribosomes and mitochondria interspersed between. Surrounding the nurse tissue (germarium) is a thin layer of squamous cells comprising the inner sheath. The inner sheath is encompassed by the non-cellular tunica propria superficial to which are two external cellular sheaths. The syncytial nature of the tropharium appears to arise as a result of the fusion of many entangled nurse cell-oocyte complexes during the late fifth instar. The structural similarities, and possible homologies with the polytrophic type of ovariole is discussed.     

Ovary cords organization in Hirudo troctina Johnson, 1816 and Limnatis nilotica (Savigny, 1822) (Clitellata,Hirudinea)

In both examined species of Hirudinea there are paired spheroid ovisacs, and within each ovisac two convoluted ovary cords occur. The morphology of the cords is characteristic: their apical end is club-shaped, the central part is narrow and may contain developing oocytes, whereas the basal end of the cord is irregularly shaped and composed of degenerating cells. The ovary cords are built of somatic and germ-line cells; the latter are united into syncytial cysts. Each germ cell in such a cyst has only one stable cytoplasmic bridge connecting it to the central anuclear cytoplasmic mass, the cytophore. Initially all germ-line cells in a given cyst are morphologically identical, then the fates of cells diversify. Most of them become nurse cells and eventually degenerate; the rest continue meiosis, gather macromolecules, cell organelles and nutritive material and become oocytes. The oogenesis found in the species studied should be regarded as meroistic. Previtellogenic oocytes protrude from the cord into the ovisac lumen, whereas the vitellogenic ones float freely in the ovisac lumen. The somatic cells found in the ovary cords are: follicular cells which form the envelope of the cord and are also found among germ cells inside the cord, and one, huge apical cell that always is located at the top of the club-shaped end of the ovary cord. The apical cell has several characteristic features, e.g., it forms long cytoplasmic projections filled with intermediate filaments and it is connected to the neighbouring cells (both somatic and germ-line) via hemidesmosomes. We suggest that the apical cell forms the niche for maintaining germ and somatic stem cells. Generally, the organization of the ovary cords found in both studied species is broadly similar to those described in other hirudiniform leeches studied to date.     

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.