Ovariole Development Research Articles

Morphological differences in the ovary of Libellulidae (Odonata)

All female Odonata have been assumed to produce oocytes continuously during their mature life span. However, a recent study of ovariole orientation and development led to the suggestion that Libellulidae are divided into two groups of species, one with continuous, the other with stepwise oocyte production. To find more evidence of this division, we compared the size variation and growth within the vitellarium of the ovary, studying oocytes, and follicle cells. We found that morphological characters discriminate between the two ovary types in eight of the 10 investigated species. In both types we found an increase in all measurements from the anterior to the posterior end of the vitellarium. The increase in oocyte width and follicle cell length was significantly higher in species with a continuous oocyte production. We also noted that follicle cells may have more than one nucleus and that their number can vary during vitellogenesis. Our study confirmed the hypotheses that two different ovary types exist in Libellulidae. The two species not fitting into this grouping could be an artefact of small sample size due to intraspecific phenotypic plasticity, or else there might be more than two ovary groups, or even a continuum. We could not offer an explanation as to how the process of stepwise oocyte production differs from continuous based production on morphological characters.

Sequestration of storage protein 1 (SP1) in differentiated fat body tissues of the female groundnut pest Amsacta albistriga (Lepidoptera: Arctiidae)

The transformation from larval caterpillar to non-feeding pupa and adult moth involves a complete remodelling and restructuring of an insect and its organs. In the groundnut pest Amsacta albistriga Walker, the female sex-specific storage protein 1 (SP1) was monitored from last larval instars, during pupal development to the adult stage. Staining intensity of SP1 (which resolved at 82 kDa) in the peripheral fat body (PF) tissues subjected to 10% SDS-PAGE was maximum at mid-stage last larval instars and declined subsequently. However, in perivisceral fat body (PVF) tissues, the staining intensity of SP1 increased significantly from mid-stage final instar. The presence of SP1 during pupal ovary and adult ovariole development and its availability during egg development was confirmed by immunoblot analysis. Electron microscopy data revealed that the decline of biosynthesis of SP1 in PF tissues and its disintegration were associated with the appearance of irregular nucleus and autophagic vacuoles during transformation of larva to pupa. In vitro and in vivo studies using [S]-methionine-labelled storage proteins showed that, unlike PF tissues, PVF tissue sequestered a significant amount of labelled SP1. During this transformation, SP1 was mainly sequestered as storage protein granules until they served as sources of amino acids for the production of egg yolk proteins. Localization of clathrin-coated pits and crystalline storage proteins was confirmed by immunogold tracer techniques.

Germ-cell cluster formation in the telotrophic meroistic ovary of Tribolium castaneum (Coleoptera, Polyphaga, Tenebrionidae) and its implication on insect phylogeny

Tribolium castaneum has telotrophic meroistic ovarioles of the Polyphaga type. During larval stages, germ cells multiply in a first mitotic cycle forming many small, irregularly branched germ-cell clusters which colonize between the anterior and posterior somatic tissues in each ovariole. Because germ-cell multiplication is accompanied by cluster splitting, we assume a very low number of germ cells per ovariole at the beginning of ovariole development. In the late larval and early pupal stages, we found programmed cell death of germ-cell clusters that are located in anterior and middle regions of the ovarioles. Only those clusters survive that rest on posterior somatic tissue. The germ cells that are in direct contact with posterior somatic cells transform into morphologically distinct pro-oocytes. Intercellular bridges interconnecting pro-oocytes are located posteriorly and are filled with fusomes that regularly fuse to form polyfusomes. Intercellular bridges connecting pro-oocytes to pro-nurse cells are always positioned anteriorly and contain small fusomal plugs. During pupal stages, a second wave of metasynchronous mitoses is initiated by the pro-oocytes, leading to linear subclusters with few bifurcations. We assume that the pro-oocytes together with posterior somatic cells build the center of determination and differentiation of germ cells throughout the larval, pupal, and adult stages. The early developmental pattern of germ-cell multiplication is highly similar to the events known from the telotrophic ovary of the Sialis type. We conclude that among the common ancestors of Neuropterida and Coleoptera, a telotrophic meroistic ovary of the Sialis type evolved, which still exists in Sialidae, Raphidioptera, and a myxophagan Coleoptera family, the Hydroscaphidae. Consequently, the telotrophic ovary of the Polyphaga type evolved from the Sialis type.

Ovariole number—a predictor of differential reproductive success among worker subfamilies in queenless honeybee (Apis mellifera L.) colonies

A honeybee queen normally mates with 10–20 drones, and reproductive conflicts may arise among a colony’s different worker patrilines, especially after a colony has lost its single queen and the workers commence egg laying. In this study, we employed microsatellite markers to study aspects of worker reproductive competition in two queenless Africanized honeybee colonies. First, we determined whether there was a bias among worker patrilines in their maternity of drones and, second, we asked whether this bias could be attributed to differences in the degree of ovary activation of workers. Third, we relate these behavioral and physiological factors to ontogenetic differences between workers with respect to ovariole number. Workers from each of three (colony A) and one (colony B) patrilineal genotypes represented less than 6% of the worker population, yet each produced at least 13% of the drones in a colony, and collectively they produced 73% of the drones. Workers representing these genotypes also had more developed follicles and a greater number of ovarioles per ovary. Across all workers, ovariole development and number were closely correlated. This suggests a strong effect of worker genotype on the development of the ovary already in the postembryonic stages and sets a precedent to adult fertility, so that “workers are not born equal”. We hypothesize a frequency-dependent or “rare patriline” advantage to queenless workers over the parentage of males and discuss the maintenance of genetic variance in the reproductive capacity of workers.

The mechanism of the queen signal in regulation of worker reproduction in the myrmicine ant Aphaenogaster smythiesi japonica

In ants, it is generally accepted that worker reproduction is regulated by a chemical signal informing workers of the queen's presence and stimulating workers to refrain from their own reproduction. This is known as the ‘queen signal’ — the mechanism for which is not well understood. In the myrmicine ant, Aphaenogaster smythiesi japonica, the queen signal mechanism was investigated by laboratory experiments. Firstly, in artificial nests where the nest chambers were separated by meshes, the workers were kept under queenright and queenless conditions in the laboratory. After 1 month in queenless conditions, a remarkable development of ovarioles with reproductive eggs was observed in a few queenless workers of each colony. Such development was not observed in queenright workers. This indicates that information of queen presence cannot be transmitted through meshes and that the chemical substances transmitting queen signal are not volatile. Secondly, in other artificial nests, the contact with the queen by workers was limited by attaching a piece of plastic string to their dorsal alitrunk and connecting nest chambers with small tubes. According to the limitation of contact, the workers were classified into three groups, queenright workers (Q+), queenless workers (Q–) and workers which could freely contact with the queen and all workers (FM). The development of ovaries with reproductive eggs was never observed in all workers of the three groups Q+, Q– and FM, indicating that their reproduction was regulated. This strongly suggests that A. s. japonica workers could recognize the queen's presence by direct contact with the queen and that the information could be transmitted via workers in the colony.

Ovariole development in telotrophic ovaries of snake flies (Raphidioptera)

Snake flies (Raphidioptera), alder flies (Megaloptera: Sialidae) and also some myxophagan coleopterans share the same, peculiar telotrophic organization of their ovarioles usually referred to as ovarioles of the Sialis-type. Ovariole ontogenesis in Raphidia sp. is described and the basic events that lead to the formation of germ cell clusters and their subsequent transformations are reported. It was found that the major cellular events during ovariole formation in Raphidia and Sialis are essentially the same. Discrepancies concern details of germ cell cluster formation, differentiation of cystocytes within clusters and their location within the developing tropharium. Based on these results the hypothetical model of the Sialis-type ovariole formation, previously presented by King and Büoning (1985) is verified. A hypothesis on the mechanisms of oocyte determination in telotrophic ovaries is also presented.

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.

Short-term changes in the abundance and parity rate of Anopheles quadrimaculatus species C (Diptera: Culicidae) in a central Florida swamp.

Updraft CDC traps baited with dry ice were used to monitor changes in the abundance and parity rate of Anopheles quadrimaculatus Say complex mosquitoes in an intermittently flooded swamp in Central Florida during an 18-d period. Mosquitoes collected each day were identified to species using DNA hybridization and isozyme electrophoretic techniques and were dissected to determine follicular maturation and parity. Of 1,178 An. quadrimaculatus mosquitoes identified to species, 4% were species A and 96% were species C. Dissections of females of both species indicated that 98% were nonblood fed and nongravid with ovariole development at Christophers' stage II. Overall parity rates were 0.19 and 0.51 for populations of species A and species C, respectively. The duration of the gonotrophic cycle for species C females was estimated to be 5 d based on the interval between peaks in the number of nulliparous females collected on days 1 and 6 and peaks in the number of parous females collected 5 d later. Significant trends were observed in the number of parous species C females collected each day, indicating that the parity rate could not be used as an unbiased estimator of survivorship.

Ovariole development in Staphylinidae (Coleoptera)

Summary Twenty percent of the species from 88% of the genera, which comprise the British Staphylinidae fauna, were dissected and their ovaries attributed to one often defined types. Three-quarters of the species studied possessed six ovarioles in each ovary although the eight species of Bledius examined were found to have only a single ovary, a condition previously thought to be unique to the family Scarabaeidae within the Coleoptera. The type of ovariole development within most staphylinid subfamilies is remarkably constant. Any inconsistencies are described. Species of Aleochara, known to have parasitic larvae, were found to have a larger number of ovarioles per ovary than any other member of the Staphylinidae examined. They also exhibited a greater variation in ovariole number within each species which is correlated with the size of the adult beetle.

Effects of avermectin residues in cattle dung on dung beetle (Coleoptera: Scarabaeidae) reproduction and survival

Scarabaeine dung beetles feeding on dung from cattle treated with an injection of avermectin at a therapeutic dose to control internal parasites, show larval mortality, mortality of immature adults, reduced egg production, and inhibited ovariole development for periods of 1–4 weeks following treatment. In winter rainfall regions of Australia, feeding by newly emerged adults of an introduced species, Onthophagus binodis, resulted in shredding of cattle dung between December and May. Production of brood masses and eggs resulted in dung being buried from September to November. Feeding by newly emerged adults of a native species, Onthophagus ferox, resulted in dung being buried in May and June, and production of brood masses for breeding resulted in dung burial between September and November. There are thus 2–6 months of the year when injection of cattle with avermectin would affect mortality of newly emerged beetles, and 3 months of the year when avermectin treatment of cattle would affect dung beetle oviposition or larval survival. Beetles were attracted to fresh dung for 2–4 days, and most had left the pad within a week. There are no data to indicate the effects of avermectin residues in dung on dung beetle populations and on beetle fitness. Tests should be done to determine if avermectins in slow release devices have a greater effect on dung beetles than injections, and to determine what effects both have on dung beetle populations.

Effects of Postdiapause Adult Diet and Temperature on Oogenesis of the Cabbage Seedpod Weevil (Coleoptera: Curculionidae)

The effects of adult diet and temperature on oogenesis of the postdiapause cabbage seedpod weevil, Ceutorhynchus assimilis Paykull, were studied to examine the reproductive development of this important pest of rapeseed, Brassica napus L. Diets consisting of racemes with open flowers, racemes without open flowers, racemes with open flowers without stamens, stamens, sugar water (10% sucrose), and distilled water were evaluated with respect to C. assimilis oogenesis. Oogenesis, rated on a 1-3 scale, and measurements of follicle length, width, and volume, were significantly (P 0.05) differences in oogenesis (stage, follicle length, width, and volume) among weevils fed racemes of each variety over a 2-wk period. Ovariole development differed significantly (P 0.05) differences in weevil mortality among the temperature treatments over the 4-wk period of study.

Adaptations in trogid carrion beetles to extremely arid conditions

Trogid (Coleoptera: Trogidae) species of the genus Omorgus in the arid Kalahari are morphologically, behaviourally and physiologically adapted to survive extremely arid periods interspersed with short favourable periods during which feeding and breeding take place. The most important strategies for survival are: a biphasic daily activity pattern which coincides with peaks in relative humidity and the inverse in temperature; the ability of adults and larvae to enter a quiescent state under adverse environmental conditions, which can be terminated within hours of an improvement in conditions; rapid immature development, long adult life and consequent overlapping generations; suspended ovariole development; and a tendency to a flightless condition. The availability of the mummified remains of large antelope for up to several years enables populations to build up beneath carcasses without the risks involved in dispersal to find food and mates.

The linear clusters of oogonial cells in the development of telotrophic ovarioles in polyphageColeoptera

During the premetamorphic development of coleopteran telotrophic ovaries the culsters of sister oogonial cells, in which the differentiation of nurse cells and oocytes occurs, are arranged in linear chains. This results from a series of mitoses with the consistent orientation of the spindle parallel to the long axis of the ovariole. As a result of incomplete cytokinesis, the oogonial cells in each sibling cluster are linked to each other by intercellular bridges occupied by fusomes. As a rule, at each cluster division the basal cell (i.e. the oocyte progenitor) starts to divide first. From this cell a wave of mitoses spreads toward the anterior end of the cluster, resulting in a mitotic gradient. It is suggested that the failure of the fusomes in adjacent cells to fuse into one continuous fusome (i.e. polyfusome) allows the spindles to orientate with their long axes parallel to the long axis of the sibling cluster. This would explain why the oogonial divisions in coleopteran telotrophic ovaries generate linear chains of cells rather than the cyst-like arrangement which is typical for polytrophic sibling clusters. Dividing sibling clusters within ovarioles are arranged in bundles. The presence of intercellular bridges between sibling clusters seems to be the underlying cause of this nonrandom distribution of the mitotically active clusters. The transverse bridges have been found to occur between the basal cells as well as between the cells located more anteriorly in adjacent sibling clusters. The transverse bridges are filled with typical fusomes, which in more anterior parts of sibling clusters may fuse with the fusomes of adjacent sister oogonial cells into polyfusomes. The transverse bridges between the basal cells are incorporated in the oocytes. The pattern of sibling cluster formation described in this paper apparently occurs widespread in polyphagous Coleoptera, since it has been found in three relatively distantly related families.

BLOOD-FEEDING IN OVERWINTERING CULEX TARSALIS (DIPTERA: CULICIDAE) FROM MANITOBA

Diapause development in Culex tarsalis Coquillett has been characterized by reduced blood-feeding to complete termination of ovariole development at or before stage IIa (Bennington et al. 1958; Schaefer and Washino 1970; Schaefer et al. 1971; Bellamy and Corbet 1973; Mitchell 1979). The role that diapausing Culex species have in overwintering arboviruses has been examined (Eldridge 1966, 1968; Eldridge et al. 1972; Reeves 1974; Eldridge and Bailey 1979; Mitchell 1979). Gonotrophic dissociation and its implications for survival of the vector and virus has been reviewed by Washino (1977). Eldridge (1966) indicated gonotrophic dissociation was possible in Culex pipiens L. incubated at low temperature and short daylength and later reported failure of ovarioles of prehibernating C. pipiens to mature following a blood meal (Eldridge and Bailey 1979). Eldridge et al. (1972) reported that Culex restuans Theobald exhibited gonotrophic dissociation in response to conditioning by short daylength and low temperature. Mitchell (1981) has reported blood-feeding and gonotrophic dissociation in a significant portion of diapausing Culex tarsalis from Colorado, when females were kept at 15°C and at short daylength conditions.

What determines the number of ovarioles in a fly ovary?

The relation between the size of a fly and the number of ovarioles in its ovary was investigated in Phormia regina and Sarcophaga bullata. Small flies of varying size were produced by taking larvae prematurely off the food. The smallest flies thus obtained were derived from larvae only 1 8 of the weight of a normal larva. The number of ovarioles in an ovary is directly proportional to the size of the fly and, in the extreme case, is about 1 5 the normal number in Sarcophaga and about 1 3 in Phormia. Larvae prematurely taken off the food, but fed again after starving for several days, grow to normal or almost normal size and develop ovaries with about the normal number of ovarioles. Small or re-fed Sarcophaga do not show any changes in the anatomy of individual ovarioles but in Phormia disorders in ovariole development and a consequent reduction of fertility are frequent. The number of ovarioles remains identical from the early pupal stage all through the development of the pharate fly and then through ovarian development in the adult fly: it is determined by the size of the larva when it was taken off the food. This shows that it is not lack of space in a small adult fly abdomen which determines the number nor the occurrence of degenerative processes during ovarian 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.

OVARIAN DEVELOPMENT OF QUEEN AND WORKER BUMBLE BEES (HYMENOPTERA: APIDAE) IN SOUTHERN ALBERTA

AbstractOocytes of queen bumble bees from southern Alberta were partly developed when the queens emerged from hibernation in the spring. Early emerging species had less autumnal ovariole development and fed longer in spring before establishing a nest than did later emerging species. The main increase in oocyte size was synchronous with the finding of a suitable nest. The mean length of the largest oocyte for workers for all species was small, less than 0.7 mm, clearly indicating that workers contribute few males to the population.

Studies of Oogenesis in Natural Populations of Drosophilidae. I. Relation of Ovarian Development and Ecological Habitats of the Hawaiian Species

The fecundity potential of Drosophila populations endemic to Hawaii has been investigated by analyzing the ovarian development of species in their natural habitats. Species differ in mean number of ovarioles per fly and/or number of mature eggs per ovariole. This diversity is probably an adaptive response of the population to the larval food supply which is determined by the nature, abundance, and nutritional content for larval growth of the oviposition substrates. Three groups of species were recognized on the basis of their fecundity potential and their use of comparable ovipositing substrates: species with a low potential, breeding on flowers (pollen); species with a medium potential, breeding on decaying leaves (bacteria); and species with a large potential, breeding on decaying stems (yeast). Adaptive mechanisms in oviposition behavior (single egg or cluster oviposition) and in the development and function of ovarioles (alternating ovariole development or synchronous ovariole development) which coordinate the reproductive potential of the species with the nutritional content of their breeding substrates are discussed, as is the importance of environmental parameters in determining realized fecundity.