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Current Opinion in Genetics &... Jun 2024Embryonic diapause in mammals is a period of developmental pause of the embryo at the blastocyst stage. During diapause, the blastocyst has minimal cell proliferation,... (Review)
Review
Embryonic diapause in mammals is a period of developmental pause of the embryo at the blastocyst stage. During diapause, the blastocyst has minimal cell proliferation, metabolic activity and gene expression. At reactivation, blastocyst development resumes, characterised by increases in cell number, biosynthesis and metabolism. Until recently, it has been unknown how diapause is maintained without any loss of blastocyst viability. This review focuses on recent progress in the identification of molecular pathways occurring in the blastocyst that can both cause and maintain the diapause state. A switch to lipid metabolism now appears essential to maintaining the diapause state and is induced by forkhead box protein O1. The forkhead box protein O transcription family is important for diapause in insects, nematodes and fish, but this is the first time a conclusive role has been established in mammals. Multiple epigenetic modifications are also essential to inducing and maintaining the diapause state, including both DNA and RNA methylation mechanisms. Finally, it now appears that diapause embryos, dormant stem cells and chemotherapeutic-resistant cancer cells may all share a universal system of quiescence.
Topics: Animals; Blastocyst; Diapause; Embryonic Development; Epigenesis, Genetic; Gene Expression Regulation, Developmental; Humans; Lipid Metabolism; Forkhead Transcription Factors
PubMed: 38604005
DOI: 10.1016/j.gde.2024.102192 -
Comparative Biochemistry and... Dec 2021Many temperate insects, such as the Colorado potato beetle, enter diapause in winter, during which they arrest their development, suppress their metabolic rate and have...
Many temperate insects, such as the Colorado potato beetle, enter diapause in winter, during which they arrest their development, suppress their metabolic rate and have high stress tolerance. Diapause phenotypes can be transcriptionally regulated, however many studies to date report only whole animal gene expression rather than tissue-specific processes during diapause. We used RNA-seq to measure gene expression in fat body and flight muscle of diapausing and non-diapausing beetles. We used differential expression and GO enrichment analyses to evaluate longstanding hypotheses about the mechanisms that drive arrested development, changes in energy metabolism, and increased stress tolerance during diapause. We found evidence of G2/M cell cycle arrest, juvenile hormone catabolism, increased antioxidant metabolism, epigenetic modification, transposable element regulation, and cytoskeletal remodeling in both the fat body and flight muscle of diapausing beetles. Beetles differentially modulated the fat body and flight muscle transcriptomes during diapause with fat body playing a larger role in the hypoxia response and immunity, whereas flight muscle had higher abundance of transcripts related to the chaperone response and proteostasis. Our transcriptome provides evidence for distinct roles and responses of fat body and flight muscle during diapause in the Colorado potato beetle, and we provide testable hypotheses for biological processes that appear to drive diapause phenotypes in insects.
Topics: Animals; Coleoptera; Diapause; Fat Body; Muscles; Solanum tuberosum; Transcriptome
PubMed: 34509173
DOI: 10.1016/j.cbd.2021.100906 -
Nature Communications Feb 2022In many species including humans, aging reduces female fertility. Intriguingly, some animals preserve fertility longer under specific environmental conditions. For...
In many species including humans, aging reduces female fertility. Intriguingly, some animals preserve fertility longer under specific environmental conditions. For example, at low temperature and short day-length, Drosophila melanogaster enters a state called adult reproductive diapause. As in other stressful conditions, ovarian development arrests at the yolk uptake checkpoint; however, mechanisms underlying fertility preservation and post-diapause recovery are largely unknown. Here, we report that diapause causes more complete arrest than other stresses yet preserves greater recovery potential. During dormancy, germline stem cells (GSCs) incur DNA damage, activate p53 and Chk2, and divide less. Despite reduced niche signaling, germline precursor cells do not differentiate. GSCs adopt an atypical, suspended state connected to their daughters. Post-diapause recovery of niche signaling and resumption of division contribute to restoring GSCs. Mimicking one feature of quiescence, reduced juvenile hormone production, enhanced GSC longevity in non-diapausing flies. Thus, diapause mechanisms provide approaches to GSC longevity enhancement.
Topics: Animals; Cell Differentiation; Cellular Senescence; Checkpoint Kinase 2; DNA Damage; Diapause, Insect; Drosophila Proteins; Drosophila melanogaster; Embryonic Germ Cells; Female; Fertility; Juvenile Hormones; Ovary; Reactive Oxygen Species; Signal Transduction; Stem Cell Niche; Tumor Suppressor Protein p53
PubMed: 35132083
DOI: 10.1038/s41467-022-28347-z -
Environmental Entomology Jun 2023The Western cherry fruit fly, Rhagoletis indifferens (Curran), is a Tephritid fly in the Pacific Northwest and is known to infest native bitter cherry, Prunus emarginata...
The Western cherry fruit fly, Rhagoletis indifferens (Curran), is a Tephritid fly in the Pacific Northwest and is known to infest native bitter cherry, Prunus emarginata (Douglas ex Hooker), which is distributed throughout the Cascade Mountain range. This species occupies temperate to alpine climates and exhibits overwintering adaptations of diapause and supercooling. Isothermal and differential scanning calorimetry were used to determine the effects of diapause chilling duration and post-chilling warm rearing on the metabolic rate and supercooling point of R. indifferens. Previous studies have included the effects of chilling duration on post-diapause development and emergence as well as on the levels of metabolic reserves. Metabolic rate of R. indifferens, was used to calculate the ability of this species to remain in diapause for more than 1 yr as well as predicting the potential effects of climate change on the future abundance and distribution. It was determined that R. indifferens could diapause for more than 1 yr based on the levels of metabolic reserves and metabolic rate.
Topics: Animals; Tephritidae; Diapause, Insect; Drosophila; Northwestern United States; Acclimatization
PubMed: 37119126
DOI: 10.1093/ee/nvad030 -
Journal of Insect Physiology 2020Transgenerational effects act on a wide range of insects' life-history traits and can be involved in the control of developmental plasticity, such as diapause...
Transgenerational effects act on a wide range of insects' life-history traits and can be involved in the control of developmental plasticity, such as diapause expression. Decrease in or total loss of winter diapause expression recently observed in some species could arise from inhibiting maternal effects. In this study, we explored transgenerational effects on diapause expression and traits in one commercial and one Canadian field strain of the aphid parasitoid Aphidius ervi. These strains were reared under short photoperiod (8:16 h LD) and low temperature (14 °C) conditions over two generations. Diapause levels, developmental times, physiological and morphological traits were measured. Diapause levels increased after one generation in the Canadian field but not in the commercial strain. For both strains, the second generation took longer to develop than the first one. Tibia length and wing surface decreased over generations while fat content increased. A crossed-generations experiment focusing on the industrial parasitoid strain showed that offspring from mothers reared at 14 °C took longer to develop, were heavier, taller with wider wings and with more fat reserves than those from mothers reared at 20 °C (8:16 h LD). No effect of the mother rearing conditions was shown on diapause expression. Additionally to direct plasticity of the offspring, results suggest transgenerational plasticity effects on diapause expression, development time, and on the values of life-history traits. We demonstrated that populations showing low diapause levels may recover higher levels through transgenerational plasticity in response to diapause-induction cues, provided that environmental conditions are reaching the induction-thresholds specific to each population. Transgenerational plasticity is thus important to consider when evaluating how insects adapt to changing environments.
Topics: Adaptation, Physiological; Animals; Aphids; Body Size; Climate Change; Cohort Effect; Diapause, Insect; Environment; Fat Body; Hymenoptera; Life History Traits; Temperature
PubMed: 31874137
DOI: 10.1016/j.jinsphys.2019.104001 -
Insect Biochemistry and Molecular... Mar 2022Diapause is one of the major strategies for insects to prepare for and survive harsh seasons. In females, the absence of juvenile hormone (JH) is a hallmark of adult...
Diapause is one of the major strategies for insects to prepare for and survive harsh seasons. In females, the absence of juvenile hormone (JH) is a hallmark of adult reproductive diapause, a developmental arrest, which is much less characterized in males. Here we show that juvenile hormone III skipped bisepoxide (JHSB) titers in hemolymph remarkably differ between reproductive males and females of the linden bug Pyrrhocoris apterus, whereas no JH was detected in diapausing adults of both sexes. Like in females, ectopic application of JH mimic effectively terminated male diapause through the canonical JH receptor components, Methoprene-tolerant and Taiman. In contrast to females, long photoperiod induced reproduction even in males with silenced JH reception or in males with removed corpus allatum (CA), the JH-producing gland. JHSB was detected in the accessory glands (MAG) of reproductive males, unexpectedly, even in males without CA. If there is a source of JHSB outside CA or a long-term storage of JHSB in MAGs remains to be elucidated. These sex-related idiosyncrasies are further manifested in different dynamics of diapause termination in P. apterus by low temperature. We would like to propose that this sexual dimorphism of diapause regulation might be explained by the different reproductive costs for each sex.
Topics: Animals; Corpora Allata; Diapause; Diapause, Insect; Female; Heteroptera; Juvenile Hormones; Male; Methoprene; Reproduction; Sex Characteristics
PubMed: 35007710
DOI: 10.1016/j.ibmb.2022.103721 -
Insect Science Apr 2020Environmental cues, mainly photoperiod and temperature, are known to control female adult reproductive diapause in several insect species. Diapause enhances female...
Environmental cues, mainly photoperiod and temperature, are known to control female adult reproductive diapause in several insect species. Diapause enhances female survival during adverse conditions and postpones progeny production to the favorable season. Male diapause (a reversible inability to inseminate receptive females) has been studied much less than female diapause. However, if the males maximized their chances to fertilize females while minimizing their energy expenditure, they would be expected to be in diapause at the same time as females. We investigated Drosophila montana male mating behavior under short-day conditions that induce diapause in females and found the males to be reproductively inactive. We also found that males reared under long-day conditions (reproducing individuals) court reproducing postdiapause females, but not diapausing ones. The diapausing flies of both sexes had more long-chain and less short-chain hydrocarbons on their cuticle than the reproducing ones, which presumably increase their survival under stressful conditions, but at the same time decrease their attractiveness. Our study shows that the mating behavior of females and males is well coordinated during and after overwintering and it also gives support to the dual role of insect cuticular hydrocarbons in adaptation and mate choice.
Topics: Animals; Diapause, Insect; Drosophila; Female; Hydrocarbons; Male; Oviparity; Reproduction; Sexual Behavior, Animal
PubMed: 30176124
DOI: 10.1111/1744-7917.12639 -
Journal of Insect Physiology 2018Unlike many insects where photoperiod per se induces diapause, reproductive arrest in Drosophila melanogaster adult females is observed at colder temperatures and can be...
Unlike many insects where photoperiod per se induces diapause, reproductive arrest in Drosophila melanogaster adult females is observed at colder temperatures and can be enhanced by shorter photoperiods. Traditional experimental protocols raise flies at 25 °C from the larval stage and then the adults are placed at 12 °C for between 12 and 28 days. After 12 days diapause levels are usually higher than at 28 days, suggesting that the flies are in a cold induced quiescence, rather than a true diapause. By raising flies at more realistic lower temperatures, we observe quite dramatic and counter-intuitive effects on diapause, whose levels nevertheless correlate with various indices of cryoprotectant metabolites as well as resistance to chill shock. We also observe that photoperiodic effects are minimised when very small temperature oscillations associated with the light-dark incubator cycles are neutralised. Our results suggest that the reported photoperiodic component of fly diapause, at least in these strains, is mostly due to thermoperiodic rather than photoperiodic stimuli. In addition, the metabolite and chill shock analyses reveal that even by 12 days, flies are entering a state that is resistant to environmental stresses.
Topics: Acclimatization; Animals; Cold Temperature; Diapause, Insect; Drosophila melanogaster; Female; Glucose; Male; Photoperiod; Trehalose
PubMed: 29339232
DOI: 10.1016/j.jinsphys.2018.01.003 -
Parasites & Vectors Sep 2022Aedes koreicus is an invasive alien mosquito species native to Asia now introduced in several European countries, including northern Italy. In this temperate region,...
Aedes koreicus is an invasive alien mosquito species native to Asia now introduced in several European countries, including northern Italy. In this temperate region, mosquito populations survive cold winter temperatures thanks to diapausing eggs or adults, depending on the species. In its native area, Ae. koreicus was reported to overwinter in the egg stage, but to the best of our knowledge, it is not confirmed whether overwintering eggs are actually diapausing or only in a quiescence stage, i.e., they might hatch as soon as external conditions are favorable. Based on previous laboratory studies, we established a diapausing Ae. koreicus colony, maintained at 21 °C with a photoperiod of 12L:12D. Females were allowed to lay eggs, which were consequently placed in water at different time intervals after oviposition, from 30 days to 5 months. We found that diapausing eggs younger than 3 months have a poor hatching rate, while after about 100 days we observed that almost all eggs hatched. Our findings highlight that water immersion alone did not lead to the hatching of eggs, as age was found to be a significantly important factor. We thus confirm effective diapause, occurring at the egg stage, for Ae. koreicus in a recently invaded area. Moreover, our quantification of diapause duration and hatching success might help in better designing future experiments and improving modeling efforts.
Topics: Aedes; Animals; Diapause; Female; Introduced Species; Oviposition; Water
PubMed: 36068549
DOI: 10.1186/s13071-022-05376-7 -
Parasite (Paris, France) 2021The invasive mosquito Aedes japonicus japonicus (Theobald, 1901) settled in 2013 in the Alsace region, in the northeast of France. In this temperate area, some mosquito...
The invasive mosquito Aedes japonicus japonicus (Theobald, 1901) settled in 2013 in the Alsace region, in the northeast of France. In this temperate area, some mosquito species use diapause to survive cold winter temperatures and thereby foster settlement and dispersal. This study reports diapause and its seasonality in a field population of Ae. japonicus in the northeast of France. For two years, eggs were collected from May to the beginning of November. They were most abundant in summer and became sparse in late October. Diapause eggs were determined by the presence of a fully developed embryo in unhatched eggs after repeated immersions. Our study showed effective diapause of Ae. japonicus in this part of France. At the start of the egg-laying period (week 20), we found up to 10% of eggs under diapause, and this rate reached 100% in October. The 50% cut-off of diapause incidence was determined by the end of summer, leading to an average calculated maternal critical photoperiod of 13 h 23 min. Interestingly, diapause was shown to occur in part of the eggs even at the earliest period of the two seasons, i.e. in May of each year. Even though we observed that the size of eggs was positively correlated with diapause incidence, morphology cannot be used as the unique predictive indicator of diapause status due to overlapping measurements between diapausing and non-diapausing eggs. This study provides new knowledge on diapause characterisation and invasive traits of Ae. japonicus.
Topics: Aedes; Animals; Diapause; France; Oviposition; Seasons
PubMed: 34037519
DOI: 10.1051/parasite/2021045