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.     

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.     

Lifetime ovipositional patterns of mated and virgin onion flies,Delia antiqua (Diptera: Anthomyiidae)

Over their 47.2±1.9 (mean±SEM) day lifespan, mated onion flies, Delia antiqua, oviposited more uniformly than did virgins. Mated females began ovipositing at 6.4±0.2 days old and regularly deposited 14.2±0.6 eggs/day for 3-4 weeks. Thereafter, oviposition slowed and stopped at about 1 week before death. Virgin flies began ovipositing 24.7±1.5 days into their 59.0±3.8 day lifespan, and deposited eggs at an increasing rate for 3-4 weeks, generating a mean overall ovipositional rate of 5.8±0.5 eggs/day. The later onset of virgin oviposition (ovipositional activation) and not a shorter ovipositional period largely accounted for the disparity between virgin and mated female lifespans. Mean lifetime egg production of mated females was 475±27 eggs versus 179±30 eggs for virgins. Ovipositional and post-ovipositional periods (34.4±1.8 and 7.2±1.0 days) for mated females were not significantly different from those of virgin females (30.9±3.6 and 6.7±1.2 days). Over 90% of virgin females laid eggs. The distinction between mated and virgin ovipositional patterns may be specifically attributed to differences in: (1) egg maturation, (2) age at ovipositional activation, and (3) egg-laying rate.     

Evidence that the ovaries of Musca domestica do not maintain cyclicity by regulating the corpus allatum.

When the female housefly retains eggs, vitellogenesis in the penultimate oöcytes is suppressed during continued protein feeding. Allatectomy of gravid females or of females with developing oöcytes did not prevent maturation of a second batch of eggs. This result does not support the claim of Adams (1970) that an oöstatic hormone, produced by ovaries with retained eggs, inactivates the corpus allatum (CA) and thereby prevents development of the next batch of eggs.The report of Adams and Hintz (1969) that the CA regulates egg maturation depends on their removal of ring gland, which they incorrectly refer to as ‘allatectomy’. In the present report, removal of the ring gland from 1 day old females suppressed egg development, whereas removal of the CA alone did not. Therefore, sufficient CA hormone for reproduction was secreted within 24 hr of emergence, and it was the removal of the corpus cardiacum, and not the CA, that had prevented egg development in the experiments of Adams and Hintz.     

Post‐mating enhancement of fecundity in female Lygus hesperus

Although mated females of the western tarnished plant bug Lygus hesperus Knight are known to produce more eggs than virgins, the nature of the inducing stimuli and the specific changes occurring in the female require additional elucidation. Compared with virgin females isolated from males, those exposed to male precopulatory behaviours produce similar numbers of eggs, whereas inseminated females produce 50% more during the observation period. Although the quantity of seminal fluids received by a female does not influence egg number, mating twice within a 10‐day span causes a 16% increase in fecundity, on average. Females mating more than twice during the same period do not exhibit additional increases in egg number. Because virgin females contain more chorionated eggs than are laid, mating appears to enhance the rate of oviposition. However, to achieve a sustained increase in fecundity, an augmented rate of oocyte maturation would also be required. Male‐derived spermatophores lack substantive quantities of nutrients that might otherwise have enhanced female fecundity. The total amounts of carbohydrate, protein and lipid, as well as eight essential minerals transferred by the male, are insufficient for producing even a single egg, and the female has already produced a large number of chorionated oocytes before she mates. Collectively, the data suggest that seminal fluid contains one or more activational molecules, such as a peptide, which triggers an increase in egg deposition. A prolonged increase in oviposition rate may be achieved through multiple matings to ensure a supply of sperm or to offset the degradation of the putative activational factor.     

Spermatophore formation and regulation of egg maturation and oviposition in female Heliothis virescens by the male

This study was undertaken, using various surgical manipulations, to examine the role and functions of accessory sex glands and testes in Heliothis virescens in spermatophore formation and stimulation of egg maturation in mated females. Normal females mated to accessory sex glandectomized (-ASG) males produced fewer eggs and retained most of their eggs in ovarioles compared with females mated to sham-operated (+ASG) or normal males. The ASG are the source of the components for spermatophore formation in H. virescens. Females mated to castrated (-Testes) males showed similar pattern of egg production as did females mated to -ASG males. Females mated to -Testes males and those mated to sham-operated (+Testes) or normal males were found to have spermatophore in the bursa after uncoupling. Normal females mated to allatectomized (-CA) males developed similar numbers of total eggs as did females mated to sham-operated (+CA) males and normal males.     

The role of the blood meal in egg-laying periodicity and fecundity in Triatoma infestans

The number of eggs produced by Triatoma infestans is determined by the amount of blood ingested; the formation of one egg requires 16 mg blood. An exogenous supply of juvenile hormone, provided by the implantation of extra corpora aliata, increases egg production per unit of blood ingested. The corpus allatum is therefore implicated in the relationship between nutrition and fecundity. The rhythm of egg production is regulated by the nutritional state of the adult female: when the females are fed at frequent intervals, egg production becomes regular and continuous. This calls into question previous interpretations of egg-laying rhythms in the Triatominae as cyclic.     

The relationship between mating and oogenesis in monarch butterflies (Lepidoptera: Danainae)

We studied the relationship between the timing of mating and oogenesis in monarch butterflies (Danaus plexippus) to determine (1) the potential for male nutrient input into eggs and (2) whether mating stimulates egg development. Most females mated soon after they started maturing eggs. One and 2 days after mating, females contained the same number of mature oocytes as virgin females of the same age, while 3 days after mating they contained more mature oocytes than did virgins. These results confirm the potential for male-derived nutrients to augment oocyte production, but indicate that mating is not required for oocyte maturation to occur.     

Effects of severance of stomatogastric nerves on egg-laying,feeding, and the neuroendocrine system in Melanoplus sanguinipes

The rate of egg-laying by female Melanoplus sanguinipes was reduced to about 60 per cent of that for normal mated females following severance of the recurrent nerve or the frontal ganglion connectives or removal of the frontal ganglion, but it was still somewhat higher than the rate for normal virgin females. Although the fat body was markedly reduced in size, the fact that eggs and some faeces were produced suggests that protein digestion and synthesis did not stop in our experimental insects. Feeding was not affected but food passage along the gut was severely restricted following these operations; however, the corpus allatum was not affected.     

Biosynthetic maturation of the corpus allatum of the female adult medfly,Ceratitis capitata,and its putative control

The major juvenile hormone (JH) homolog synthesized in vitro by the adult female Medfly (Ceratitis capitata) corpus allatum (CA) is JHB(3), with JH-III the minor homolog. Methyl-incorporation in vitro in post-eclosion virgin females is age-dependent. Basal activity occurs during the first four days post-eclosion and increases significantly thereafter, peaking at five days. Biosynthetic maturation of the mated female CA is delayed by one day and reduced considerably. The delayed response may be due to direct cerebral or neural inhibition. Synthetic Drosophila melanogaster sex peptide depresses JH biosynthesis by the Medfly female CA in vitro. Male-derived accessory gland peptides of the Medfly are transferred to the female during mating and a Medfly SP-analog may be responsible for down-regulation of JH synthesis by the CA in mated Medfly females. Mevinolin, an inhibitor of the mevalonate pathway, significantly reduces the biosynthesis of JHB(3), while farnesoic acid, a proximate precursor of JHIII, significantly stimulates the biosynthesis of both JHB(3) and JHIII in vitro.     

Influence of the ovaries on JH titer in Teleogryllus commodus

Mating and availability of substrate were found to have a dramatic effect on the level of egg production and juvenile hormone III (JH III) titer in Teleogryllus commodus. Mated females with egg laying opportunity produced twice as many eggs, and exhibited an 8-fold increase in JH titer, as compared with virgin females or mated females forced to retain most of their eggs due to the absence of substrate for egg deposition. Denervation of the ovaries, or nerve cord transection, also caused accumulation of eggs and lowered the JH level, suggesting a feedback mechanism in which the state of egg depletion of the ovaries determines the level of JH secretion by the corpora allata (CA). Results from ovariectomy of mated or virgin animals suggest that the feedback mechanism includes inhibitory humoral factors secreted by the ovary.     

Some aspects of oögenesis in the stable fly Stomoxys calcitrans (Diptera: Muscidae)

Two distinct patterns of blood ingestion in the female stable fly, Stomoxys calcitrans L. were observed, based on whether or not the female was mated. Mating is not required for oögenesis, but is necessary for oviposition. Virgin females develop eggs but, in the absence of mating, they retain eggs until death. In stable flies, oögenesis appears to be atypical among other dipterans as the penultimate follicles develop and deposit up to 50% yolk before the terminal follicles are matured. Oösorption was seen in the penultimate follicles of virgin females retaining eggs. Accessory-gland implants initiated oviposition in virgin females. However, the total number of eggs laid by such females was 50% less than the number of eggs laid by mated flies.     

Factors responsible for the initiation of a second oöcyte maturation cycle in the ovoviviparous cockroach Nauphoeta cinerea

The factors responsible for the initiation of a second oöcyte maturation cycle were investigated by measuring oöcyte growth, vitellogenin titre, and corpus allatum activity after injection of juvenile hormone and/or removal of the egg-case from pregnant females and by performing ovary and corpus allatum transplant experiments.Egg-case removal in late pregnancy results in immediate oöcyte growth, whereas in early pregnancy oöcyte growth is resumed only after a lapse of time, even after injection of juvenile hormone. This, however, induces an immediate increase in the haemolymph vitellogenin titre. A single injection of 2 or 10 μg of juvenile hormone II first stimulates some oöcyte growth after this lapse of time and later activates the corpora allata, which in turn leads to completion of oöcyte maturation. A repeat injection of 10 μg stimulates continuous oöcyte growth without activating the corpora allata. In the presence of an egg case, activation of the corpora allata is suppressed, even after injection of 2 μg of juvenile hormone III, and the oöcytes do not grow. Injection of higher doses stimulates oöcyte growth and leads to expulsion of the egg case in up to 95% of the females. This, however, is not a direct consequence of the increase in size of the ovaries. Ovary transplant experiment show that in young pregnant females the second generation of oöcyte is not yet competent for growth and that ovaries which are competent can mature in young pregnant females, treated with juvenile hormone, whose egg case has been removed.The results are summarized in a model demonstrating the various factors involved in regulating corpus allatum activity in oöcyte maturation and pregnancy and after application of juvenile hormone. We prepose that the corpus allatum activating effect of exogenous juvenile hormone is mediated by the growing oöcyte and that this activation can be suppressed by the continuous presence of exogenous juvenile hormone.     

Effects of chilling stress on allatal growth and juvenile hormone synthesis in the cockroach, Diploptera punctata

During the ovarian cycle of the cockroach, Diploptera punctata, a mitotic wave occurs in the corpora allata before an increase in gland volume and juvenile hormone (JH) synthesis. Previous studies have demonstrated that the brain inhibits mitosis and JH synthesis in corpus allatum (CA) cells until adult females have mated. Herein, we report that chilling stress effectively suppresses mating induced proliferation of CA cells. In mated females, chilling on melting ice for 0.5-3 hours caused a strong, dose-dependent decrease in mitotic activity. In insects chilled for 3 hours, although the mitotic wave in the CA was practically abolished, CA volume and JH synthesis finally reached peak levels typical of unchilled insects, despite a 2-day delay. Consequently, oocyte maturation and oviposition were also delayed by 2 days, yet in both chilled and unchilled insects, peak values of basal oocyte length were the same. By allowing virgin females to mate on different days after chilling, we found that the chilling effect could be retained in the insect body for at least 2 days. During this period, signals from mating could not effectively remove inhibition of CA cell proliferation. Unilaterally disconnecting the CA from the brain revealed that chilling stress mediated CA cell proliferation via the brain, and did not directly affect the CA.     

Presence and titer of methyl palmitate in the Medfly (Ceratitis capitata) during reproductive maturation

The relative amounts of methyl palmitate (MP) during the first 10 days post-eclosion were determined in whole-body extracts of adult female Ceratitis capitata by SIM monitoring of the 74 m/z fragment. MP peaks in receptive 3-day-old virgin females coincide with previously reported production of Juvenile Hormone (JH) by the corpus allatum (CA). Mating in the Medfly induces female non-receptivity. Indirect evidence suggests that the mevalonate pathway to sesquiterpene biosynthesis is underdeveloped in newly eclosed females. We propose that the pathway leading to synthesis of JH is markedly diverted in non-receptive virgin females to fatty acid synthesis, and partly so-in non-receptive mated females, leading to production of palmitic acid, presumably methylated thereafter. MP is depressed and remains marginal thereafter for the 7 days examined in the virgin female but goes through an apparent second cycle in the mated female. This contrasts with the consistent increase of allatal biosynthesis of MP of virgin and mated females previously reported and suggests additional control mechanisms in vivo. During the period of reduced receptivity following the first mating a second apparent peak of MP is observed. MP is a metabolic default metabolite of reproductively immature females whose putative role in reproductive physiology remains to be defined.     

Virgin wasps develop ovaries on par with mated females, but lay fewer eggs

In the primitively eusocial wasp Ropalidia marginata, mating is not necessary for a female wasp to develop her ovaries, lay eggs, and even to become the sole egg layer of her colony despite the presence of other mated nestmates. Here, we show that virgin wasps do not differ from their mated counterparts in the extent and rapidity of their ovarian development, in the proportion of individuals that build a nest and laid eggs, and in the time taken to do so. However, a significantly larger proportion of virgin females showed resorbing oocytes, and laid fewer eggs as compared to mated individuals. Thus, virgin females have the ability to develop ovaries and lay eggs but also to refrain from necessarily laying all mature eggs produced, before mating opportunities arise. This dual ability would be adaptive in haplodiploid, tropical species with perennial nesting cycles and frequent opportunities for workers to become replacement queens or solitary nest foundresses throughout the year.     

The effect of C18 juvenile hormone and Altosid on the efficiency of egg production in Rhodnius prolixus

The product (R) of the weight of the blood meal and the initial weight of the insect is shown to be a reliable predictor of egg production. The egg production efficiency (E), defined as the number of eggs produced per R, has a value characteristic of virgin females, and another, higher, value characteristic of mated females. Topical applications of C18 JH or Altosid to virgin females increase the value of E to the mated level in a fashion which suggests that these compounds act via a trigger mechanism. These compounds do not affect the rate at which oviposition occurs.     

Role of juvenile hormone-esterase in mating-stimulated egg development in the moth Heliothis virescens

Juvenile hormone (JH) titer in virgin females of Heliothis virescens is significantly lower than that in mated females of the same age. The JH titer in virgin females follows a diel pattern in which it begins to increase towards the end of photophase, remains high around the onset of scotophase, and declines during scotophase. The titer reaches its lowest levels at the onset of photophase, and remains low during the first half of photophase. In mated females, the diel pattern of JH titers is not as pronounced. JH-esterase (JHE) activity in mated females is significantly lower than that of virgin females during photophase; JHE levels in the former are similar to levels seen in newly emerged females. JHE activity in mated females also exhibits a diel pattern, in which activity is low during photophase and high at the onset of scotophase. Evidence for the indirect involvement of JHE in the mating-stimulated egg development is provided by the effect of selected JHE inhibitors in inhibiting JHE activity and stimulating egg production in virgin females.     

Vitellogenin and egg production in the moth,Heliothis virescens

The characteristics of vitellogenin (Vg) and the relationship between Vg production and egg production in the tobacco budworm, Heliothis virescens, were studied. The relationship between Vg production and juvenile hormone (JH) and the impact of mating on Vg and egg production were also investigated. Vg appears in the hemolymph of H. virescens about 6 h after moth eclosion. Vg may be separated into two apoproteins (ApoVg-I and ApoVg-II) by sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE). The molecular weights were calculated to be 156,065 ± 800 for ApoVg-I and 39,887 ± 323 for ApoVg-II. SDS-PAGE analysis revealed that the female hemolymph Vg polypeptides appear to be identical to those from eggs but are absent in male hemolymph. Vg concentration was significantly higher in mated females than in virgin females of the same age at 48 h after emergence. Rates of egg production increased as Vg production increased; rates of egg production in mated females were significantly higher than those of virgin females at 48, 72, 96, and 120 h postemergence. Vg production is dependent on JH, because hemolymph from decapitated females lacked Vg while that of decapitated females treated with synthetic JH had Vg at levels comparable to similarly aged, normal H. virescens females. Hemolymph JH titers in mated females were significantly higher compared with those in virgin females at all sampling periods. The high JH level in mated females may explain the high Vg and egg production in mated H. virescens. Arch. Insect Biochem. Physiol. 34:287–300, 1997. © 1997 Wiley-Liss, Inc.