Inheritance of the photoperiodic response controlling imaginal summer diapause in the cabbage beetle, Colaphellus bowringi

Adults of the cabbage beetle Colaphellus bowringi display a summer diapause in response to the exposure of their larvae to long photoperiods. In the present study, the inheritance of the photoperiodic response controlling summer diapause in C. bowringi by crossing a high diapause strain (D strain) with a laboratory selected nondiapause strain (N strain) was investigated under different photoperiods at 22, 25 and 28 °C. The beetles in both reciprocal crosses and backcrosses showed a clear short-day response for the induction of diapause at all temperatures, similar to that of the D strain, suggesting that photoperiodic response of this beetle is heritable. The diapause incidences in the progeny from all the crosses under LD 15:9 or LD 12:12 at 25 °C suggest that genetic and genetic-environmental interactions are involved in diapause induction. The incidence of diapauses in F₁ progeny was significantly lower than that in the D × D strain but significantly higher than that in the N × N strain, indicating that the diapause capability is inherited in an incomplete dominant manner. The incidence of diapause was greater among the offspring of hybrid females when those females had a D strain mother or grandmother rather than a N strain mother or grandmother, indicating that maternal effects on diapause induction are stronger than paternal effects. The laboratory selected nondiapause strain also showed a short-day photoperiodic response at a low temperature of 22 °C, indicating that the photoperiodic photoreceptor and photoperiodic clock still function in the nondiapause strain.     

Photoperiodic induction of prepupal diapause and its role in synchronization with host phenology in the hibiscus caterpillar,Xanthodes transversa

The hibiscus caterpillar, Xanthodes transversa (Lepidoptera: Noctuidae), is a multivoltine insect that is an important pest of Malvaceae plants such as the okra, Abelmoschus esculentus, and the common rose mallow, Hibiscus mutabilis, in Japan. In the present study, the effects of photoperiod and temperature on the induction of prepupal diapause and the adaptive significance of this diapause were examined in a local population of X. transversa in Miyazaki, Kyushu, southwestern Japan. Larvae showed a long‐day photoperiodic response for controlling the induction of prepupal diapause with a critical day length between 13 and 14 h at 20 to 25°C. Under long‐day conditions larvae rapidly pupated from the sixth instar, but under short‐day conditions they entered diapause in the prepupal stage. Diapause occurrence in the field increased in late September, which was consistent with the laboratory results in terms of the photoperiodic response. Non‐diapause development after this time is maladaptive because most larvae of the next generation could not reach the critical stage (prepupae) before winter and died during early winter in outdoor experiments. Larvae suffered from a high rate of mortality when fed leaves collected late in autumn. The photoperiodic response for controlling the induction of diapause in this insect may play an important role in synchronizing the life cycle with the seasonal changes in food and temperature conditions.     

Photoperiodic induction of diapause in normal and allatectomized precocious pupae of Papilio machaon

Diapause in the swallowtail, Papilio machaon occurs at the pupal stage in response to short days during larval development. The precocious pupae obtained by allatectomy also entered diapause in response to short days. The photoperiodic induction of diapause in precocious pupae was very similar to that in normal pupae in spite of the abbreviation of the last-larval instar. The critical photoperiod for diapause in the precocious pupae was 14.5 h, being about the same as that in normal pupae. Occurrence of diapause in the swallowtail is closely associated with the pupal stage and the induction process may be triggered by the cessation of juvenile hormone secretion.     

In vivo and in vitro photoperiodic induction of diapause using isolated brain-suboesophageal ganglion complexes of the silkworm,Bombyx mori

By use of a bivoltine silkworm race which shows a long-day photoperiodic response after induction during the last (5th) instar, we tried to programme photoperiodic induction in the isolated brain-suboesophageal ganglion complex in vivo and in vitro. A pair of the complexes from a newly ecdysed 5th-instar female was transplanted into the abdomen of a late 5th-instar larva and exposed to long-day (20 h light: 4 h dark) or short-day (8 h light: 16 h dark) conditions for 3 cycles. The short-day-exposed complexes elicited the production of diapause eggs in the recipient silkworms destined to become non-diapause egg producers, whereas the long-day-exposed brain complexes produced non-diapause eggs. Transplant experiments of the brain-suboesophageal ganglion complex using isolated abdomens showed a similar result. The brain complexes from newly ecdysed females of the 5th-instar were cultured in Grace's insect medium under 20 h light: 4 h dark or 8 h light: 16 h dark for 4 cycles, respectively. After in vitro culture, a pair of complexes was implanted into the abdomen of a late 5th-instar larva destined to become a non-diapause egg producer, and the diapause incidence in the resultant moths was examined. The brain complexes which received the short-day cycles induced a large portion of diapause eggs, whereas those which received the long-day conditions induced non-diapause eggs. The connection of corpora cardiaca and corpora allata with the brain complex had no influence on the result. Suboesophageal ganglia which had been cultured in vitro and implanted elicited a remarkable production of diapause eggs, but cultured brains were ineffective in producing diapause eggs, regardless of the photoperiod experienced. These results demonstrate that photoperiodic induction of the silkworm can be programmed in in vivo and in vitro culture systems, and that components of the photoperiodic clock (photoreceptor, clock, and counter system) are located in the brain-suboesophageal ganglion complex, possibly in the brain itself.     

Rapid evolution of photoperiodic response in a recently introduced insect Ophraella communa along geographic gradients

The introduced beetle Ophraella communa was first found in 1996 in Japan and has rapidly expanded its distribution to include regions that encompass a wide range of latitude and altitude and are dominated by different host‐plants. In this study, we investigated geographic variation in its photoperiodic response for the induction of reproductive diapause, with which the beetle adjusts its life cycle to local climate and host‐plant phenology. The beetle lines were collected from 18 sites in Japan. The diapause incidence under a photoperiodic condition of 13 h light : 11 h dark (LD 13:11) and the critical day length differed among the beetle lines. Analysis with the generalized linear model showed that latitude, altitude and host‐plant species (Ambrosia artemisiifolia vs. Ambrosia trifida) had significant effects on diapause incidence under LD 13:11. These results suggest that the O. communa populations have rapidly adapted to local environmental conditions after their colonization. However, the photoperiodic response of the O. communa population in Tomakomai, the northernmost part of its distribution range in Japan, deviated significantly from the general trend. We suggest that this deviation is attributed to either: (i) that this beetle has colonized Tomakomai more recently compared to the other sites; or (ii) that the Tomakomai population has adapted to local environments in a different way from other populations.     

Photoperiodic response in the subtropical and warm‐temperate zone populations of the southern green stink bug Nezara viridula: why does it not fit the common latitudinal trend?

The photoperiodic response of diapause induction is studied in females of five subtropical and warm‐temperate zone populations of Nezara viridula (L.) (Heteroptera: Pentatomidae) in Japan (26.4–34.7°N; 127.4–135.7°E). Laboratory tests at 25 °C demonstrate that both warm‐temperate and subtropical populations have pronounced photoperiodic responses of adult diapause induction. Under short‐day conditions (LD 10 : 14 h), 73–100% of females enter diapause, whereas, under long‐day conditions (LD 15 : 9 h), 87–100% of females are nondiapause and reproduce. When the critical photoperiod for diapause induction is plotted against the latitude of origin of each population, the data points do not show the expected tendency of increasing critical photoperiod northwards but, instead, vary between 12 h 15 min and 13 h 30 min. It is suggested that adults from different populations of such a highly migratory species move often among subtropical islands (by themselves or being assisted by typhoons), thus constantly destabilizing the photoperiodic responses. Although important for general synchronization of seasonal development in the tropics and subtropics, winter diapause might not be so critical for survival in mild winters in these zones. Such circumstances might make the selective pressure over the photoperiodic response less severe in the tropics and subtropics than in the temperate zone. It is suggested that the current climate warming might contribute to this situation as well by promoting polewards migrations and lessening the selective pressure of overwintering conditions.     

Photoperiodic and temperature control of diapause induction and colour change in the southern green stink bug Nezara viridula

Abstract. The effect of photoperiod and temperature on the duration of the nymphal period, diapause induction and colour change in adults of Nezara viridula (L.) (Heteroptera: Pentatomidae) from Japan was studied in the laboratory. At 20 °C, the developmental period for nymphs was significantly shorter under LD 10 : 14 h (short day) and LD 16 : 8 h (long day) than under intermediate photoperiods, whereas at 25 °C it was slightly shorter under intermediate than short- and long-day conditions. It is assumed that photoperiod-mediated acceleration of nymphal growth takes place in autumn when day-length is short and it is unlikely that nymphal development is affected by day-length under summer long-day and hot conditions. Nezara viridula has an adult diapause controlled by a long-day photoperiodic response. At 20 °C and 25 °C in both sexes, photoperiodic responses were similar and had thresholds close to 12.5 h, thus suggesting that the response is thermostable within this range of temperatures and day-length plays a leading role in diapause induction. Precopulation and preoviposition periods were significantly longer under near-critical regimes than under long-day ones. Short-day and near-critical photoperiods induced a gradual change of adult colour from green to brown/russet. The rate of colour change was significantly higher under LD 10 : 14 h than under LD 13 : 11 h, suggesting that the colour change is strongly associated with diapause induction. The incidences of diapause or dark colour did not vary among genetically determined colour morphs, indicating that these morphs have a similar tendency to enter diapause and change colour in response to short-day conditions.     

Effect of variation in photoperiodic response on diapause induction and developmental time in the willow leaf beetle, Plagiodera versicolora

The willow leaf beetle, Plagiodera versicolora (Coleoptera: Chrysomelidae) overwinters in adult diapause. In this study, the photoperiodic responses for diapause induction and developmental time were examined in the Ishikari (Hokkaido, Japan) population of P. versicolora. All females entered reproductive diapause under short daylength (L10:D14), but 31.7% of females did not enter diapause under long daylength (L16:D8). The developmental time from oviposition to adult emergence was significantly longer at L10:D14 than that at L16:D8. Norm of reaction curves illustrated variation among families in the photoperiodic responses for diapause induction and for developmental time. ANOVA indicated significant family × photoperiod interactions in the developmental time. At L16:D8, developmental time was positively correlated with the incidence of diapause in females. This means that a female having a longer developmental time tends to have a longer critical photoperiod. Such variation may be maintained by differences in selection pressures on the growth rate and the critical photoperiod for diapause induction between univoltine and bivoltine genotypes because Ishikari is located in a transitional area between populations with univoltine and bivoltine life cycles.     

Developmental requirements of the univoltine species Chrysopa downesi: Photoperiodic stimuli and sensitive stages

Chrysopa downesi reproduces only in the spring and the resulting adults enter an aestival-autumnal-hibernal diapause which is primarily controlled by photoperiod. In the laboratory, constant photoperiods result in diapause induction and maintenance, whereas a series of short days followed by long days prevents or terminates diapause and promotes reproduction. The stages most sensitive to the diapause-averting stimulus are the free-living third instar, the third instar within the cocoon, and the pupa.C. downesi responds in different ways to three aspects of photoperiod: (a) an all-or-none response (diapause prevention or induction) to a sequence of two critical photoperiods, (b) an all-or-none response (diapause prevention or induction) to the difference between the long and short daylengths (a 4 hr difference is sufficient to avert diapause but a 2 hr difference is not), and (c) a quantitative response to the absolute duration of day (or night) length (after the short day requirement is fulfilled the rate of diapause termination is related to daylength).Differences and similarities in phenological adaptations and in photoperiodic responses of C. downesi, C. carnea, and C. harrisii reflect the degree of phylogenetic relationship between these closely related species.     

Photoperiodic induction of diapause in the spider mite Tetranychus urticae: qualitative or quantitative time measurement?

Abstract. Insects and mites may measure photoperiods eitfier by classifying them as long or short relative to a critical value (qualitative time measurement) or by using the absolute value (quantitative time measurement). The spider mite Tetranychus urticae is thought to use a qualitative mechanism of time measurement. In this paper we present the results of experiments with an inbred line of the spider mite (to keep genetic variation in photoperiodic responses small), to test whether quantitative aspects also play a role. Differences in diapause incidence in different long-night photoperiods at different temperatures may be an indication of quantitative responses to photoperiod. The effect of temperature on the photoperiodic response curve was studied at 16^oC, 19^oC and 22^oC. The response curves appeared to be similar at 16^oC and 19^oC, with a critical nightlength between 10 and 11 h. At 22^oC, diapause induction was less than 100% in all long-night regimens and die critical nightlength had shifted to 12 h. Maximum diapause induction (93%) occurred in a light-dark cycle with a 16 h dark phase (LD 8:16 h). Diapause induction was lowest in long-night photoperiods with dark phases of 20 h and longer. The number of light-dark cycles needed for 50% diapause induction at 19^oC varied. between 12.1 and 14.7 for LD 6:18 h, between 10.9 and 12.5 for LD 8:16 h, between 10.6 and 11.6 for LD 10:14 h, and between 10.1 and 10.7 for LD 12:12 h. Independent of die light-dark regimen, diapause induction took place in some individuals after receiving 8 cycles and virtually all individuals entered diapause after 16 cycles. No effect was found of the photoperiodic treatment during prediapause development (LD 6:18 h, LD 8:16 h, LD 10:14 h, LD 12:12 h) on diapause duration. The average diapause duration at LD 10:14 h and 19^oC was 61 days over all four treatments. We explained the results by hypothesising that nightlengths are assessed qualitatively and mat the photoperiodic clock operates more accurately near the critical nightlength.     

Effect of photoperiod on winter and summer diapause of the soybean pod borer Leguminivora glycinivorella (Lepidoptera: Tortricidae)

To understand the geographical differences between diapause systems and synchronization of adult occurrence in the soybean pod borer Leguminivora glycinivorella (Lepidoptera: Tortricidae), we examined the timing of winter diapause termination and intensity of summer diapause using univoltine and potentially bivoltine individuals in Iwate, Japan. In laboratory rearing experiments of mature larvae maintained at constant temperature (20 °C), winter diapause intensity weakened by January without photoperiodic responses. Meanwhile, summer diapause was maintained by the long day length and presumably terminated with the photoperiodic transition from long to short day length. The intensity of summer diapause was stronger for cocoons that transitioned from a 16 h light to 8 h dark (LD 16:8) to a LD 15:9 photoperiod than for those that transitioned from LD 15:9 to LD 14:10. These results suggest that populations distributed in relatively low-latitude areas, with partly or potentially bivoltine individuals, would have a weaker summer diapause or none at all. Moreover, sexual differences in the number of days to emergence were not detected when individuals experienced a photoperiodic transition from long to short day length, suggesting that the summer diapause system may function to synchronize the emergence of males and females in the population examined.     

Experimental investigation of the seasonal aspect of the relationship between blowflies and their parasites

It has been shown experimentally that the diapause in the life cycles of blowflies Parasarcophaga similis, P. argyrostoma, Bellieria melanura, Calliphora vicina and their parasites Aphaereta minuta and Alysia manducator is induced by the seasonal shortening of the daylength. The host species modifies the photoperiodic reaction of the A. minuta parasite. In A. manducator, there is intraspecific geographical variability of the photoperiodic reaction. In certain conditions, diapause induction in this parasite depends on the physiological state of the host. The parasite's influence on the host's development: parasitization by A. minuta terminates the diapause and induces the premature pupation of Lucilia illustris larvae.     

Induction of larval diapause in the blowfly, Calliphora vicina R.-D. (Diptera, Calliphoridae) under field and laboratory conditions

Field experiments conducted in the environs of St. Petersburg (Russia) with a local population of Calliphora vicina showed that induction of larval diapause under natural conditions was significantly dependent on day lengths and temperature. The maternal photoperiodic response had a distinct threshold: the first diapausing larvae hatched from the eggs laid in the middle of August when the day length was 16 h; at shorter photoperiods, the fraction of diapausing larvae depended only on temperature. At the mean temperature of 16°C, larval diapause was rarely recorded; at 12–13°C, about 50% of the larvae entered diapause; at 7–9°C, nearly all the larvae entered diapause. These results of the field experiments agree well with the parameters of photoperiodic and thermal responses studied in the laboratory at constant temperatures and photoperiods.     

Both the anterior and posterior eyes function as photoreceptors for photoperiodic termination of diapause in the two-spotted spider mite

Photoreceptors involved in photoperiodism in insects and mites can be either the retinal photoreceptors in the visual system or nonvisual extraretinal photoreceptors. Mites with no eyes have a clear photoperiodic response, suggesting the involvement of extraretinal photoreceptors in mite photoperiodism. In mites equipped with eyes, however, it is not known whether the retinal or extraretinal photoreceptors are involved in photoperiodism. The two-spotted spider mite Tetranychus urticae possesses two pairs of eyes. Adult females of this species terminate diapause in response to long days. To investigate whether the eyes function as photoperiodic photoreceptors in T. urticae, their eyes were ablated using a laser ablation system. Mites with their eyes intact terminated diapause under long days after low temperature exposure, whereas they remained in diapause under short days. Under constant darkness, they did not terminate diapause. When all eyes were removed, the mites remained in diapause even when they were maintained under long days. In contrast, the mites showed clear photoperiodic response when only the anterior or posterior eyes were removed. These results indicate that both the anterior and posterior eyes function as photoreceptors in photoperiodic termination of diapause in T. urticae.     

Adaptive latitudinal cline of photoperiodic diapause induction in the parasitoid Nasonia vitripennis in Europe

Living in seasonally changing environments requires adaptation to seasonal cycles. Many insects use the change in day length as a reliable cue for upcoming winter and respond to shortened photoperiod through diapause. In this study, we report the clinal variation in photoperiodic diapause induction in populations of the parasitoid wasp Nasonia vitripennis collected along a latitudinal gradient in Europe. In this species, diapause occurs in the larval stage and is maternally induced. Adult Nasonia females were exposed to different photoperiodic cycles and lifetime production of diapausing offspring was scored. Females switched to the production of diapausing offspring after exposure to a threshold number of photoperiodic cycles. A latitudinal cline was found in the proportion of diapausing offspring, the switch point for diapause induction measured as the maternal age at which the female starts to produce diapausing larvae, and the critical photoperiod for diapause induction. Populations at northern latitudes show an earlier switch point, higher proportions of diapausing individuals and longer critical photoperiods. Since the photoperiodic response was measured under the same laboratory conditions, the observed differences between populations most likely reflect genetic differences in sensitivity to photoperiodic cues, resulting from local adaptation to environmental cycles. The observed variability in diapause response combined with the availability of genomic tools for N. vitripennis represent a good opportunity to further investigate the genetic basis of this adaptive trait.     

Inheritance of photoperiodic induction of larval diapause in the Asian corn borer Ostrinia furnacalis

The Asian corn borer Ostrinia furnacalis (Guenée) enters facultative diapause as fully‐developed larvae in response to short‐day conditions. As a consequence of geographical variation in photoperiodic response, moths from Nanchang (28°46′N, 115°50′E) enter diapause in response to short day‐lengths (D strain), even at the high temperatures whereas moths from Ledong (18°47′N, 108°89′E) exhibit almost no diapause under the same conditions (N strain). In the present study, crosses between the two strains are used to evaluate the inheritance of diapause under different photoperiods at temperatures of 22, 25 and 28 °C. The moths, both reciprocal crosses and backcrosses, show a clear long‐day response, similar to that of the D strain, suggesting that the photoperiodic response controlling diapause in this moth is heritable. However, the critical day‐length for induction of diapause is shorter in hybrids than in the D strain. The N strain also shows a short‐day photoperiodic response at the lower temperature of 22 °C, indicating that the N strain still has the capacity to enter a photoperiodically‐induced diapause, depending on the rearing temperature. The incidence of diapause in all crosses is highest with D strain fathers or grandfathers and lowest with N strain fathers or grandfathers, indicating that the male parent has significantly more influence on the incidence of diapause of subsequent progeny than the female. The results obtained from all crosses under LD 12 : 12 h or LD 13 : 11 h photocycles at 25 °C show that inheritance of diapause in O. furnacalis does not fit an additive hypothesis and that the capacity for diapause is transmitted genetically in the manner of incomplete dominance.     

Photoperiodic induction in the silkworm, Bombyx mori, reared on artificial diet: Evidence for extraretinal photoreception

When a bivoltine race of the silkworm, Bombyx mori, was reared on artificial diets, the silkworm became photoperiodically responsive during larval development. The response curve for the embryonic-diapause induction of the next generation was of the long-day type, showing a sharply defined critical day-length of 16.5 hr. Complete blindness caused by covering the larval stemmata with black paint was confirmed electrophysiologically. It did not influence the diapause incidence. Vitamin A deficiency, which produced a similar defect in visual function in the stemmata, was also without effect on diapause. These observations show that extraretinal photoreception is involved in photoperiodic induction in the silkworm.     

Effects of photoperiod and temperature on diapause induction in Conogethes punctiferalis (Lepidoptera: Pyralidae)

The yellow peach moth, Conogethes punctiferalis (Guenée), a multivoltine species that overwinters as diapausing larvae, is one of the most serious insect pests on maize in China. Effect of photoperiod and temperature on larval diapause was examined under empirical laboratory conditions. Short‐day treatments caused larval diapause at 25°C, and the critical photoperiod was between 12 and 13 h (or 12 h 51 min) light per day. No sensitive instar was identified for diapause induction under alternated short‐ (L : D 11 : 13 h) and long‐day (L : D 14 : 10 h) treatments at different larval stages. However, accumulative treatment of three instars and 10 d under short‐day treatment was required for the induction of 50% larval diapause. All larvae entered diapause at 20°C, whereas less than 3% did so at 30°C, irrespective of the long‐ or short‐day treatment. Furthermore, under the short‐day treatment, more than 90% of larvae went into diapause with temperatures ≤ 25°C, but less than 17% did so at 28°C. In contrast, under the long‐day treatment, less than 19% of larvae went into diapause with temperatures ≥ 23°C. The forward shift (5°C) of critical temperature under the long‐day regime demonstrated the compensatory effect of temperature and photoperiod on diapause induction. In conclusion, C. punctiferalis had a temperature‐dependent type I photoperiodic diapause response; there was no sensitive instar for diapause determination, but the photoperiodic accumulation time countermeasures both of the short‐day cycles and the number of instars exposed, and the photoperiodic diapause response, was a temperature‐compensated phenomenon.     

黄杨绢野螟滞育诱导及光温反应

为了探讨黄杨绢野螟Diaphania perspectalis(Walker)越冬滞育特性,在自然条件与室内恒温下对黄杨绢野螟滞育诱导的光周期反应与光敏感龄期进行了研究。结果表明:该虫的光周期反应属于长光照反应型,短光照是引起黄杨绢野螟幼虫滞育的主要因子。幼虫的光周期反应对温度敏感,在恒温25℃和28℃条件下,诱导滞育的临界光周期分别为13h36min和12h50min。在日平均温度为26.7℃条件下,诱导滞育的临界光周期为13h40min。在恒温25℃条件下的滞育敏感虫龄试验表明,2～3龄幼虫即孵化后4～9d的幼虫对光周期反应最敏感。     

Diapause induction and photoperiodic clock in Chilo suppressalis (Walker) (Lepidoptera: Crambidae)

The mature larvae of the rice stem borer, Chilo suppressalis Walker (Lepidoptera: Crambidae) enters facultative diapause in response to short‐day conditions in the autumn (August–September). Diapause induction and photoperiodic clock mechanism were investigated in C. suppressalis larvae reared on an artificial diet in the present study. The critical night length for diapause induction was about 9 h 53 min to 10 h 39 min at 22 to 28°C. The third‐instar larvae were found to be relatively sensitive to diapause induction. Photoperiodic response under non‐24‐h light–dark cycles showed that scotophase length played an essential role in the induction of larval diapause in C. suppressalis, and consecutive exposure to long‐night cycles was necessary for a high diapause incidence. In the Nanda–Hamner experiment, diapause incidence peaked at scotophase of 12 h and dropped rapidly at scotophases > 24 h. In the Bünsow experiment, diapause incidence was clearly suppressed, especially at the light pulse located 8 h in the scotophase. Both the Nanda–Hamner and Bünsow experiments showed no rhythmic fluctuations with a period of about 24 h; thus the photoperiodic clock in C. suppressalis is a non‐oscillatory hourglass timer or a rapidly damping circadian oscillator.