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.     

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.     

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.     

Morphological and histological examination of short‐wing formation in the winter moth Protalcis concinnata (Insecta: Lepidoptera,Geometridae)

Winter geometrid moths exhibit sexual dimorphism in wing length and female‐specific flightlessness. Female‐specific flightlessness in insects is an interesting phenomenon in terms of sexual dimorphism and reproductive biology. In the winter geometrid moth, Protalcis concinnata (Wileman), adult females have short wings and adult males have fully developed wings. Although the developmental process for wing reduction in Lepidoptera is well studied, little is known about the morphology and the developmental pattern of short‐winged flightless morphs in Lepidoptera. To clarify the precise mechanisms and developmental processes that produce short‐winged morphs, we performed morphological and histological investigations of adult and pupal wing development in the winter geometrid moth P. concinnata. Our findings showed that (a) wing development in both sexes is similar until larval‐pupal metamorphosis, (b) the shape of the sexually dimorphic wings is determined by the position of the bordering lacuna (BL), (c) the BL is positioned farther inward in females than in males, and (d) after the short pupal diapause period, the female pupal wing epithelium degenerates to approximately two‐thirds its original size due to cell death. We propose that this developmental pattern is a previously unrecognized process among flightless Lepidoptera.     

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.     

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.     

Effects of Courtship Song in Interspecific Crosses Among the Species of the Drosophila auraria Complex (Diptera: Drosophilidae)

The courtship behavior and the effects of courtship song in inter- and intraspecific crosses were studied in the four sympatric species of the Drosophila auraria complex: D. auraria, D. biauraria, D. subauraria, and D. triauraria. Orientation, tapping, and vibration (the repertoires of male courtship) were observed in both inter- and intraspecific crosses, suggesting that signals from heterospecific females were enough to elicit such male behaviors. The crossability tests with wingless or winged heterospecific males (tests for wing effects) revealed that winged heterospecific males copulated less than wingless ones in all four species but not all the pairwise cases. Since the crossability tests with aristaless females (deaf) or normal females showed essentially the same results as the tests for wing effects, we concluded that the sound produced by wing vibration plays an important role and that the wing movement itself is less important. These findings suggest that courtship songs are of great importance in mate discrimination and the sexual isolation between the species of this complex.     

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.     

Neurons projecting from the brain to the corpora allata in orthopteroid insects: anatomy and physiology

Retrograde and orthograde labeling of neurons projecting to the corpus allatum was performed in locust, grasshopper, cricket, and cockroach species in order to identify brain neurons that may be involved in the regulation of juvenile hormone production. In the acridid grasshopper Gomphocerus rufus L., and the locusts Locusta migratoria (R.&F.) and Schistocerca gregaria Forskal, the corpora allata are innervated by two morphologically distinguishable types of brain neurons. One group of 9–13 neurons (depending on species) with somata in the pars lateralis extend axons via the nervus corporis cardiaci 2 and nervus corporis allati 1 to the ipsilateral corpus allatum, whereas two cells in each pars lateralis have bilateral projections and innervate both glands. No direct connection between the pars intercerebralis and corpus allatum has been found. In contrast, neurons with paired axons innervating both glands are not present in Periplaneta americana (L.) and Gryllus bimaculatus de Geer. Instead, two cells in each pars lateralis project only to the gland contralateral to their somata. Electrophysiological experiments on acridid grasshoppers have confirmed the existence of a direct conduction pathway between the two glands via the paired axons of four cells that have been identified by neuroanatomy. These cells are not spontaneously active under experimental conditions. Ongoing discharges in the left and right nerves are unrelated, suggesting that the corpora allata receive independent neuronal inputs from the brain.     

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.     

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.     

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.     

The architecture of the accessory reproductive glands of the male desert locust. 5: ultrastructure during maturation

The accessory reproductive glands of the male desert locust were studied with the electron microscope from the time of adult emergence until full sexual maturity was attained (10 days). Observations on the changes in the nucleus and the cytoplasm of the glandular epithelium, particularly those organelles involved in the elaboration of cell secretions, were made during the maturation of the accessory glands. Cells of gland 16 (the functional seminal vesicle) exhibit numerous ribosomal aggregates, have a concentration of mitochondria along their luminal surface, and show some secretory activity, even at the time of adult emergence. On the other hand, all other accessory glands show very little development of the secretory apparatus (rough-surfaced endoplasmic reticulum, polyribosomes, Golgi elements, elaborate mitochondria, etc.) until after the fifth adult day. These changes parallel changes in the secretory activity of the adult corpus allatum; and it is suggested that the corpus allatum hormone regulates the maturation of the truly glandular accessory glands of the locust, but not that of the functional vesicle.     

The activity of the corpora allata in the fourth and fifth larval instars of the migratory locust

The presence of juvenile hormone in the haemolymph of larvae of Locusta has been detected by a modified Galleria bioassay and these results are compared with indirect methods of estimating corpus allatum activity. Juvenile hormone is present in the haemolymph during the fourth larval instar except on the last day of the instar, and is absent from the haemolymph of the fifth and final larval instar except on the last day of the instar. Changes in the volumes of the corpora allata simply reflect changes in the growth of the whole insect and are of no value in predicting endocrine activity. Changes in the size of the cells of the corpora allata can be correlated with the presence of juvenile hormone in the haemolymph in the fourth larval instar, but similar changes in cell size occur in the fifth larval instar when no juvenile hormone is present in the haemolymph. The effects of the implantation of corpora allata are unreliable as estimates of corpus allatum activity as isolated corpora allata from fifth instar larvae release juvenile hormone. Indirect methods of measuring corpus allatum activity are thus shown to be unreliable. The R_f value of Locusta juvenile hormone as determined by thin-layer chromatography differs from that of Roeller's juvenile hormone, suggesting that the two hormones might be chemically distinct.     

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.     

Precocene sensitivity of corpora allata in adult female Locusta migratoria after electrocoagulation of the pars intercerebralis neurosecretory cells

Destruction, by electrocoagulation, of the median neurosecretory cells of the pars intercerebralis of 2-day old adult female Locusta migratoria completely suppressed normal juvenile hormone-biosynthetic activity of the corpora allata in most animals. For example, 6 days after electrocoagulation the rates of spontaneous juvenile hormone biosynthesis, measured by radiochemical assay of freshly isolated glands, showed a median value of less than $\text{1}\text{100}$ that of the corresponding sham operated controls, which were then in mid-vitellogenesis. Injection of graded doses (200–1600 μg) of precocene I at this time, followed by assays five days later, resulted in a similar decline of both corpus allatum volume and precocene epoxidase activity (measured by radiochemical assays of precocene I dihydrodiol formation in vitro) in pars intercerebralis-coagulated and sham-operated animals, when expressed as a percentage of their own zero precocene controls. Electrocoagulation of the pars intercerebralis largely prevented the normal increase in both corpus allatum volume and its epoxidase activity, so that by age 13 days these parameters were about 2.5-fold lower in coagulated vs control (sham operated) animals. In fact, electrocoagulation had no marked effect on the value of epoxidase activity per unit corpus allatum volume. It is concluded that the corpora allata from this species and stage are sensitive to precocene irrespective of whether they are active in biosynthesis of juvenile hormone.     

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.     

Differential photoperiodic responses in genetically identical winged and wingless pea aphids, Acyrthosiphon pisum, and the effect of day length on wing development

Abstract. Winged and wingless individuals of a pink clone of the pea aphid, Acyrthosiphon pisum (Harris), showed differences in the response curves for photoperiodic induction of both males and sexual females (oviparae). The critical night length (CNL) for ovipara induction in winged aphids was 0.75 h shorter than in wingless aphids, whereas the CNL for male induction in winged aphids was 1.0h longer than in wingless aphids. This means that in winged aphids the CNL for male induction in winged aphids was 0.5 h longer than that for ovipara induction, while in wingless aphids the CNL for male induction was 1.0–1.5 h shorter than that for ovipara induction, and also the shapes of the curves differed.
Winged aphids were produced by wingless mothers which were crowded as young adults. However, when young adults were crowded in long nights, winged aphids were not produced, and the CNL for wing inhibition was between 9.5 and 10h. This effect of photoperiod on wing induction was maternal.     

Seasonal changes in the flight apparatus of winged females and sexual males of the aphid <Emphasis Type="Italic">Tuberculatus quercicola</Emphasis> (Hemiptera: Aphididae)

Tuberculatus quercicola (Matsumura) feeds on Quercus dentata Thunberg, and has mutualistic interactions with ants. Tuberculatus quercicola has two winged morphs in its life cycle, winged females appear in summer and sexual males appear in autumn. Previous studies have shown that wing loading (ratio of body volume to wing area) is higher for the winged females, because of ant attendance, resulting in extremely low dispersal. It is known that the nutritional quality of host plants is high in spring and autumn, when leaves are growing or senescent, and low in summer when leaves are mature. This study examined the effects of seasonal plant deterioration on the development of flight apparatus (wing size and flight muscle) of winged females and males. Moreover, field intercept traps were used to examine the extent of dispersal of males. The results showed that seasonal plant deterioration affected development of the flight apparatus of winged females, particularly flight muscle. Flight muscle development was significantly higher in winged males in autumn than in winged females. However, winged males were not caught in any of the traps. The different resource allocation to the flight apparatus of winged females and males is discussed.     

Courtship song recognition in the Drosophila melanogaster complex: heterospecific songs make females receptive in D. melanogaster, but not in D. sechellia

Abstract. The courtship song emitted by male wing vibration has been regarded as one of the most important signals in sexual isolation in the species of the Drosophila melanogaster complex. Inter- and intraspecific crosses were observed using males whose wings were removed (mute) or females whose aristae were removed (deaf). Females of D. melanogaster, D. simulans , and D. mauritiana mated with heterospecific males in the song-present condition (cross between normal females and winged males) more often than in the no-song condition (cross between normal females and wingless males or between aristaless females and winged males) or they showed no preference between the two conditions. It is possible that in these females heterospecific courtship songs play a role as if they were conspecific. In contrast, the females of D. sechellia mated with D. melanogaster or D. simulans males in the no-song condition more often than in the song-present condition, suggesting that they reject males with heterospecific song. Female mate recognition depending on the courtship song in D. melanogaster, D. simulans , and D. mauritiana is considered to be relatively broader and that in D. sechellia narrower.