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In Lepidoptera and Diptera, the fat body dissociates into single cells in nondiapause pupae, but it does not dissociate in diapause pupae until diapause termination. Using the cotton bollworm, Helicoverpa armigera, as a model of pupal diapause insects, we illustrated the catalytic mechanism and physiological importance of fat body cell dissociation in regulating pupal development and diapause. In nondiapause pupae, cathepsin L (CatL) activates matrix metalloproteinases (Mmps) that degrade extracellular matrix proteins and cause fat body cell dissociation. Mmp-induced fat body cell dissociation activates lipid metabolism through transcriptional regulation, and the resulting energetic supplies increase brain metabolic activity (i.e., mitochondria respiration and insulin signaling) and thus promote pupal development. In diapause pupae, low activities of CatL and Mmps prevent fat body cell dissociation and lipid metabolism from occurring, maintaining pupal diapause. Importantly, as demonstrated by chemical inhibitor treatments and CRISPR-mediated gene knockouts, Mmp inhibition delayed pupal development and moderately increased the incidence of pupal diapause, while Mmp stimulation promoted pupal development and moderately averted pupal diapause. This study advances our recent understanding of fat body biology and insect diapause regulation.

Insects often overcome unfavorable seasons in a hormonally regulated state of diapause during which their activity ceases, development is arrested, metabolic rate is suppressed, and tolerance of environmental stress is bolstered. Diapausing insects pass through a stereotypic succession of eco-physiological phases termed “diapause development.” The phasing is varied in the literature, and the whole concept is sometimes criticized as being too artificial. Here we present the results of transcriptional profiling using custom microarrays representing 1,042 genes in the drosophilid fly, Chymomyza costata. Fully grown, third-instar larvae programmed for diapause by a photoperiodic (short-day) signal were assayed as they traversed the diapause developmental program. When analyzing the gradual dynamics in the transcriptomic profile, we could readily distinguish distinct diapause developmental phases associated with induction/initiation, maintenance, cold acclimation, and termination by cold or by photoperiodic signal. Accordingly, each phase is characterized by a specific pattern of gene expression, supporting the physiological relevance of the concept of diapause phasing. Further, we have dissected in greater detail the changes in transcript levels of elements of several signaling pathways considered critical for diapause regulation. The phase of diapause termination is associated with enhanced transcript levels in several positive elements stimulating direct development (the 20-hydroxyecdysone pathway: Ecr, Shd, Broad; the Wnt pathway: basket, c-jun) that are countered by up-regulation in some negative elements (the insulin-signaling pathway: Ilp8, PI3k, Akt; the target of rapamycin pathway: Tsc2 and 4EBP; the Wnt pathway: shaggy). We speculate such up-regulations may represent the early steps linked to termination of diapause programming.

Many insects enter a state of dormancy (diapause) during winter in which they lower their metabolism to save energy. Metabolic suppression is a hallmark of diapause, yet we know little about the mechanisms underpinning metabolic suppression in winter or how it is reversed in the spring. Here, we show that metabolic suppression in dormant Colorado potato beetles results from the breakdown of flight muscle mitochondria via mitophagy. Diapausing Colorado potato beetles suppress their metabolism by 90%, and this lowered metabolic rate coincides with a similar reduction in flight muscle mitochondrial function and density. During early diapause, beetles increase the expression of mitophagy-related transcripts (Parkin and ATG5) in their flight muscle coincident with an increase in mitophagy-related structures in the flight muscle. Knocking down Parkin expression with RNA interference in diapausing beetles prevented some mitochondrial breakdown and partially restored the whole animal metabolic rate, suggesting that metabolic suppression in diapausing beetles is driven by mitophagy. In other animals and in models of disease, such large-scale mitochondrial degradation is irreversible. However, we show that as diapause ends, beetles reverse mitophagy and increase the expression of PGC1α and NRF1 to replenish flight muscle mitochondrial pools. This mitochondrial biogenesis is activated in anticipation of diapause termination and in the absence of external stimuli. Our study provides a mechanistic link between mitochondrial degradation in insect tissues over the winter and whole-animal metabolic suppression.

Background Diapause is a crucial adaptive strategy employed across numerous insect species, endowing them to survive in unfavorable environments. Helicoverpa armigera , one of the most destructive pests globally, undergoes diapause in the pupa stage, which is essential for its survival during the overwintering period and ultimately determines the following year's population density. 20E is a primary hormone that regulates the process of pupae diapause. However, a comprehensive analysis of the mechanisms by which 20E regulates the initiation and termination of diapause in H. armigera remains lacking. Results In the present study, exogenous 20E was initially administered to diapausing pupae, and the results demonstrated that 20E markedly enhanced the development and eclosion rate of diapausing pupae, indicating that 20E treatment effectively terminated the diapause of H. armigera . Subsequently, RNA-Seq was employed to construct a comprehensive transcriptome map of the 20E-induced termination of diapause. The results demonstrated that there were 2836 differentially expressed genes, including 1315 genes that were upregulated and 1521 genes that were downregulated, in the 20E injection group relative to the control group. KEGG and GO enrichment analysis showed that these genes were associated with various metabolic pathways. Moreover, additional analysis revealed that the majority of the pivotal genes associated with metabolism (including glycolysis/gluconeogenesis, glycerolipid, amino sugar and nucleotide sugar metabolism), cell signaling pathways (such as insulin, Wnt, MAPK signaling pathways), the cell cycle, and stress resistance exhibited altered expression following 20E injection. These findings suggest that 20E exerts its primary influence on metabolic processes, cell signaling pathways, cell cycle, and stress resistance during the termination of diapause. Conclusions Our study presents a systematic and comprehensive analysis of the genes associated with 20E-induced diapause termination, thereby providing a foundation for elucidating the molecular mechanism of 20E regulating diapause. Furthermore, the findings lend support to the utilization of ecdysone analogs as pesticides in diapause-based pest management.

Spongy moth ( Lymantria dispar Linnaeus) is a globally recognized quarantine leaf-eating pest. Spongy moths typically enter diapause after completing embryonic development and overwinter in the egg stage. They spend three-quarters of their life cycle (approximately nine months) in the egg stage, which requires a period of low-temperature stimulation to break diapause and continue growth and development. In this study, we explored the molecular mechanism underlying the diapause process in spongy moth. We performed bioinformatics analysis on four Asian populations of spongy moth and one Asian–European hybrid population through a transcriptome analysis combined with proteomics. The results revealed that 1,842 genes were differentially expressed upon diapause initiation, while 264 genes were identified upon diapause termination. Eight diapause-related genes were screened out from the three-level pathways that were significantly enriched by differentially expressed genes at the time of diapause and diapause termination, and the phylogenetic tree and protein three-dimensional structure model were constructed. This study elucidates the diapause mechanism of spongy moth at the gene and protein levels, providing theoretical insights into the early and precise prevention and control of spongy moth. This study can facilitate the development of an efficient, environmentally friendly control system for managing spongy moth populations in the field.

Seasonal and geographical adaptations in terms of obligatory embryonic diapause in the parthenogenetic stick insect, Ramulus mikado, were studied. First and second instar nymphs were collected at locations at three latitudes in Japan and reared in the laboratory under a photoperiod of 16L : 8D or 12L : 12D at 25°C. Their eggs were kept at 30°C for 30 or 60 days after oviposition, but no eggs hatched. Hatching was observed more than 100 days after transfer from 30°C to 15°C. The long period between transfer and hatching indicate that eggs in an early embryonic stage of development enter diapause at high-temperatures. The time from oviposition to hatching of eggs laid by adults that originated from the three locations kept under constant conditions between 15 and 25°C were compared. In all these experiments, eggs laid by individuals originating from high latitudes took longer to hatch. The eggs of those originating from Okayama and Ehime did not hatch at 25°C. However, more than 80% of the eggs of those that originated from the northernmost population hatched. Hatching before winter was observed when the eggs of those that originated from the northern population were placed outdoors in Okayama, even when the maternal insects were reared under long-day conditions in the laboratory. These fi ndings indicate that univoltine R. mikado enters diapause twice during embryonic development, which enables it survive adverse conditions in summer and winter, respectively. Furthermore, diapause intensity was lowest in insects that originated from the lowest latitude.

Pupal diapause in the Chinese oak silkmoth (Antheraea pernyi) is maintained under short-day (SD) photoperiods but is terminated when pupae are exposed to long-day (LD) photoperiods for a specific number of days. This process suggests that pupae can count or retain memory of the number of LD days experienced. In this study, we investigated how long diapause pupae retain photoperiodic information acquired during LD exposure. Diapause pupae were first reared under SD conditions and then exposed to LD for 8 days - an insufficient duration to terminate diapause. Following this, the pupae were placed back under SD for 7, 14, or 21 days, and subsequently returned to LD to induce adult eclosion. Using the final transfer to LD as a reference point, we found that pupae exposed to SD for 7 or 14 days reached adulthood significantly earlier than control pupae that had not previously experienced LD. However, no significant difference in eclosion timing was observed between the 21-day SD group and the control group. These results suggest that photoperiodic information acquired during the 8-day LD exposure gradually decayed under SD conditions and was lost between 14 and 21 days after the transfer from LD to SD. Complete erasure of photoperiodic information under SD appeared to require approximately twice the duration of the initial LD exposure.

The design and implementation of Philaenus spumarius control strategies can take advantage of properly calibrated models describing and predicting the phenology of vector populations in agroecosystems. We developed a temperature-driven physiological-based model based on the system of Kolmogorov partial differential equations to predict the phenological dynamics of P. spumarius . The model considers the initial physiological age distribution of eggs, the diapause termination process, and the development rate functions of post-diapausing eggs and nymphal stages, estimated from data collected in laboratory experiments and field surveys in Italy. The temperature threshold and cumulative degree days for egg diapause termination were estimated as 6.5 °C and 120 DD, respectively. Preimaginal development rate functions exhibited lower thresholds ranging between 2.1 and 5.0 °C, optimal temperatures between 26.6 and 28.3 °C, and upper threshold between 33.0 and 35 °C. The model correctly simulates the emergence of the 3rd, 4th, and 5th nymphal instars, key stages to target monitoring actions and control measures against P. spumarius . Precision in simulating the phenology of the 1st and 2nd nymphal stages was less satisfactory. The model is a useful rational decision tool to support scheduling monitoring and control actions against the late and most important nymphal stages of P. spumarius .

Survival and adaptation to seasonal changes are challenging for insects. Many temperate insects such as the rice stem borer (Chilo suppressalis) overcome the adverse situation by entering diapause, wherein development changes dynamically occur and metabolic activity is suppressed. The photoperiod and temperature act as major environmental stimuli of diapause. However, the physiological and molecular mechanisms that interpret the ecologically relevant environmental cues in ontogenetic development during diapause termination are poorly understood. Here, we used genome-wide high-throughput RNA-sequencing to examine the patterns of gene expression during diapause termination in C. suppressalis. Major shifts in biological processes and pathways including metabolism, environmental information transmission, and endocrine signalling were observed across diapause termination based on over-representation analysis, short time-series expression miner, and gene set enrichment analysis. Many new pathways were identified in diapause termination including circadian rhythm, MAPK signalling, Wnt signalling, and Ras signalling, together with previously reported pathways including ecdysteroid, juvenile hormone, and insulin/insulin-like signalling. Our results show that convergent biological processes and molecular pathways of diapause termination were shared across different insect species and provided a comprehensive roadmap to better understand diapause termination in C. suppressalis.

Diapause is an endocrine controlled arrested metabolic state to delay development or reproduction under unfavorable conditions. To gain an understanding of importance of diapause for ecological adaptation, it is important to study regulation of diapause in insects. We examined genetics of diapause in Chilo partellus by crossing the hibernating (HD), aestivating (AD), post-hibernating (PHD), post-aestivating (PAD), and nondiapause (ND) strains. Reciprocal crosses were also made to gain full understanding of diapause regulation and the maternal effects, if any. Data were recorded on fecundity, egg hatching, larval survival, diapause induction and termination, adult emergence, and morphometrics of larvae, pupae and adults in the parents (P1, P2), F1 hybrids, and the reciprocal crosses. Genetic analysis showed that AD strain is general combiner, which also improved egg hatching, larval survival, diapause termination, adult emergence and proportion of females in the progenies. Incidence of diapause was highest in HD × AD, whereas termination was greatest in PHD × AD. However, ND strain and its reciprocal crosses with other strains did not exhibit any noticeable developmental response associated with diapause. Specific combining ability analysis suggested that where PHD and AD strains exist together there will be likely reduction in diapause incidence, increased survival with greater fitness and faster multiplication of their progenies resulting in outbreak of C. partellus. Degree of dominance estimates revealed that diapause, developmental and morphometric traits in C. partellus are governed by over dominance gene effects, and mainly depend on parental diapause history.