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Proceedings of the National Academy of... Jul 2024To survive adverse environments, many animals enter a dormant state such as hibernation, dauer, or diapause. Various species undergo adult reproductive diapause in...
To survive adverse environments, many animals enter a dormant state such as hibernation, dauer, or diapause. Various species undergo adult reproductive diapause in response to cool temperatures and/or short day-length. While flies are less active during diapause, it is unclear how adverse environmental conditions affect circadian rhythms and sleep. Here we show that in diapause-inducing cool temperatures, exhibit altered circadian activity profiles, including severely reduced morning activity and an advanced evening activity peak. Consequently, the flies have a single activity peak at a time similar to when nondiapausing flies take a siesta. Temperatures ≤15 °C, rather than photoperiod, primarily drive this behavior. At cool temperatures, flies rapidly enter a deep-sleep state that lacks the sleep cycles of flies at higher temperatures and require high levels of stimulation for arousal. Furthermore, we show that at 25 °C, flies prefer to siesta in the shade, a preference that is virtually eliminated at 10 °C. Resting in the shade is driven by an aversion to blue light that is sensed by Rhodopsin 7 outside of the eyes. Flies at 10 °C show neuronal markers of elevated sleep pressure, including increased expression of Bruchpilot and elevated Ca in the R5 ellipsoid body neurons. Therefore, sleep pressure might overcome blue light aversion. Thus, at the same temperatures that cause reproductive arrest, preserve germline stem cells, and extend lifespan, are prone to deep sleep and exhibit dramatically altered, yet rhythmic, daily activity patterns.
Topics: Animals; Drosophila melanogaster; Sleep; Circadian Rhythm; Rhodopsin; Drosophila Proteins; Photoperiod; Temperature; Light; Diapause, Insect
PubMed: 38917005
DOI: 10.1073/pnas.2400964121 -
Journal of Comparative Physiology. A,... Jun 2024Drosophila ezoana is a virilis group Drosophila species inhabiting northern latitudes. The flies enter adult reproductive diapause to survive winter upon exposure to...
Drosophila ezoana is a virilis group Drosophila species inhabiting northern latitudes. The flies enter adult reproductive diapause to survive winter upon exposure to short photoperiod conditions (short-day) over several consecutive days. Insect pre-diapause phase - the duration between the beginning of exposure to short days and expression of diapause is thought to be comprised of two distinct phases - (a) photoperiodic time measurement that detects short-days, followed by (b) physiological events leading to the expression of diapause phenotype. A short-day dependent segment of the pre-diapause phase thus approximates the process of photoperiodic time measurement. Continuous darkness has been found to be a neutral condition with respect to diapause regulation in many insect species. The effect of variable number of short-days followed by continuous darkness on diapause incidence thus allows identification of short-day dependent segment of pre-diapause phase thereby mapping the process of photo-periodic time measurement. Although, few weeks of exposure to short-days in adult stage is known to be sufficient for the expression of diapause in D. ezoana, the number of short days required for the completion of photo-periodic time measurement has never been systematically analysed. Our experiments show that continuous darkness is a neutral condition for diapause regulation also in D. ezoana. We utilized the neutral nature of continuous darkness to map the process of photoperiodic time measurement in the D. ezoana strain 124OJ8 which showed that integration of short-day photic cues over the first 10 days of pre-diapause phase is essential for diapause induction.
PubMed: 38916659
DOI: 10.1007/s00359-024-01707-4 -
Frontiers in Insect Science 2024Females of the Northern house mosquito, , enter an overwintering dormancy, or diapause, in response to short day lengths and low environmental temperatures that is...
INTRODUCTION
Females of the Northern house mosquito, , enter an overwintering dormancy, or diapause, in response to short day lengths and low environmental temperatures that is characterized by small egg follicles and high starvation resistance. During diapause, Major Royal Jelly Protein 1 ortholog (CpMRJP1) is upregulated in females of . This protein is highly abundant in royal jelly, a substance produced by honey bees (), that is fed to future queens throughout larval development and induces the queen phenotype (e.g., high reproductive activity and longer lifespan). However, the role of CpMRJP1 in is unknown.
METHODS
We first conducted a phylogenetic analysis to determine how the sequence of CpMRJP1 compares with other species. We then investigated how supplementing the diets of both diapausing and nondiapausing females of with royal jelly affects egg follicle length, fat content, protein content, starvation resistance, and metabolic profile.
RESULTS
We found that feeding royal jelly to females reared in long-day, diapause-averting conditions significantly reduced the egg follicle lengths and switched their metabolic profiles to be similar to diapausing females. In contrast, feeding royal jelly to females reared in short-day, diapause-inducing conditions significantly reduced lifespan and switched their metabolic profile to be similar nondiapausing mosquitoes. Moreover, RNAi directed against significantly increased egg follicle length of short-day reared females, suggesting that these females averted diapause.
DISCUSSION
Taken together, our data show that consuming royal jelly reverses several key seasonal phenotypes of and that these responses are likely mediated in part by CpMRJP1.
PubMed: 38911605
DOI: 10.3389/finsc.2024.1358619 -
Trends in Cell Biology Jun 2024Embryonic and adult stem cells enable development and regeneration. Embryonic cells, like adult stem cells, can enter dormancy as part of their lifecycle. Recent...
Embryonic and adult stem cells enable development and regeneration. Embryonic cells, like adult stem cells, can enter dormancy as part of their lifecycle. Recent evidence suggests that this cellular transition to dormancy requires active rewiring of metabolism. The dormancy-induced metabolic switches in embryonic and adult stem cells are explored here.
PubMed: 38897887
DOI: 10.1016/j.tcb.2024.05.006 -
IScience Jun 2024Many insect pests are long-distance migrants, moving from lower latitudes where they overwinter to higher latitudes in spring to exploit superabundant, but seasonally... (Review)
Review
Many insect pests are long-distance migrants, moving from lower latitudes where they overwinter to higher latitudes in spring to exploit superabundant, but seasonally ephemeral, host crops. These seasonal long-distance migration events are relatively easy to recognize, and justifiably garner much research attention. Evidence indicates several pest species that overwinter in diapause, and thus inhabit a year-round range, also engage in migratory flight, which is somewhat "invisible" because displacement is nondirectional and terminates among conspecifics. Support for aseasonal, undirected migration is related to recognizing true migratory flight behavior, which differs fundamentally from most other kinds of flight in that it is nonappetitive. Migrating adults are not searching for resources and migratory flight is not arrested by encounters with potential resources. The population-level consequence of aseasonal, undirected migration is spatial mixing of individuals within the larger metapopulation, which has important implications for population dynamics, gene flow, pest management, and insect resistance management.
PubMed: 38883831
DOI: 10.1016/j.isci.2024.110040 -
Ecological and Evolutionary Physiology 2024AbstractThe common eastern bumble bee () queens endure cold winter months by entering a diapause state. During this overwintering period, these animals use stored energy...
AbstractThe common eastern bumble bee () queens endure cold winter months by entering a diapause state. During this overwintering period, these animals use stored energy reserves while maintaining a low metabolic rate. This study investigates changes in the metabolic rate of bumble bee queens during diapause-like laboratory conditions and the potential reorganization of the flight muscle metabolic properties during this period. We first confirmed the hypometabolic state of queens during diapause in the laboratory, which lowered their resting metabolic rate to less than 5% of normal resting values. Body mass decreased during diapause, body composition changed where carbohydrates decreased initially, and later protein declined, with a similar trend for lipid content. Using cellular respirometry, we determined the capacity of the flight muscle cells of bumble bee queens to use various metabolic fuels and whether this capacity changes during the progression of diapause to favor stored lipid-derived substrates. Queens showed a low capacity to oxidize the amino acid proline, compared with workers, and their capacity to oxidize all metabolic substrates did not change during a 4-mo diapause period in the laboratory. We also show no detectable ability to oxidize fatty acid by flight muscle mitochondria in this species. The metabolic properties of flight muscle tissue were further characterized using metabolic enzyme activity profiles showing little change during diapause, indicating that profound metabolic suppression is induced without major changes in muscle metabolic phenotypes. Overall, queens undergo diapause while maintaining flight muscle capacity under the conditions used.
Topics: Animals; Bees; Female; Flight, Animal; Diapause, Insect; Muscles; Energy Metabolism; Basal Metabolism; Body Composition
PubMed: 38875138
DOI: 10.1086/730587 -
Journal of Molecular Histology Jun 2024Diapause is an endocrine-mediated metabolic and growth arrest state in response to unfavorable external environments. The nematode Caenorhabditis elegans can enter...
Diapause is an endocrine-mediated metabolic and growth arrest state in response to unfavorable external environments. The nematode Caenorhabditis elegans can enter diapause/arrest during embryonic, larval, or adult stages when subjected to detrimental external environments. Larval stage 1 (L1) arrest happens when animals hatch without food. Previous work has shown that the insulin pathway plays a prominent role in regulating L1 arrest. However, the downstream signal molecular mechanisms and biomarkers are still missing. In this study, we showed that SaPosin-like Protein family member SPP-5 is significantly upregulated during L1 arrest, suggesting that it could act as an L1 arrest biomarker. Using RNA interference we demonstrated that spp-5 knockdown accelerated larval development, while the overexpression resulted in L1 arrest. Consistently, SPP-5 level was significantly up-regulated in the L1 arrest daf-2(e1370) mutants, and spp-5(RNAi) suppressed the daf-2(e1370) induced L1 arrest. These results suggest that SPP-5 can serve as an L1 arrest biomarker and promote the arrest probably via the insulin signaling pathway.
PubMed: 38869752
DOI: 10.1007/s10735-024-10205-5 -
Genome Research Jun 2024Diapause represents a crucial adaptive strategy used by insects to cope with changing environmental conditions. In North China, the Asian corn borer () enters a winter...
Diapause represents a crucial adaptive strategy used by insects to cope with changing environmental conditions. In North China, the Asian corn borer () enters a winter larval diapause stage. Although there is growing evidence implicating epigenetic mechanisms in diapause regulation, it remains unclear whether dynamic genome-wide profiles of epigenetic modifications exist during this process. By investigating multiple histone modifications, we have discovered the essential roles of H3K9me3 and H3K27me3 during diapause of the Asian corn borer. Building upon previous findings in vertebrates highlighting the connection between DNA methylation and repressive histone methylations, we have examined changes in the genome-wide profile of H3K9me3, H3K27me3, and DNA methylation at the nondiapause, prediapause, and diapause stages. Data analysis reveals significant alterations in these three modifications during diapause. Moreover, we observe a correlation between the H3K9me3 and H3K27me3 modification sites during diapause, whereas DNA modifications show little association with either H3K9me3 or H3K27me3. Integrative analysis of epigenome and expression data unveils the relationship between these epigenetic modifications and gene expression levels at corresponding diapause stages. Furthermore, by studying the function of histone modifications on genes known to be important in diapause, especially those involved in the juvenile pathway, we discover that the juvenile hormone pathway lies downstream from H3K9me3 and H3K27me3 histone modifications. Finally, the analysis of gene loci with modified modifications unreported in diapause uncovers novel pathways potentially crucial in diapause regulation. This study provides a valuable resource for future investigations aiming to elucidate the underlying mechanisms of diapause.
Topics: Animals; DNA Methylation; Histones; Moths; Epigenesis, Genetic; Larva; Diapause, Insect; Genome, Insect; Diapause; Histone Code; Insect Proteins
PubMed: 38866549
DOI: 10.1101/gr.278661.123 -
Ecology and Evolution Jun 2024Organisms inhabiting mountainous regions can experience large vertical environmental changes, and show different ecological characteristics between altitudes, thus...
Organisms inhabiting mountainous regions can experience large vertical environmental changes, and show different ecological characteristics between altitudes, thus facilitating allopatric fragmentation even in geographically close populations. This study compared the life-history patterns of a species of limnephilid caddisfly, , in several genetically differentiated populations between alpine and sub-alpine zones in a temperate mountainous region. We showed that in the sub-alpine populations, larval development started earlier with increasing water temperature in spring, and adult emergence was also earlier. The occurrence of adults was extremely low in mid-summer, probably due to summer diapause, followed by a larger number of ovary-developed females in autumn. On the other hand, in the alpine zone, increasing water temperature was delayed compared to the sub-alpine zone, and larval development occurred from early to mid-summer. Adult emergence and ovary-developed individuals were concentrated in mid-summer. Hence, summer diapause was not observed. These results indicated life-history differences between genetically differentiated populations at different altitudes. As the timing of adult occurrence and ovarian developmental patterns differ between populations at different altitudes, it is possible that reproductive isolation is facilitated or maintained between populations.
PubMed: 38855316
DOI: 10.1002/ece3.11428 -
Oecologia Jun 2024Changes in the timing and duration of life cycles are distinctive fingerprints of environmental change. Yet, the biotic and abiotic cues underpinning phenology and...
Changes in the timing and duration of life cycles are distinctive fingerprints of environmental change. Yet, the biotic and abiotic cues underpinning phenology and voltinism, i.e., number of generations per year, are poorly understood. Here, I experimentally test how temperature and provision size influence voltinism and survival to emergence in a solitary bee Colletes validus, and how temperature influences voltinism in the brood parasite Tricrania sanguinipennis. Within the same population, univoltine individuals emerge after 1 year (1-year form), whereas semivoltine individuals enter prolonged dormancy and emerge after 2 years (2-year form). I reared field-collected bees under 2 × 2 factorial experiments with cool (18.5 °C ± 0.5 °C) vs. warm (24 °C ± 0.5 °C) temperature treatments (bees and beetles) and no supplement vs. supplemental food treatments (+ 20% ± 5% pollen provision by mass); beetles were reared under temperature treatments only. Cool temperatures consistently increased the proportion of 2-year bees regardless of provision size, a finding that was consistent with three years of field observations. There was a demographic cost to prolonged dormancy in that both 1- and 2-year bees survived to emergence as adults, but survival of 2-year bees was approximately 50% lower than 1-year bees. Two-year beetles were produced under cooler temperatures, but unlike bees, beetles had nearly perfect survival to emergence in all treatments. This experiment advances our mechanistic understanding of the environmental drivers of voltinism in diverse insect taxa and underscores the importance of considering cryptic life stages when interpreting responses to environmental change.
PubMed: 38850313
DOI: 10.1007/s00442-024-05580-5