Sexual morph determination in the aphid, Acyrthosiphon pisum

The effects of two temperatures and a series of photoperiods on sexual morph determination in an aphid are examined. Photoperiodic response curves are presented and analysed. Female morph determination and male production were influenced by both these environmental factors. Sexuals were produced only at shorter photoperiods and the critical photoperiods for sexual production were shorter at the higher temperature. The critical photoperiod for male production differed from that for female morph determination and was more sensitive to temperature. These results are discussed in relation to the ‘maternal switching mechanism’ and sex determination. The significance of the temperature effect and also the variation in photoperiodic response are discussed.     

The effect of temperature on the photoperiodic 'counters' for female morph and sex determination in two clones of the black bean aphid, Aphis fabae

Experiments were performed on two clones of the black bean aphid, Aphis fabae Scopoli – one from Aberdeen, Scotland (57°N), the other from Cambridge, England (52°N) ? to determine the number of long- or short-night cycles required for 50% induction of winged versus wingless females on the one hand and males versus females on the other (i.e. required day number, RDN), at three temperatures, 12.5, 15 and 17.5°C. In the case of female morph determination, the RDN for long-night cycles was temperature compensated, whereas that for short-night cycles was highly temperature dependent. For sex determination, the RDN for long-night cycles was again temperature compensated, whereas, due to the mechanism of sex determination, male production was close to 100% in our protocol, even with a maximal number of short-night cycles, and the RDN could therefore not be assessed. Model-generated response curves, using the recently developed ‘double circadian oscillator model’ for photoperiodic time measurement in insects and mites, closely resembled the observations. It could also be shown that differences observed between response curves of female morph and sex determination in the Scottish clone were due, according to the model, to differences in their photoperiodic ‘counters’, rather than to differences in their clocks.     

Environmental factors controlling seasonal morph determination in the small copper butterfly, Lycaena phlaeas daimio Seitz.

Environmental factors controlling seasonal morph determination and extension of the larval stages in Lycaena phlaeas daimio were studied in field observations and laboratory experiments, using criteria based on the numbers of red scales in the wing spots. Photoperiod and temperature conditions applied during the larval period and a low-temperature (5°C) introduced in pupal period were expected to be factors affecting the seasonal morph determination: the effects were confirmed by laboratory experiments. Furthermore, the length of the larval period extended by exposure to short days at 20°C, but not at 25°C, were found to show a clear correlation with the spring morph determination, but the correlation coefficient was negative in marked contrast to the situation in Polygonia and Papilio.     

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.     

Photoperiod- and temperature-dependent regulation of pupal beige/black polymorphism in the small copper butterfly, Lycaena phlaeas daimio Seitz

The small copper butterfly, Lycaena phlaeas daimio, has pupal beige/black polymorphism, the development of which is found to be controlled in an apparent association with the development of adult seasonal polymorphism (spring and summer morphs) by photoperiod and temperature in the larval stages. That is, the pupae of beige and black types developed under long-day and short-day conditions tend to develop into brown-winged and red-winged adults, respectively. In addition, a large proportion of long-day pharate pupae chilled at 4 degrees C for 5 days were observed to develop into pupae whose head-thoracic complexes and abdomens were judged to be of the black and intermediate types, respectively. They developed into adults with redder wings as compared to those obtained from unchilled pupae. The results indicate that the physiological mechanism underlying the photoperiodic control of the development of adult seasonal polymorphism may also play a significant role in the determination of pupal beige/black polymorphism in L. phlaeas daimio. Furthermore, cuticle melanization was found to be induced in the head-thoracic complexes of pupae by chilling of the pharate pupae. Melanization of pupal cuticle seems to occur in a close association with the development of reddish-winged adults.     

The photoperiodic responses and phenology of an English strain of the pea aphid Acyrthosiphon pisum

Abstract. 1. The response curves for the photoperiodic induction of the sexual forms (oviparae and males) differ significantly in an English clone of the pea aphid Acyrthosiphon pisum Harris. Male production is sharply peaked. The late summer scotophases (dark periods) that initiate male production are 1.0–1.5 h shorter than those that initiate ovipara production; the induction of males, but not oviparae, virtually ceases at scotophases longer than 12 h. This disparity suggests that there are two photoperiodic clocks.
2. All ovipara-producing aphids switch spontaneously to virginopara production part-way through the progeny sequence, irrespective of photoperiod. This may confer the ability to overwinter partheno-genetically under favourable climatic conditions. Since males are always born last in the progeny sequence this possibility would be pre-empted unless the terminal male sequences were suppressed by long winter scotophases.
3. The role of the photoperiodic response in determining the seasonal phenology was tested in the field by exposing a succession of laboratory-reared aphids to natural photoperiods, in late summer and autumn. Adult males and oviparae developed synchronously in early October, the difference in critical scotophase compensating for the late appearance of males in the progeny sequence. A large part of the 'civil twilight' is photoperiodically active.
4. Clones propagated outdoors by isolating aphids in each generation from the terminal sequence of virginoparae did not survive the whole winter of 1985/86. The chances of survival were reduced by severe weather and by the inability of the photoperiodic system to 'turn off' the production of early born oviparae which are, therefore, 'wasted'.     

Role of natural day-length and temperature in determination of summer and winter diapause in Pieris melete (Lepidoptera: Pieridae)

Under field conditions, the cabbage butterfly, Pieris melete, displays a pupal summer diapause in response to relatively low daily temperatures and gradually increasing day-length during spring and a pupal winter diapause in response to the progressively shorter day-length. To determine whether photoperiod is 'more' important than temperature in the determination of summer and winter diapause, or vice versa, the effects of naturally changing day-length and temperature on the initiation of summer and winter diapause were systematically investigated under field conditions for five successive years. Field results showed that the incidence of summer diapause significantly declined with the naturally increasing temperature in spring and summer generations. Path coefficient analysis showed that the effect of temperature was much greater than photoperiod in the determination of summer diapause. In autumn, the incidence of diapause was extremely low when larvae developed under gradually shortening day-length and high temperatures. The incidence of winter diapause increased to 60-90% or higher with gradually shortening day-length combined with temperatures between 20.0°C and 22.0°C. Decreasing day-length played a more important role in the determination of winter diapause induction than temperature. The eco-adaptive significance of changing day-length and temperature in the determination of summer and winter diapause was discussed.     

Photoperiodic and thermal regulation of antifreeze protein levels in the beetle Dendroides canadensis

The importance of photoperiod, temperature and their interaction in controlling the seasonal pattern of haemolymph antifreeze protein levels in larvae of the beetle Dendroides canadensis was investigated. A complete photoperiodic response curve for antifreeze protein production was generated at 20°C with larvae collected in early fall. Individuals exposed to a 10-h photoperiod or less, including constant darkness, had significantly elevated antifreeze levels over those maintained in an 11-h photoperiod or more, including constant light. The critical daylength resulting in 50% population response lies between LD 11:13 and LD 10:14. This photoperiodic response was masked at sufficiently low (threshold between 15 and 10°C) and high (threshold between 25 and 30°C) temperatures. Partial photoperiodic response curves (at 17 and 25°C) obtained within this specified temperature range indicate that the position of the critical photoperiod (between 10 and 11 h) is stable while the amplitude of the response curve is temperature dependent.Experiments investigating the mechanisms controlling the spring depletion of protein antifreeze levels suggest that both photoperiod and temperature are important.The dominant response of photoperiod in the fall along with the modifying effects of temperature are considered to provide the necessary precision to assure adequate cold tolerance early in the fall and the flexibility to protect the species from yearly variation in weather conditions.     

Summer and winter diapause in pupae of the cabbage butterfly,Pieris melete Ménétriés

The cabbage butterfly, Pieris melete is multivoltine with a pupal summer and winter diapause. Summer and winter diapause are induced principally by relatively long and short daylengths, respectively. The intermediate to relatively short daylengths of autumn permitted some pupae to develop without diapause in the field. A short daylength had a stronger diapause inducing effect than a relatively long one under higher temperatures. The principal sensitive phase for photoperiodic response occurred before the late 3rd larval instar. The critical daylength for wild autumnal populations was between 12h 30min and 12h 40min at an average temperature of 20.5 degrees C. A night interruption by 2h of light averted diapause most effectively when it was placed 10 to 12h after lights-off. High temperatures and long days during summer inhibited the incidence of diapause, suggesting that the occurrence of summer diapause is due to the specific climatic conditions occurring in April and early May, rather than to the high temperatures in summer. This indicates that the butterfly has a cryptic ability to reproduce in summer. High temperatures delayed diapause development, whereas low temperatures enhanced it, indicating that the optimum temperature of diapause development is lower. The diapause regulating mechanisms thus ensure that the species synchronises its development and reproduction with the growth seasons of the host plants and provide the species with a high degree of flexibility in its life cycle.     

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.     

The prediapause copulation and its significance in the butterflyEurema hecabe

In the pierid butterflyEurema hecabe, which shows seasonal polymorphism (summer and autumn morphs) and overwinters at adult stage, whether or not the prediapause copulation may be of usual occurrence and reproductively functional was examined. From the counts of the spermatophores carried by the females, it is clear that the prediapause copulation characteristically occurs in reproductively inactive females of the autumn corph. From behavioral observations in the field, mating partners of those females are mostly males of the summer morph rather than from the autumn morph. In autumn, males of the summer morph remained abundant and searched for females on the larval food plants. Furthermore, they mated frequently with autumn morph females. Autumn morph males seemed to be sexually less active or inactive before hibernation. Microscopic examinations of the spermathecae were made in mated autumn-morph females collected before and after hibernation. The results indicate that sperm is passed by the males at autumnal copulation. The sperm may be stored in the female reproductive tract and utilized for fertilization in spring. This supposition is strongly supported by field data; that is, once-mated autumn-morph females laid fertilized eggs in spring. Finally, physiological basis of the prediapause copulation, its adaptive signficance and the behavioral advantage inE. hecabe are discussed from the viewpoint of seasonal adaptation.     

The role of temperature and larval crowding in morph determination in a tropical beetle, Callosobruchus subinnotatus

Many insect species can produce individuals of more than one form or morph. Different morphs of the same species may differ in their physiology, morphology and in behaviour. Understanding the factors and mechanisms involved in determining the production of different morphs of insect species is of major importance in understanding the evolution of specific life-history strategies. In this paper, we studied the importance of temperature as an environmental factor involved in morph determination of the tropical beetle, Callosobruchus subinnotatus. Adults occur as relatively sedentary, highly fecund, 'normal' morphs or as an 'active' morph adapted to dispersal. Larval crowding, seed density and external temperature were independently manipulated in a series of controlled experiments and the proportions of 'active' and 'normal' adult morphs among the emergent adult populations were quantified and compared. Development in crowded conditions was found to be associated with the production of a significantly higher proportion of 'active' adults than development in isolation, and was also responsible for a predictable rise in the localised temperature of infested heaps of seeds of between 4 and 8 degrees C above ambient (27 degrees C). This rise in temperature is subsequently shown to be directly and quantitatively associated with the proportion of 'active' adults among emerging adults, both in the presence of larval crowding and independently from it. Thus, it is suggested that in the crowded environment representative of an infested seed store, it is rising temperature, occurring at a specific point in insect development which is the proximate cue for 'active' morph induction in C. subinnotatus. The results are compared to the strategies used by other polymorphic insects to survive in heterogeneous environments.     

Neuroendocrine regulation of seasonal morph development in a bivoltine race (Daizo) of the silkmoth, Bombyx mori L

We investigated the neuroendocrine regulation of the development of seasonal morphs in a bivoltine race (Daizo) of the silkmoth, Bombyx mori, by decerebration, the transplantation of brain-suboesophageal ganglion (Br-SG) complexes and the injection of active neuropeptides. When brains were removed from fresh pupae destined to develop into summer morphs (SD pupae) by embryonic and larval exposures to short days at low temperature, the pupae developed into autumn or intermediate morphs. However, in pupae destined to develop into autumn morphs (LD pupae), the operation did not show an effect on seasonal morph development. Br-SG complexes were excised from fifth-instar LD and fifth-instar SD larvae 2 days after larval ecdysis and were transplanted into the abdomen of SD larvae of the same age. The Br-SG complexes of LD larvae, but not the Br-SG complexes of SD larvae, shifted the host's seasonal morph development toward the autumn morph. Furthermore, when treated with crude pupal SGs extract and diapause hormone (DH), fresh SD pupae developed into autumn or intermediate morphs, respectively. Possibly the development of seasonal morphs in the silkmoth, B. mori, is regulated by a novel function of DH. Alternatively, DH may act on the imaginal wing disks at an earlier stage than on the ovaries.     

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.     

Larval temperature experience determines sensitivity to cold-shock-induced wing color pattern changes in the blue pansy butterfly Junonia orithya

The butterfly wing color patterns are unique to a species but are modified in response to cold-shock and tungstate treatments at the pupal stage, producing characteristic temperature–shock (TS) phenotypes that are distinct from the color patterns of seasonal polyphenism. In this study, we examined the efficiency of cold-shock and tungstate treatments for color pattern modifications at the pupal stage in relation to larval rearing conditions for the fall or summer morph using the blue pansy butterfly Junonia orithya. We found that larvae reared under the low-temperature condition that induces the fall morph exhibited hardiness against the color pattern changes imposed by cold-shock or tungstate treatment at the pupal stage. When larvae were fed an artificial diet containing tungstate under the high-temperature condition that induces the summer morph, they were still vulnerable to color pattern changes imposed by cold-shock or tungstate treatment at the pupal stage. Furthermore, larvae reared under the high-temperature condition were subjected to cold-shock or tungstate treatments at the pupal stage. In addition to the expected TS-type changes, these individuals exhibited a reduced number of eyespots in adults, which is a feature of the fall morph. These results suggest that the temperature condition experienced by the larvae, but not their consumption of tungstate, determines the sensitivity of the wing imaginal discs to cold-shock and tungstate treatments at the pupal stage.     

Diapause induction and clock mechanism in the pine caterpillar Dendrolimus tabulaeformis (Lep., Lasiocampidae)

Abstract:  Dendrolimus tabulaeformis overwinters as third to fourth instar larvae at short days in autumn. Using 24-h light–dark cycles, the photoperiodic response curves were similar at 24 and 28°C. The critical night length was 9 h 20 min at 24°C and 9 h 50 min at 28°C. Under non-24 h light–dark cycles, duration of scotophase proved crucial in the determination of diapause. In night interruption experiments using 24-h light–dark cycle, a 1-h light pulse falling 8 h in the darkness strongly averted diapause in comparison with other light pulses. Nanda–Hamner experiments showed two weak troughs of diapause inhibition, suggesting the possible involvement of the circadian system. However, Bünsow experiments did not support the evidence of the involvement of circadian oscillatory system in photoperiodic time measurement. These results suggest that photoperiodic time measurement in this moth shows a non-oscillatory 'hourglass-like' response model or a rapidly damping oscillator model.     

Maladaptive photoperiodic response in an invasive alien insect, <Emphasis Type="Italic">Milionia basalis pryeri</Emphasis> (Lepidoptera: Geometridae), in southern Kyushu,Japan

The geometrid moth, Milionia basalis pryeri Druce, is an important pest of Podocarpaceae trees that has recently become established in the southern part of the main island of Kyushu, Japan. The species exhibits a multivoltine seasonal life cycle, with adults emerging mostly from spring to autumn, and occasionally being observed in winter. In this study, life-history traits and overwintering success were examined for a population collected in southern Kyushu. A long-day photoperiodic response was shown in larval and pupal development, with larvae and pupae developing significantly more slowly under short-day conditions than under long-day conditions. The critical photophases for this response were 12–13 h/day at 20 °C and 10–12 h/day at 25 °C. In the field, only individuals that pupated at a particular time in autumn remained in the pupal stage during winter, but all of them failed to eclose normally to adults, although some of them attained the wing pigmentation stage in winter to spring. This maladaptive seasonality in M. basalis pryeri in southern Kyushu is attributed to inconsistency between the climate of the new habitat and the innate ability of M. basalis pryeri to respond to seasonal cues, and is considered to be an ecological cost of a range-expanding insect.     

Effects of changing photoperiods in the life cycle regulation of the comma butterfly, Polygonia c-album (Nymphalidae)

Abstract. 1. Regulation of adult reproductive diapause and seasonal polyphenism was studied in two populations of the comma butterfly, Polygonia c-album (L.) (Nymphalidae), from Stockholm, Sweden, and Oxford, England.
2. In the univoltine Stockholm population short and long constant day-lengths (in the range 12–22 h) at 20°C were ineffective in averting the production of the dark, generally diapausing, morph, but the non-diapausing light morph could be produced if daylengths were increased during larval development. The procedure was especially effective with increases from 12 to 22 h, but the tendency was the same with a more realistic increase, from 18 to 20 h.
3. In the partially bivoltine English population a critical constant day-length for morph and diapause induction was found between 12 and 18 h. Decreasing daylengths above the critical daylength early or late in larval development resulted in production of the diapausing morph.
4. These results suggest a system for environmental control where day-lengths which increase throughout the larval period indicate an early date before summer solstice, meaning that there is sufficient time for a second generation of offspring to reach the hibernating adult stage before winter. The ecological significance of the results is discussed.     

Mate preference in males of the cabbage butterfly, Pieris rapae crucivora, changes seasonally with the change in female UV color

We initially investigated whether females of the cabbage butterfly, Pieris rapae crucivora, exhibit a seasonal change in ultraviolet wing color, which is a key stimulus for mate recognition by conspecific males, and whether and how a seasonal change affects the mating behavior of the males. We found that female UV wing color changes seasonally, the color being more pronounced in summer than in spring or autumn. We also demonstrated that male mate preference changes seasonally, concomitantly with the change in female UV color. Specifically, males appearing in summer exhibit a mating preference for summer-form females over spring- or autumn-form females, while those appearing in spring or autumn exhibit no seasonal preference, thereby facilitating more effective mate location. Our results suggest that this field of study will require more strictly controlled experimental investigation in which the seasonal change in UV color is considered when UV-influenced mating behaviors such as mate choice are investigated.