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.     

Effects of precocene and methoprene application in young adult Musca autumnalis

Abstract Observations were made on the relative rates of growth among corpora allata, ovarian follicles and fat bodies in diapausing and reproductive Musca autumnalis DeGeer. Rates of corpora allata growth were greater in long-day than in short-day animals. Topically applied precocene II reduced the size of the corpora allata. Two sequential doses of precocene inhibited vitellogenesis. Topically applied methoprene produced vitellogenesis in short-day flies and inhibited development of hypertrophied fat body. This work provides evidence that Juvenile Hormone is the primary agent controlling diapause and non-diapause (vitellogenic) development in the ovaries of face flies.     

Effects of nutrition and methoprene treatment upon reproductive diapause in Caloptilia fraxinella (Lepidoptera: Gracillariidae)

Abstract Female Caloptilia fraxinella exhibit a prolonged reproductive diapause immediately post adult emergence in mid‐summer until the next spring when mating, egg development and oviposition on fresh Fraxinus spp. leaflets occur. Factors that effect the termination of reproductive diapause are investigated in this species. Caloptilia fraxinella diapausing adults held in overwintering conditions (2 °C, LD 0 : 24 h) for 24 weeks terminate diapause after placement for 2 weeks in simulated summer conditions (24 °C, LD 16 : 8 h) only if they are provided with 10% sugar water. Exogenous application of the Juvenile Hormone (JH) analogue methoprene to moths in both early‐ (summer) and mid‐ (autumn) reproductive diapause demonstrates that JH affects diapause termination but a carbohydrate nutrition source also mediates mating and vitellogenesis. Mating between moth pairs early in diapause occurs only after treatment with methoprene and provision with sugar water. However, there is no impact of mating on the propensity of females to produce vitellogenic oöcytes. Moths collected in the autumn in mid‐diapause respond in a dose‐dependent fashion to methoprene treatment and the response is greater than that of moths early in diapause collected in the summer. Treatment with methoprene and access to sugar water results in vitellogenic oöcytes in 18.75% of females from mid‐diapause moth pairs treated with 0.01 μg methoprene per insect and in all females from pairs treated at the two highest doses of methoprene (0.1 and 1 μg per insect). Mating occurs only between moths in mid‐diapause treated with the two highest doses of methoprene and these doses induce 91% and 100% mating, respectively. Both control and methoprene‐treated males in mid‐diapause held under summer conditions mate successfully and pass a spermatophore to their methoprene‐treated female partner. These data demonstrate that female C. fraxinella undergo a prolonged reproductive diapause in which termination is dependent on JH and further mediated by a carbohydrate nutrition source. The production of vitellogenic oöcytes is independent of mating. These data also provide evidence that response of moths in diapause to exogenous applications of methoprene differs throughout the diapause period and between male and female C. fraxinella.     

Influence of photoperiod on low temperature acclimation for cold-hardiness in Drosophila auraria

ABSTRACT. Imagines of Drosophila auraria Peng, a reproductive diapause species, developed cold-hardiness at low temperatures to a greater extent when exposed to a diapause-inducing photoperiod (LD10:14 h) than when exposed to a diapause-preventing photoperiod (LD 16:8h). Imagines kept at 18°C, which was the temperature at which they were reared to eclosion, did not survive a test exposure to -5°C for 8 days regardless of age or photoperiod. When transferred to 10 or 5°C, either from eclosion or from 8 days after eclosion, the survival rate, on testing, rose with time since transfer and rose faster and higher with a photoperiod of LD 10:14h than with LD16:8h. Flies transferred to 15°C only showed improved ability to survive the test if they were kept in LD 10:14h. When cultured at 18°C to the age of 8 days after eclosion, diapause was terminated in about 30% of females even at LD 10:14h. In these post-diapause females the ability to develop cold-hardiness at lower temperatures was somewhat less than in the diapausing females, but apparently greater than in the non-diapause females. These results suggest that the physiological mechanism which promotes cold-hardiness under a diapause-inducing photoperiod is not directly linked to the process causing reproductive diapause.
In Sapporo, flies from a natural population became tolerant to cold in October when they entered diapause and daily mean temperature fell below 15°C and the light/dark cycle fell below LD 12:12h.     

Diapause detection and monitoring in the Mediterranean corn stalk borer

Abstract. Sesamia nonagrioides Lefebvre diapauses as mature larvae. Once diapause is induced, larvae continue to grow and moult with no apparent changes, so distinction between non-diapausing and diapausing larvae is difficult. In the present work two physiological markers of diapause induction are obtained and their efficacy in detecting diapause onset and in monitoring diapause development in field populations is evaluated. The first marker is based on the differential capacity of two photoregimes, LD 0:24 h and LD 16:8 h, to reverse diapause induction. When larvae of the first and second stadia were subjected to the diapause-inducing LD 12:12 h light cycle and then transferred to LD 0:24 h, larvae pupated after a development duration significantly higher than that of the larvae transferred to LD 168 h. This criterion was used to monitor diapause development in overwintering larvae until field-collected larvae submitted to LD 0:24 h pupated synchronously with those submitted to LD 16:8 h. This occurred between late January and early March. The second marker refers to development of imaginal wing discs. A relative index of the tracheal mass area divided by the total disc area diminishes steadily during development in non-diapausing sixth-instar larvae until it becomes zero just before pupation, whereas it remains constant in diapausing larvae. Though wing disc development was blocked in diapausing sixth-instar larvae, the disc continued to grow and, consequently, the total area of the disc was not a suitable marker of diapause induction. When the constancy of the relative area index was used to monitor diapause development and termination in overwintering larvae, the results agreed with those obtained using the first criterion and with previous field observations.     

Drosophila americana Diapausing Females Show Features Typical of Young Flies

Diapause is a period of arrested development which is controlled physiologically, preprogrammed environmentally and characterized by metabolic depression that can occur during any stage of insect development. Nevertheless, in the genus Drosophila, diapause is almost always associated with the cessation of ovarian development and reproductive activity in adult females. In this work, we show that, in D. americana (a temperate species of the virilis group), diapause is a genetically determined delay in ovarian development that is triggered by temperature and/or photoperiod. Moreover, we show that in this species diapause incidence increases with latitude, ranging from 13% in the southernmost to 91% in the northernmost range of the distribution. When exposed to diapause inducing conditions, both diapausing and non-diapausing females show a 10% increase in lifespan, that is further increased by 18.6% in diapausing females, although senescence is far from being negligible. ActinD1 expression levels suggest that diapausing females are biologically much younger than their chronological age, and that the fly as a whole, rather than the ovarian development alone, which is phenotypically more evident, is delayed by diapause. Therefore, diapause candidate genes that show expression levels that are compatible with flies younger than their chronological age may not necessarily play a role in reproductive diapause and in adaptation to seasonally varying environmental conditions.     

Role of the Corpus Allatum in the Control of Adult Diapause in the Blow Fly,Protophormia terraenovae

Adults of the blow fly, Protophormia terraenovae developed their ovaries promptly after emergence under long-day conditions at 25 degrees C, although they entered diapause under short-day conditions at 20 degrees C. Application of a juvenile hormone analog (JHA), implantation of the corpus allatum (CA) from reproductive adults, or transection of the nervus corporis allati induced ovarian development under diapause-inducing conditions. Removal of the CA suppressed ovarian development under diapause-averting conditions, and JHA application induced ovarian development in allatectomized adults. Therefore adult diapause in P. terraenovae is caused by a reduction of juvenile hormone secretion from the CA, and the endocrine activity of the CA is inhibited through a nervous pathway by the brain in diapause adults. Copyright 1997 Elsevier Science Ltd. All rights reserved     

Juvenile hormone induces ovarian development in diapausing cave-dwelling Drosophila species

Drosophila grisea and macroptera were collected in caves overwintering as adults. The females remained in a state of reproductive diapause which extended until May for macroptera and until July for grisea, whereas the males of both species had mature sperm at all times. Termination of the reproductive diapause under laboratory conditions was accomplished in grisea by exposing them to 14 hr of illumination daily and in macroptera by increasing the temperature to 20°C. Topical application of juvenile hormone (JH) on diapausing grisea caused a prompt termination of diapause and maturation of oöcytes within 10 days. Yolk proteins were found in the haemolymph of diapausing flies but not in their ovaries. In the JH-treated flies, yolk proteins were found in both the haemolymph and the ovaries, suggesting that in this species JH regulates the uptake of yolk proteins.     

Hydrocarbon profiles of diapausing and reproductive adult face flies (Musca autumnalis)

Hydrocarbons present on the cuticle surface of adult face flies, Musca autumnalis, were identified by GC-MS and quantified by GC. Hydrocarbons consisted of n-, monomethyl, and dimethyl alkanes ranging in chain length from 23–29 carbons. Also present were monounsaturated alkenes with chain lengths of 23, 25, 27, and 29 carbons. Wild-caught flies were extracted and hydrocarbon profiles determined for both diapausing and reproductive adult males and females. Few qualitative differences were found between males and females in the hydrocarbon profile. Differences in percent composition were found between diapausing and reproductive flies in monounsaturated alkenes, 4 and 45%, n-alkanes, 24 and 37%, monomethylalkanes, 57 and 15%, and dimethylalkanes, 15 and 2%, respectively, for females. A small difference was found in the total amount of hydrocarbon present, 7.3 ± 0.6 and 9.7 ± 1.1 μg/fly, between diapausing and reproductive female flies, respectively. Adult males also exhibited a similar change in hydrocarbon profile and amount between diapausing and reproductive flies. A laboratory strain of face flies originating in Minnesota was also analyzed, and again similar differences were observed in both male and female flies that were kept under a reproductive or diapause condition. Arch. Insect Biochem. Physiol. 37:206–214, 1998. © 1998 Wiley-Liss, Inc.     

Photo-thermal regulation of diapause in Trichogramma piceum Djur. (Hymenoptera, Trichogrammatidae)

Interaction of the photoperiodic conditions of development of maternal females (day lengths of 2 to 22 h at 20°C) with the thermal regime of development of their progeny (temperature of 12 to 15°C at day length of 12 h) in determination of prepupal diapause in Trichogramma piceum was studied under laboratory conditions. At 15°C the diapause was practically absent. At lower temperatures, the proportion of diapausing prepupae was maximal (25% of larvae at 14°C, 70% of larvae at 13°, and 80% of larvae at 12°C) if the maternal females developed under short day conditions (10–12 h). When maternal females developed at day lengths of 18–20 h, diapause was rarely recorded at all temperatures, while ultra-short (less than 8–10 h) days also caused a decrease in the proportion of diapausing progeny. The right (ecologically important) threshold of this maternal long-day photoperiodic response was about 14–15 h independently of the temperature during the progeny development. These results make it possible to clarify the mechanism of the “maternal photoperiodic correction of the progeny thermal response.” Although the impact of the maternal photoperiodic response can be revealed only within a very narrow thermal range, the relative strength of the diapause-inducing effect of different day lengths is independent of the temperature regimen of the progeny development.     

Cold-hardiness in the predatory miteAmblyseius potentillae (Acari: Phytoseiidae)

Cold-hardiness was studied in the predatory miteAmblyseius potentillae (Garman) by determining the mortality after exposure to –5°C. Predators reared under diapause-inducing conditions were more cold-resistant than mites that had been kept under long-day conditions. An acclimatization period at 4°C prior to exposure to sub-zero temperatures had a positive effect on the cold-hardiness of the predator, and was remarkable in diapausing mites.Lower temperatures during diapause induction had a positive effect on cold resistance in this predator; mites in which diapause was induced at 15°C were more cold-resistant than mites that had been subjected to short-day conditions at 18 and 20°C.A day/night temperature rhythm did not increase the cold-hardiness of the mite when grown under long-day conditions. Such a rhythm did increase the cold-hardiness of the diapausing predator when given a short acclimatization period, but this effect disappeared after longer acclimatization periods.     

Polymorphism in the couch potato gene clines in eastern Australia but is not associated with ovarian dormancy in Drosophila melanogaster

Natural selection can generate parallel latitudinal clines in traits and gene frequencies across continents, but these have rarely been linked. An amino acid (isoleucine to lysine, or I462K) polymorphism of the couch potato (cpo) gene in Drosophila melanogaster is thought to control female reproductive diapause cline in North America (Schmidt et al. 2008, Proc Natl Acad Sci USA, 105, 16207-16211). Here, we show that under standard diapause-inducing conditions (12 °C and short photoperiod) (Saunders et al. 1989, Proc Natl Acad Sci USA, 86, 3748-3752), egg maturation in Australian flies is delayed, but not arrested at previtellogenic stages. At 12 °C, the phenotypic distribution in egg development was bimodal at stages 8 and 14 and showed a strong nonlinear pattern on the east coast of Australia, with incidence of egg maturation delay (ovarian dormancy) increasing both toward tropical and temperate climates. Furthermore, we found no evidence for an association between the cpo I462K polymorphism and ovarian dormancy at either 12 or 10 °C (when egg maturation was often delayed at stage 7). Owing to strong linkage disequilibrium, the latitudinal cline in cpo allele frequencies was no longer evident once variation in the In(3R)P inversion polymorphism was taken into account. Our results suggest that the standard diapause-inducing conditions (12 °C and short photoperiod) were not sufficient to cause the typical previtellogenic developmental arrest in Australian flies and that the cpo I462K polymorphism does not explain the observed delay in egg development. In conclusion, ovarian dormancy does not show a simple latitudinal cline, and the lack of cpo-dormancy association suggests a different genetic basis to reproductive dormancy in North America and Australia.     

Diapause induction in the oblique-banded leafroller Choristoneura rosaceana (Lepidoptera: Tortricidae): Role of photoperiod and temperature

Induction of diapause in the larval stage of the oblique-banded leafroller, Choristoneura rosaceana (Harris), was found to be dependent on both photoperiod and temperature. At constant temperatures of 24, 20 and 16°C, short photoperiods induced diapause. The critical photoperiod was between 14–15 h of light per day at 20 and 16°C. At 14 h light: 10 h dark, all larvae expressed diapause. Temperature had a modifying effect, and slightly shifted the larval response to diapause-inducing photoperiods. High constant temperatures of 28°C and above induced diapause in some individuals (< 20%), while fluctuating temperatures of 32 and 16°C in a 12-h cycle resulted in 67% diapause induction, suggesting that diapause could also be induced by fluctuating temperatures, particularly if the higher temperature exceeds 25°C.The first- and the second-instar larvae were the only two stages sensitive to diapause induction. Exposure of adult, egg and third, fourth, and fifth-larval instars to diapause-inducing conditions did not produce diapause. Although diapause was induced in the first or the second instars, it was always expressed in the third or fourth instar.     

Diapause and seasonal life cycle strategy in the house spider, Achaearanea tepidariorum (Araneae, Theridiidae)

Abstract In order to elucidate the mechanism regulating its seasonal life cycle, the photoperiodic response of Achaearanea tepidariorum has been analysed. Nymphal development was faster in long-day and slower in short-day photoperiods. The combined action of low temperature, poor food supply and short daylength induced diapause at an earlier developmental stage than short days alone. Thus, photoperiod is a primary factor inducing nymphal diapause, but the diapausing instar is influenced by both temperature and food supply. Hibernating nymphs became unresponsive to photoperiod in late December. After hibernation, however, sensitivity was restored and the nymphs remained sensitive to photoperiod throughout their life. This spider could also enter an imaginal or reproductive diapause. Photoperiod was again a primary inducing factor and temperature modified the photoperiodic response to some extent. The induction of the reproductive diapause was almost temperature-compensated whereas development was not. So the involvement of a photoperiodic counter system was suggested. Irrespective of whether the nymph had experienced diapause or not, the imaginal diapause was induced in response to a short-day photoperiod after adult moult. Based on these observations, the seasonal life cycle and the adaptive significance of nymphal and imaginal diapause are discussed.     

Photoperiodic control of adult diapause in the predacious mite, Amblyseius potentillae: repeated diapause induction and termination

ABSTRACT. Photoperiodic control of facultative reproductive diapause was examined in females of the phytoseiid mite, Amblyseius potentillae (Garman). Full diapause was induced by rearing the mites from egg to adult under short-day photoperiods. Egg-laying females, however, which had experienced a long-day photoperiodic regime during pre-imaginal development, could still be induced to enter diapause when they were transferred to a short-day regime. Diapause development proceeded slowly under a short-day photoperiod, but was accelerated under long days. During diapause development under short days the photoperiodic sensitivity of the females diminished gradually and ultimately disappeared completely. However, after completion of diapause, sensitivity to photo-period reappeared. A second diapause could be induced in post-diapause females under short-day photoperiods and completed again under long-day photoperiods. These results show that A. potentillae remains sensitive to diapause-inducing and diapause-averting daylengths during the adult stage and that a second diapause may be induced after completion of the first one.     

Environmental induction of larval diapause and life-history consequences of post-diapause development in the Large Copper butterfly,Lycaena dispar (Lepidoptera: Lycaenidae)

Many insects in temperate zones withstand the adverse conditions of winter through entering diapause and the two most important environmental stimuli that induce diapause are photoperiod and ambient temperature. The Large Copper butterfly, Lycaena dispar Haworth (Lepidoptera: Lycaenidae), is a Palearctic butterfly that hibernates as larvae. Since this butterfly is a near threatened species in some regions, there has been a growing need for a standardized protocol for mass rearing of this butterfly based on the adequate knowledge of its ecology. In the present study, we first identified that L. dispar larvae were sensitive to the photoperiodic induction of diapause during their first larval instar. We then investigated to what extent the diapause-inducing effects of photoperiod could be modified by ambient temperatures in L. dispar larvae by exposing them to the range of day-lengths (L:D 14:10, 12:12, 10:14 and 8:16) at three different temperatures (15, 20 and 25 °C). All larvae were induced to enter diapause at low ambient temperature (15 °C) regardless of photoperiod, whereas most of them (86 %) exhibited direct development when temperature was high (25 °C). The photoperiodic induction of diapause was evident when day-length was shorter than 14 h at intermediate temperature (20 °C). Pre-diapause development was prolonged at low temperatures. Finally, we found that post-diapause development of L. dispar larvae was determined by both the chilling temperature experienced by diapausing larvae and the duration of larval diapause. Adult emergence was enhanced when larvae were chilled at 8 °C and when they had been under the state of diapause for 20 days before they were treated to terminate diapause.     

The effect of allatectomy and photoperiod on the supercooling point in Pyrrhocoris apterus adults

Abstract Adults of Pyrrhocoris apterus (L.) (Heteroptera: Pyrrhocoridae) reared at 26°C had a considerably lower supercooling point (SCP) in diapause-inducing (LD 12:12 h) than in diapause-inhibiting (LD 18:6 h) photoperiodic regimes. Exposure of the insects to diapause-inducing acclimation conditions (LD 8:16 h and a temperature of 20°C during photophase and 5°C during scotophase) for 2–3 weeks had very little effect on the SCP, irrespective of the rearing photoperiod. Allatectomized adults kept continuously at LD 18:6 h and 26°C had high SCP similar to intact or sham-operated insects. In contrast to non-allatectomized insects, the SCP of allatectomized insects decreased after an exposure of from 2 to 3 weeks to diapause-inducing acclimation conditions (see above) almost to the level found in the intact diapausing insects. The relationship between the decrease of SCP and ‘diapause syndrome’ (de Wilde, 1970) is discussed.