1 Introduction

Earwigs, belonging to the order Dermaptera, are a fascinating group of insects known for their distinctive forceps-like appendages and diverse ecological roles. With over 2 000 described species, earwigs exhibit a wide range of behaviors and adaptations, including maternal care and social interactions (Meunier, 2023). These insects are found in various habitats, from tropical to temperate regions, and their ability to thrive in different environments highlights their ecological versatility (Liu et al., 2022). However, earwigs, like many other organisms, face numerous environmental stressors, such as temperature fluctuations, pollutants, and habitat changes, which can significantly impact their survival and fitness (Fattorini, 2022).

The ability of earwigs to adapt to environmental stress is closely linked to their molecular responses. Key molecular mechanisms, such as the expression of heat shock proteins (HSPs) and detoxification enzymes, play crucial roles in protecting cells from damage and maintaining homeostasis under stress conditions. Heat shock proteins are known to assist in protein folding, repair, and degradation, thereby preventing the accumulation of damaged proteins. Detoxification enzymes, on the other hand, help in neutralizing and eliminating harmful substances, thus safeguarding the organism from toxic effects (Stuart et al., 2019). Understanding these molecular responses is essential for elucidating how earwigs cope with environmental challenges and maintain their ecological adaptability (Kamimura et al., 2023).

This study provides a comprehensive analysis of the molecular responses of earwigs to environmental stress, focusing on heat shock proteins, detoxification enzymes, and their ecological adaptability. By synthesizing findings from various studies, this study highlights the significance of these molecular mechanisms in stress adaptation and their implications for the survival and distribution of earwigs. The scope includes an examination of the genetic and biochemical pathways involved in stress responses, the evolutionary aspects of these adaptations, and the potential applications of this knowledge in pest management and conservation efforts.

2 Heat Shock Proteins (HSPs) in Earwigs

2.1 Role of hsps in stress tolerance

Heat shock proteins (HSPs) are crucial molecular chaperones that assist in the proper folding of proteins, repair of damaged proteins, and prevention of protein aggregation under stress conditions (Morimoto, 1998). They play a significant role in enhancing the stress tolerance of organisms, including earwigs, by stabilizing proteins and cellular structures during environmental stress. HSPs are known to be upregulated in response to various stressors such as heat, cold, and oxidative stress, thereby contributing to the survival and adaptability of insects in fluctuating environments (Davoudi et al., 2022). For instance, in the carob moth, Ectomyelois ceratoniae, HSP70 and HSP90 were found to be upregulated in response to both heat and cold stress, indicating their role in acquired thermotolerance (Cheng et al., 2016).

2.2 Gene regulation of hsps under heat stress

The expression of HSP genes is tightly regulated by heat shock factors (HSFs) that bind to heat shock elements (HSEs) in the promoter regions of HSP genes. Under normal conditions, HSFs are inactive, but upon exposure to heat stress, they become activated and induce the transcription of HSP genes. This regulatory mechanism ensures a rapid and efficient response to thermal stress, allowing organisms to cope with sudden temperature changes (Feder and Hofmann, 1999). In the corn earworm, Helicoverpa zea, hsp70 and hsp90 were found to be heat-inducible, with hsp70 showing a stronger induction compared to hsp90, highlighting the differential regulation of HSP genes under heat stress (Quan et al., 2020).

2.3 Comparative analysis of hsp expression in different stress conditions

The expression patterns of HSPs can vary significantly depending on the type and severity of stress. For example, in the wheat blossom midge, Sitodiplosis mosellana, hsp70 was more strongly expressed in response to heat stress during summer, while hsp90 was more responsive to cold stress during winter1. Similarly, in the spruce budworm, Choristoneura fumiferana, different HSP genes showed varied expression levels under heat, cold, and starvation conditions, indicating the complex regulatory mechanisms governing HSP expression in response to diverse stressors. In the carob moth, Ectomyelois ceratoniae, HSP70 transcripts increased more with cold treatment, whereas HSP90 transcripts were more responsive to high temperatures, demonstrating the specific roles of different HSPs in mediating stress responses (Chen et al., 2018). These findings underscore the importance of HSPs in the stress physiology of earwigs and other insects, highlighting their roles in enhancing stress tolerance, regulating gene expression under heat stress, and exhibiting differential expression patterns in response to various environmental stressors (Sørensen et al., 2003).

3 Detoxification Enzymes in Earwigs

3.1 Types of detoxification enzymes (e.g., P450 enzymes)

Detoxification enzymes play a crucial role in the ability of earwigs to survive in environments laden with various chemical stressors. Among these enzymes, cytochrome P450 monooxygenases (P450s), glutathione S-transferases (GSTs), and carboxylesterases (CCEs) are particularly significant. These enzymes are involved in the metabolism and detoxification of xenobiotics, including pesticides and other environmental pollutants. For instance, a study on the stored-product pest Liposcelis entomophila identified 68 putative cytochrome P450 genes, 37 putative GST genes, and 19 putative CCE genes, highlighting the diversity and abundance of detoxification enzymes in insects9. Similarly, research on European earwigs from apple orchards revealed the overexpression of four cytochrome P450s, one esterase, and one GST in response to different orchard management strategies, indicating their role in detoxification processes (Fricaux et al., 2023).

3.2 Molecular mechanisms of detoxification

The molecular mechanisms underlying detoxification in earwigs involve the enzymatic conversion of lipophilic compounds into more hydrophilic forms, which can then be excreted from the body. Cytochrome P450 enzymes catalyze the oxidation of organic substances, making them more soluble and easier to eliminate. Glutathione S-transferases facilitate the conjugation of glutathione to toxic compounds, further enhancing their solubility and excretion. Carboxylesterases hydrolyze ester bonds in xenobiotics, rendering them less toxic. These processes are crucial for the survival of earwigs in environments with high levels of chemical stressors. For example, the transcriptome analysis of Liposcelis entomophila provided insights into the molecular basis of insecticide resistance, identifying numerous detoxification-related genes. Additionally, the study on European earwigs demonstrated that the expression of detoxification genes is influenced by the type of orchard management, with higher expression levels observed in earwigs from organic orchards (Suzuki et al., 2008).

3.3 Regulation of detoxification enzyme genes in response to pesticides

The regulation of detoxification enzyme genes in earwigs is a dynamic process that responds to the presence of pesticides and other environmental stressors. Gene expression can be upregulated in response to exposure, enhancing the insect's ability to detoxify and survive. For instance, the study on European earwigs showed that exposure to different pesticide regimes in apple orchards led to the differential expression of detoxification genes, including cytochrome P450s, esterases, and GSTs (Lu et al., 2017). This adaptive response is crucial for the earwigs' survival and ecological adaptability. Similarly, research on the brown planthopper, Nilaparvata lugens, demonstrated that the expression of Hsp70 increased after exposure to the insecticide imidacloprid, indicating a role in detoxification and stress response. These findings underscore the importance of regulatory mechanisms in the expression of detoxification enzymes, enabling earwigs to cope with the challenges posed by pesticide exposure (Wei et al., 2013).

4 Ecological Adaptability of Earwigs

4.1 Molecular basis of environmental adaptability

Earwigs exhibit remarkable adaptability to various environmental stressors, primarily through the expression of heat shock proteins (HSPs) and detoxification enzymes. HSPs, such as HSP70 and HSP90, play crucial roles in maintaining cellular homeostasis under stress conditions by acting as molecular chaperones that assist in protein folding and prevent aggregation of misfolded proteins (Figure 1) (Chen et al., 2018). These proteins are highly conserved across species and are induced in response to a range of abiotic and biotic stressors, including extreme temperatures and exposure to toxic substances. The transcriptional dynamics of HSPs in response to thermal acclimation have been well-documented in various insect species, highlighting their role in enhancing thermal tolerance and overall stress resilience (Farahani et al., 2020).

Chen et al. (2018) found that evolutionary changes at different biological levels, such as epigenetic modifications, regulatory or coding mutations, and genomic alterations, contribute to distinct evolutionary effects across various timescales. Epigenetic changes, such as DNA and RNA methylation, are linked to ecological effects, potentially enabling organisms to adapt rapidly to environmental fluctuations. Meanwhile, regulatory and coding mutations, including insertions, deletions, and transcription factor binding alterations, drive microevolutionary changes that can fine-tune gene expression in response to selective pressures. At a broader scale, genomic changes like gene expansion, gene loss, and pseudogenization are associated with macroevolutionary effects, which contribute to larger evolutionary shifts in species over extended periods. This multi-layered approach highlights how different molecular mechanisms play crucial roles in shaping both short-term adaptations and long-term evolutionary trends.

4.2 Impact of climate change on earwig populations

Climate change poses significant challenges to earwig populations by altering their habitats and increasing the frequency and intensity of environmental stressors (Idczak-Figiel et al., 2023). The ability of earwigs to adapt to these changes is closely linked to the expression of HSPs and other stress-related proteins. Studies have shown that HSPs are upregulated in response to elevated temperatures, which are becoming more common due to global warming. This upregulation helps earwigs cope with heat stress by stabilizing proteins and protecting cells from damage. However, the long-term effects of continuous exposure to high temperatures and other climate-related stressors may lead to trade-offs, such as reduced growth and reproductive rates, which could impact population dynamics (Quan et al., 2022).

4.3 Interaction of HSPs and detoxification enzymes in adaptive mechanisms

The interaction between HSPs and detoxification enzymes is a key component of the adaptive mechanisms in earwigs. Detoxification enzymes, such as superoxide dismutase (SOD) and catalase (CAT), work in tandem with HSPs to mitigate oxidative stress caused by environmental stressors. For instance, the increased production of reactive oxygen species (ROS) under stress conditions triggers the upregulation of both HSPs and antioxidant enzymes, which together help to maintain cellular integrity and function. This coordinated response enhances the overall stress tolerance of earwigs, allowing them to survive and thrive in fluctuating and often harsh environments. The differential expression of these proteins in response to various stressors underscores the complexity and efficiency of the earwig's adaptive strategies (Haq et al., 2019).

5 Evolutionary Genetics and Adaptation

5.1 Evolutionary dynamics in response to environmental pressures

Heat shock proteins (Hsps) play a crucial role in the evolutionary dynamics of organisms facing environmental pressures. These proteins act as molecular chaperones, helping to maintain cellular function under stress by preventing protein denaturation and assisting in protein refolding. The expression of Hsps is a common response to environmental stressors, and their role in stress tolerance is well-documented across various taxa. The evolutionary significance of Hsps is highlighted by their ubiquitous presence across species and their ability to confer resistance to a range of stressors, including extreme temperatures, toxins, and oxidative stress. The evolutionary control of Hsp expression is a balance between the benefits of stress resistance and the costs associated with their overexpression, such as reduced growth and fertility (Ravaschiere et al., 2017).

5.2 Genetic adaptation to ecological niches

Genetic adaptation to ecological niches is facilitated by the differential expression of Hsps and other stress-related proteins. Studies have shown that organisms inhabiting stressful environments often exhibit higher baseline levels of Hsps and a more robust heat shock response compared to those in less stressful conditions. This adaptive mechanism allows organisms to better cope with the specific challenges of their habitats. For example, the Atlantic Ribbed mussel, Geukensia demissa, from the Bronx River Estuary exhibits higher constitutive levels of Hsp70 and a more rapid heat shock response than its counterparts from less polluted environments, indicating a genetic adaptation to its contaminated habitat7. Such adaptations are crucial for survival and reproductive success in diverse ecological niches.

5.3 Role of natural selection in shaping earwig populations

Natural selection plays a pivotal role in shaping earwig populations by favoring individuals with advantageous stress response mechanisms. The expression of Hsps and other stress-related proteins is subject to selective pressures, with individuals exhibiting optimal levels of these proteins having a higher fitness in stressful environments. The genetic variability in Hsp expression and the associated regulatory mechanisms are key factors in the adaptive evolution of populations. For instance, the regulatory variation and epigenetic changes in Hsp genes contribute to the diversity and adaptability of stress responses in natural populations. This evolutionary process ensures that earwig populations can withstand environmental changes and maintain their ecological roles. In summary, the evolutionary genetics and adaptation of earwigs to environmental stress are intricately linked to the expression and regulation of heat shock proteins and other stress-related enzymes. These molecular responses are shaped by natural selection, enabling earwigs to thrive in diverse and challenging ecological niches (Sørensen, 2010).

6 Earwigs and Agricultural Pest Management

6.1 Earwig species as agricultural pests

Earwigs, particularly the European earwig (Forficula auricularia), are often considered beneficial insects in agricultural settings due to their predatory nature, which helps control pest populations such as aphids in apple orchards. However, their role can be dual-faceted as they may also feed on crops, causing damage. The balance between their beneficial and pestiferous roles depends on the specific agricultural context and the management practices employed (Bourne et al., 2019).

6.2 Impact of population genetics on pest control strategies

The genetic diversity within earwig populations can significantly influence the effectiveness of pest control strategies. For instance, earwigs from different orchard management systems (organic, conventional, and integrated pest management) exhibit variations in resistance-associated genes. Mutations in genes such as acetylcholinesterase 2 and nicotinic acetylcholine receptors, along with the overexpression of detoxification genes like cytochromes P450, esterases, and glutathione S-transferases, have been identified. These genetic differences can affect the susceptibility of earwigs to pesticides and their role in pest control. Additionally, regional endemism and genetic diversity within species, as observed in Australian Anisolabididae earwigs, highlight the importance of understanding local genetic variations for effective pest management.

6.3 Integrated pest management (IPM) approaches utilizing molecular data

Integrated Pest Management (IPM) strategies can benefit from molecular data to optimize the use of earwigs as biological control agents. By understanding the molecular resistance mechanisms and genetic diversity of earwig populations, IPM programs can tailor their approaches to enhance the efficacy of earwigs in controlling pest populations while minimizing the use of chemical pesticides. For example, the identification of resistance-associated genes and their expression levels in earwigs from different management systems can inform the selection of compatible biocontrol agents and the design of environmentally friendly pest control strategies (Happe et al., 2018).

6.4 Challenges and future prospects in agricultural pest control

One of the main challenges in utilizing earwigs for pest control is the potential development of resistance to pesticides, which can reduce their effectiveness as biocontrol agents. Additionally, the dual role of earwigs as both beneficial predators and potential pests complicates their management. Future research should focus on further elucidating the molecular mechanisms underlying earwig resistance and adaptability to different environmental stresses. This knowledge can help develop more targeted and sustainable pest management strategies. Moreover, expanding the genetic and ecological studies to include a broader range of earwig species and regions will provide a more comprehensive understanding of their role in agricultural ecosystems. In conclusion, earwigs hold significant potential for agricultural pest management, but their effective use requires a deep understanding of their molecular responses to environmental stress and genetic diversity. Integrating this knowledge into IPM programs can lead to more sustainable and efficient pest control solutions (Khurshid et al., 2021).

7 Case Study

7.1 Geographic location and ecosystem of the case study

The case study focuses on European earwigs, Forficula auricularia, in apple orchards located in Europe. Apple orchards are among the most heavily treated crops in Europe, with up to 35 chemical treatments per year. These orchards can be managed using different strategies, including organic, conventional, and integrated pest management (IPM) approaches.

7.2 Molecular analysis of earwig population structure in the area

Molecular analysis of earwig populations in these orchards revealed significant genetic variations and adaptations to the different management strategies. Earwigs from organic, IPM, and conventional orchards showed mutations in acetylcholinesterase, α1, and α2 nicotinic acetylcholine receptors. Additionally, the expression levels of these targets and several detoxification genes, such as cytochromes P450, esterases, and glutathione S-transferases, were monitored using RT-qPCR. Notably, earwigs from organic orchards exhibited the highest expression levels for acetylcholinesterase (Ruan et al., 2022).

7.3 Phylogeographic patterns and their relevance to pest management

The phylogeographic patterns observed in earwig populations indicate that different orchard management strategies can lead to distinct molecular adaptations. These adaptations are crucial for understanding how earwigs respond to environmental stressors, such as pesticide exposure. The presence of specific mutations and the differential expression of detoxification genes suggest that earwigs have developed resistance mechanisms that could impact their effectiveness as biological control agents in pest management (Zhao et al., 2023).

7.4 Insights for developing region-specific pest control strategies

The insights gained from this case study highlight the importance of considering the molecular responses of beneficial insects like earwigs when developing pest control strategies. The identification of resistance-associated genes and their expression patterns can inform the design of more sustainable and effective pest management practices. For instance, reducing the reliance on chemical treatments and promoting the use of biological control agents can help maintain the biodiversity of natural enemies in orchards and enhance their ecological adaptability (Li et al., 2020).

8 Concluding Remarks

The molecular responses of earwigs to environmental stress involve a complex interplay of heat shock proteins (HSPs), detoxification enzymes, and other stress-related biomolecules. Heat shock proteins, particularly HSP70 and HSP90, play crucial roles in mediating stress tolerance by acting as molecular chaperones that assist in protein folding, trafficking, and preventing aggregation under stress conditions. These proteins are upregulated in response to various stressors, including heat, cold, starvation, and parasitism, indicating their broad role in stress adaptation. Additionally, antioxidant enzymes such as superoxide dismutase (SOD) and catalase (CAT) are upregulated to mitigate oxidative stress, which is a common consequence of environmental stressors. The expression of these proteins is tightly regulated at the genetic level, with significant variations observed across different developmental stages and tissues.

The findings have significant implications for evolutionary genetics and pest management. The ability of HSPs to confer stress tolerance suggests that these proteins are key players in the evolutionary adaptation of earwigs to changing environments. The genetic diversity and regulatory variation in HSP genes highlight their potential role in natural selection and evolutionary fitness. From a pest management perspective, understanding the molecular mechanisms underlying stress responses can inform strategies to control earwig populations. For instance, targeting specific HSPs or antioxidant pathways could be a viable approach to reduce the resilience of earwigs to environmental stressors, thereby making them more susceptible to control measures.

Future research should focus on several key areas to further elucidate the molecular responses of earwigs to environmental stress. First, comprehensive genome-wide studies are needed to identify and characterize the full repertoire of HSPs and other stress-related genes in earwigs. Second, functional studies using techniques such as RNA interference (RNAi) or CRISPR-Cas9 could help determine the specific roles of individual HSPs and antioxidant enzymes in stress tolerance. Third, exploring the epigenetic regulation of stress response genes could provide insights into how environmental factors influence gene expression and adaptation1. Finally, integrating molecular data with ecological and behavioral studies will be crucial for developing holistic pest management strategies that consider the adaptive capabilities of earwigs.

Acknowledgments

The authors would like to thank the anonymous reviewers for their insightful comments and suggestions that greatly improved the manuscript.

Conflict of Interest Disclosure

The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

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