Reproductive and developmental consequences of a diapause maternal effect in the flesh fly, Sarcophaga bullata

Abstract Progeny of Sarcophaga bullata produced from mothers with a history of short day will not enter pupal diapause even if they are reared in a strong diapause-inducing environment (LD 12:12 h at 20^oC). Short-day exposure and diapause commitment are normally inseparable, but this maternal effect provides a tool for examining separately the effect of photoperiod and diapause commitment. Duration of the wandering period of the third instar is longer in diapause-destined larvae than in non-diapause-destined larvae, and fecundity of flies that have experienced pupal diapause is lower than in long-day flies that have not been through diapause. The puparia of diapausing pupae contain more hydrocarbons than puparia of nondiapausing pupae, and this contributes to higher rates of net transpiration for the nondiapausing flies. Flies showing the maternal effect (short-day experience but no diapause) show an intermediate response: length of wandering, fecundity rate and quantities of puparial hydrocarbon are between the extremes observed in the other two groups of flies. Thus, the maternal effect switches the developmental programme to nondiapause, but the progeny retain some characteristics of diapause. Evidence from reciprocal crosses indicates that the photoperiodic history of the female, rather than the male, is responsible for the influence on fecundity.     

Photoperiodic sensitivity and diapause induction during ovarian,embryonic and larval development of the flesh fly,Sarcophaga argyrostoma

Sensitivity to the daily photoperiod, particularly with respect to pupal diapause induction, was studied during ovarian, embryonic, and larval development of the flesh flySarcophaga argyrostoma. Large flies were shown to have a greater number of primary follicles in their ovaries and to be capable of limited ovarian maturation in the absence of exogenous protein (autogeny). Such ovarian development occurred independently of photoperiod. However, long days experienced during embryogenesis caused more rapid development, and earlier larviposition, than short days. Short days during embryonic and subsequent larval development also induced pupal diapause, whereas long days led to continuous or non-diapause development of the pupae. Pupal diapause could not be induced by photoperiods during the vitellogenic phase of ovarian development. InSarcophaga argyrostoma, a maternal effect preventing pupal diapause among the progeny of files with a diapause history was not observed.     

GABA and picrotoxin alter expression of a maternal effect that influences pupal diapause in the flesh fly, Sarcophaga bullata

A maternal effect that operates in the flesh fly, Sarcophaga bullata Parker (Diptera: Sarcophogidae), prevents the expression of pupal diapause in the progeny of females that have been reared under short day conditions. This set of experiments tests the possibility that the maternal effect can be prevented by the use of various environmental stresses or chemical treatments administered to the mother. High and low temperature shocks, food deprivation and reducing the size of the mother were all ineffective in altering transmission of the diapause-suppressing maternal effect. Several chemical agents, however, were effective. Gamma-aminobutyric acid (GABA) and one of its antagonists, picrotoxin, elicited opposite responses when injected into female flies. Whereas GABA suppressed the incidence of diapause in the female's progeny, picrotoxin increased the diapause incidence, thus suggesting the possibility of a central role for GABA in regulation of the maternal effect. Octopamine and pilocarpine injected into females also were effective in countering the maternal effect and thus permitting expression of diapause in the female's progeny.     

Diapause incidence of progeny in relation to parental geographic origin,host plant and rearing density in the cabbage beetle,Colaphellus bowringi

The cabbage beetle, Colaphellus bowringi Baly (Coleoptera: Chrysomelidae), which is widely distributed in China, undergoes an imaginal diapause in the soil. In this study, we investigated the influences of parental geographic origin, host plant, and rearing density on the diapause incidence of progeny in this beetle. In studies conducted at 25 °C and L12:D12 photoperiod, the proportions of adults entering diapause were significantly different among latitudes from which the parents had been collected. The incidence of diapause increased with increasing latitude. Reciprocal cross tests between post‐diapause adults from different latitudes showed that there were significant differences in diapause incidence between pure‐bred and hybrid adults, suggesting that diapause incidence among progeny was determined by both the female and male, although the female appeared to have a stronger effect than the male. These results revealed that parental origin has an important influence on progeny diapause. Parental host plant species not only affected diapause incidence of the current generation, but also affected the incidence of diapause in the progeny produced by the non‐diapause parents; yet, the parental host plant had no influence on the incidence of diapause in the progeny produced by the post‐diapause parents. Rearing density of the parental generation had no significant effect on the incidence of diapause in the progeny.     

Dopamine is a key factor for the induction of egg diapause of the silkworm, Bombyx mori.

The silkworm, Bombyx mori, enters diapause in the early embryonic stage. Embryonic diapause is induced by incubating eggs of the maternal generation at high temperature (diapause type), whereas incubation at low temperature results in non-diapausing progeny (non-diapause type). Measurement of catecholamine concentrations in haemolymph and brain-subesophageal ganglia (Br-SGs) showed that only dopamine concentrations in both tissues are consistently higher in diapause-type than non-diapause-type larvae and pupae. In particular, the difference in dopamine concentrations in both tissues increases around pupal ecdysis. During the early pupal stage, Dopa decarboxylase activities and mRNA concentrations in Br-SGs were also much higher in diapause-type than non-diapause-type insects. Elevation of dopamine levels induced by feeding Dopa to penultimate-instar and last-instar larvae, and by injecting Dopa or dopamine into pupae 2 days after pupation made the non-diapause-destined insects lay diapause-destined eggs at 59% and approximately 70% frequencies, respectively. Furthermore, injection of Dopa or dopamine elevated mRNA levels of the diapause hormone in the Br-SGs of non-diapause-type pupae 1 day after injection. Incubation of Br-SGs isolated from non-diapause-type day-2 pupae with Dopa or dopamine also stimulated the expression of diapause hormone mRNA. These data indicate that environmental stimuli during embryonic development increase dopamine levels in both hemolymph and Br-SGs from the larval stage to early pupal stage, which results in laying of diapause-destined eggs by female adults through enhanced expression of the diapause hormone gene.     

Geographical variation and inheritance of the photoperiodic response controlling larval diapause in two distinct voltine ecotypes of the Asian cornborer Ostrinia furnacalis

The Asian corn borer Ostrinia furnacalis Guenée (Lepidoptera: Crambidae) enters facultative diapause as fully‐grown larvae in response to short day lengths during autumn. As a result of geographical variations in photoperiodic response, the moths from Nanchang (28.8°N, 115.9°E; NC strain) judge both LD 14 : 10 h and LD 15 : 9 h photocycles as long days and develop directly, whereas moths from Haerbin (44.9°N, 127.2°E; HB strain) judge the same photocycles as short days and enter diapause. Crosses between the two strains are used to evaluate the inheritance of diapause. The critical day lengths for diapause induction in the HB strain are significantly longer than those in the NC strain at all temperatures. The critical day length of F₁ progeny is intermediate between the two strains. However, the critical day length in all crosses is significantly longer with HB strain fathers or grandfathers than with NC strain fathers or grandfathers, indicating that the male parent has significantly more influence on the critical day length of subsequent progeny than the female. The results from all crosses under LD 14 : 10 h or LD 15 : 9 h photocycles at 25 °C show that the inheritance of diapause in O. furnacalis does not fit a purely additive hypothesis and that the capacity for diapause is transmitted genetically in the manner of incomplete dominance. The incidence of diapause for F₁ progeny under an LD 14 : 10 h photocycle is significantly higher than that under an LD 15 : 9 h photocycle, suggesting that the induction of diapause can be influenced by interactions between the F₁ genotype and photoperiod.     

Imidazole derivative KK-42 boosts pupal diapause incidence and delays diapause termination in several insect species

The imidazole derivative KK-42 is a synthetic insect growth regulator known previously to be capable of averting embryonic diapause in several Lepidoptera, but whether it also affects diapauses occurring in other developmental stages remains unknown. In the present study, we examined the effect of KK-42 on pupal diapause in two species of Lepidoptera, the Chinese oak silkworm Antheraea pernyi and the corn earworm Helicoverpa zea, and in one species of Diptera, the flesh fly Sarcophaga crassipalpis. In A. pernyi, KK-42 delayed pupal diapause termination under the long day conditions that normally break diapause in this species. Likewise, in H. zea, KK-42 delayed termination of pupal diapause, a diapause that, in this species, is normally broken by high temperature. KK-42-treated pupae of these two species eventually terminated diapause and successfully emerged as adults, but the timing of diapause termination was significantly delayed. KK-42 also significantly increased the incidence of pupal diapause in H. zea and S. crassipalpis when administered to larvae that were environmentally programmed for diapause, but it was not capable of inducing pupal diapause in H. zea if larvae were reared under environmental conditions that do not normally evoke the diapause response. Experiments with H. zea showed that the effect of KK-42 on pupal diapause was dose- and stage-dependent, but not temperature-dependent. Results presented here are consistent with a link between KK-42 and the ecdysteroid signaling pathway that regulates pupal diapause.     

Pupal diapause of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) mediated by larval host plants: pupal weight is important

Facultative diapause, a strategy that allows insects to initiate additional generations when conditions are favorable or to enter diapause when they are not, has a profound effect on the ecology and evolution of species. Most previous studies have concentrated on the role of photoperiod and temperature in inducing facultative diapause in insects. In contrast, here we studied pupal diapause mediated by larval host plants in the cotton bollworm Helicoverpa armigera, and confirmed that pupal weight is a critical factor. Two groups of third instar H. armigera larvae, kept at 25 °C with L:D = 8:16 and 20 °C with photoperiod of L:D = 8:16, respectively, were fed on six host plants and on artificial diet (as a control) to determine how larval host plants affect diapause incidence and related traits (such as pupal weight and developmental duration). The data showed larval host plants affected diapause incidence significantly and the effects could be masked by low temperature. Further analysis showed that pupal size, not the length of the sensitive stage, affected the decision to enter diapause. In a further experiment, third-instar to final-stage larvae deprived of artificial diet for 2 days demonstrated a direct relationship between pupal weight and diapause incidence. These results suggest that larval host plants, by affecting pupal size, may influence diapause occurrence in H. armigera. This has important adaptive significance for both over-wintering survival and the possibility for completing an additional generation.     

Effects of photoperiod and temperature on reproductive diapause in Ophraella communa (Coleoptera: Chrysomelidae), a potential biocontrol agent against Ambrosia artemisiifolia

Abstract To investigate the seasonal adaptation strategies of Ophraella communa to new habitats, the effects and regulation mechanisms of photoperiod and temperature on the reproductive diapause in a population collected from Changsha, Hunan were examined. Adults showed obvious reproductive diapause, which was regulated by photoperiod and temperature. At 30°C, there was no adult diapause occurring under either long‐day or short‐day conditions; at 25°C the pre‐oviposition period was short and fecundity was high in adult females under L : D 16 : 8 h, whereas under L : D 12 : 12 h, a few females entered reproductive diapause; at 20°C under short‐day conditions, all female adults entered diapause. The pre‐oviposition period was significantly prolonged when the pupae and adults were transferred from long‐days to short‐days, but the day length influence was not obvious when they were transferred only in the adult stage. However, the fecundity dropped greatly no matter whether the photoperiod shifted to short‐days only in the adult stage or whether the shift occurred in both the pupal and adult stage. The fecundity was extremely low when photoperiod shifted from long‐days to short‐days in both pupal and adult stages. This was an indication that the pupal and adult stages were the photoperiod‐sensitive stage for adult reproductive diapause. This was especially true for the photoperiod in the pupal stage, which has a distinctly significant regulative effect on reproductive diapause. Additionally, this article also addresses the reason for different photoperiodic response patterns in reproductive diapause induction between the Changsha strain and the Tsukuba strain (Japan) of O. communa.     

光周期对三带喙库蚊发育期间体内核酸动态的影响

作者测试了长短光周期处理的三带喙库蚊Culex tritaeniornynchus(Giles)各虫态与滞育及解滞蚊体内RNA与DNA的变化.结果表明:幼虫与蛹核酸含量最高,成虫期变化比较稳定.短光周期可以降低该蚊发育期间核酸的合成作用.雌蚊卵形成期间DNA相对稳定,吸血后卵巢开始发育,RNA含量明显增加,36—48小时达到高峰,然后逐渐下降.10—15日龄的滞育蚊体内DNA比发育蚊低,解滞蚊RNA与DNA含量均比发育蚊为高.新蚊、发育、滞育与解滞蚊间DNA、RNA含量不同,DNA、RNA减少与增加可用作判断滞育发生与解除的一个生化指标.     

Parental effects: physiological age, mating pattern, and diapause duration on diapause incidence of progeny in the cabbage beetle, Colaphellus bowringi Baly (Coleoptera: Chrysomelidae)

The cabbage beetle, Colaphellus bowringi Baly, is a short-day species that has both a facultative summer and winter adult diapause. In this study, we systematically investigated the effects of parental physiological age, mating pattern (including mating frequency and delayed mating), and diapause duration on the diapause incidence of progeny in the beetle. As parents aged, progeny diapause incidences showed considerable inter-parental variability and an abnormally varying pattern, but their predicting line was approximate to horizontal when reared under constant conditions. There was significant difference in progeny diapause incidence between multiple-mating and once-mating treatments. Higher diapause incidences in the progeny were observed in delayed-mating treatments. Progeny diapause incidences increased as diapause duration in the parental generation increased, and hibernating individuals produced more diapausing progeny than aestivating ones. Reciprocal cross tests between the post-diapause adults and non-diapause adults with no diapause history showed that the effect of parental diapause duration on the progeny diapause incidence was determined by both mothers and fathers but the mothers appeared to have a stronger effect than the fathers. Our results suggest that the parental age effect in Colaphellus bowringi might not be simply age-dependent, but may be controlled by the interaction of multiple factors, including physiological, environmental, behavioral and genetic factors. We discuss the ecological and physiological significance of these findings.     

Some effects of constant temperature and photoperiod on the diapause response of the flesh fly, Sarcophaga argyrostoma

ABSTRACT. The sensitive period for the induction of pupal diapause in Sarcophaga argyrostoma (R.-D.) (Diptera, Sarcophagidae) extends from the intra-uterine embryos to puparium formation, although the degree of 'sensitivity' declines during that period. Embryos and larvae 'add up' both long and short nights to a threshold. The incidence of diapause may also be influenced by the photoperiodic manipulation of female flies containing ovarian eggs. High temperatures eliminate or override the diapause response, whilst lower temperatures enhance it. Still lower temperatures (10–12°C) bring about a high larval and pupal mortality and a failure to pupate which is more marked in long than in short nights. The results are discussed in terms of the external coincidence model and the concept of the 'photoperiodic counter'.     

Variations in the “spontaneous” dynamics of the tendency to diapause among generations of Trichogramma telengai Sor. (Hymenoptera, Trichogrammatidae)

Variations in the tendency to diapause were investigated in 5 successive generations of 6 parthenogenetic clones of Trichogramma telengai Sor. reared under constant laboratory conditions (the temperature of 20°C and the day length of 18 h). The tendency to diapause was estimated by the proportion of the progeny which diapaused at temperatures of 13, 14 and 15°C. Although the variations in the tendency to diapause in successive generations of different clones were positively correlated, the dynamics of the proportion of diapausing progeny in one of the studied clones was significantly different from that in the other clones reared under the same conditions. Moreover, the differences among subclones originated from the same female were also revealed. Analysis of the results suggests that the interclonal variations in the proportion of diapausing progeny were at least partly caused by endogenous factors. The differences between clones can arise during the development of one generation but can also damp very fast or, at least, they are not accumulated over generations. These variations are probably based on the same epigenetic mechanisms that form the basis of the maternal effect on the progeny diapause in Trichogramma species.     

The impact of diapause on the evolution of other life history traits in flesh flies

Summary Flesh flies (Sarcophagidae) collected in Costa Rica and Panama lack the pupal diapause that is characteristic of flesh flies from the temperate zone and tropical Africa. The absence of a diapause capacity in the neotropical species correlates with several other life history traits: in most species the post feeding wandering phase of the third larval instar is longer and duration is more variable, adult life is longer, clutch size is smaller, and more clutches are produced. Among species that have the capacity for diapause, risk is invested primarily in the diapausing stage and other life stages are brief. Though diapausing species are short-lived, they produce as many or more progeny than nondiapausing species by increasing clutch size. The slower and more variable developmental rate and increased adult longevity desynchronizes development and permits the nondiapausing species to spread an environmental risk over different stages of the life cycle, thus offering an alternative to diapause. Other traits such as body size, developmental velocity, thermal constant thresholds, thermal constants, age at first reproduction, and the interval between clutches do not appear related to the capacity for diapause.     

Environmental Cues, Endocrine Factors, and Reproductive Diapause in Male Insects

Environmental cues, mostly photoperiod and temperature, mediated by effects on the neuroendocrine system, control reproductive diapause in female insects. Arrest of oocyte development characterizes female reproductive diapause, which has two major adaptive functions: It improves chances of survival during unfavorable season(s), and/or it confines oviposition to that period of the year that is optimal for survival of the eggs and progeny. Although reproductive diapause is less well studied in male insects, there may be no sex-dependent differences in regard to the first of these functions. The second one, however, is not valid for the male; instead, selection pressure directs the male's reproductive strategy toward maximum chances of fertilization of the female's eggs with minimum waste of energy. Therefore, in species with female reproductive diapause, the males may or may not exhibit diapause, but if they do, their diapause must be adapted to that existing in conspecific females. Male reproductive diapause is defined as a reversible state of inability of the male to inseminate receptive females. In relation to reproductive diapause, there are several patterns of coadaptations between male reproductive strategy and timing of female receptivity, (a) In some insects, the females are receptive in the early part of their diapause; mating occurs during this period and there is no diapause in the male. The male dies shortly after copulation and the female stores the sperms to fertilize the eggs that develop after termination of the female's diapause, (b) In some species, as in the grasshopper Anacridium aegyptium, females are receptive during diapause; though oocyte development is arrested, copulation occurs and the stored sperms fertilize the eggs when the female's diapause ends. Males were claimed to have no diapause, but recent studies have revealed the presence of a reproductive diapause in a proportion of the males. This and other cases show that female receptivity during reproductive diapause may or may not be accompanied by male reproductive diapause. If there is a reproductive diapause in the male, it is controlled by the same endocrine mechanism, the corpora allata (CA), as in the females, (c) In many species females are refractory during their diapause. In these cases, males exhibit reproductive diapause, which may be light, as in the beetle Oulema melanopus, or well established, as in certain grasshoppers, butterflies, and beetles. In the latter cases, male diapause is controlled by similar environmental cues (photoperiod, temperature) and by the same intrinsic mechanism (neuroendocrine system, especially CA) as female diapause. Nevertheless, male diapause is less intense; the environmental cues leading to its termination are less complex and/or less extreme, so male diapause terminates before that of the females. Presumably, male diapause is under two antagonistic selection pressures: A male should not waste energy by courting dia-pausing refractory females, but he should be ready to copulate as soon as the females become receptive, otherwise he may lose in the competition between males for females. Some further strategies, which do not seem to fit the above patterns, are also outlined.     

苜蓿切叶蜂滞育的诱导因素研究

苜蓿切叶蜂Megachile rotundata(F.)预蛹的滞育主要受光周期和温度的影响。雌蜂感受光周期的变化是决定子代预蛹是否进入滞育的一个主要因素;当代的幼期,特别是高龄幼虫(约3龄)到预蛹这一阶段所感受的温度变化,对预蛹滞育有很大的影响,此期如果环境温度低于(21.59±1.03)℃,可有超过50%的个体进入滞育。此外,放蜂地区的纬度及蜂的代次对预蛹的滞育亦有重要的影响。     

Changes in microRNA abundance may regulate diapause in the flesh fly,Sarcophaga bullata

Diapause, an alternative developmental pathway characterized by changes in developmental timing and metabolism, is coordinated by molecular mechanisms that are not completely understood. MicroRNA (miRNA) mediated gene silencing is emerging as a key component of animal development and may have a significant role in initiating, maintaining, and terminating insect diapause. In the present study, we test this possibility by using high-throughput sequencing and qRT-PCR to discover diapause-related shifts in miRNA abundance in the flesh fly, Sarcophaga bullata. We identified ten evolutionarily conserved miRNAs that were differentially expressed in diapausing pupae compared to their nondiapausing counterparts. miR-289-5p and miR-1-3p were overexpressed in diapausing pupae and may be responsible for silencing expression of candidate genes during diapause. miR-9c-5p, miR-13b-3p, miR-31a-5p, miR-92b-3p, miR-275-3p, miR-276a-3p, miR-277-3p, and miR-305-5p were underexpressed in diapausing pupae and may contribute to increased expression of heat shock proteins and other factors necessary for the enhanced environmental stress-response that is a feature of diapause. In S. bullata, a maternal effect blocks the programming of diapause in progeny of females that have experienced pupal diapause, and in this study we report that several miRNAs, including miR-263a-5p, miR-100-5p, miR-125-5p, and let-7-5p were significantly overexpressed in such nondiapausing flies and may prevent entry into diapause. Together these miRNAs appear to be integral to the molecular processes that mediate entry into diapause.     

The effect of gypsy moth metamorphosis on the development of nuclear polyhedrosis virus infection

The development of nuclear polyhedrosis virus (NPV) infection in gypsy moth (Lymantria dispar) was studied before, during, and after host metamorphosis, and in larvae and pupae in the subsequent generation, to determine whether NPV ingested by late instars can replicate in host tissues through metamorphosis and whether it can be vertically transmitted to progeny. Individuals that survived sublethal dosages of NPV did not differ from undosed insects in pupal weight, fecundity, larval and pupal weight of progeny, or response of progeny to NPV challenge. No evidence of NPV infection or of abnormal histology was found in adult tissues examined by light microscopy and no virus was detected on the surface of eggs produced by NPV-treated moths. No NPV-caused mortality was recorded among undosed progeny of dosed or undosed parents. The progeny of dosed parents were neither more resistant nor more susceptible to LdMNPV than were progeny of undosed parents and lethal times did not differ between groups. Examination of larval, pupal, and adult tissues by DNA hybridization revealed that insects in which NPV DNA was detected died prior to adult eclosion. NPV was not detected in any hosts surviving to the adult stage. These results suggest that survivors of sublethal dosages of NPV avoid infection and are therefore incapable of vertically transmitting infectious virus to progeny.     

Relationships between body size,reproductive traits,and food resource in three species of tropical flesh flies

Intra- and inter-specific comparisons in progeny size and clutch size were used to identify possible selection pressures acting on three sympatric species of ovoviviporous flesh flies. Both progeny and clutch sizes increased with body weight of the female parent in all species. There was no evidence for a simple trade-off between the two traits. In one species, the larger the female adult the smaller the relative biomass of larvae per clutch (total weight of larvae/body weight of female parent). Female flies produced similar progeny and clutch sizes over successive batches. Variation in progeny size did not influence either larval survival or duration of larval and pupal development. However, larger first instar larvae tended to form larger pupae in two of the species. The experiments testing the effect of progeny size on pupal weight under limited food conditions suggest a selective advantage for larger progeny size.