Termination Of Larval Diapause Research Articles

Divergence in cell cycle progression is associated with shifted phenology in a multivoltine moth: the European corn borer, Ostrinia nubilalis.

Evolutionary change in diapause timing can be an adaptive response to changing seasonality, and even result in ecological speciation. However, the molecular and cellular mechanisms regulating shifts in diapause timing remain poorly understood. One of the hallmarks of diapause is a massive slowdown in the cell cycle of target organs such as the brain and primordial imaginal structures, and resumption of cell cycle proliferation is an indication of diapause termination and resumption of development. Characterizing cell cycle parameters between lineages differing in diapause life history timing may help identify molecular mechanisms associated with alterations of diapause timing. We tested the extent to which progression of the cell cycle differs across diapause between two genetically distinct European corn borer strains that differ in their seasonal diapause timing. We show the cell cycle slows down during larval diapause with a significant decrease in the proportion of cells in S phase. Brain-subesophageal complex cells slow primarily in G0/G1 phase whereas most wing disc cells are in G2 phase. Diapausing larvae of the earlier emerging, bivoltine E-strain (BE) suppressed cell cycle progression less than the later emerging, univoltine Z-strain (UZ) individuals, with a greater proportion of cells in S phase across both tissues during diapause. Additionally, resumption of cell cycle proliferation occurred earlier in the BE strain than in the UZ strain after exposure to diapause-terminating conditions. We propose that regulation of cell cycle progression rates ultimately drives differences in larval diapause termination, and adult emergence timing, between early- and late-emerging European corn borer strains.

Modelling diapause termination and phenology of the Japanese beetle, Popillia japonica

We developed a mechanistic, stage-structured model simulating the phenology of Popillia japonica. The model simulates the influence of soil temperature on the larval diapause termination and on the development rate function of post-overwintering larvae and pupae. Model parameters are estimated based on literature evidence for pupae development and on a parameterisation process that allows estimating parameters for larval diapause termination and for the development rate function (and the related uncertainty) of post-overwintering larvae. Data used for model parameterisation and validation refer to time-series adult trap catches collected during the P. japonica monitoring programme performed by the Phytosanitary Service of Lombardy Region within the infested area in Lombardy (Italy) from 2015 to 2019. A total of 12 randomly selected locations are used to estimate biologically realistic model parameters (parameterisation dataset). We applied a Jackknife nonparametric resampling procedure on the parameterisation dataset to quantify uncertainty associated with parameters’ estimates. Parameterised model is then validated on time-series adult trap catches data referring to a different set of 12 randomly selected locations (validation dataset) surveyed in Lombardy. The model successfully predicted the beginning of adult emergence and the overall curve of adult emergence in the validation dataset. The model presented can support the definition of the best timing for the implementation of monitoring and control activities for the local and the area-wide management of P. japonica.

Assessing phenological synchrony between the Chinese sawfly, Cephus fumipennis (Hymenoptera: Cephidae), its egg-larval parasitoid, Collyria catoptron (Hymenoptera: Ichneumonidae), and the North American sawfly, Cephus cinctus: implications for biological control

AbstractMany pest and beneficial insects overwinter as larvae in a state of diapause, with development resuming in the spring. In these cases, rates of post-diapause development of parasitoids must be synchronised with the vulnerable life stages of their hosts. Phenological asynchrony between introduced parasitoids and their targeted hosts has limited the success of some biological control efforts. Here, we assess the potential synchrony between Collyria catoptron Wahl (Hymenoptera: Ichneumonidae), a parasitoid of the Chinese wheat stem sawfly, Cephus fumipennis Eversmann (Hymenoptera: Cephidae), which is being considered as a biological control against a novel host species, Cephus cinctus Norton, in North America. We compared development timing and emergence patterns of both native and exotic species of sawflies with that of the parasitoid. We found that the mean number of days between termination of larval diapause and adult eclosion varied by less than one day across species, and patterns of emergence were also similar. The rate of development of this egg-larval parasitoid was within the range necessary to attack C. cinctus eggs. Furthermore, the development of C. cinctus from western Montana, United States of America most closely matched that of the parasitoid, suggesting western Montana as a possible release area.

Possible roles of Juvenile Hormone and Juvenile Hormone binding protein on changes in the integument during termination of larval diapause in the bamboo borer Omphisa fuscidentalis

AbstractTo understand the role of Juvenile Hormone (JH) on changes in the integument of Omphisa fuscidentalis Hampson (Lepidoptera: Pyralidae) during larval–pupal development, the expression patterns of transcripts of the O. fuscidentalis JH binding protein gene (OfJHBP) are determined in the integument of diapausing larvae. Quantitative real‐time polymerase chain reaction (qRT‐PCR) studies show that the relative levels OfJHBP mRNA in the integument do not differ significantly in different segments of the body. Application of the JH analogue (JHA) methoprene to diapausing larvae results in a relatively low expression of OfJHBP mRNA from days 0 to 8 after JHA application and reaches maximal levels in the pupal stage. Changes in OfJHBP expression after 20‐hydroxyecdysone (20E) injection also show low levels of OfJHBP mRNA from days 0 to 8 and show a peak of expression in the pupal stage. Incubation of the integument in vitro in the presence of JHA (3.22 µm) induces high levels of OfJHBP expression within 120 min, whereas incubation with 20E (2.08 µm) induces gene expression at 150 min. To study the cooperative effect on OfJHBP expression of these two hormones, dose–response experiments are performed. Larval integument is maintained in the presence of 0.32 µm JHA or 2.08 µm 20E or a combination of both hormones in vitro for 120 min. Induction of OfJHBP expression by JHA and 20E in combination is significantly higher than that of either hormone alone. The results impact not only on our understanding of how methoprene (and hence JH) terminates larval diapause through an increase in ecdysteroid titre in the haemolymph, but also on how JH acts directly on the integument to stimulate the expression of a JH binding protein gene.

Microarrays Reveal Early Transcriptional Events during the Termination of Larval Diapause in Natural Populations of the Mosquito, Wyeomyia smithii

BackgroundThe mosquito Wyeomyia smithii overwinters in a larval diapause that is initiated, maintained and terminated by day length (photoperiod). We use a forward genetic approach to investigate transcriptional events involved in the termination of diapause following exposure to long-days.Methods/Principal FindingsWe incorporate a novel approach that compares two populations that differentially respond to a single day length. We identify 30 transcripts associated with differential response to day length. Most genes with a previously annotated function are consistent with their playing a role in the termination of diapause, in downstream developmental events, or in the transition from potentially oxygen-poor to oxygen-rich environments. One gene emerges from three separate forward genetic screens as a leading candidate for a gene contributing to the photoperiodic timing mechanism itself (photoperiodic switch). We name this gene photoperiodic response gene 1 (ppdrg1). WsPpdrg1 is up-regulated under long-day response conditions, is located under a QTL for critical photoperiod and is associated with critical photoperiod after 25 generations of recombination from a cross between extreme phenotypes.ConclusionsThree independent forward genetic approaches identify WsPpdrg1 as a gene either involved in the photoperiodic switch mechanism or very tightly linked to a gene that is. We conclude that continued forward genetic approaches will be central to understanding not only the molecular basis of photoperiodism and diapause, but also the evolutionary potential of temperate and polar animal populations when confronted with rapid climate change.

Correlation of oxygen consumption, cytochrome c oxidase, and cytochrome c oxidase subunit I gene expression in the termination of larval diapause in the bamboo borer, Omphisa fuscidentalis

The moth Omphisa fuscidentalis (Lepidoptera, Pyralidae) is a univoltine insect with a larval diapause period lasting up to 9 months. We studied changes in O 2 consumption in conjunction with cytochrome c oxidase activity and cytochrome c oxidase subunit I ( cox1) gene expression. O 2 consumption changed within a day, showing a supradian rhythm with a ca.12-h cycle at 25 °C. During the first two-thirds of the diapause period, from October to March, O 2 consumption was constant until January and then increased by March. Topical application of methoprene, a juvenile hormone analog (JHA), to diapausing larvae terminated the diapause and was associated with an increase in O 2 consumption rate at diapause termination. In JHA-treated larvae, cytochrome c oxidase activity in fat bodies was high at the beginning of the prepupal period and highest at pupation. cox1 expression in fat bodies displayed a transient peak 8 days after JHA application and peaked in the prepupal period. Taken together, our results show that the break of diapause by JHA is associated with the activation of cox1, bringing about an increase in cytochrome c oxidase activity, followed by an increase in O 2 consumption rate.

Sensitivities to juvenile hormone and ecdysteroid in the diapause larvae of Omphisa fuscidentalis based on the hemolymph trehalose dynamics index

The final instar larva of the bamboo borer, Omphisa fuscidentalis, is in diapause for 9 months from September to the following June. Trehalose and ecdysteroid concentrations in hemolymph were measured through the larval diapause period and in the pupal stage. The ecdysteroid concentration remained low until November, followed by a gradual increase to about 30 ng/ml in May. The trehalose concentration remained at levels ranging between 40–50 mM until May, and decreased to an almost undetectable level after pupation. Since a juvenile hormone analogue (JHA), methoprene, is capable of terminating diapause by stimulating larval prothoracic glands, we examined its effects on ecdysteroid and trehalose concentrations in larvae in December and February. The hemolymph ecdysteroid increased more quickly in February than in December, indicating that the sensitivity of the prothoracic glands to JHA increased towards the end of diapause termination. Similarly, hemolymph trehalose in February decreased within a few days after JHA application, while in December the decrease occurred in the third week. Exogenous 20-hydroxyecdysone (20E) caused a decrease in trehalose concentration in a dose-dependent manner. The effective dose of 20E, however, did not change from January until April, implying that the sensitivity of tissue(s) to 20E may not change until the end of diapause. Taken together, our results suggest that the sensitivities of tissues to JH and 20E do not increase simultaneously with the progress of diapause development and that termination of larval diapause is not associated simply with the restoration of hormone deficiencies.

Diapause Termination in Sesamia nonagrioides (Lepidoptera: Noctuidae) Under Laboratory and Field Conditions

The influence of photoperiod and temperature on the termination of diapause of Sesamia nonagrioides (Levebvre) was evaluated under laboratory and field conditions. Long-day photoperiod enhanced termination of diapause. Larvae held under a short-day photoperiod (10:14 [L:D] h) for various times and then transferred to a long-day photoperiod (16:8 [L:D] h) proceeded to pupate in a14 d, indicating that regardless of the state of diapause intensity, diapause completion and postdiapause development lasted similar lengths of time. Larval diapause termination was not hastened when diapausing larvae kept at a photoperiod of 10:14 (L:D) h and 25°C were exposed for short periods at 30, 35, and 40°C, whereas it was shortened when diapausing larvae were transferred from 25 to 30°C and kept continuously at this temperature. At higher temperatures (35 and 40°C), all transferred larvae died. It was also shown that exposure of diapausing larvae to low temperature (5°C) simply accelerated diapause development but termination of diapause did not require a period of chilling. Moreover, after low temperature treatment, diapausing larvae showed a faster diapause development when transferred to a long-day photoperiod than those kept in a short-day photoperiod. In the latter case, the longer the exposure the faster the termination occurred. Diapause termination of field-collected larvae was practically spontaneous. After transfer to laboratory conditions, 25°C and a photoperiod of 16:8 (L:D) h, they quickly proceeded to pupate. Field-diapausing larvae terminated diapause in January but exhibited a postdiapause development; the 1st record of pupation was observed in the field at the end of March.

Diapause in Platynota idaeusalis (Lepidoptera: Tortricidae): Effects of Temperature, Photoperiod, and Time of Inoculation in the Field on Diapause Termination

Termination of larval diapause in the tufted apple budmoth, Platynota idaeusalis (Walker), is a dynamic process in which insect development is influenced by both the nature and the timing of the various stimuli to which it is exposed. Parameters investigated in this study with respect to diapause termination included time of inoculation (egg hatch) in the field, temperature, and photoperiod. Each factor was shown to affect significantly diapause development in diapausing larvae. However, the magnitude of the effect of each consistently diminished as the season progressed. Comparisons of laboratory and field strains of P. idaeusalis, reared under similar conditions, showed no significant differences in their respective diapause responses to each of the factors investigated. Larvae inoculated out of doors earlier in autumn exhibited a less intense diapause than those inoculated later. Diapause termination was accelerated when larvae were exposed to higher constant temperatures and longer stationary daylengths, or both. Because natural temperatures rarely rise above 27°C (the optimum temperature tested for diapause termination) between November and March in North Carolina, larval diapause in P. idaeusalis is most likely terminated by increasing daylengths in the spring, with temperature acting as a modifying influence in the overall rate of diapause development.

Studies on some effects of relative humidity, food and light in termination of larval diapause in Busseola fusca (Lepidoptera: Noctuidae)

Time required in the laboratory for field collected Busseola fusca Fuller larvae to complete diapause development and to pupate decreased as the dry season progressed. Low relative humidity, darkness and the absence of food retarded diapause development as compared to (he opposing factors. However, the completion of diapause development and pupation did not occur solely because a particular threshold of any of the factors was exceeded, but rather, because of the cumulative effects of time and anyone of, or all the factors tested.

Factors Influencing Adult Emergence from Diapausing Sorghum Midge, Contarinia sorghicola (Diptera: Cecidomyiidae)1

Sorghum midge, Contarinia sorghicola (Coquillett) diapause was terminated in the laboratory, and factors affecting adult emergence from diapausing larvae were investigated. Temperatures in the range from 20 to 30°C were optimum for diapause termination and adult emergence. Diapausing larvae exposed to moist conditions at 30°C began to emerge as adults after 12 days of incubation. Based on adult emergence rates per day, an emergence threshold temperature was estimated to be 14.8°C. Exposure to 12 to 13 days of continuous moisture at 30°C was essential for diapause termination and adult emergence. Moisture acted to initiate diapause termination, but diapausing larvae were unable to accumulate shorter periods of moisture toward the 12- to 13-day requirement. Photoperiod had no significant effect on the termination of larval diapause.

Corpora Cardiaca-Allata Complex of the Larvae of the Pink Bollworm, Pectinophora gossypiella. An Ultrastructural Study in Relation to Diapause

Raina, A. K., Borg, T. K. 1980. Corpora cardiaca-allata complex of the larvae of the pink bollworm, Pectinophora gossypiella. An ultrastructural study in relation to diapause. (Department of Entomology, North Dakota State University of South Carolina, School of Medicine, Columbia, U.S.A.) — Acta zool. (Stockh.) 61(2): 65–77. The corpora cardiaca (CC) and corpora allata (CA) of the pink bollworm, Pectinophora gossypiella, were studied at the ultrastructural level during induction maintenance, and termination of larval diapause. The CC is composed of 5–6 intrinsic secretory (IS) cells, glial cells, and axons that carry electron dense (ED) and electron lucent (EL) granules from the brain. The IS cells produce ED granules with an average diameter of 110 ± 26 nm. During diapause, the axons with ED granules showed large accumulations of neurosecretory granules, but the axons with the EL granules contained lesser amounts. The CA is made up of approximately 25 large cells and axons that pass through the CC from the brain. Most of the axons take up a peripheral position. A characteristic feature of CA cells during diapause was the presence of stacks of convoluted tubules of the smooth endoplasmic reticulum (SER) that may be associated with juvenile hormone synthesis. The IS cells of the CC appeared to be inactive during diapause.

The role of juvenile hormone in the larval diapause of the European corn borer, Ostrinia nubilalis

The possible role of juvenile hormone (JH) in the induction and termination of larval diapause in the European corn borer, Ostrinia nubilalis, was investigated using topical applications of both JH I and a JH mimic as well as by monitoring JH titers with the Galleria bioassay. Neither JH nor the JH mimic ZR515 was capable of influencing diapause termination when administered topically. The Galleria bioassay revealed little or no JH in the hemolymph of mid diapause (>30 days) insects, indicating no demonstrable role for JH in diapause maintenance. When ZR515 was administered to nondiapause, newly ecdysed fifth instar larvae the pupal molting cycle was delayed. By use of photoperiodic regimes we were able to show that the molting delay was not equivalent to diapause induction. The Galleria bioassay showed differences in JH titer profiles between diapause and nondiapause animals during the final larval stadium. The nondiapause insects showed titers that decline rapidly to trace amounts following the molt to fifth instar then rose prior to pupation. The diapause insects had generally higher titers and exhibited a more gradual decline after the molt. No evidence was obtained to support the hypothesis that JH plays a key role in the induction, maintenance, or termination of larval diapause.

Termination of Larval Diapause in the European Elm Bark Beetle1,2

Overwintering larvae of Scolytus multistriatus that had been subjected to artificial and natural cold treatments emerged sooner and more synchronously than did larvae not exposed to subfreezing temperatures. Photoperiod and length of incubation appeared not to influence termination of diapause. Although subfreezing temperatures appeared necessary to bring about a change in diapause state, temperatures as low as −23.5°C resulted in significant mortality. The diam of the host material did not affect emergence pattern but did govern the prevalence of species of hymenopterous parasites and the density of brood adults.

Insect photoperiodism: the "T experiment" as evidence for an hourglass mechanism.

"T experiments" demonstrate that the clock controlling termination of larval diapause in Ostrinia nubilalis is an hourglass mechanism that measures 8 hours of darkness. Circadian oscillations are not involved in photoperiodic time measurement in this species.

Photoperiodic control of the maintenance and termination of larval diapause in Wyeomyia smithii (Coq.) (Diptera: Culicidae) with notes on oogenesis in the adult female.

Some aspects of overwintering and oogenesis in the pitcher-plant mosquito, Wyeomyia smithii (Coq.), were examined. The species was shown to overwinter in a diapause state as a third-instar larva. The diapausing larvae overwinter within the frozen ice cores of the host plant but they were nevertheless shown to be intolerant of prolonged periods of freezing at temperatures only a few degrees below 0 °C. The winter survival of the species probably depends almost entirely on the insulating benefits of a snow cover. Larval diapause was stable under short-day conditions but was very rapidly broken when the larvae were exposed to long-day photoperiods. The critical photoperiod required to break larval diapause in a population from the Kenora region of Ontario was between [Formula: see text] and 15 h of light per diem. This critical photoperiod did not change during a prolonged period of overwintering. Larvae which experienced 5 or fewer long-day cycles remained in diapause when they were returned to short-day conditions but diapause was irreversibly broken in larvae exposed to 8 or more long-day cycles in succession. Data on growth rates of larvae as a function of temperature and photoperiod were used to predict the seasonal cycle of W. smithii in northwestern Ontario where the species is probably restricted to a maximum of two generations per year. All females of W. smithii were autogenous for the first ovarian cycle and adult diets of carbohydrate did not affect fecundity. Unlike other mosquitoes, the female of W. smithii was found to be precocious, emerging with the ovarian follicles already initiated with development of the follicles up to stage IIIa of Christophers.

Interaction of food and photoperiod in the termination of larval diapause in Chaoborus americanus (Diptera: Culicidae).

The role of food in the termination of diapause is probably without significance in the many diapausing insects which are inactive and which seldom, if ever, feed. There are, however, certain nematocerous Diptera which overwinter as larvae and are capable of both movement and feeding. Indeed, studies concerning the photo periodic induction of development in diapausing larvae of the chironomids Metrioc nemus (Paris and Jenner, 1959) and Chironomus (Engelmann and Shappirio, 1965) or of the culicids Anopheles barberi (Baker, 1935), Anopheles bifurcatus (Vinogradova, 1964), Anopheles plumbeus (Vinogradova, 1962), Aedes triseriatus (Love and Whelchel, 1955), and Tozorhinchites rutilus (McCrary and Jenner, 1965) involved the effects of photoperiod on fed animals only. Studies concerning the overwintering larvae of the culicid Chaoborus americanus (Bradshaw, 1969) considered the effects of photoperiod on both fed and starved animals. The assess ment of the contribution of food is difficult, if not impossible, in filter feeders or detritus eaters like the chironomids or the culicine and anopheline mosquitoes. Chaoborine and toxorhinchitine mosquitoes, on the other hand, are carnivores. In Chaoborus, food and photoperioci have been shown to interact synergistically to effect the termination of larval diapause (Bradshaw, 1969). Furthermore, develop ment in Chaoborus is proportional to the number of long days with food. Chao borus, therefore, is conveniently adapted for the study of the food component in the termination of diapause.

MAJOR ENVIRONMENTAL FACTORS INDUCING THE TERMINATION OF LARVAL DIAPAUSE INCHAOBORUS AMERICANUSJOHANNSEN (DIPTERA: CULICIDAE)

1. The termination of larval diapause in C. americanus is cued by simultaneous long day and food.2. One long day cycle with food elicits development in a significant proportion of the population.3. A shift in the major developmental stimulus from long day during the winter to food after prolonged chilling in the laboratory was observed and is hypothesized to be an adaptation to life in shallow ponds in temperate climatic regions.4. The action of food may occur via the ventral abdominal nervous system as described by Fuller (1960) with ultimate neuro-endocrine control of development residing in the brain.

Photoperiodic control of the maintenance and termination of larval diapause in Chironomus tentans.

DURING recent years, dipterous larvae possessing giant polytene chromosomes have provided important new insight into developmental physiology at the sub-cellular level. This is in large measure attributable to the phenomenon of chromosomal ‘puffing’, which has afforded the opportunity for visualizing the changing pattern of genetic activity within individual tissues during the course of development1. Clever2 has reported significant alterations in the puffing pattern of salivary gland chromosomes from a laboratory population of Chironomus tentans which experienced a state of spontaneously arrested development under conditions seemingly favourable for continued growth and metamorphosis. Although not previously described for this organism, the developmental arrest resembles the diapause which typifies the life-histories of many insect species. Diapause is commonly induced or terminated by extrinsic environmental factors, particularly temperature and photoperiod, which exert their effect by influencing the activity of the endocrine system which regulates insect growth and metamorphosis3. In view of the paucity of information on these matters in the case of C. tentans, coupled with the general utility of dispausing insects and the special cytological attractions of this species for investigations of biochemical mechanisms underlying growth and differentiation, we have examined the natural occurrence of a larval diapause and its photoperiodic control under laboratory conditions.

A method of destroying Tsetse-flies

Studies were conducted in northern Ghana in 1997 and 1998 on the effects of contact moisture and photoperiod on the termination of larval diapause in the stem borer, Coniesta ignefusalis (Hampson). Results obtained over the two years consistently showed that on its own, photoperiod had no significant effect on diapause termination. In combination with contact moisture, however, a long day photoperiod of 13L:11D accelerated diapause termination and increased the cumulative percentage pupation. Contact with moisture was crucial for diapause termination but its influence was more pronounced in larvae collected from the field after March. Generally, access to moisture earlier than April resulted in very high larval mortality. These observations, together with the fact that some of the larvae (12%) denied access to water throughout the experimental period subsequently pupated, suggest that moisture may not be the sole factor triggering diapause termination in C. ignefusalis. The implications of these findings are discussed.