Regulation of adult diapause inCoccinella septempunctata septempunctata andC. septempunctata brucki from two regions of Japan (A Minireview)

In similar climatic conditions of central/northern Europe and Hokkaido, Japan, both subspecies ofCoccinella septempunctata L. have similar life-cycles: long-day photoperiodic response ensures the induction of winter diapause. In the mild climate of Honshu, Japan,C. s. brucki Mulsant shows a different life cycle: short-day photoperiodic response leads to the induction of summer diapause while overwintering is quiescence. All populations show an important variation in photoperiodic response.     

RearingGlypta fumiferanae [Hym.: Ichneumonidae] on a multivoltine laboratory colony of the western spruce budworm (Choristoneura occidentilis) [Lep.: Tortricidae]

Methods were developed for rearingGlypta fumiferanae Viereck on a nondiapausing laboratory colony of the western spruce budworm,Choristoneura occidentalis Freeman. Both host and parasite are univoltine and undergo diapause in nature. In this study, the parasite's voltinism was synchronized with that of a nondiapausing host.G. fumiferanae mated readily in the laboratory, and 5 consecutive generations were reared with an average generation time of less than 8 weeks-much less than the 23 weeks needed for 1 generation to develop in the field. Developmental times are reported, and some aspects of behavior described.     

Functional identification of an FMRFamide-related peptide gene on diapause induction of the migratory locust,Locusta migratoria L

FMRFamide-related peptides (FaRPs) are a type of neuropeptide, which participate in a variety of physiological processes in insects. Previous study showed that myosuppressin, being a member of FaRPs, initiated pupal diapause in Mamestra brassicae. We presumed that FaRPs genes might play a critical role in photoperiodic diapause induction of L. migratoria. To verify our hypothesis, flrf, a precursor gene of FaRP from L. migratoria, was initially cloned under long and short photoperiods that encoded by flrf gene identified from central nervous system (CNS). Phylogenetic analysis showed that the protein encoded by L. migratoria flrf gene, clustered together with Nilaparvata lugens (Hemiptera: Delphacidae) with 100% bootstrap support, was basically an FMRFamide precursor homologue. We noticed the availability of -RFamide peptides (GSERNFLRFa, DRNFIRFa) under short photoperiod only, which suggested their functions related to photoperiodic diapause induction. RNAi and quantitative real-time PCR (qRT-PCR) results further confirmed that the flrf gene promoted locust's diapause.     

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

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

Shifts in metabolomic profiles of the parasitoid Nasonia vitripennis associated with elevated cold tolerance induced by the parasitoid's diapause,host diapause and host diet augmented with proline

The ectoparasitoid wasp, Nasonia vitripennis can enhance its cold tolerance by exploiting a maternally-induced larval diapause. A simple manipulation of the fly host diapause status and supplementation of the host diet with proline also dramatically increase cold tolerance in the parasitoid. In this study, we used a metabolomics approach to define alterations in metabolite profiles of N. vitripennis caused by diapause in the parasitoid, diapause of the host, and augmentation of the host's diet with proline. Metabolic profiles of diapausing and nondiapausing parasitoid were significantly differentiated, with pronounced distinctions in levels of multiple cryoprotectants, amino acids, and carbohydrates. The dynamic nature of diapause was underscored by a shift in the wasp's metabolomic profile as the duration of diapause increased, a feature especially evident for increased concentrations of a suite of cryoprotectants. Metabolic pathways involved in amino acid and carbohydrate metabolism were distinctly enriched during diapause in the parasitoid. Host diapause status also elicited a pronounced effect on metabolic signatures of the parasitoid, noted by higher cryoprotectants and elevated compounds derived from glycolysis. Proline supplementation of the host diet did not translate directly into elevated proline in the parasitoid but resulted in an alteration in the abundance of many other metabolites, including elevated concentrations of essential amino acids, and reduction in metabolites linked to energy utilization, lipid and amino acid metabolism. Thus, the enhanced cold tolerance of N. vitripennis associated with proline augmentation of the host diet appears to be an indirect effect caused by the metabolic perturbations associated with diet supplementation.     

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

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

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

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

Physical and physiological factors in diapause initiation of two hyperparasites of the tobacco hornworm,Manduca sexta

Hypopteromalus tabacum diapauses as a last larval instar and Catolaccus aeneoviridis as a non-pharate pupa within cocoons of the primary parasite, Apanteles congregatus. Four factors (photoperiod, temperature, maternal age, and physiological state of the host) were tested for their significance in diapause initiation of both species. A 10L : 14D photoperiod produced a higher incidence of diapausing individuals than a 13L : 11D photoperiod. In the temperature range from 18 to 24°C, the incidence of diapause was inversely related to temperature. The incidence of progeny entering diapause varied with the age of the mother, younger ones producing fewer diapausing offspring. An increase in the number of C. aeneoviridis entering diapause was observed when the host, A. congregatus, was in the diapausing, rather than the nondiapausing condition. Analysis of the data indicated that interactions between these four factors also played an important rôle in diapause initiation of both species.     

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 time measurement in the spider mite Tetranychus urticae: A novel concept

To explain photoperiodic induction of diapause in the spider mite Tetranychus urticae a new theoretical model was developed which took into account both the hourglass and rhythmic elements shown to be present in the photoperiodic reaction of these mites. It is emphasized that photoperiodic induction is the result of time measurement as well as the summation and integration of a number of successive photoperiodic cycles: the model, therefore, consists of separate ‘clock’ and ‘counter’ mechanisms. In current views involvement of the circadian system in photoperiodism is interpreted in terms of the hypothesis that the photoperiodic clock itself is based on one or more circadian oscillators. Here a different approach has been chosen as regards the role of the circadian system in photoperiodism: the possibility, previously put forward by other authors, that some aspect of the photoperiodic induction mechanism other than the clock is controlled by the circadian system was investigated by assuming a circadian influence on the photoperiodic counter mechanism. The derivation of this ‘hourglass timer oscillator counter’ model of photoperiodic induction in T. urticae is described and its operation demonstrated on the basis of a number of diel and nondiel photoperiods, with and without light interruptions.     

Role of the brain and ring gland in regulation of pupal diapause in the flesh fly Sarcophaga crassipalpis

Larvae of Sarcophaga crassipalpis photoperiodically programmed for pupal diapause pupariate later than larvae programmed for continuous development. Pupariation time is determined by the brain-ring gland complex as evidenced by transplantation experiments in which the timing of pupariation was transferred from one larva to another by transplantation of the brain-ring gland complex. The developmental commitment (diapause or nondiapause) of the larva also can be transferred with the brain-ring gland complex if the recipient's own neuroendocrine system is suppressed by ring gland extirpation. Thus, photoperiodic programming of the brain-ring gland complex is not only responsible for developmental commitment but also for determining the duration of the prepupal period. Surgical experiments with pupae indicate that an intact brain-ring gland complex is required for diapause termination and initiation of adult development. Pupae fail to break diapause if either the brain or the ring gland is removed or if their nervous connections are severed.     

Effect of photoperiod on a winter and on a summer diapause in two species of cranefly (Tipulidae)

Two craneflies, Tipula subnodicornis and Tipula pagana, both undergo diapause in the final larval instar. The species showed differences in the intensity of diapause and in the timing of the photoperiodic reaction during diapause, that could be related to season. Tipula subnodicornis undergoes a winter diapause that is induced and maintained in its early stages by short photoperiod (L:D:6:18). In the laboratory individuals in the early stages of diapause terminated diapause and pupated earlier when they were exposed to daylengths of, or greater than, 12 hr. However, it is suggested that in the field diapause is broken before the natural daylength is long enough to have any accelerating effect on development. Tipula pagana has a summer diapause which is of greater intensity than that of Tipula subnodicornis and some larvae were maintained for 197 days in the laboratory, without pupating, on an 18 hr daylength. Diapause was broken by a L:D;16:8 photoperiod and development was accelerated by a further decrease in daylength. The acceleration in development rate was attended by a decrease in the variance about the mean date of emergence and resulted in a highly synchronised emergence period. It is suggested that this quantitative response to daylength is particularly important to a species that emerges in the autumn when the temperature in the field is falling.     

Temperature and photoperiodic control of diapase induction in the ant <Emphasis Type="Italic">Lepisiota semenovi</Emphasis> (Hymenoptera,formicidae) from Turkmenistan

The ants L. semenovi has been found to belong to species with endogenous-heterodynamic seasonal life cycles with the obligate diapause induced predominantly by factors internal for a colony, whereas external ecological factors (photoperiods and temperature) produce merely modifying effects by accelerating or delaying the diapause onset. The photoperiodic and temperature regulation of diapause induction in larvae and queens is shown. Under effect of short days and low temperature the periods of larval pupation and queen oviposition in a colony are shortened markedly, i.e., the diapause of larvae and queens occurs earlier. The daily rhythms of temperature 15/25°C and particularly 20/30°C as compared with constant temperatures 20 and 25°C that correspond to the mean circadian temperatures of the thermorhythm, inhibit manifestations of the short day effects by stimulating the non-diapause development and increasing duration of the seasonal development cycle of ant colonies. The L. semenovi photoperiodic reaction is quantitative, as development and pupation of larvae and egg-laying of queens cease sooner or later under both the short and the long days, but in the latter case significantly later. Thus L. semenovi is one more example among very rare ant species that are revealed to have the photoperiodic regulation of the colony development seasonal cycle.     

Control mechanisms of larval diapause and quiescence in Trogus mactator, an endoparasite of papilionids

First instar larvae of Trogus mactator Tosquinet (Hymenoptera: Ichneumonidae) developed to second instar immediately after pupation of the host, Papilio xuthus L., under a short photoperiod (L10: D14) as well as under a long photoperiod (L15: D9). The host went into diapause as pupa under short photoperiods, and the parasite at the third instar in the host pupa. They responded independently to short photoperiods. The critical photoperiods for diapause induction both in the parasite and the host were between 12 and 13 h, but there was a slight disparity between them. Diapause of neither the parasite nor the parasitized host was terminated under short photoperiods. Diapause of the parasite in a diapausing host pupa was completed when it was transferred to an incubator having a long photoperiod. This suggests that the exposure to a long photoperiod breaks diapause in the parasite irrespective of physiological conditions of the host. The period from the change in photoperiod to time of parasite emergence shortened as the change was made later. The parasite remaining in a host pupa for 60 days completed diapause even under a short photoperiod when it was implanted into a nondiapausing host pupa, or when 20-hydroxyecdysone was injected into the parasitized and diapausing host pupa. These results indicate that the physiological development for diapause termination in T. mactator seems to complete 60 days after host pupation and endogenous ecdysteroids are somehow involved in termination of diapause in the parasite.

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Résumé Que la photopériode soit brève (L10/D14) ou longue (L15/D9), le premier stade de T. mactator Tosquinet (Hym. Ichneumonidae) donne un second stade immédiatement après la nymphose de son hôte, Papilio xuthus L.,. L'hôte entre en diapause au stade nymphal sous photopériodes courtest et le parasite au troisiéme stade larvaire dans la nymphe de l'hôte. Ils réagissent indépendamment aux courtes photopériodes. Les photopériodes critiques pour l'induction de la diapause, tant de l'hôte que du parasite, se situent entre 12 et 13 h, mais il y a une légère différence. Ni la diapause de l'hôte, ni celle du parasite ne se terminent sous de courtes photopériodes. Le transfert dans une étuve ayant une longue photopériode rompt la diapause du parasite dans un hôte diapausant. Ceci laisse supposer que l'exposition à une longue photopériode rompt la diapause du parasite quel que soit l'état physiologique de l'hôte. Le délai entre le moment du changement de la photopériode et la date d'émergence du parasite, est d'autant plus raccourci que le changement est tardif. Les parasites restés dans une nymphe hôte pendant 60 jours, achèvent leur diapause même avec une photopériode courte quand ils sont transplantés dans un hôte sans diapause, ou quand de la 20-hydroxyecdysone a été injectée dans la nymphe hôte parasitée et diapausante. Ces résultats montrent que le développement physiologique nécessaire à la fin de la diapause semble achevé 60 jours après la nymphose de l'hôte et que les ecdystéroïdes endogènes semblent impliqués d'une manière ou d'une autre dans la fin de la diapause du parasite.

     

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

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

Length variation in a specific region of the period gene correlates with differences in pupal diapause incidence in the flesh fly, Sarcophaga bullata

We report differences in the length of a specific region of the circadian clock gene period (per) that correlate with different capacities for pupal diapause in the flesh fly, Sarcophaga bullata. The conspicuous difference is located in a region we refer to as the putative C-terminal photoperiodic (CP) region. The length of the CP region correlates inversely with the incidence of diapause. A deletion of 33 amino acids in this region correlates with a significant increase in the incidence of diapause, from 78.1% to 93.0%, and an insertion of 9 amino acids in the same area correlates with a drop in the diapause incidence to 4.0%. This correlation suggests a possible functional role for this region of per in photoperiodism.     

Relationship between photoperiod and secretion of the diapause hormone during larval stages of the silkworm, Bombyx mori L., reared on an artificial diet

The suboesophageal ganglion of the silkworm, Bombyx mori synthesizes sufficient diapause hormone to produce diapause eggs, regardless of the photoperiodic conditions experienced during the larval stages. When larvae destined to produce non-diapause eggs are implanted with the brain-suboesophageal ganglion complex from larvae which have been reared under short-day conditions, the resulting adults lay diapause eggs. The larvae receiving the complex from larvae reared under long-day conditions gave rise to adults which did not produce any diapause eggs. The brains from pupae which have been reared under long-day conditions show an activity inhibiting the secretion of diapause hormone by the suboesophageal ganglion. The mechanism through which the brain controls the secretion of diapause hormone from the suboesophageal ganglion can be modified by photoperiodic conditions during the larval stages.