D2‐like dopamine receptors mediate regulation of pupal diapause in Chinese oak silkmoth Antheraea pernyi

The present study investigated the pharmacological properties of dopamine receptors that functioned in the termination of pupal diapause in the Chinese oak silkmoth, Antheraea pernyi (Lepidoptera: Saturniidae). Dopamine receptors are classified according to their structure and function into two subfamilies as D1‐ and D2‐like receptors. D1‐like receptors activate, whereas D2‐like receptors inhibit, adenylate cyclase. We examined the effects of agonists and antagonists selective for D1‐ and D2‐like receptors on the diapause state. As A. pernyi is a long‐day species, pupal diapause is maintained during short days and can be terminated by exposure to a long‐day photoperiod. The D2‐like receptor‐selective agonist quinpirole delayed the timing of adult emergence under long days, and the D2‐receptor‐selective antagonist sulpiride terminated pupal diapause even under a short‐day photoperiod. The D1‐like receptor‐selective agonist and antagonist, SKF‐38393 and SCH‐23390, respectively, caused no significant effects on diapause pupae. These results suggest that not D1‐ but D2‐like receptors mediated diapause regulation in A. pernyi. This dopamine pathway appeared to block the termination of pupal diapause. Furthermore, the actions of the cAMP analog 8‐CPT‐cAMP and dopamine receptor antagonists upon diapause pupae were similar, which supports the notion that D2‐like receptors involved in diapause of this insect prevent adenylate cyclase from producing cAMP like vertebrate D2‐like receptors. Taken together, our findings suggest that dopamine blocked diapause termination through D2‐like receptors that inhibited adenylate cyclase in A. pernyi. During short days under which diapause was maintained in pupae, the dopaminergic mechanism might be stimulated to suppress cAMP levels in cells regulating diapause.     

Photoperiodic response of diapause induction in the pine caterpillar, Dendrolimus punctatus

The pine caterpillar, Dendrolimus punctatus (Walker) (Lepidoptera: Lasiocampidae), is a multivoltine pest of pine trees in China, overwintering as larvae. Winter diapause was induced by short day length. The critical night length was about 10 h 40 min at 25, 28, and 31 °C in the field, showing a temperature‐compensated diapause induction. Transfer experiments from a short night (L16:D8) to a long night (L12:D12) or vice versa at different times after hatching showed that sensitivity to day length was restricted to the first 14 days; the required day number for a 50% response at 25 °C was about 3.5 days for short nights but 7.5 days for long nights, indicating that short nights are photoperiodically more effective. When four successive short nights (L16:D8) were used to interrupt the long‐night regime (L12:D12) at different development stages and vice versa, the results showed that the highest sensitivity to photoperiod occurred on the 4th?8th day, corresponding to the second larval instar. Experiments of alternating short‐night (L16:D8) and long‐night (L12:D12) cycles during the larval period showed that the information of short nights as well as long nights could be accumulated. By rearing the larvae under conditions other than 24‐h light–dark cycles, we clearly showed that the dark period (scotophase) played a major role in the determination of diapause. The Nanda‐Hamner and Bünsow experiments failed to reveal rhythmic fluctuations with a period of about 24 h in the occurrence of diapause. Therefore, the photoperiodic clock in D. punctatus is an hourglass timer or a damped circadian oscillator.     

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.     

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.     

Diapause decision in the small tortoiseshell butterfly,Aglais urticae

Insects in temperate areas spend the inhospitable winter conditions in a resting stage known as diapause. In species that diapause in the larval or pupal stage, the decision whether to diapause or develop directly is customarily taken during the late instars, with long days (i.e., long light phases) and high temperatures promoting direct development. Among butterflies that overwinter as adults, data are rare and variable, but imply that the larval daylength conditions can affect the pathway decision. We studied the small tortoiseshell, Aglais urticae L. (Lepidoptera: Nymphalidae, Nymphalini), which is partially bivoltine from Central Scandinavia and southwards, and tested whether the pathway decision is taken in the larval or adult stage. We reared larvae under long‐day (L22:D2) or short‐day (L12:D12) photoperiods, and recorded the pathway taken by the eclosing adults by scoring their propensity to mate and produce eggs. We also tested whether the larval photoperiod influenced adult ability to diapause by assessing adult survival. The results clearly indicate that (1) there is no detectable effect of larval photoperiod treatment on the pathway decision taken by adults whether to enter diapause or to develop directly, (2) some individuals are obligately univoltine and insensitive to photoperiod during adulthood, whereas (3) other individuals can facultatively enter diapause or direct development, depending on the photoperiod experienced after adult eclosion.     

Testicular development in Siberian hamsters depends on frequency and pattern of melatonin signals

We investigated the impact of frequency and pattern of melatonin signals on reproductive development in Siberian hamsters. Juvenile males gestated in short day lengths and housed in constant illumination to suppress melatonin secretion were infused with melatonin for 5 h either once or twice per day for 20 days. Melatonin infusions at either frequency produced equivalent increases in testes and body weights that exceeded those of animals infused with saline but were indistinguishable from those of hamsters transferred to long day lengths. The reproductive system appears to be maximally stimulated by a single short melatonin signal each day. Other animals kept from birth in a short photoperiod were treated 6 h after onset of darkness with the beta-adrenergic receptor antagonist DL-propranolol to shorten melatonin secretion on the night of injection but not on subsequent nights. This permitted interpolation of short nightly melatonin signals of 4-5 h duration against a background of long melatonin signals of 10-12 h duration on other nights. Treatment regimes that maintained a 1:1 ratio of short to long melatonin signals for 8 wk stimulated reproductive development; a 1:2 signal ratio, in each of three different patterns, was uniformly ineffective. The number of successive short melatonin signals had little influence on the interval across which successive melatonin signals were summated to influence photoperiodic traits. The neuroendocrine axis appears more responsive to short melatonin signal frequency than pattern for development of the summer phenotype.     

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.     

Genetic analysis of diapause capability and association between larval and pupal photoperiodic responses in the flesh fly Sarcophaga similis

Abstract A variant of the flesh fly Sarcophaga similis, which does not enter pupal diapause even under diapause‐inducing conditions, is established by artificial selection. Interline crosses of the wild‐type and the variant revealed that the diapause capability is inherited in an incomplete dominant manner. Neither sex linkage nor a maternal factor is involved in the mode of inheritance. Genetic and genetic–environmental interactions are involved in the induction of diapause. In the wild‐type, the post‐feeding larval period is prolonged in response to short days. However, in the variant, the duration of the larval period under short‐day conditions is identical to that under long‐day conditions. Long‐day responses under short‐day conditions at both the larval and pupal stages in the variant indicate that the responses are established by common factors in both stages. The factors causing the long‐day responses under short‐day conditions at different developmental stages in the variant remain to be identified. However, it is plausible to hypothesize that common factors regulate ecdysteroid release at both the larval and pupal stages, and that malfunction of the system regulating these factors triggers such ecdysteroid release, irrespective of the photoperiod. Hence, the photoperiodic responses disappear in the variant in both stages. The adult stage of the variant has a functional circadian clock, suggesting that the nondiapause phenotype is not necessarily involved in malfunction of the circadian clock.     

Hormonal control of diapause in the tick Argas arboreus

During the mid-diapause period of the female tick Argas arboreus, nerve ganglion (G) extract (GE) from nondiapause (ND) females injected into diapause (D) female haemocoel after feeding, but not before feeding, terminated diapause in 50% of the ticks. ND haemolymph (H) failed to terminate diapause. Reciprocal injections of D GE, and H induced diapause in most ND females. During the late diapause season, ND GE, and H terminated diapause in D females and reciprocal injections of D GE, and H failed to induce diapause in ND females. The results suggest that in A. arboreus the facultative diapause results from gonadotropic hormone (GTH) deficiency in the presence of a diapause inducing factor (DIF). We suggest that the DIF is formed under the influence of short photoperiod in unfed females. The DIF interferes with normal release of the GTH formed in ganglion after feeding and also with the effect of GTH in the H by direct inhibition and/or by preventing the target organs (ovary and/or gut cells) from responding to GTH. The DIF is degraded slowly during short photoperiod and rapidly during long photoperiod.     

Variations of biogenic amine levels in the brain of Pieris brassicae pupae during nondiapausing and diapausing development

The post-embryonic development of Pieris brassicae can either be continuous (under a long photoperiod) or interrupted at the pupal stage (induced by a short photoperiod); this phenomenon is termed facultative diapause. Several studies have indicated that certain brain mechanisms could be directly involved in the perception of variations in the photoperiod and could mediate some physiological effects particular to dormancy. Biogenic amines have been particularly implicated in the response to photoperiod variations and also in the regulation of development, especially in diapause induction and termination. High performance liquid chromatography with dual electrochemical detection has therefore been used to measure several biogenic amines in pupal nervous tissues at various stages of nondiapausing and diapausing development. During direct development, the levels of dopamine (DA) and N-acetyldopamine (NADA: a DA metabolite) in brain were relatively high in 3-day-old pupae and at the end of pupal life (on the 8th day). Dihydroxyphenylacetic acid (another metabolite of DA) showed no variation. Serotonin was mainly observed in 2–3-day-old pupae but 5-hydroxyindoleacetic acid was never detected. In young diapausing insects, similar variations of DA levels were observed even though a slight decrease of DA metabolites was noted. Serotonin appeared somewhat later (4–5 days) and attained higher levels. In late diapausing pupae, a marked increase in DA levels was observed, especially when pupae were kept at low temperature (4°C). During diapause, serotonin levels were reduced or even absent.     

Diapause induction and termination in the predatory mite Euseius finlandicus in peach orchards in northern Greece

The course of diapause induction as well as of diapause termination infemales of the predatory mite Euseius (Amblyseius)finlandicus Oudemans (Acari: Phytoseiidae) in Northern Greece wasdetermined by transferring females during winter and early spring from peachtrees to a short day (LD 8:16) or a long day (LD 16:8) photoperiod both at 20°C. The first diapause females were found in mid September andby the first week of October all the females were in diapause. The mean numberof days required for diapause termination under the short day photoperiod LD8:16 was gradually reduced from 93.7 days in the beginning of October to lessthan 20 days in mid February and early March. Under the long day photoperiod ofLD 16:8 diapause was terminated in less than 20 days irrespective of the dateof collection. These results indicate that by mid February photoperiodicsensitivity of females was lost and diapause was terminated. However, femaleswere found in their overwintering sites until the second half of March,probablybecause of the prevailing relatively low temperatures and lack of adequatefood.     

Diapause‐inducing signals prolong nymphal development in the two‐spotted spider mite Tetranychus urticae

Female two‐spotted spider mite Tetranychus urticae are grown under different photoperiods and the photoperiodic regulation of diapause is examined. The photoperiodic response curve for diapause induction was of the long day–short day type, with critical day lengths (CDLs) of 2 and 12.5 h; diapause was induced between these CDLs. The preimaginal period is significantly longer in diapausing females than in non‐diapausing females; moreover, a significant positive correlation is detected between diapause incidence and deutonymphal period. Diapause incidence is high when long‐night photoperiods are applied against a background of continuous darkness in the stages including the deutonymph; this stage appears to be the most sensitive to photoperiod. These observations suggest that diapause‐inducing conditions inhibit nymphal development, particularly in the deutonymphal stage when photoperiodic time measurement for determination of reproduction or diapause is carried out.     

Control of summer and winter diapause in the leaf-mining fly Pegomyia bicolor Wiedemann (Dipt., Anthomyiidae)

Effects of photoperiod and temperature on diapause induction and termination were investigated in both aestival and hibernal pupae of Pegomyia bicolor Wiedemann under field and laboratory conditions. In the field, summer diapause had occurred already in part of the first pupal population; the proportion of diapause gradually rose as the day length and temperature increased. This fly is a short-day species with a pupal summer and winter diapause. Summer diapause was induced by both long day-lengths and mild temperatures. The whole larval life is sensitive to photoperiod. Winter diapause was induced mainly by low temperatures, especially in the first 10 days after pupation. High temperatures strongly enhanced summer diapause induction regardless of photoperiod. The diapause-averting influence of short photoperiods was fully expressed only at moderately low temperatures. High temperatures delayed diapause development, resulting in a rather long summer diapause; whereas low temperatures hastened it, leading to a short winter diapause and showing a low thermal threshold for diapause development. In the field, the post-diapause development started in January, the coldest month, suggesting that the thermal requirements for post-diapause development is also low.     

The effect of cold temperature exposure and long-day photoperiod on the termination of the reproductive diapause of newly emerged female Pissodes strobi (Coleoptera: Curculionidae)

Abstract

• 1 There is confusion in the literature concerning a possible reproductive diapause in the adult white pine weevil Pissodes strobi.
• 2 We evaluated the effects of temperature, photoperiod, feeding substrate and mating status on the sexual maturation and oviposition of female white pine weevils.
• 3 Less than 30% of female P. strobi became sexually mature and laid eggs without experiencing dormancy under a temperature regime of 2 °C for 4 weeks.
• 4 Among the females that experienced a cold temperature treatment after emergence, 80% laid eggs after dormancy when exposed to a long‐day (LD 16 : 8 h) photoperiod and 17.6% laid eggs when exposed to a short‐day (LD 8 : 16 h) photoperiod.
• 5 Significantly more eggs were laid by all the females (with and without a cold treatment) when subjected to a long‐day photoperiod compared with a short‐day photoperiod.
• 6 A period of cold temperature followed by exposure to a long‐day photoperiod with warmer temperatures is required to break reproductive diapause and to obtain a good oviposition response in female P. strobi.
• 7 This study reveals the existence of much intraspecific variation in the response of the white pine weevil to temperature and photoperiod with respect to the induction and termination of reproductive diapause.

     

Effect of photoperiod on the induction and maintenance of diapause and on development of the predatory bugPodisus maculiventris (Hem.: Pentatomidae)

The predatory bugPodisus maculiventris Say displays a reproductive diapause. In the laboratory, at 23±1°C, when the pre-imaginal stages were reared on larvae ofGalleria melonella L. (Lepidoptera: Pyralidae) under a short photoperiod of 8L: 16D, diapause was induced in all adult females, whereas under a long photoperiod of 16L: 8D none entered diapause. Nymphal development was faster under the diapause-inducing short photoperiod than under the diapause-averting long photo-period. By contrast, embryonic development was faster under the long than under the short photoperiod. Diapause maintenance was also under the control of photoperiod. After a 10-d-period of chilling at 4°C, diapause was quickly terminated in adults kept under long photoperiod whereas it was maintained in most of those kept under short photoperiod. The predation rate of non-diapause or post-diapause adult females was much higher than that of diapause females.     

Pupal diapause of Helicoverpa armigera (Lepidoptera: Noctuidae): sensitive stage for thermal induction in the Okayama (western Japan) population

Helicoverpa armigera (Hübner) exhibits a facultative pupal diapause, which depends on temperature and photoperiod. Pupal diapause is induced at 20 degrees C by short photoperiods and inhibited by long photoperiods during the larval stage. However, in some pupae (35% of males and 57% of females) of a non-selected field population from Okayama Prefecture (34.6 degrees N), diapause is not induced by short photoperiods. In the present experiment, the importance of temperature for diapause induction was studied in the non-diapausing strain, which was selected from such individuals reared at 20 degrees C under a short photoperiod of 10L:14D. Furthermore, the sensitive stage for thermal determination of pupal diapause was determined by transferring larvae of various instars and pupae between 20 degrees C and 15 degrees C. Diapause was induced by 15 degrees C without respect to photoperiod. When larvae or pupae reared from eggs at 20 degrees C under a short or a long photoperiod were transferred to 15 degrees C in the periods of the middle fifth instar to the first three days after pupation, the diapause induction rate was significantly reduced in both males and females, especially in females. In contrast, when larvae or pupae reared at 15 degrees C were transferred to 20 degrees C in the same periods, diapause was induced in males, but not in females. However, the diapause induction rate of pupae transferred to 20 degrees C on the fourth day after pupation was significantly increased in females. The results show that temperature is the major diapause cue in the photoperiod-insensitive strain and the periods of middle fifth larval instar to early pupal stage are the thermal sensitive stages for pupal diapause induction with some different responses to temperatures between males and females in H. armigera.     

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'.     

The effect of larval photoperiod on pupal colour and diapause in swallowtail butterflies

ABSTRACT.

• 1 There are significant differences in the effects of larval photo-period on diapause and pupal colour among the species Papilio polyxenes Fabr., P.troilus L., Battus philenor (L.) and Eurytides marcellus (Cramer).
• 2 Diapause and pupal colour in P.polyxenes and P.troilus are strongly influenced by larval photoperiod, short photophase eliciting brown diapausing pupae. Photoperiods of 15L:9D permit the expression of the green and brown pupal colour alternatives.
• 3 Pupal colour in B.philenor and E.marcellus is not affected by larval photoperiod, but short photophase induces diapause in these species.
• 4 All species except B.philenor show an association between brown pupal colour and diapause: Emarcellus when reared on long (midsummer) photophase, P.polyxenes and P.troilus when reared on short (autumnal) photophase.
• 5 In P.polyxenes, short photophase can affect pupal colour responses directly, whether the individual enters diapause or not.
• 6 Differences among the species are related to differences in the ecology of their natural pupation sites.