Variations in the tendency to diapause among successive generations of laboratory strains of <Emphasis Type="Italic">Trichogramma</Emphasis> species (Hymenoptera,Trichogrammatidae): Endogenous or exogenous?

Variations in the tendency to diapause among successive generations of laboratory strains reared under constant conditions were reported for many insects and mites. However, as far as we know, the relative importance of the endogenous and exogenous components of this variability has not been investigated experimentally. We have conducted such a study with 12 successive generations of laboratory strains of Trichogramma telengai Sor. and T. principium Sug. et Sor. In total, 12 strains originated from different females and / or reared under different photothermal conditions (temperature of 20 and 25°C and day length of 12 and 18 h) were investigated. The tendency to diapause was estimated by the proportion of the progeny diapausing at temperatures of 13, 14 and 15°C. Although the variations in the tendency to diapause in sequential generations of different strains of the same species were positively correlated, the correlation between different species was also very strong suggesting that endogenous (species-specific) factors are not the main reason for the observed changes. The data for different photothermal conditions of incubation of the studied strains and of their progeny were also correlated suggesting that occasional changes in temperature or day length are not the reason of the changes in the proportion of diapausing progeny. Evidently, the differences in the tendency to diapause among generations of the studied Trichogramma species were mainly caused by some uncontrolled environmental factors. This in no way excludes the possible role of the endogenous processes, but suggests the necessity for a critical analysis of the available data on the “spontaneous” dynamics in the tendency to diapause among successive generations of the laboratory strains of insects and mites.     

Multigenerational maternal inhibition of prepupal diapause in two Trichogramma species (Hymenoptera: Trichogrammatidae)

It is known that in some insect species the incidence of diapause among the progeny of females that had undergone diapause is relatively low or zero even under strong diapause-inducing conditions. Moreover, the maternal inhibition, preventing the induction of a maladaptive diapause in spring, can persist over several generations. This multigenerational effect based on hypothetical ‘interval timer’ was thoroughly studied in Aphididae. We first described a similar phenomenon in Hymenoptera: laboratory experiments demonstrated that the proportion of diapausing progeny of Trichogramma females that had undergone diapause was practically zero independently of photoperiodic and temperature conditions used (day lengths of 12 and 18 h and temperatures of 12–15 °C). Then the ability to enter diapause recovered gradually and returned to the normal level over two (in Trichogramma telengai) or even five (in Trichogramma principium) generations. We conclude that the observed effect may be based on an interval timer similar to that in aphids.     

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.     

Multigenerational maternal effect on diapause induction in Trichogramma species (Hymenoptera: Trichogrammatidae)

Maternal photoperiodic response is known to influence the percentage of diapausing prepupae in Trichogramma species. However, the influence of several preceding generations has not yet been studied. We have investigated the stability of photoperiod-induced changes in multiple generations of Trichogramma buesi Voegele and Trichogramma principium Sug. et Sor. Short-day conditions during preimaginal development induced an increase in the percentage of diapausing progeny and grand progeny of both Trichogramma species. A similar trend was also detected in the fourth and fifth generations, but the response was weak although statistically significant. This grand-grandmaternal photoperiodic effect (which has not been demonstrated before for Trichogramma or for any other insect parasitoid) is most probably based on the transgenerational transmission of variations in DNA expression. We conclude that in mass rearing, to facilitate diapause induction before cold storage, it is advisable to rear both maternal and grandmaternal generations under the short-day conditions. In scientific studies, several generations preceding the experiment should be kept under equal conditions to exclude multigenerational maternal effects.     

Maternal thermal and photoperiodic effects on the progeny diapause in Trichogramma telengai Sorokina (Hymenoptera: Trichogrammatidae)

Although maternal photoperiodic and maternal thermal effects on the progeny diapause have been demonstrated in a number of insect species, their interaction has been rarely studied. We investigated this interaction in Trichogramma telengai. In a series of experiments, maternal females were reared at day lengths of 12–18 h and at temperatures of 17, 20, 25 and 30°C. Their progeny developed under day length of 12 h and temperatures of 13, 14 and 15°C. The experiments showed that both short day and low temperature experienced by the maternal generation significantly increased the proportion of diapausing progeny. In particular, the threshold of the maternal photoperiodic response decreased with temperature. Under combinations of photoperiod with daily thermoperiod, the role of the “night” temperature in the induction of diapause in the progeny was much more important than that of the “day” temperature. We conclude that the interaction pattern between the photoperiodic and thermal maternal effects in T. telengai is generally the same as that between the photoperiodic and thermal responses directly influencing diapause induction in other long‐day insects. The threshold temperature of the maternal thermal response of T. telengai was about 25–27°C, while diapause can be induced if larvae develop at temperatures not higher than 15–16°C. This suggests that, at least in the studied Trichogramma species, the maternal thermal effect has no ecological value. In the practice of biocontrol, however, rearing of Trichogramma wasps at high temperature can drastically reduce the proportion of diapausing progeny.     

Photoperiodic responses of pupa and adult determining maternal influence on progeny diapause in two species of the genus Trichogramma (Hymenoptera, Trichogrammatidae)

The adult photoperiodic responses of two Trichogramma species were investigated by exposing adults during 3 days to one of the seven light: dark regimes: L: D = 4: 20, 8: 16, 12: 12, 14: 10, 16: 8, 18: 6, and 20: 4. The preimaginal stages of these individuals developed under short (L: D = 12: 12), long (L: D = 20: 4) or intermediate photoperiods (L: D = 14: 10 and L: D = 16: 8 for Trichogramma principium and T. embryophagum, respectively). The progeny of these females developed under short day L: D = 12: 12 and at two moderately diapause-inducing temperatures (13 and 14°C for T. principium, 14 and 15°C for T. embryophagum). In both Trichogramma species which developed at both temperatures, the percentage of diapausing prepupae was significantly dependent both on the photoperiodic conditions of the preimaginal development of the maternal generation and on the photoperiod which influenced the adult females. The adults showed a typical long-day photoperiodic response with a threshold day length of ca 13 h in T. principium and ca 16 h in T. embryophagum, which practically coincided with the thresholds of the pupal photoperiodic responses of these species revealed in our previous studies. However, the ultra-short photoperiods (L: D = 4: 20 and 8:16) caused a relatively stronger diapause-inducing effect on the progeny when applied to the adult females than when it was applied to the pupae. Thus, in both the Trichogramma species studied, the patterns of photoperiodic responses of pupa and adult were somewhat different although they almost coincided in the “ecologically significant” part of the photoperiodic scale.     

Maternal influence on diapause induction in Trichogramma (Hymenoptera: Trichogrammatidae): the dynamics of photosensitivity

It is known that the prepupal diapause in Trichogramma is dependent on temperature conditions of embryonic and larval development and on the photoperiodic conditions of preimaginal development of maternal females. However, the relative photosensitivity of different preimaginal stages has been never investigated. We studied the position of the photosensitive period over the preimaginal development of maternal females in T. embryophagum Htg. and T. principium Sug. et Sor. by transferring preimaginal stages between diapause‐averting ‘long’ day (L : D = 20 : 4) and diapause‐inducing ‘short’ day (L : D = 12 : 12). Results showed that the influence of maternal photoperiod on progeny diapause was determined during the late pupal stage (last days of preimaginal development at 20°C). During this time, the critical duration of the photoperiodic induction was extremely small: one short or long day caused almost the same effect as the permanent development under these conditions. As a whole, photoperiodic response in Trichogramma was found to be unusually rapid, labile and easily reversible which is probably explained by extremely small size and fast development of these egg parasitoids. The results of this study could be used for elaboration of optimal methods for Trichogramma mass rearing and storage and for prediction of its seasonal cycles under natural conditions.     

On the factors inducing the inhibition of diapause in the progeny of diapause females of Trichogramma telengai

The ability to enter diapause in the progeny of Trichogramma Westw. (Hymenoptera: Trichogrammatidae) females that have undergone diapause is markedly reduced or even completely absent. This maternal inhibition of diapause can result from three types of factors: (i) environmental factors that induce maternal diapause; (ii) maternal diapause itself; and (iii) diapause‐terminating environmental factors. The present study aims to determine the factors that prevent diapause in the progeny of a Trichogramma telengai Sor. generation that has undergone diapause. Different tendencies to enter diapause in the maternal generation are induced by different photoperiods (LD 12 : 12 h, 16 : 8 h and 18 : 6 h) during development of the grandmaternal generation and different temperatures (from 10 to 15 °C) during larval development of the maternal generation. To terminate diapause, prepupae of the maternal generation are kept at 4–5 °C in the dark. To estimate the ability to enter diapause, the progeny generation is incubated at 14 °C. The results suggest that the inhibition of the tendency to enter diapause in the progeny of T. telengai females that have undergone diapause is caused by diapause itself rather than by diapause‐inducing or diapause‐terminating environmental factors. This result can be used to clarify the mechanism of the inhibition of diapause in the progeny of females that have undergone diapause.     

Photoperiodic Regulation of the Daily Rhythm of <Emphasis Type="Italic">Trichogramma</Emphasis> Adult Emergence (Hymenoptera,Trichogrammatidae)

Laboratory experiments demonstrate that the adult emergence rhythms of two Trichogramma species (T. telengai Sor. and T. principium Sug. et Sor.) significantly depend on photoperiod. The synchronicity of adult emergence is maximal at day lengths of 12–16 h. Under longer days (18–20 h) adult emergence is extended, whereas under very short days (4–8 h) a substantial proportion of adults emerge before light-on. The pattern of T. telengai emergence under day length of 4 h suggests the possibility of the existence of two fractions (the first that emerges in the dark and the second that waits for light-on) which results in two peaks of emergence. As a whole, these data agree well with the hypothesis of the periods of “potential readiness” and “obligate activity” forwarded by V.B. Chernyshev. The results of the study can be used for optimization of the methods for laboratory and mass rearing of Trichogramma species.     

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.     

Maternal thermal effect on diapause in Trichogramma species (Hymenoptera: Trichogrammatidae)

Both direct thermal and maternal photoperiodic effects on diapause induction have been thoroughly investigated in many insect species, while maternal thermal effects have been infrequently studied. We studied the effect of temperature during development of maternal generation on the proportion of diapausing progeny in four species of the genus Trichogramma Westw., minute egg parasitoids, widely used for biological control of lepidopteran pests. The maternal generations were reared at day lengths of 12 and 18 h and temperatures of 17, 20, 25 and 30°C, and their progeny developed under day length of 12 h and temperatures of 13 and 14°C. In T. evanescens and T. piceum, the proportion of diapausing progeny decreased with increasing temperature under all tested photoperiods and thermal regimes of progeny development; the high temperature of 30°C totally averted diapause of progeny. In T. buesi and T. principium, low temperatures of 17 and 20°C resulted in relatively high proportion of diapausing progeny only when the maternal generation developed under short‐day conditions. The threshold of the maternal thermal response varied from 17–18 to 22–23°C. Under field conditions, Trichogramma females are exposed to such high temperatures only during summer, when diapause in their progeny is in any case prevented by the maternal photoperiodic response and by the thermal response of the larvae. We conclude that the maternal thermal effect on diapause induction, although to a different extent, is inherent to Trichogramma species but, at least as suggested by laboratory experiments, it does not play any role in the regulation of seasonal development under natural conditions. However, during mass rearing of Trichogramma wasps, it should be taken into account that high temperature, even when combined with short photoperiod, can avert diapause in the next generation.     

Photoperiodic regulation of the diapause of the progeny in <Emphasis Type="Italic">Trichogramma embryophagum</Emphasis> Htg. (Hymenoptera,Trichogrammatidae): Dynamics of sensitivity to photoperiod at the immature stages of maternal females

Photoperiodic regulation of T. embryophagum progeny prepupal diapause was investigated under laboratory conditions. Maternal females developed at 20°C, the position of the photosensitive period was detected by transferring immature stages between the diapause-inducing “short” day (L:D = 12:12) and the diapause-averting “long” day (L:D = 20:4). Progeny generation developed at L:D = 12:12 under the near-threshold temperature of 13°, 14°, or 15°C. Experiments showed that, at least under the used photo-thermal regimens, only the pupal stage was sensitive to the photoperiod influence. The highest photosensitivity was recorded during the last two days before the adult emergence. In this critical period, even a single short day cycle induced diapause in most of individuals. However, the reaction to the long day was weaker: at least two long light days immediately preceding the maternal adult emergence were necessary to avert the diapause. If a short day was preceded by a long day by more than 2–3 days before the adult emergence, the stepwise photoperiodic response caused an increase in the tendency to diapause. The results of this study could be used in pest biocontrol practice for elaboration of optimal methods for Trichogramma mass rearing and storage and also for prediction of its seasonal cycles under natural conditions.     

Environmental and endogenous control of diapause inTrichogramma species

The 1st feature revealed typical for diapause phenomena inTrichogramma species is the interaction of environmental conditions in both parental and filial generations in induction of diapause in the latter. Lowered temperature during larval development is the ultimate factor evoking diapause in pronymphs but the norm of this thermal reaction is not fixed but varies depending on photoperiod and temperature in the previous generation due to maternal influence. Short day and in some cases high temperature in parental generation enhance tendency to diapause in the progeny. Unlike maternal influence the development to filial generation itself is not (or almost is not) governed by its own photoperiodic reaction. The 2nd typical feature revealed is the occurrence of endogenous process running in the sequence of generations and causing changes in the diapause tendency and underlying reaction norms even under constant rearing conditions.      

On the direct influence of photoperiod on diapause in <Emphasis Type="Italic">Trichogramma embryophagum</Emphasis> (Hymenoptera,Trichogrammatidae)

A direct photoperiodic reaction of T. embryophagum larvae was investigated in the laboratory. Maternal females developed at 20°C and day length of 12 h. Progeny generation developed at 14°C and day lengths of 0, 4, 8, 12, 16, 20, and 24 h. Experiments showed that under the short days (12, 8, and 4 h) and in continuous darkness, the percentage of diapausing individuals was significantly higher than under the long days of 16 and 20 h. Under permanent light, however, the inclination to diapause also increased. The earlier investigated maternal influence on T. embryophagum progeny diapause showed a somewhat different pattern of photoperiodic reaction. These results suggest that the direct effect of the day length on Trichogramma diapause is a relatively autonomous process rather than just a side-effect of the photoperiodic reaction determining maternal influence. However, this direct effect is very weak and could possibly be a “rudimentary reaction.”     

Photoperiodic Control of Pre-Adult Development and Adult Diapause Induction in Zoophytophagous Bug Dicyphus errans (Wolff) (Heteroptera,Miridae)

Zoophytophagous plant bugs (Heteroptera, Miridae) increasingly attract interest as agents of biological plant protection. In the laboratory experiment, the effects of the day length and temperature on the duration of the pre-adult period and on induction of facultative winter adult diapause were studied in Dicyphus errans (Wolff, 1804) collected in Italy. The experiment demonstrated that at 20°C the duration of the pre-adult period of D. errans significantly depended on the day length. On average, females developed 1.3 days longer than males and, at the same time, the day length equally influenced the duration of the pre-adult period in both sexes. The pre-adult period was the shortest under short-day conditions (10 to 12 h of light per day), reached its maximum at day length of 14 h, but then decreased at 15 h, and at day length of 16 h it was as short as under short-day conditions. Also, a pronounced long-day type photoperiodic response of adult diapause induction was recorded in females of D. errans at 20°C: under short-day conditions (10 to 14 h of light per day) almost all females entered diapause, whereas under long-day conditions (15 and 16 h of light per day) about 90% of females were mature. The threshold of this photoperiodic response was close to 14 h 30 min. The mean (± S.D.) egg load of mature females was 6.3 ± 4.0 eggs per female and did not depend on the day length at which the female was reared before and after the final molt. When photoperiodic response of adult diapause induction was observed at two constant temperatures (20 and 25°C), the proportion of mature females depended significantly on the day length but not on the temperature: the shapes of the photoperiodic response curves of diapause induction were almost the same within the near-threshold zone at 20 and 25°C, i.e., the photoperiodic response was thermostable. The set of two photoperiodic responses manifested at different stages of the species’ life cycle has an obvious adaptive significance. In Central Europe, D. errans has 2 or 3 generations per year and hibernates at the adult stage. Due to the thermostable photoperiodic response, females enter diapause always at the same time at the end of summer, regardless of the weather conditions of a particular year. When oviposition and pre-adult development are extended over a prolonged period in summer, nymphs from the later eggs might not be able to molt to adults in due time and then fully prepare for stable winter diapause. Under such circumstances, the photoperiodic response controlling the rates of pre-adult development acquires apparent adaptive meaning: with an autumnal shortening of the day length to 10–12 h, even under conditions of seasonal decrease in temperature, the rates of nymphal development increase and, thus, the chances of nymphs from the later eggs to molt to adults and properly prepare for overwintering also increase. The new data should be taken into account when analyzing the seasonal cycle of D. errans and developing the programs of mass rearing of this zoophytophagous mirid as an agent of biological plant protection.

     

Diapause induction in Trichogramma telengai: the dynamics of maternal thermosensitivity

Transferring Trichogramma telengai Sorokina (Hymenoptera: Trichogrammatidae) from 17 to 30 °C or vice versa at different stages of pre‐imaginal development shows that the pupa (particularly late pupa) is a sensitive stage of the maternal thermal response. During this period, even a relatively short period (1–2 days) of cold or heat exposure results, correspondingly, in a marked increase or decrease in the percentage of diapausing progeny. Thus, the maternal thermal response has the same features of sensitivity as those of the previously investigated maternal photoperiodic response, suggesting that photoperiodic and thermal responses share the same mechanism. For the practice of rearing and storage Trichogramma as a biocontrol agent, it is important to note that even relatively short‐term environmental heating (i.e. for one to several days) immediately before adult emergence can drastically decrease the percentage of diapausing progeny.     

The seasonal development cycle of <Emphasis Type="Italic">Aphantopus hyperantus</Emphasis> (L.) (Lepidoptera,Nymphalidae: Satyrinae) in Leningrad Province

The simultaneous influence of the photoperiodic and temperature conditions on pre-diapause and postdiapause larval development of the ringlet Aphantopus hyperantus was studied. At the short day (12 h of light a day) all larvae reached the III instar and entered diapause at all the temperatures tested (18–24°C). At the long day (22 h) the number of diapausing larvae increased with decreasing temperature, and the larvae diapaused at the III and IV instars. The I and II instar larvae (before winter) developed and grew faster under short-day, and the hibernated larvae, under long-day conditions. At the short day the growth rate of the I and II instar larvae did not depend on the temperature, and at the long day it decreased as the temperature increased. After hibernation the growth rate of the IV instar larvae increased with the temperature under long-day conditions, and did not depend on the temperature under short-day ones. Thus, acceleration or deceleration of development, depending on the photoperiodic and temperature conditions, regulated the timing of diapause in the overwintering stage (the III instar larva) and maintained the univoltine seasonal cycle. The males of A. hyperantus developed and grew faster than females while their weight at the larval and pupal stages was smaller. The thermal reaction norms for development (the lower temperature threshold and the coefficient of thermal sensitivity of development) were calculated for the eggs, IV and V instar larvae, and pupae. The coefficient of thermal sensitivity of development for the IV and V instar larvae taken together was lower, and the threshold was higher than the corresponding values for eggs and pupae. The thermal reaction norms for development of the latter stages were the same. The larvae of A. hyperantus retained their sensitivity to the photoperiod after hibernation. Resumption of development after cold reactivation occurred only under long-day conditions, whereas under short-day ones the overwintered larvae entered a repeated diapause. The possibility of photoperiodic reactivation and the absence of spontaneous resumption of development in these larvae were demonstrated.     

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.     

Artificial selection for responsiveness to photoperiodic change alters the response to stationary photoperiods in maternal induction of egg diapause in the rice leaf bug Trigonotylus caelestialium

Female adults of the rice leaf bug Trigonotylus caelestialium (Kirkaldy) (Heteroptera: Miridae) produce non-diapause eggs under long-day conditions, whereas they produce diapause eggs under short-day conditions. These egg-production modes change following a photoperiodic change from long-day to short-day conditions or vice versa, with individual variations in responsiveness shown in the time from the photoperiodic change to the mode change. Strains of this insect with higher or lower responsiveness to photoperiodic change were established after several generations of selection, indicating that the individual variation has a genetic basis. The selected strains that were more responsive and less responsive to one photoperiodic change were found to be less responsive and more responsive to the opposite photoperiodic change, respectively, indicating a significant negative correlation between responsiveness to reciprocal photoperiodic changes. The selected strains also had a significantly different incidence of diapause-egg producers in stationary photoperiods compared to a non-selected strain, showing that selections for responsiveness to photoperiodic change were essentially the same as selections for a higher or lower incidence of diapause-egg producers. These results indicate that responsiveness to photoperiodic change is one aspect of the tendency to produce diapause or non-diapause eggs.     

The role of photoperiod and temperature in determination of summer and winter diapause in the cabbage beetle,Colaphellus bowringi (Coleoptera: Chrysomelidae)

The cabbage beetle, Colaphellus bowringi, is a short-day species undergoing an imaginal summer and winter diapause. Its photoperiodic response highly depends on temperature. All adults entered diapause at ≤ 20 °C regardless of photoperiods. High temperatures strongly weakened the diapause-inducing effects of long daylengths. The diapause-averting influence of short daylengths was expressed only at high temperatures (above 20 °C). This indicates that the beetle has a cryptic ability to reproduce in summer. In fact, summer and winter diapause were induced principally by relatively low temperatures in the field, whereas photoperiod had less influence on diapause induction. The critical daylength for the autumnal population was between 12 h and 13 h. By transferring from a long day to a short day or vice versa at different times after hatching, it was shown that the sensitive stage with regard to photoperiod was the larva, whereas a long day was photoperiodically more potent than a short day. The sensitive stage to temperature encompassed the larval, pupal and adult stages. This different response pattern serves to ensure that the beetle enters summer and winter diapause in time. The selections for non-diapause trait under laboratory (at 25 °C) and natural conditions (at >24 °C) showed that the beetle could lose its sensitivity to photoperiod very rapidly.