Hormonal Regulation of Diapause and Development in Nematodes, Insects, and Fishes

Diapause is a state of developmental arrest adopted in response to or in anticipation of environmental conditions that are unfavorable for growth. In many cases, diapause is facultative, such that animals may undergo either a diapause or a non-diapause developmental trajectory, depending on environmental cues. Diapause is characterized by enhanced stress resistance, reduced metabolism, and increased longevity. The ability to postpone reproduction until suitable conditions are found is important to the survival of many animals, and both vertebrate and invertebrate species can undergo diapause. The decision to enter diapause occurs at the level of the whole animal, and thus hormonal signaling pathways are common regulators of the diapause decision. Unlike other types of developmental arrest, diapause is programmed, such that the diapause developmental trajectory includes a pre-diapause preparatory phase, diapause itself, recovery from diapause, and post-diapause development. Therefore, developmental pathways are profoundly affected by diapause. Here, I review two conserved hormonal pathways, insulin/IGF signaling (IIS) and nuclear hormone receptor signaling (NHR), and their role in regulating diapause across three animal phyla. Specifically, the species reviewed are Austrofundulus limnaeus and Nothobranchius furzeri annual killifishes, Caenorhabditis elegans nematodes, and insect species including Drosophila melanogaster, Culex pipiens, and Bombyx mori. In addition, the developmental changes that occur as a result of diapause are discussed, with a focus on how IIS and NHR pathways interact with core developmental pathways in C. elegans larvae that undergo diapause.

Modelling of post-diapause development and spring emergence of Cydia nigricana (Lepidoptera: Tortricidae)

The prediction of the post-diapause emergence is the first step towards a comprehensive decision support system that can contribute to a considerable reduction of pesticide use by forecasting a precise spraying date. The cumulative field emergence can be described as a function of the cumulative development rate. We investigated the impact of seven constant temperatures and five light regimes on post-diapause development in laboratory experiments. Development rate depended significantly on temperature but not on photoperiod. We therefore fit non-linear thermal performance curves, a better and more modern approach over past linear models, to describe the development rate as a function of temperature. The four parameter Brière function was the most suitable and was subsequently applied to temperature data from 36 previous pea fields, where pea moth emergence was measured with pheromone traps in Northern Hesse (Germany). In order to describe the variation in development times between individuals, we fit five nonlinear distribution models to the cumulative development rate as a function of cumulative field emergence. The three parameter Gompertz model was selected as the best fitted model. We validated the model performance with an independent field data set. The model correctly predicted the first moth in the trap and the peak emergence in 81.82% of cases, with an average deviation of only 2.00 and 2.09 days respectively.

Comparison of the Hatch of Newly Laid Lycorma delicatula (Hemiptera: Fulgoridae) Eggs From the United States After Exposure to Different Temperatures and Durations of Low Temperature

Comparisons were made of the effects of temperature and duration of low temperature on hatch of newly laid egg masses of the invasive spotted lanternfly, Lycorma delicatula (White). Egg masses were collected in mid-October 2019 and estimated to be less than 14 d old. There was a significant positive nonlinear relationship between temperature and developmental rate (1/d) for eggs held at constant temperatures. The lower threshold for egg development was estimated as 7.39°C. Eggs held at constant 10, 15, and 20°C were estimated to require 635, 715, and 849 DD7.39, respectively, to develop. Egg hatch was variable, egg hatch rates were highest (58.4%) when held at a constant 15°C, though high rates (52.7%) were also obtained when eggs were held for 84 d at 10°C, then moved to 25°C. Almost all eggs enter diapause since very few eggs were able hatch when moved to 25°C after 7 d of chill at either 5 or 10°C. Chilling at 5 or 10°C increased percentage egg hatch as the duration in chill increased up to ~100 d and eggs held at 10°C were able to complete some or all the post-diapause development before being moved to 25°C. All egg masses were held at constant 16:8 (L:D) photoperiod and 65%RH. Our data suggest that temperature is the driving factor for diapause termination in spotted lanternfly, but other abiotic factors should be investigated. These identified developmental temperature threshold and degree day requirements for egg hatch will improve predictive distribution and phenological models.

High-throughput profiling of diapause regulated genes from Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae)

Background: The parasitoid wasp, Trichogramma dendrolimi, can enter diapause at the prepupal stage. Thus, diapause is an efficient preservation method during the mass production of T. dendrolimi. Previous studies on diapause have mainly focused on ecological characteristics, so the molecular basis of diapause in T. dendrolimi is unknown. We compared transcriptomes of diapause and non-diapause T. dendrolimi to identify key genes and pathways involved in diapause development.Results: Transcriptome sequencing was performed on diapause prepupae, pupae after diapause, non-diapause prepupae, and pupae. Analysis yielded a total of 87,022 transcripts with an average length of 1,604 bp. By removing redundant sequences and those without significant BLAST hits, a non-redundant dataset was generated, containing 7,593 sequences with an average length of 3,351 bp. Among them, 5,702 genes were differentially expressed. The result of Gene Ontology (GO) enrichment analysis revealed that regulation of transcription, DNA-templated, oxidation-reduction process, and signal transduction were significantly affected. Ten genes were selected for validation using quantitative real-time PCR (qPCR). The changes showed the same trend as between the qPCR and RNA-Seq results. Several genes were identified as involved in diapause, including ribosomal proteins, zinc finger proteins, homeobox proteins, forkhead box proteins, UDP-glucuronosyltransferase, Glutathione-S-transferase, p53, and DNA damage-regulated gene 1 (pdrg1). Genes related to lipid metabolism were also included.Conclusions: We generated a large amount of transcriptome data from T. dendrolimi, providing a resource for future gene function research. The diapause-related genes identified help reveal the molecular mechanisms of diapause, in T. dendrolimi, and other insect species.

High-throughput profiling of diapause regulated genes from Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae)

Background The parasitoid wasp, Trichogramma dendrolimi, can enter diapause at the prepupal stage. Thus, diapause is an efficient preservation method during the mass production of T. dendrolimi. Previous studies on diapause have mainly focused on ecological characteristics, so the molecular basis of diapause in T. dendrolimi is unknown. We compared transcriptomes of diapause and non-diapause T. dendrolimi to identify key genes and pathways involved in diapause development. Results Transcriptome sequencing was performed on diapause prepupae, pupae after diapause, non-diapause prepupae, and pupae. Analysis yielded a total of 87,022 transcripts with an average length of 1604 bp. By removing redundant sequences and those without significant BLAST hits, a non-redundant dataset was generated, containing 7593 sequences with an average length of 3351 bp. Among them, 5702 genes were differentially expressed. The result of Gene Ontology (GO) enrichment analysis revealed that regulation of transcription, DNA-templated, oxidation-reduction process, and signal transduction were significantly affected. Ten genes were selected for validation using quantitative real-time PCR (qPCR). The changes showed the same trend as between the qPCR and RNA-Seq results. Several genes were identified as involved in diapause, including ribosomal proteins, zinc finger proteins, homeobox proteins, forkhead box proteins, UDP-glucuronosyltransferase, Glutathione-S-transferase, p53, and DNA damage-regulated gene 1 (pdrg1). Genes related to lipid metabolism were also included. Conclusions We generated a large amount of transcriptome data from T. dendrolimi, providing a resource for future gene function research. The diapause-related genes identified help reveal the molecular mechanisms of diapause, in T. dendrolimi, and other insect species.

Effects of Low Temperature Exposure on Diapause, Development, and Reproductive Fitness of the Emerald Ash Borer (Coleoptera: Buprestidae): Implications for Voltinism and Laboratory Rearing

The emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), native to Northeast Asia, is the most destructive invasive ash (Fraxinus spp.) pest in the United States. In the present study, we evaluated the effect of exposure of diapausing mature fourth instars (J-shaped larvae, JL) of EAB to cool temperatures, either 1.7 or 12.8°C for 1–9 mo, on their post-chill development including adult emergence, longevity, and lifetime fecundity under standard rearing conditions (26 ± 0.5°C, 16:8 h L:D). In addition, we determined the effect of different stages of the larvae chilled at 12.8°C for 3 mo on the subsequent post-chill development to EAB adults. Findings from the study revealed that a period (≥2 mo) of chill at 12.8°C is required for the termination of the EAB diapause. However, chill treatment of the larvae at the near zero temperature (1.7°C) does not result in the post-diapause larval development to adults, regardless of the chill time (1–9 mo). In addition, our results showed that chill treatment of immature young larvae (L1–L4 prior to JL) results in little production of EAB adults, indicating that EAB diapause predominantly as JL. Findings of this study may be useful to laboratory rearing of EAB from eggs through continuous generations and help us understand the pest’s voltinism resulting from the diapause and post-diapause development under different climatic conditions.

High-throughput profiling of diapause regulated genes from Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae)

Background: The parasitoid wasp, Trichogramma dendrolimi, can enter diapause at the prepupal stage. Thus, diapause is an efficient preservation method during the mass production of T. dendrolimi. Previous studies on diapause have mainly focused on ecological characteristics, so the molecular basis of diapause in T. dendrolimi is unknown. We compared transcriptomes of diapause and non-diapause T. dendrolimi to identify key genes and pathways involved in diapause development.Results: Transcriptome sequencing was performed on diapause prepupae, pupae after diapause, non-diapause prepupae, and pupae. Analysis yielded a total of 87,022 transcripts with an average length of 1,604 bp. By removing redundant sequences and those without significant BLAST hits, a non-redundant dataset was generated, containing 7,593 sequences with an average length of 3,351 bp. Among them, 5,702 genes were differentially expressed. The result of Gene Ontology (GO) enrichment analysis revealed that regulation of transcription, DNA-templated, oxidation-reduction process, and signal transduction were significantly affected. Ten genes were selected for validation using quantitative real-time PCR (qPCR). The changes showed the same trend as between the qPCR and RNA-Seq results. Several genes were identified as involved in diapause, including ribosomal proteins, zinc finger proteins, homeobox proteins, forkhead box proteins, UDP-glucuronosyltransferase, Glutathione-S-transferase, p53, and DNA damage-regulated gene 1 (pdrg1). Genes related to lipid metabolism were also included.Conclusions: We generated a large amount of transcriptome data from T. dendrolimi, providing a resource for future gene function research. The diapause-related genes identified help reveal the molecular mechanisms of diapause, in T. dendrolimi, and other insect species.

Genome-wide variation and transcriptional changes in diverse developmental processes underlie the rapid evolution of seasonal adaptation

Many organisms enter a dormant state in their life cycle to deal with predictable changes in environments over the course of a year. The timing of dormancy is therefore a key seasonal adaptation, and it evolves rapidly with changing environments. We tested the hypothesis that differences in the timing of seasonal activity are driven by differences in the rate of development during diapause inRhagoletis pomonella, a fly specialized to feed on fruits of seasonally limited host plants. Transcriptomes from the central nervous system across a time series during diapause show consistent and progressive changes in transcripts participating in diverse developmental processes, despite a lack of gross morphological change. Moreover, population genomic analyses suggested that many genes of small effect enriched in developmental functional categories underlie variation in dormancy timing and overlap with gene sets associated with development rate inDrosophila melanogaster. Our transcriptional data also suggested that a recent evolutionary shift from a seasonally late to a seasonally early host plant drove more rapid development during diapause in the early fly population. Moreover, genetic variants that diverged during the evolutionary shift were also enriched in putativecisregulatory regions of genes differentially expressed during diapause development. Overall, our data suggest polygenic variation in the rate of developmental progression during diapause contributes to the evolution of seasonality inR. pomonella. We further discuss patterns that suggest hourglass-like developmental divergence early and late in diapause development and an important role for hub genes in the evolution of transcriptional divergence.