Types of diapause.
Abstract
Diapause is a physiological process in which insects can survive in a natural environment that is not conducive to their survival, which is the result of long-term adaptation to environmental conditions. It provides a great adaptive advantage for insects, allowing insects to survive in unsuitable seasonal environments to synchronize their life cycles with those suitable for growth, development, and reproduction. The process of regulating insect diapause is a complex process interacting with multiple mechanisms. In this chapter, a review is given of the current knowledge of diapause types, environmental inducing factors, sensitive states, and the endogenous molecular mechanism associated with diapause in flies (Diptera). Research regarding both the diapause process and intrinsic mechanism is reviewed.
Keywords
- diapause
- stages of diapause
- biotic and abiotic factors
- molecular mechanisms
- Diptera
1. Introduction
Diapause is a state in which insects suspend or arrest the development in response to unfavorable environmental cues. It is an adaptive mechanism with a genetic basis, regulated by the external and internal environment factors, and occurs in a specific stage during the life cycle of an insect such as embryonic, larval, pupal, and active adult stage. Once induced, diapause cannot be immediately terminated even if unfavorable conditions disappear, unless a certain break period has been experienced. Diapause is terminated with the return of appropriate environmental conditions (temperature, light, moisture, etc.), and physical and chemical conditions [1]. Diapause provides an adaptive advantage for insects, allowing them to continue surviving in unfavorable seasonal environments and ensuring that their life cycle is synchronized with conditions suitable for growth, development, and reproduction.
There are two types of diapause, obligatory diapause and facultative diapause. Obligatory diapause, also known as absolute diapause, means that insects have to enter diapause to complete their life cycle, regardless of environmental conditions. It is most found in univoltine insects (one generation per year). For example,
2. Taxa of diapause
Diptera is the fourth largest order after Coleoptera, Lepidoptera, and Hymenoptera. In terms of diapause research, 85 species of Diptera have been studied, including Tephritidae, Culicidae, Calliphoridae, Agromyzidae, Oestridae, Muscidae, Anthomyiidae, Tachinidae, Drosophilidae, and Cecidomyidae (Figure 1).
3. Types of diapause
Diapause can be categorized according to life stages as an egg (embryonic), larval, nymphal, or adult diapause (Table 1). Based on the hereditary feature, there are two types of diapause, one mandatory (obligate diapause) and one optional (facultative diapause) (Table 1).
Classification | Characteristics | |
---|---|---|
Diapause induction stage | Embryonic diapause | occurs at any stage of insect embryo development; regulated by the brain-hypopharyngeal gland-diapause hormone endocrine system |
Larval diapause | occurs at any instar of larval larvae, but mostly occurs at the late larval stage | |
Nymphal diapause | commonly happen in Diptera and Lepidoptera, which is regulated by brain-prothoracic-corpora allata interaction | |
Adult diapause | commonly occurs in Coleoptera, Lepidoptera, Hemiptera, Diptera, Homoptera, and Orthoptera, and is regulated by the islet- corpora allata | |
Hereditary feature | Obligatory diapause | insects have no choice but to enter this process at some stage in their life. |
Facultative diapause | insects will start this process only when environmental conditions become adverse |
Insects with obligate diapause enter diapause at a fixed developmental stage on schedule no matter how the external environmental conditions are, while those with facultative diapause can be induced into diapause at a certain stage but uncertain generation. Diapause is mainly affected by the changes in external environmental conditions. When the environmental conditions are unfavorable, insects enter the diapause, otherwise they continue to develop. Flies also experience diapause in the pupal stage (quiescent stage), during which the activity is extremely weak.
4. Incidence of diapause
The diapause process can be divided into three phases: pre-diapause, diapause, and post-diapause. Pre-diapause occurs before the beginning of unfavorable environmental cues. Insects in this phase forecast an impending transformation in certain environmental stimuli in a special way, and change their internal neuroendocrine system and metabolism level to enter diapause. At this stage, insects maintain normal development, which include induction and preparation stage [14]. The induction stage happens before the beginning of unfavorable environmental cues. Insects receive these specific environmental stimuli called “token stimuli” such as photoperiod, temperature, humidity, and food, to regulate their development and decide whether to enter diapause or not. Larvae of
Because of frequent observations of changing responses to various environmental conditions, diapause is divided into three eco-physiological sub-phases: initiation, maintenance, and termination [14]. The incidence of diapause is affected by a variety of factors. Many insects enter diapause at any stage of their life cycle, but for some species, the diapause stage is fixed, which can be judged by observing the color, appearance, and cocoon making of insect bodies [14, 19, 20, 21]. The maintenance phase refers to the period in which the insect remains undeveloped even under favorable developmental conditions, and the respiration and metabolic rates are at low levels. The diapause maintenance period of different insects varies greatly, ranging from a few weeks to several months or even several years. With the return of favorable environmental conditions, the intensity of diapause gradually decreases and enters the diapause termination. At this stage, insects are sensitive to temperature factors, especially low temperatures. In addition, photoperiod can induce diapause termination. Application of exogenous substances can also break insect diapause. For example, exogenous ecdysterone can terminate the diapause of
In the termination phase, insects enter the next inactivity period if the environmental conditions are still unfavorable; however, they start resuming their physiological development [14].
5. Parental effects on diapause
Parents exhibit a greater effect on the diapause phenotype of their offspring, which defines as parental effect [23]. Parental effect is subject to natural selection, and it is the response mechanism of phenotypes to environmental heterogeneity [24, 25]. Among the parental effects, the female parent exhibits a greater influence than the male parent, so maternal inheritance is considered to be a short form of non-Mendelian parental effect (including maternal and paternal inheritance). For insects, female effects on offspring are relatively common. The parental effect of diapause in Diptera is mainly affected by environmental conditions such as diapause duration, photoperiod, temperature, and parental factors. Ordinarily, parents produce more diapausing progeny if they experience short-day length, limited resources, or low temperature [26]. In the study of
Larval diapause in the blow fly
6. Environmental cues for diapause induction
Insect diapause is a complex process in which many mechanisms interact with each other. The major environmental signals regulating diapause onset in insects include temperature, photoperiod, food, and population density. Studies on insect diapause show that the primary cause and state of diapause can be identified and insects could be induced into diapause by artificially simulating diapause conditions in the field. Environmental cues, mostly temperature and photoperiod, control reproductive diapause in flies (Diptera), which regulate the induction, maintenance, and termination of diapause.
Seasonal change in photoperiod is the most reliable information to detect the time of year and is the major environmental signal regulating diapause onset in most insects. Photoperiod refers the period of time in a day that an organism is exposed to light or, more simply, day length. Photoperiodism is a biological response to a change in the proportions of light and dark in a daily (24 h) cycle, and the average number of daylight hours that cause insect diapause is known as “critical photoperiod.” When insects respond to changes in light intensity through the brain or compound eyes, the internal “timer” automatically evaluates the length of day or night and regulates the insects to enter the diapause [32]. Usually, the diapause of Diptera is caused by short-day length.
Temperature is another major environmental signal regulating diapause, especially for Diptera.
Diapause in some species of flies is subject to both photoperiod and temperature; for example, the dominant diapause cues of
7. Molecular mechanisms of diapause
7.1 Hormonal and metabolic regulation
Endogenous regulatory factors of insect diapause mainly focused on neuroendocrine systems, hormone signaling pathways, and energy metabolism pathways. Studies on
Juvenile hormone (JH), a sesquiterpenoid hormone produced by the corpus allatum (CA) of insects, is one of the most important hormones in insects and plays a key role in preventing larval metamorphosis, maintaining larval state, and regulating adult developmental and physiological process. It also plays a crucial role in the expression of vitellogenin, oocyte maturation, and development. The interaction between genes associated with juvenile hormone pathway is complex, which means genes directly or indirectly participate in the regulation of JH signaling pathway. Studies on the fly
During diapause, there are a lot of significant changes that occur in energy and metabolism due to the organism need to maintain life activities under extreme environmental conditions. Expression of the trehalase gene expression and enzyme activity of
7.2 Diapause-associated changes in genes
With the development of high-throughput sequencing technology, the sequencing and annotation of
The use of RNA-Seq to determine genes with distinct levels of expression between diapause and non-diapause has been confined to flies, and Kyoto Encyclopedia of Genes (KEGG) analysis is performed to identify the pathways that are significantly enriched in diapause. A high-throughput RNA-Seq analysis from non-diapause and summer diapause pupae of
Based on transcriptome sequencing, some candidate diapause-related genes have been further studied in Diptera. For example, heat shock proteins (HSPs) have been studied in
7.3 Diapause-associated changes in proteins
Proteins are complex molecules that play a central role in biological processes. Proteomics is used to elucidate the expression and function of protein on the basis of genome research. Changes in protein expression during diapause can be explored by two-dimensional gel electrophoresis and mass spectrometry. Isobaric tag for relative and absolute quantitation (iTRAQ) can quantitatively analyze proteins from different sources in a single assay, and is used to study quantitative changes in the proteome by tandem mass spectrometry. Due to its high efficiency and sensitivity, iTRAQ has the potential to further advance the study of molecular mechanisms involved in diapause. Proteomic analysis of Diptera has also been reported. A proteomic approach was used to investigate the proteins extracted from larvae of
7.4 Diapause-associated changes in metabolite profiles
Metabolome refers to a collection of small molecular compounds that participate in the metabolism of an organism or cell with a relative molecular weight of less than 1000 DA in a specific physiological period. Metabolomics is a new discipline that simultaneously conducts qualitative and quantitative analysis of small molecule metabolite. It can be used to investigate how metabolites change with time when the organism is stimulated [66]. The cellular activities of living organisms are jointly undertaken by genes, proteins, and small molecule. The metabolic level can reflect the functional changes of macromolecules and amplify the small changes in gene expression. Various techniques are widely used to determine metabolic phenotypes, including liquid chromatography-mass spectrometry (LC-MS), gas chromatography-mass spectrometry (GC/MS), and nuclear magnetic resonance (NMR). LC-MS analysis does not require sample volatileness and thermal stability, and is suitable for compounds with high boiling points, strong polarity, and poor thermal stability. Most metabolites involved in life science have these qualities, so LC-MS has broad application. In recent years, metabolomics has been applied in the area of medicine and microbiology, but there are still relatively few studies on insect diapause. The metabolic profiles of diapause and non-diapause
8. Conclusion
Knowledge of diapause in Diptera is essential for the development of effective pest management strategies and to increase the shelf-life of parasitoids used in the biological control industry. This chapter summarizes the recent progress on diapause of Diptera. We do believe that further studies should be investigated in the diapause of Diptera. Current research studies suggest that histone modification, DNA methylation, RNA methylation, and small noncoding RNAs all may be involved in the regulation of diapause in Diptera. However, it remains unclear whether they regulate the hormonal and physiological changes associated with diapause of Diptera; research has primarily focused on physiological changes associated with pre-diapause with limited attention given to post-diapause. Studies showed that the indices of insects, such as oviposition quantity, oviposition duration, and life span, increased positively during post-diapause phase. The accumulation and consumption of energy storage substances in pre-diapause and diapause will affect the biological characteristics in post-diapause phase. Combined with biological characteristics in post-diapause, studies on development rate, feeding, individual size, diapause maintain environmental conditions, and nutritional supplements after the diapause are necessary. Existing studies on diapause in Diptera are mainly based on single omics, and studies using multi-omics are still vacant. Therefore, for a deeper understanding of the complex molecular landscape of diapause in Diptera, all the available omics data should be utilized in combination rather than treating them individually.
Acknowledgments
This study was supported by the Science and technology planning project of Inner Mongolia Autonomous Region (2021GG0057, 2020ZY0001, 2019BS03011).
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