Endocrine control of vitellogenesis in the harlequin bug, Dindymus versicolor

An active corpus allatum is essential for the maturation of eggs in the harlequin bug, Dindymus versicolor. The corpus allatum of virgin females remains virtually inactive and the oöcytes are resorbed once they have grown to the stage at which they become competent to incorporate yolk. Mating provides a stimulus which is essential for the initiation and maintenance of corpus allatum activity and, therefore, vitellogenesis. Corpus allatum activity (and vitellogenesis) can be induced in virgin females either by cutting the allatic nerves or by excision of a certain part of the protocerebrum. It is concluded that the corpus allatum of virgin females is inhibited nervously by the brain and that copulation provides a nervous stimulus which lifts this cerebral inhibition thereby permitting allatum activity.The median neurosecretory cells are not essential for vitellogenesis in Dindymus; however, it is suggested that they are necessary for maximum allatum activity. Evidence is provided to show that the growth and maintenance of the previtellogenic oöcytes are also under the control of the corpus allatum. A mechanism is described whereby the number of vitellogenic oöcytes in the ovarioles is maintained constant.     

Metamorphosis of the corpus allatum and degeneration of the prothoracic glands during the larval-pupal-adult transformation of Drosophila melanogaster: a cytophysiological analysis of the ring gland

The degeneration of the prothoracic glands of Drosophila melanogaster during pupal-adult metamorphosis was analyzed by light microscopy, scanning, and transmission electron microscopy. The ultrastructural observations were correlated with the ability of the ring gland to synthesize ecdysteroids in vitro. The ring gland is prominent during larval life and is identifiable until just before adult eclosion but undergoes dramatic changes in location, shape, size, ultrastructure, and function during pupal-adult development. Prothoracic gland degeneration is characterized by: a gradual decrease in its ability to synthesize ecdysteroids; a decreasing quantity of smooth endoplasmic reticulum (SER) and mitochondria; the absence of intercellular channels; cytoplasmic fragmentation; and the separation of the prothoracic gland from the corpus allatum and corpus cardiacum. An ultrastructural analysis of the corpus allatum during larval-pupal-adult metamorphosis and adult life was also correlated with function, i.e., juvenile hormone biosynthesis, using a radiochemical assay of ring glands and adult corpora allata in vitro. A relatively high concentration of SER, mitochondria, and mitochondrion-scalariform junction complexes are typical features of an active corpus allatum cell. The migration of the corpus allatum from the ring gland to its position as a separate gland in the adult fly was studied in detail. The capacity of the corpus allatum to synthesize juvenile hormone is at its peak in the ring gland of the early wandering third instar larva, whereas the corpus allatum of 2-day-old female adults displayed the greatest synthetic activity during adult life. The physiological significance of the alterations in gland activity is discussed.     

Hormonal controls on reproduction in female heteroptera

A survey of the literature related to hormonal control of reproduction in female heteropterans reveals many common features. Juvenile hormone secreted by the corpus allatum is the principal hormone governing vitellogenesis. Feeding and nutrition affects egg development via juvenile hormone secreted by the corpus allatum, which is under inhibitory control from the brain. Information about feeding reaches the brain via a humoral route. Similarly, mating increases egg production by altering the degree of inhibition of the corpus allatum by the brain, although the nature of the mating stimulus and the route by which the stimulus reaches the brain remains uncertain. There may be one or more stimulatory factors acting on the corpus allatum. Progress in identifying controls on the corpus allatum is hindered by our ignorance of the identity of the juvenile hormone(s) acting in Heteroptera. Ovulation and oviposition are under the control of a myo-active peptide from the brain, and its release is governed by hormonal inputs from both mating and the ovary. The ovarian input appears to consist of ecdysteroid. A role for ovarian ecdysteroid in controlling the corpus allatum remains uncertain. Arch. Insect Biochem. Physiol. 35:443–453, 1997. © 1997 Wiley-Liss, Inc.     

Changes in mechanical properties of the cuticle and lipid accumulation in relation to adult diapause in the bean bug,Riptortus clavatus

Photoperiodically controlled adult diapause in the bean bug, Riptortus clavatus (Thunberg) (Heteroptera: Alydidae) was due to suppression of corpus allatum activity under short-day conditions. The mechanical extensibility of the cuticle of the pronotum was significantly higher in nondiapause adults reared under long-day conditions than in diapause adults reared under short-day conditions. Furthermore, diapause adults accumulated significantly larger amount of lipids than nondiapause ones. It was then examined whether these two characteristics of adult diapause also depend on activity of the corpus allatum, by removal of the corpus allatum and transection of the nervi corporis allati. Even after these two kinds of surgery, adults responded to photoperiod and showed similar differences both in mechanical properties of the cuticle and in lipid content between long-day and short-day conditions. Therefore, inactivity of the corpus allatum is not responsible for the stiffer cuticle or higher lipid accumulation in diapause adults.     

The rôle of the corpus allatum in prenatal wing determination in Megoura viciae

Crowding stimulates alatae production by the apterous morph of Megoura viciae, but it has no effect on the volume and ultrastructure of the maternal corpus allatum. In adult apterae the corpus allatum appears to be inactive. It is therefore considered that the maternal corpus allatum is not involved in the prenatal control of alary polymorphism in this aphid.     

Corpus allatum activity in vitro during ovarian maturation in the desert locust, Schistocerca gregaria.

1. Radiochemical in vitro assays show that there are large and rapid changes in the spontaneous rate of juvenile hormone synthesis and release during the course of sexual maturation in the locust. 2. Parallel observations on glands incubated with farnesenic acid show that the rate-limiting step is always prior to the stage of esterification of farnesenic acid to the final intermediate, methyl farnesoate. 3. Corresponding changes in oocyte morphometrics do not reveal any clear correlation between endocrine activity of the corpus allatum and either the induction or maintenance of rapid vitellogenesis. 4. Peaks of synthetic activity in the corpus allatum correspond well with the onset of previtellogenic growth in the oocytes. 5. The data do not provide any evidence that 'corpus allatum insufficiency' is responsible for resorption of growing oocytes. 6. It is concluded that short-term in vitro radio-assays provide a valid method for estimating quantitatively the physiological activity of the corpus allatum.     

Juvenile hormone biosynthesis in moths: synthesis and evaluation of farnesol homologs as alternate substrates of farnesol oxidase

The oxidation of farnesol to farnesal is an important step in insect juvenile hormone (JH) biosynthesis and is mediated by one or more alcohol oxidases located within the minute endocrine gland, the corpus allatum. Because lepidopteran insects have the capacity to produce homologous JH structures, the substrate selectivity of farnesol oxidase was examined by determining the ability of several terpenol homologs to inhibit farnesol oxidation in moths. Results utilizing corpora allata homogenates from larval, adult, and embryonic Manduca sexta indicate that increased steric bulk at the C-3 position of the sesquiterpenol chain is detrimental to inhibitory potency. Triethylhomofarnesol (1h), which is precursor to JH 0 and therefore a physiologically important metabolite of M. sexta embryos, was found to be a poor inhibitor of farnesol oxidation but was oxidized in almost same amount as farnesol. This data indicate that farnesol oxidase of the corpus allatum plays a limited role in controlling JH homolog production in moths, and suggests that another oxidative enzyme, which is present at early stages of moth development, is involved in JH homolog construction.     

An ultrastructural and developmental analysis of the corpus allatum of juvenile hormone deficient mutants ofDrosophila melanogaster

Summary The ultrastructure of the corpus allatum of theapterous mutantsap ⁴ andap ^56f ofDrosophila melanogaster during larval-pupal-adult metamorphosis and adult life was correlated with the gland's ability to synthesize juvenile hormone in vitro. During the early wandering period of the third instar of both mutants, a high concentration of smooth endoplasmic reticulum, mitochondria and mitochondrion-scalariform junction complexes are typical features of an active corpus allatum cell. Juvenile hormone biosynthesis by the glands is high at that time and, in fact, only slightly lower than that of wild type glands. In contrast to the wild type gland, the cells of the pupal and pharate adult corpus allatum of both mutants contains highly electron dense mitochondria with tubular cristae but no whorls of smooth endoplasmic reticulum nor glycogen clusters. The frequency and size of the lipid droplets, putatives depots of the juvenile hormone precursors, in cells of theap ^56f gland is a function of the insect's age, but both are lower than in wild type gland cells. Juvenile hormone biosynthesis by both mutant glands remains at the basal level when compared to increased synthesis by the wild type gland. The frequency and density of lipid droplets in cells of theap ⁴ corpus allatum are much lower than in theap ^56f glands. During adult life, the ultrastructural profile of theap ^56f corpus allatum is similar to that of the wild type gland although the in vitro production of juvenile hormone by the former is much lower than that of the wild type gland. The ultrastructural features of the adult corpus allatum ofap ⁴ homozygotes reveal precocious degeneration and support the view that this non-vitellogenic mutant is a juvenile hormone deficient mutation.     

Histophysiological studies on the corpus allatum during prepupal diapause in Monema flavescens (Lepidoptera)

The appearance of the corpus allatum, the central endocrine gland of diapause, was examined histologically in the slug moth prepupae, Monema flavescens (Lepidoptera) Before beginning of diapause, the secretory cells of the corpus allatum increase in size with the enrichment of the cytoplasm in quantity and in number of organelles, while RNA synthesis also starts. As diapause progresses, the secretory cells have many large unstained vacuoles in the cytoplasm, which were demonstrated to contain some substances of lipoidal nature. It is not clear that the substance is juvenile hormone itself or a material related to juvenile hormone. Agranular ER is the most characteristic organelle connected with mitochondria and situated around the vacuoles during diapause. Electron micrographs show that agranular ER and mitochondria have an essential role for the production of juvenile hormone. The function of the corpus allatum during diapause and the relationship between juvenile hormone and diapause are discussed.     

Regulation of the corpora allata in the black mutant of Manduca sexta

Regulation of corpus allatum activity in the black mutant strain of Manduca sexta was studied in vivo and in vitro. Allatectomy, denervation, and implantation studies demonstrated that black mutant corpus allatum activity remains low in both wild-type and black mutant host larvae. Attempts to distinguish humoral control mechanisms versus mechanisms dependent on intact allatal nerves indicated that intact allatal nerves were not required for the reduced black mutant corpus allatum activity in vivo. Incubation of corpora allata, using [1-¹⁴C]propionate as a juvenile hormone biosynthetic precursor and haemolymph as culture medium, confirmed that black mutant corpora allata are suppressed by a factor(s) in the haemolymph. Under identical conditions wild-type corpora allata were unaffected. Finally, the lowered black mutant corpus allatum activity in haemolymph in vitro correlates with the lowered juvenile hormone titre in black mutant larvae.     

Neural control of the corpus allatum in the Colorado potato beetle, Leptinotarsa decemlineata: An electron microscope study utilizing the in vitro tannic acid Ringer incubation method

The release of material from neurosecretory synapses in the corpora allata of the Colorado potato beetle, Leptinotarsa decemlineata was visualised by an electron microscope procedure which involved tissue incubation in tannic acid. Using morphometry, the frequency of exocytosis phenomena was quantified in beetles kept under two different photoregimes. The number of exocytosis phenomena in the neurosecretory synapses in the corpora allata of beetles kept under short days was significantly higher than that of beetles reared under long-day conditions. In addition, the corpus allatum gland cells appeared to be more richly innervated by neurosecretory synapses under short-day than under long-day conditions. Previous studies using the in vitro radiochemical assay showed that the corpus allatum activity of short-day beetles is at least partly restrained by neurally mediated factors. The present morphological data strongly imply that this corpus allatum inhibitory substance is released from the neurosecretory synapses.     

Hormonal Integration of Egg Production in Rhodnius prolixus

SYNOPSIS. This paper reviews the evidence dealing with hormonalcontrols on egg production in Rhodnius prolixus by which theinputs of feeding and mating are integrated. Juvenile hormone,secreted by the corpus allatum, plays a central role in eggproduction, intervening at several sites to control the durationof egg production. The controls on the corpus allatum are complexand apparently highly redundant, and the necessity for thisredundancy is analysed in terms of the strategic advantage conferredon the insect by this network of controls.     

Allatostatin-immunoreactive neurons projecting to the corpora allata of adult Diploptera punctata

Summary A monoclonal antibody against allatostatin I was used to demonstrate the allatostatin-immunoreactive pathways between the brain and the corpus cardiacum-corpus allatum complex in the adult cockroach Diploptera punctata. The antibody was two to three orders of magnitude more sensitive to allatostatin I than to the other four known members of the allatostatin family. Whole and sectioned brains in which immunoreactivity was localized with horseradish peroxidase-H₂O₂-diaminobenzidine reaction showed strongly immunoreactive cells in the pars lateralis of the brain with axons leading to and arborizing in the corpus cardiacum and the corpus allatum. Although many neurosecretory cells of the pars intercerebralis project to the corpora allata only, four strongly immunoreactive cells were evident here (two pairs on either side), and these did not project to the corpus cardiacum and corpus allatum but rather terminated within the protocerebrum in areas in which lateral cells also formed arborizations. Immunoreactivity was found in many other cells in the brain, especially in the tritocerebrum.     

The effects of corpus allatum implantation on the development of flight muscles and fat body in Locusta migratoria

Implantation of corpora allata early in the fifth instar of female larvae of Locusta migratoria results in a faster development both during the last instar and the adult somatic growth period. The adult locusts attain a significantly higher maximum wet weight. The increase in dry weight, however, is smaller than in control insects. So the high titer of corpus allatum hormone results in a considerably higher water content.In CA-implanted locusts the growth of the indirect dorsal longitudinal flight muscles is inhibited and the protein content is lower as compared with control specimens. Especially the differentiation of these muscles is strongly inhibited. A hypothesis for a regulation of the indirect flight muscle development by the changing titer of the corpus allatum hormone is proposed.During the second part of the adult period investigated the high titer of the corpus allatum hormone strongly diminishes the growth of the fat body, but the protein content is not altered in comparison with the normal developing fat body. The data reveal that the influence of an induced high titer of corpus allatum hormone on protein metabolism in the flight muscles is different from that in the fat body.

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Die wirkung von corpora allata-implantation auf die entwicklung der flugmuskeln und des fettkörpers bei Locusta migratoria

Zusammenfassung Nach Corpora allata-Implantation am Anfang des L₅ von weiblichen Larven von Locusta migratoria folgt eine schnellere Entwicklung sowohl im letzten Larvenstadium als auch in der adulten somatischen Wachstumsperiode. Die adulten Heuschrecken erreichen ein signifikant höheres Frischgewicht-Maximum. Die Zunahme des Trockengewichts ist jedoch geringer als bei Kontrollen. Der hohe Titer an Corpus allatum-Hormon resultiert also in einem beträchtlich höheren Wassergehalt.Der Zuwachs der indirekten dorsalen Flugmuskeln ist in mit Corpora allata implantierten Heuschrecken gehemmt und der Eiweißgehalt ist niedriger als bei Kontrollen. Besonders die Differenzierungsphase der Muskeln ist stark gehemmt. Es wird eine Hypothese über die Regulation der Entwicklung indirekter Flugmuskeln durch den sich ändernden Titer des Corpus allatum-Hormons aufgestellt.Während des zweiten Teils der untersuchten adulten Periode nimmt das Wachstum des Fettkörpers unter dem Einfluss des hohen Hormontiters ab, aber der Proteingehalt dieses Gewebes ändert sich im Vergleich zu dem sich normal entwickelnden Fettkörper nicht.Diese Daten zeigen, daß der Einfluss eines induzierten hohen Titers an Corpus allatum-Hormon beim Proteinstoffwechsel in den Flugmuskeln anders ist als im Fettkörper.

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Abbreviations CA corpus allatum - CAH corpus allatum hormone - LFM indirect dorsal longitudinal flight muscle - Tris tris (hydroxymethyl)aminomethane     

Biosynthesis and release of juvenile hormone during the reproductive cycle of the ring-legged earwig

Corpora allata of adult female Euborellia annulipes, incubated in medium containing ³H-methionine, synthesized and released juvenile hormone III. Labelled material co-migrating with methyl farnesoate was also found, suggesting this as an intermediate in the pathway of juvenile hormone III production. Juvenile hormone was not appreciably stored in the glands, but was released into the medium. In normal medium, 93.6 ± 1.6% of the total juvenile hormone III synthesized was released and 96.5% ± 0.3 in medium supplemented with 60 μM farnesoic acid. The rate of juvenile hormone III biosynthesis/release in vitro remained constant for at least 8 hr for glands of different activities. The rate of juvenile hormone production was closely correlated with the gonadotrophic cycle. In females with previtellogenic ovarian follicles (0.26 ± 0.004 mm), hormone production was only 0.59 ± 0.13 fmol hr⁻/corpus allatum; production increased to 1.52 ± 0.25 fmol hr⁻¹/corpus allatum when basal follicles were growing rapidly, and remained high during the period of oviposition. By 3 days following oviposition when females were brooding clutches, hormone production had declined to 0.46 ± 0.13 fmol hr⁻¹/corpus allatum. The addition of 60 μM farnesoic acid to the medium enhanced juvenile hormone biosynthesis at each stage examined. Lastly, elevating the level of l-methionine in the medium also enhanced hormone biosynthesis. Maximal hormone production was 32.8 ± 10.9 fmol hr⁻¹/corpus allatum, at an l-methionine concentration of 51 μM.     

Effects of food and water availability,and of NCA-1 section,upon juvenile hormone biosynthesis and oöcyte development in adult female Periplaneta americana

The combined stimuli from feeding, drinking, mating and crowding are required for the highest rates of oöcyte development in maturing adult female Periplaneta americana. A graded series of “sexually suppressed” females can be produced by withholding one or more of these stimuli, and this stepwise retardation of ovarian development appears to be achieved by a progressive increase in corpus allatum restrain. It seems that all of these environmental cues are centrally integrated such that juvenile hormone-dependent processes can proceed at an appropriate pace. Water availability is evidently the most important factor. Water-deprived females are sexually unreceptive, and are found to have very low rates of juvenile hormone biosynthesis and ovarian development. This holds true even when they are provided with food. In contrast, 75% of starved females are sexually receptive if allowed free access to drinking water. At the same time they have enhanced corpus allatum activity, and show significant oöcyte growth.The mode of regulation of corpus allatum function in adult female P. americana appears to be significantly different to the model proposed for the cockroaches Leucophaea maderae and Diploptera punctata. Allatotropic signals may be more important than inhibitory signals in the former species. The glands continue to be moderately active in fed, mated female P. americana after NCA-1 section (although a major peak of corpus allatum activity is not obvious), and the rate of oöcyte development is not greatly reduced. However, NCA-1 mediated inhibition of juvenile hormone biosynthesis is less readily demonstrated. We could observe no enhancement of corpus allatum activity nor stimulation of oöcyte growth after unilateral NCA-1 section when the operation was performed on starved virgins, and the same result was found after bilateral NCA-1 section when starvation or virginity were separately enforced. A slight stimulation of juvenile hormone biosynthesis, together with a small increase in oöcyte development, could only be demonstrated after both NCA-1 were cut in starved virgins.We conclude that neurally mediated corpus allatum inhibition in has yet to be adequately verified, and that the available evidence does not contradict the theory that juvenile hormone biosynthesis in adult females could be regulated predominantly by chemicals released into the haemolymph.     

Structural analysis of the corpus allatum of an aphid, Aphis craccivora

The structure of the corpus allatum of Aphis craccivora was examined when the gland was in both the active and inactive state. Active glands contained large rounded nuclei around the periphery and a central nervous section with many neurosecretory axons. The cell membranes were very convoluted and often associated with vesicles, particularly in the axonal region and adjacent to the stromal sheath. Inactive glands exhibited smaller and irregular shaped nuclei and extensive vacuolation resulting in the loss of all or part of the central axonal region.The possible role of the gland components in relation to the endocrine function of the corpus allatum is discussed.     

Localization and physiological effects of RFamides in the corpora allata of the cockroach Diploptera punctata in relation to allatostatins

The distribution of FMRFamide immunoreactivity in the brain-retrocerebral complex of adult female Diploptera punctata was examined. Immunoreactivity was observed in the brain and corpus allatum as well as in the corpus cardiacum. Immunoreactivity co-localized with allatostatin immunoreactivity within several lateral neurosecretory cells of the brain and in their endings within the corpus allatum. By in vitro radiochemical assay of juvenile hormone release, the effect of two native D. punctata RFamides, an FLRFamide (Leucomyosuppressin) and an FIRFamide were examined. The latter, for which the sequence (SKPANFIRFamide) is reported here, stimulated juvenile hormone release but acted only on corpora allata from females at the end of vitellogenesis (day 6). The interaction of these two RFamides and three D. punctata allatostatins, Dippu-AST 2, 5, and 7 were similarly examined. Only Dippu-AST 2 stimulated release of RFamides from the corpora allata and only on day 6 whereas both RFamides were able to attenuate the inhibitory activity of Dippu-AST 2.     

Probable mechanism of sexual dimorphism in insulin control of Drosophila heat stress resistance

Adult males of Drosophila species (Drosophila melanogaster L. and Drosophila virilis) show a lower tolerance to heat stress compared with females. The present study investigates the effects of RNA interference (RNAi) knockdown of the insulin‐like receptor in the corpus allatum of D. melanogaster males on dopamine metabolism and content, heat stress resistance and juvenile hormone metabolism. In male flies, the knockdown of insulin‐like receptor in the corpus allatum is shown to change metabolism of juvenile hormone but not dopamine. It is also shown that knockdown of the insulin‐like receptor in the corpus allatum results in a decrease of heat stress resistance in females but not males, and that juvenile hormone rescues this decrease. The results suggest that at least one of the ways in which insulin‐like growth factors affect heat stress resistance is by successive mediation through juvenile hormone and dopamine, which could lead to sexual dimorphism in the trait.     

Activation of egg production and the corpus allatum without feeding in the adult female of the insect Rhodnius prolixus

Summary

In unfed virgin or mated females of Rhodnius prolixus, a proportion of females makes some eggs. Vitellogenesis in this prefeed period resembles closely that in fed females: it involves the activation of follicle cells, the development of spaces between the follicle cells, and a dependency on the corpus allatum and juvenile hormone. It is concluded that juvenile hormone is normally secreted in the period between emergence and the first adult blood meal. Eggs are produced only if sufficient blood remains in the crop from the previous larval meal. The data concerning crops size are consistent with the hypothesis that the activity of the corpus allatum is governed by the degree of distension of the crop or abdomen.