Reznik. Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia. Received May 20, 2011. AbstractâFacultative winter diapause in the genus ...
ISSN 0022-0930, Journal of Evolutionary Biochemistry and Physiology, 2011, Vol. 47, No. 6, pp. 512—523. © Pleiades Publishing, Ltd., 2011. Original Russian Text © S. Ya. Reznik, 2011, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2011, Vol. 47, No. 6, pp. 434—443.
REVIEWS
To the 100th Anniversary of A.S. Danilevsky
Ecological and Evolutionary Aspects of Photothermal Regulation of Diapause in Trichogrammatidae S. Ya. Reznik Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia Received May 20, 2011
Abstract—Facultative winter diapause in the genus of Trichogramma Westw. (Hymenoptera, Trichogrammatidae), like in most other insect species, is regulated by photoperiod and temperature. Their prepupae are diapausing, but sensitivity to temperature and day length (environmental cue factors inducing diapause) is characteristic of all stages of development from embryo to the egglaying female. The environmental cues can affect not only the current, but also the next generations. Under the natural conditions, the photothermal regulation provides the timely diapause induction coordinated both with the astronomical season (the photoperiodic response) and with the peculiarity of the given year (the thermal response). The special experiments revealed “rudimentary responses” that had lost their adaptive role. The results of these studies have proved once more that the specificity of photoperiodic and thermal diapause-regulating responses, their relative importance, and association with sensitive stages of development are determined not only by the ecological peculiarities of different insect taxa, but also by their previous evolution. DOI: 10.1134/S0022093011060020 Key words: diapause, photoperiod, temperature, insects, parasitoids, Trichogramma.
INTRODUCTION Photoperiodic regulation of seasonal cycles is the universal feature peculiar not only to insects, but also to many other invertebrate and vertebrate animals as well as to fungi and plants. Numerous works have been dealing with different aspects of insect photoperiodism. A.S. Danilevsky in his fundamental monograph [1] has formulated the thesis that photoperiodic adaptations were formed independently in different insect taxa and were submitted to evolution in parallel. V.P. Tyshchenko [2] wrote that “every insect species has potential prerequisites for creation of any system of photoperiodic adaptations. Particular interrelations
of species with environment determine which of these evolutionary potentials are realized and which remain in their infancy.” V.A. Zaslavskii [3] has also come to the conclusion that “The class of insects is characterized by the physiological mechanism that is built by the common plan, presented in all groups, and responsible for all types of photoperiodic and thermal reactions,” whereas the appearance of adaptations is the result of “selection of the specific possibilities of the general mechanism, which are needed in the given ecological situation.” Indeed, the plasticity of insect photoperiodic responses providing the capability of adaptation of species and individual populations for local cli-
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mate and other peculiarities of environment was repeatedly demonstrated in many field and laboratory studies [1–7]. However, evolution is not a simple adaptation to habitat, but “the ordered adaptatiogenesis” [8, 9] whose course to the great degree is “canalized,” i.e., limited by already formed species peculiarities. The specter of potential adaptations depends not only on the current requirements of environment, but also on the whole pre-history of development. Thus, in each living organism character, two components can be identified: the ecological one provided by specificity of environment and the evolutionary one reflecting the course of phylogenesis. Of course, such division is rather conventional, but can be realized, which is what makes the phylogenetic constructions possible. Hugh Danks in one of his reviews on evolution of insect seasonal cycles rightly noted that the same function could be realized by different pathways and the same adaptations can be achieved by different ways [10]. If the type of diapause, indeed, is first of all determined by climate, the taxon specifics can be realized in determination of the diapausing stage of development. It is well known that in some insect families, a certain forms of diapause can definitely prevail, e.g., the embryonic diapause in Acrididae, the pupal diapause in Noctuidae, the adult one in Chrysomelidae and Coccinellidae, etc. [1, 6, 11, 12]. Analysis of data on the well-studied taxa of insects and mites [13–17] shows that although seasonal cycles and mechanisms of their regulation are rather labile, they also have certain conservatism. Of course this stability can be due to similarity in the mode of life of representatives of the same taxon, but a certain role in their preservation is also played by the above-mentioned “canalization” of evolutionary changes. Thus, for example, numerous representatives of families Calliphoridae and Sarcophagidae (Diptera) are very close by the mode of life and character of nutrition, they very often inhabit the same epitope, but Sarcophagidae overwinter as pupae, while Calliphoridae—as larvae or adults [18]. Large insect taxa can also differ in physiological mechanisms of photoperiodic reactions. Thus, by opinion of David Saunders [7], one of classics of photoperiodism, the photoperiodic clock in Diptera is based on the mechanism of “external
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coincidence” (interaction of endogenous oscillator with the natural light–dark cycle), while in Hymenoptera—on the mechanism of “internal coincidence” (interaction of two endogenous oscillators). Besides, the specificity of the mechanisms of photothermal regulation of diapause consists not only in the type of response that is strongly correlated with the type of seasonal cycle (e.g., the facultative winter diapause is usually induced by short day and/or low temperature). Thus, an important feature of the mechanism of the photoperiodic induction of diapause is the photosensitive stage of the insect development, which perceives the day length. The sensitivity to the photoperiod most often occurs at the stage that directly precedes the diapausing stage. However, the specificity of diapause also determines peculiarities of its regulation: for example, in the case of adult (reproductive) diapause, not only larvae and pupae, but also adults can be photosensitive, which provides a possibility of the diapause induction after the period of reproductive activity [1–3, 5–7, 12]. However, if to be based on the above-mentioned concepts of the existence of the universal physiological mechanism underlying all types of photoperiodic and thermal control of insect development, the potential ability to respond to the day length and temperature as environmental cues for diapause induction should be characteristic of all stages of development of each insect species. Moreover, according to statements of modern evolutionary physiology [19, 20], this latent photosensitivity “inhibited and screened” with the dominant responses not always disappears completely and therefore can be revealed in special experiments. However, as far as we know, the studies dealing with detection and comparative analysis of “dominating” and “secondary” photothermal responses characteristic of different developmental stages of one species (or a group of closely related species) are rather scarce. Egg parasitoids of the genus Trichogramma Westw. (Hymenoptera, Trichogrammatidae) are natural enemies of many lepidopteran pests of agriculture and forestry. They are widely used for biological protection of plants and are an important component of natural biocenoses [21, 22]. Besides, the easily and fast reared Trichogram-
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also been known for several other insect species [2, 5, 6, 11, 24, 25]. Therefore, the responses regulating in Trichogramma species the choice between diapause and active development can be separated not only by acting factors, but also by the principle of action: the direct effect (the own responses of embryos and larvae) and the maternal effect (the effects mediated by the maternal and preceding generations). DIRECT TEMPERATURE REACTION Fig. 1. Effect of temperature (°C), at which the embryonic and larval development occurred on percentage of diapausing prepupae in various Trichogramma species and laboratory strains (%). (1 ) Trichogramma cacoeciae March.; (2 ) T. aurosum Sug. et Sor.; (3 ) T. pintoi Voegele; (4 ) T. evanescens Westw., the strain originated from Voronezh (European Russia); (5 ) T. evanescens, the strain originated from Zugdidi (Georgia) (from: [30]).
Fig. 2. Effect of duration of the cold exposure (days) of embryos and larvae (10°C on the background of 15°C) on the percentage (%) of diapausing prepupae of T. embryophagum Htg. (from: [36]).
mas turned out to be rather convenient models for quite different investigations including studies of mechanisms of the diapause regulation. All studied species of the genus Trichogramma inhabiting in the moderate climate, like many other hymenopteran parasitoids, are diapausing at the prepupal stage [1, 6, 23]. One of the essential peculiarities of the diapause regulation in Trichogramma species consists in that the portion of diapausing individuals depends not only on conditions of their development, but also on the factors affecting females of one or several preceding generations. This so-called “maternal effect” has
One of the first special studies [26] has already shown that temperature is the chief diapause–inducing factor in Trichogramma evanescens Westw.: at 11°С practically all prepupae diapaused, at 20°С only few individuals did, while at 25°С the diapause was not recorded. Subsequent investigations of various authors [27–39] have revealed similar thermal responses in many other Trichogramma species. By summarizing results of these studies, it can be concluded that temperatures between 10 and 12°С are optimal for diapause induction, the higher temperatures usually stimulate active development, while the lower temperatures cause cold stupor rather than diapause induction (Fig. 1). The thresholds of these thermal responses have significant intraspecies variability that, as it was also noted for many other insect species [1–4, 6, 11, 12], determines the lower tendency for diapause in the southern populations (comp. Figs. 1, 4 and 1, 5). A characteristic feature of the facultative winter diapause is that it (unlike the cold stupor) is a preceding response: the period of sensitivity to environmental cue and the diapause per se usually take place at different life cycle stages often separated by a significant time interval [1–7, 11]. In the case of the direct Trichogramma thermal response, the period of thermosensitivity lasts from the beginning of the embryonic development to the prepupal stage, at which diapause may occur [35, 36]. However, the highest thermosensitivity is peculiar to embryos and young larvae: for this period, even occasional 24-h long periods of decrease in temperature to 10–12°С increase significantly the portion of diapausing prepupae, a rise in the total duration of the cold exposures causing a proportional increase in the portion of diapausing individuals (Fig. 2). Thus, under natural conditions, even relatively short-
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term cold periods indicating the approach of winter can induce a tendency for diapause in Trichogramma species, while an increase in the total duration of cold periods leads to the corresponding increase in the portion of diapausing individuals. DIRECT RESPONSE TO PHOTOPERIOD The dependence of the percentage of diapausing prepupae on the day length during development of larvae of the given generation was revealed in T. evanescens [26]. However, other experiments with the same species gave contradictory results: if Trichogrammae were developed at 15°С in Mamestra brassicae L. eggs, the percentage of diapausing individuals amounted to 66% and 80% at the long day (16 h) and the short day (12 h), respectively, but if the hosts were eggs of Operophtera brumata L. and Ephestia kuehniella Zell., the percentage of diapausing prepupae at the short day was lower than that at the long day [37]. The experiments carried out by V.A. Zaslavskii et al. [27, 32, 39] have shown that at 15°C the portion of diapausing prepupae of T. evanescens, T. pintoi, and T. embryophagum under conditions of the short day (12 h) was practically the same as that under conditions of the long day (20 h). However, by data of A.P. Sorokina and V.A. Maslennikova [29], T. pintoi entered diapause significantly more often at 15°С and short day (12 h) than at the same temperature and constant light. The only study performed with using a wide specter of photoperiods has shown that the portion of diapausing prepupae of T. embryophagum in the dark and at the short day (4, 8, and 12 h) was somewhat higher than at the long day (16 and 20 h). Evidently, peculiar to the T. embryophagum larvae is the long-day photoperiodic response with a threshold day length of about 14 h, although the extent of this reaction did not exceed 10–15% [40]. Identical results were obtained in similar experiments on T. buesi and T. principium (S.Ya. Reznik, N.P. Vaghina, and N.D. Voinovich, unpublished data). On the whole, we can conclude that in Trichogramma species, portion of diapausing individuals little depends on the day length during their development. Even at near-threshold temperatures, this dependence was not always revealed and in
Fig. 3. Effect of photoperiod on the percentage of diapausing progeny in various Trichogramma species (%). (1 )–(3 ) Effect of photoperiod on preimaginal stages of maternal females: (1 ) Trichogramma principium Sug. et Sor. (from: [44]); (2 ) T. pintoi Voegele (from: [27]); (3 ) T. embryophagum Htg.; (4 ) effect of photoperiod on adult maternal females in T. embryophagum (from: [47]).
certain cases the percentage of diapausing prepupae increased with the day length (for an insect with the winter diapause, this is certainly a maladaptive response). Such “inadequate” reactions occur sometimes in various insect species at temperatures that are beyond optimum for photoperiodic responses [1–3, 6], but in Trichogramma species they are noted at 15°C (it is at this temperature that the temperature diapause induction usually starts). MATERNAL RESPONSE TO PHOTOPERIOD V.A. Zaslavskii with co-authors [27, 39] were the first to show that the portion of the diapausing progeny of various Trichogramma species much depended on the photoperiodic conditions of development of the preceding generation, although this maternal effect can be realized only in the case that the daughter individuals developed at the near-threshold temperature. This conclusion was confirmed by subsequent works of many authors [23, 29–33, 38–44]. The maximal portion of diapausing progeny is induced by short light day (10–12 h), while at long day (18 h and more) the portion of diapausing progeny is relatively small. The threshold day length values in various Trichogramma species are from 13–14 to 16–17 h (Fig. 3)
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Fig. 4. Effect of duration (days) of the short day exposure (the length of day 12 h on the background of the 20-h long day) directly preceding the adult take-off on the percentage of diapausing progeny of T. embryophagum Htg (%). Temperature conditions of development of progeny: (1 ) 13°C, (2 ) 14°C, (3 ) 15°C. The zero exposure—development at the 20-h long day, the 18day long exposure—development at the 12-h long day (from: [45]).
Fig. 5. Interaction of photoperiodic conditions of development of the maternal generation and of temperature conditions of development of the daughter generation; abscissa: in determination of diapause in Trichogramma pintoi Voegele, ordinate: percentage of diapausing individuals, %. Photoperiodic conditions of development of the maternal generation: (1 ) the 20-h long day, (2 ) the 12-h long day (from: [27]).
and rise significantly with the geographical latitude—this correlation is also characteristic of many other insect species with the long-day photoperiodic response inducing winter diapause [1–7, 11]). The extent of changes caused by the maternal photoperiodic response (all other factors being equal) depends on temperature, at which the progeny develops, and, according to data obtained by various authors working with various Trichogramma spe-
cies [27, 29, 32, 33, 38, 39, 41–44], usually does not exceed 60–80%. In the course of all above-mentioned studies, the maternal effect of Trichogrammas was determined by photoperiodic conditions of the entire preimaginal development of the maternal females. However, the recent studies [45, 46] have shown that the photoperiodic response (unlike the thermal response) is determined not by the “averaged” conditions of preimaginal development, but rather by the photoperiod of 2–3 days directly preceding the adult emergence (Fig. 4). Ecologically, this difference is quite explainable: whereas 2–3 cold nights do not necessarily mean approach of the late autumn and winter, for determination of the astronomic season time during summer and autumn, quite sufficient is measurement of duration of only one light day. Special experiments [45, 46] have shown that the photoperiodic response of Trichogramma pupae is extremely labile. The critical duration of the photoperiodic induction determined as the number of short-day or long-day light–dark cycles needed to achieve 50% of the response caused by permanent action of a given day length [1–7]) in some cases even could not be determined, as only one short day preceding the first flight of female stimulates a rise of the portion of diapausing progeny as strongly as the permanent development under the short day conditions (Fig. 4). For comparison, in most studied insect species the critical duration of the photoperiodic induction amounts to no less than 5–7 days [1–7]. However, it is to be reminded that with all clearness and undoubtedly adaptive importance of the maternal effect, it is realized in Trichogramma only under the near-threshold thermal conditions of development of the daughter generation. Similar results have also been obtained in experiments with several other parasitoids [48, 49]. As mentioned above, the photoperiodic response usually dominates in the photothermal regulation of insect seasonal cycles; therefore, it is used to state about a change in the threshold day length [1–7], but in the present case, rather a change in the threshold temperature takes place under the effect of day length (Fig. 5). The adaptive significance of this “photoperiodic correction of thermal response” is obvious: it allows the first generation of Trichogrammae to avoid the diapause induction
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under effect of the late spring cold periods, as the near-threshold temperatures of 12–15°C (Fig. 1) in spring occur during much longer light days than in autumn. Also revealed in Trichogrammae was the “grand-maternal effect,” i.e., the dependence of the portion of diapausing progeny on factors that have affected individuals of one or several generations that had preceded the maternal ones [27, 44]. Further studies have shown that in T. buesi a significant grand-maternal effect of the day length on the progeny diapause is traced in three, while in T. principium—in four generations (S.Ya. Reznik, N.P. Vaghina, and N.D. Voinovich, unpublished). It is to be particularly noted that, as seen from Fig. 6, the thresholds of maternal (12–14 h) and grand-maternal (14–16 h) photoperiodic responses of T. principium differ markedly (Fig. 6). This difference is probably not accidental, as whenever diapause occurred, grand-mothers of the diapausing generation naturally developed under longer day than the mothers did. The grand-maternal effect seems to be not merely a laboratory artifact. However, its adaptive role is far from being clear, because the grand-maternal effect was found in the same Trichogramma species that also showed a strong maternal effect, which made it possible to exactly determine the astronomic season immediately before adult emergence. Possibly, the grand-maternal effect increases the tendency for diapause in the progeny of females that developed under short day conditions during two generations, and, thus, it provides a gradual correction of a threshold photoperiodic response. The adaptive value of another recently discovered mechanism of diapause regulation (the dependence of the percentage of progeny that enters diapause on the day length that has affected adult maternal females) is clearer. The extent and the threshold of this adult photoperiodic response are very close to those of the pupal photoperiodic response (comp. Figs. 3, 3 and 3, 4). Adult females (as well as pupae) showed extremely labile photoperiodic reaction: only one short light–dark cycle applied to adults caused a significant increase in the portion of diapausing progeny of T. embryophagum females that developed under long day conditions [47]. Interestingly, when the females that have developed under short day conditions were
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Fig. 6. Interaction of photoperiodic conditions of development of the maternal and grand-maternal generations in determination of diapause (%) in Trichogramma principium Sug. et Sor.
transferred to long day conditions, the response was not nearly so fast and clear-cut. Possibly, the adult photoperiodic response is intended for the “latest correction” of the preimaginal photoperiodic response: under favorable conditions, Trichogramma females that have emerged in the end of summer–beginning of autumn can survive sufficiently long, so that the decreasing day length would induce in their progeny a corresponding increase in tendency for diapause. MATERNAL RESPONSE TO TEMPERATURE Temperature during preimaginal development also can affect the tendency for diapause in the progeny, although this effect is not as strong and clear-cut as that of photoperiod. For example, portion of the diapausing progeny of T. pintoi gradually decreased when temperature was increased from 15 to 25°C (all other factors being equal) [27]. A similar response was reported for T. cacoeciae [29, 30]. In insect species with a long-day photoperiodic response, inhabiting at the moderate climate, the induction of diapause is usually stimulated by low temperatures and inhibited by high temperatures [1–7, 11, 12]. This synergism between short day and low temperatures—the two cue factors that induce winter diapause—has obvious adaptive significance. However, the experiments on T. semblidis [32] gave quite opposite results: when the temperature
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at which development of maternal females proceeded increased from 20 to 35°C, the portion of diapausing progeny significantly increased. The same, certainly maladaptive response was also found in T. embryophagum when the experiments were performed under short day conditions (in nature, this corresponds to autumn, when diapause is naturally induced). However, if maternal individuals developed during the long day (in nature, this corresponds to summer, when diapause usually was not observed), the portion of diapausing progeny decreased with an increase in the temperature that affected females of the preceding generation [22, 30]. Moreover, the experiments performed on different generations of the laboratory strain of T. evanescens gave the directly opposite results: in the first experiments, the daughter individuals were diapausing somewhat more often, if the maternal females developed at 15°C, but not at 20°C; but further studies showed that when the temperature affecting maternal females increased from 15 to 25°С, the portion of diapausing progeny also increased [32, 39]. A.P. Sorokina [22] also indicates that “in T. evanescens the high temperature (25°C) in the maternal generation, in spite of long day, increased the tendency for diapause in progeny.” REGULATION OF DIAPAUSE IN TRICHOGRAMMAE: HIERARCHY OF INTERACTING RESPONSES As seen from the above-exposed, sensitivity to temperature and day length as to two signal factors regulating the seasonal cycle is characteristic of all stages of development of the studied Trichogramma species—from embryos to adults. Although photothermal responses of different stages of development and of different generations are rather peculiar or even contradirectional, they in combination, as it is to be expected in insects with facultative winter diapause, provide an increase in the portion of diapausing individuals with autumn decrease in the day length and temperature. However, different photothermal responses of Trichogrammae are far from being equal in strength and importance. The main reaction regulating the Trichogramma diapause is effect of temperature during embryonic and larval development on the portion of dia-
pausing prepupae in the given generation. This reaction seems to be adaptive (the low temperature induces the winter diapause), it is manifested under any photothermal conditions of development of the current and preceding generations, and the percentage of diapausing individuals varies, depending on temperature, from 0% to 100%. It is to be noted that in most insects the main factor inducing the winter diapause is not a decrease in temperature, but a reduction of the day length [1–7, 11, 12]. Possibly, the adaptive significance of domination of the thermal response in the Trichogramma genus consists in that it allows correlating the seasonal cycle not merely with the astronomical season changes, but with the weather specificity of the given autumn. A similar property is found for the circadian rhythms in Trichogrammae, which, unlike those in the majority of the studied insect species [1, 2, 5, 7, 12], are regulated not much by the direct endogenous circadian rhythms, but rather by the direct action of light and temperature, which makes it possible to associate the imago takeoff not simply with the certain time of day, but with optimal weather conditions [50, 51]. This high lability of seasonal and circadian cycles can be possibly explained by extremely small (less than 1 mm) size and very high rate of development (about 10 days at 25°C) of Trichogrammae, which makes them quite vulnerable for unfavorable environmental conditions, but, on the other hand, allowing them to use favorable seasons to develop one more generation. The thermosensitive stages (embryo and larva) precede directly the diapausing stage (prepupa), which provides the rate of reaction. The thermosensitive period is rather long, which allows accumulating data on short-term cooling off. Both the rate of reaction and the capability for “averaging” seem to be necessary for the adequate response to such a variable factor as the air temperature. However, temperature is the main factor inducing diapause also in some other (rather large and slowly developing) insect species under conditions of the moderate climate. Usually, these are the inhabitants of soil or other concealed insects [11], in which domination of the temperature response can be explained by the impossibility to perceive the day length. The secondary responses. The photoperiodic re-
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sponses providing the maternal effect, in spite of their clearness and undoubted adaptive importance, are minor, as they are realized only at the near-threshold values of the main (temperature) reaction, and the range of changes in the portion of the diapausing progeny, which are caused (all other conditions being equal) by the maternal effect usually not reaching 100%. The Trichogrammae of pupae and adults are sensitive to the day length determining the maternal effect. Instead of “averaging” that is a typical characteristic of the thermal response, the photoperiodic response shows “correction” or even rather “re-recording”: the final effect is determined by the information received for 1–2 days directly preceding oviposition. In most studied hymenopterous parasitoid species with maternal effect on the progeny diapause, the day length is perceived by adult females [48, 49, 52–54]. The detailed studies performed on the model insect Nasonia vitripennis Walker have shown that the larvae hatching from the first eggs laid by a female did not enter diapause and only after 8–10 days of maintenance at the short day conditions the females “switched” to the production of diapausing progeny. Such a “delayed” reaction seems to be adaptive for relatively large parasitoid with lifespan of about 25 days (under laboratory conditions) and laying out for this time 500–600 eggs [53]. However, for small, very vulnerable and much less fertile Trichogramma females, the first batch of eggs can turn out to be the last one [21]. Possibly, that is why the day length is perceived by pupae, while adults make correction of the photoperiodic response, if necessary. As shown above, certain peculiarities of the “grand-maternal” effect suggest that the dependence of the proportion of diapausing progeny on conditions of development of generations that have preceded the maternal females can also have some adaptive value. However, it is much more difficult to explain ecologically the domination of the maternal effect over the own photoperiodic response of Trichogramma larvae. The adaptive value of maternal effect is clear in two cases: (1) when the diapausing generation just has no time for the “own” photoperiodic response (e.g., in the case of embryonic diapause in certain species of Lepidoptera) and (2) when the stages preceding diapause cannot per-
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ceive the day length because of their hidden way of life (e.g. larvae of dipterans and their parasitoids). Although the significant effect of photoperiodic conditions of development of maternal generation on the progeny diapause incidence was recorded in many other insect species, the domination of the maternal effect over the own photoperiodic response of the diapausing generation was usually found either in cryptic larvae or in insect species with an embryonic diapause [1–7, 24, 25]. Most of the reported examples of the strong maternal effect on non-embryonic diapause of the progeny are among species of Diptera and Hymenoptera. In representatives of these orders the difference between modes of life of larvae (often hidden living) and adults (very rarely hidden) is particularly clear and large. Notice that diapause inhibition in one or several generations after diapause, which was found in several insect species, is not associated directly with photoperiodic response and has quite a different adaptive significance [1–7]. Trichogrammae usually infect the openly disposed insect eggs [21, 55]. The thin and semitransparent chorion does not prevent the perception of the natural light–dark cycle, as confirmed both by the own larval photoperiodic response and by numerous experiments on synchronization of endogenous circadian rhythms with photoperiod. At the temperatures close to the threshold of diapause induction, the Trichogramma development from egg to prepupal stage takes at least 10–15 days. This period of time is quite sufficient for the own larval thermal response and thus it would be more than sufficient for the photoperiodic response that is much faster and more labile. Possibly, the domination of the maternal photoperiodic response is a feature that had been acquired by the ancestors of modern Trichogrammatidae. Analysis of the literature [48, 49, 52–58] shows that the maternal effect was recorded for many species of various families of hymenopteran parasitoids and their hosts live both in hidden and in open habitats. Possibly, the maternal effect was already inherent in their common ancestors that infected hiddenliving hosts. This hypothesis agrees well with the absence of any recorded case of maternal effect on reproductive (adult) diapause in parasitoids: freeliving adults are able to respond independently to the day length. As noted above, the domination
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of the thermal response in regulation of diapause in the current generation that is typical of Trichogramma species also is often connected with the cryptic way of life. The tertiary responses. The direct response of Trichogramma larvae to photoperiod and the maternal response to temperature can be considered as reactions of the tertiary importance. These responses are not stable (not only the scale, but also the type of reaction varies in successive generations) and often maladaptive (the percentage of diapausing individuals increases under the long day and high temperature conditions). The laboratory experiments showed that the range of these reactions usually was small and most probably their effect on diapause induction in nature is negligible. This complex of characters suggests that at least in certain Trichogramma species, these responses are rudimentary reactions: they had been inherited from ancestral forms, but then their adaptive value was lost. As noted above, such preservation of old functional relationships that have been “shielded” by new reactions and thus can be revealed only by special studies is one of the general rules of evolutionary physiology [19, 20]. Rudimentary photoperiodic responses are not unique features of Trichogramma species. Similar rudimentary photoperiodic response that has lost the adaptive value has been earlier described in the lacewing Nineta pallida Schneider by T.A. Volkovich [14]. The rudimentary feature of the thermal correction of the maternal photoperiodic response can be probably explained by that its adaptive role is “intercepted” by the direct thermal reaction of the larvae of the diapausing generation. As a result, the thermosensitive stage perceiving temperature as a cue factor immediately precedes the diapausing stage, which made the thermal response particularly fast and labile. Meanwhile, it is the high lability and sensitivity to the current specifics of the given season, which is the main advantage of temperature over the light day length as the “sensor of season of year”. It is much more difficult to explain the weakness and instability of the direct photoperiodic response of larvae of the diapausing generation. In most studied insect species, a facultative winter diapause is regulated by the direct (rather than by
the maternal) photoperiodic response [1–7, 12]. Most likely, the direct photoperiodic response in Trichogramma species also seems to be a rudimentary photoperiodic response that “gave the leading role” to the maternal effect. It is remarkable that in many species of insect parasitoids that showed the maternal effect on the progeny diapause, the direct larval photoperiodic response was not revealed at all. Interestingly, in most of these parasitoids, like in Trichogramma species, the absence of dependence of the portion of diapausing individuals on the direct response to day length is combined with the marked dependence on temperature [48, 49, 52, 53, 57]. CONCLUSION By summarizing this brief review, it should be noted, first of all, that the photothermal regulation of diapause in Trichogramma species represents a complex of many interacting reactions. All stages of Trichogramma development from the early embryo to the egg-laying female can perceive temperature and day length as environmental cues inducing or inhibiting diapause. The effect of these factors can be observed (although to different degree) not only in the current, but also in one or several subsequent generations. Note that the portion of diapausing progeny can also depend on many other factors (host species and stage of the host embryonic development, the age of the maternal female, etc.) that are beyond the present paper as well as rather significant endogenous changes in tendency for diapause, which have been reported in many Trichogramma species and in opinion of V.A. Zaslavskii [3, 32, 39] are connected with the maternal effect on progeny diapause. The similar abundance of interacting “main” and “secondary” responses has been also recorded in the blow fly Calliphora vicina R.-D., another thoroughly studied model insect with the maternal effect on progeny diapause [18, 59]. Possibly, the interaction of numerous reactions controlling diapause is not an exception, but the norm for insects, although the secondary (and, particularly, rudimentary) responses can be reliably revealed only with very high sample sizes. For example, more than 100 000 infected eggs of the grain moth were
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dissected to compare thermosensitivity of different stages of T. embryophagum [45]. Such investigations can be performed only with model insects that can be easily reared in the laboratory, while in most studies only one or few “main” responses can be detected. Anyway, the Trichogramma species show a hierarchy of interacting responses, some of which have lost their adaptive significance, can be revealed only by special experiments, and evidently do not play a significant role in regulation of natural seasonal cycles. These results once again show that insects have a unified physiological mechanism for diapause regulation, while patterns of particular responses, their relative importance, and sensitive stages of development are determined not only by ecological peculiarities, but also by the course of the preceding evolution of a taxon. In this aspect the photothermal regulation of diapause in Trichogramma does not differ from many other morphological, physiological, and ethological characters representing a result of compromises between the current requirements of environment and historical restriction of the specter of possible adaptations. In the course of further studies on mechanisms of regulation of insect diapause, it would be appropriate to combine two approaches: (1) intensive physiological studies performed on large sample sizes of model species and aimed at revealing all (including rudimentary) photoperiodic and thermals reactions, and (2) studies on ecological and phylogenetic components of inter- and intraspecies variability of dominating photothermal responses in the maximally possible number of species of different taxa. ACKNOWLEDGMENTS The author is much grateful to Drs. N.P. Vaghina, N.D. Voinovich, and T.Ya. Umarova (Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia) for the many-year fruitful cooperation. This work was partly supported by the Program of the Department of Biological Sciences of the Russian Academy of Sciences “Biological Resources of Russia: estimation of the state and fundamental grounds of monitoring.”
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