1 Introduction

Earwigs, belonging to the order Dermaptera, are omnivorous insects found in various ecological systems. They exhibit a wide range of biological and ecological traits, including maternal care, diverse feeding habits, and varied habitat preferences. Earwigs are distributed globally, with the highest diversity found in tropical regions of the southern hemisphere, a pattern likely influenced by their Gondwanan origins. They play a significant role in the ecosystem by acting as both predators and prey. Earwigs contribute to the control of pest populations and the decomposition of organic matter, thus maintaining ecological balance (Wen et al., 2017).

Understanding the population structure of earwigs is crucial for several reasons (Maccaferri et al., 2015). It helps in comprehending their ecological roles, their interactions with other species, and their adaptability to environmental changes. Knowledge of population structure can also aid in the conservation of biodiversity and the management of earwig populations in different habitats.

Earwigs can be both beneficial and detrimental to agriculture. While they help control pest populations, they can also damage crops (Poland et al., 2012). Effective pest management strategies require a thorough understanding of earwig population dynamics and their genetic diversity (Saintenac et al., 2012). High-density genetic mapping can provide insights into the genetic factors influencing earwig behavior and their interactions with crops, leading to more targeted and sustainable pest management practices.

This study synthesizes current knowledge on the molecular ecology and evolutionary genetics of earwigs, with a focus on their population structure, phylogeography, and implications for agricultural pest management. Specifically, it reviews the biogeographical history and current distribution patterns of earwigs, analyzes the genetic diversity and population structure of earwig species using molecular data, and assesses their role in agricultural ecosystems as both pests and beneficial organisms. This study concludes with recommendations for future research and pest management strategies based on these findings. By addressing these objectives, this study seeks to enhance our understanding of earwig biology and contribute to more effective and sustainable agricultural practices.

2 Molecular Markers in Earwig Studies

2.1 Microsatellite markers in population genetics

Microsatellite markers, also known as simple sequence repeats (SSRs), are highly polymorphic and co-dominant markers that have been extensively used in population genetics due to their ability to reveal recent genetic variations and subtle population structures. These markers are particularly valuable for non-model organisms, where genome-wide sequence data may not be readily available. For instance, the development of microsatellite markers in the pine catkin sawfly, Xyela concava, demonstrated their utility in resolving genetic structures among geographically distinct populations and revealed high gene flow despite historical segregation into two genetic lineages (Kulanek et al., 2019). Similarly, microsatellites have been widely applied in plant genetics and breeding, highlighting their hypervariability, multiallelic nature, and extensive genome coverage (Kalia et al., 2011). However, the use of microsatellites in phylogeography can sometimes be limited by their analytical drawbacks, such as the need for a priori groupings and potential issues with null alleles and homoplasy.

2.2 Mitochondrial DNA for phylogeographic studies

Mitochondrial DNA (mtDNA) is a popular molecular marker in phylogeographic studies due to its near-neutrality, lack of recombination, and clock-like evolutionary rate. It has been effectively used to infer population history and evolutionary processes in various species. For example, the phylogeography of the greater horseshoe bat, Rhinolophus ferrumequinum, revealed contrasting results from mtDNA and microsatellite data, emphasizing the importance of combining different markers to obtain a comprehensive understanding of species history (Behura, 2006). However, mtDNA has limitations, such as small effective population sizes and maternal inheritance, which can sometimes lead to misleading conclusions if used in isolation (Godinho et al., 2008). Combining mtDNA with nuclear DNA markers can enhance the power of molecular data to test phylogenetic and phylogeographic hypotheses, as demonstrated in studies on the Iberian lizard, Lacerta schreiberi, and other organisms (Dong et al., 2021).

2.3 Other molecular tools and their applications in evolutionary studies

In addition to microsatellites and mtDNA, various other molecular tools have been employed in evolutionary studies to explore genetic diversity and population structure. Techniques such as random amplified polymorphic DNA (RAPD), expressed sequence tags (EST), amplified fragment length polymorphism (AFLP), and single nucleotide polymorphism (SNP) assays have contributed significantly to understanding the genetic basis of insect diversity and mapping important genes in insect pests (Selkoe and Toonen, 2006). For instance, restriction site-associated DNA sequencing (RADseq) has been used to infer complex phylogeographic patterns in the Crucian carp, Carassius carassius, revealing finer population structures and stronger patterns of isolation by distance compared to microsatellites (Zink, 2010). These advanced molecular tools offer high-throughput genotyping capabilities and can provide deeper insights into the evolutionary processes shaping genetic diversity in earwigs and other organisms. By leveraging a combination of these molecular markers and tools, researchers can gain a more comprehensive understanding of the population structure, phylogeography, and evolutionary genetics of earwigs, ultimately informing agricultural pest management strategies (Jeffries et al., 2016).

3 Population Structure of Earwigs

3.1 Genetic diversity within populations

Genetic diversity within earwig populations is a critical aspect of their population structure. Studies have shown that earwig species exhibit varying levels of genetic diversity, which can be influenced by both environmental factors and historical biogeographical events. For instance, the Anisolabididae family of earwigs in southern Australia demonstrates significant genetic diversity, with distinct morphospecies supported by genetic data showing within-species genetic distances of less than 4% and between-species distances greater than 10%. This high level of genetic diversity within populations is essential for their adaptability and resilience to environmental changes (Stuart et al., 2019).

3.2 Factors influencing population structure

Several factors influence the population structure of earwigs, including environmental conditions, genetic drift, and historical biogeographical events. Environmental factors such as climate and habitat type play a significant role in shaping the genetic structure of earwig populations. For example, the historical biogeography of earwigs suggests that the breakup of Gondwana and subsequent climatic barriers, such as the Himalayan orogenesis, have significantly influenced their current distribution and population structure (Figure 1) (Fattorini, 2022). Additionally, genetic drift and gene flow are crucial in determining the genetic makeup of populations. In the case of the European earwig, Forficula auricularia, population densities and stability are influenced by factors such as migration, pesticide use, starvation, pathogens, parasites, and predation3. Understanding these factors is essential for developing effective pest management strategies.

Figure 1 Zoogeographical regions and areas of endemism used in this study (Adopted from Fattorini, 2022) Image capton: Areas of endemism: AF = Arica (south of the Sahara), AU = Australia, IN = India, MD = Madagascar, NA: North America, NG = New Guinea, PA= Palearctic, SA = South America, SE = South East Asia. (Adapted from Fattorini, 2022)

Fattorini et al. (2022) found that biogeographical regions significantly influence species endemism, particularly in how evolutionary history and geographical isolation shape biodiversity patterns. This study utilizes zoogeographical regions to examine patterns of endemism across different areas. Each region's distinct environmental and historical factors, such as the separation of continents and specific climatic conditions, create unique ecological niches. For example, the Neotropical and Afrotropical regions, due to their tropical climates and historical isolation, exhibit higher endemism in certain taxa compared to the more temperate Palearctic region. These findings underscore the importance of considering both historical and ecological contexts when studying biodiversity distribution. The regional differences also suggest that conservation efforts should prioritize maintaining habitat integrity within these specific zones to preserve endemic species. By identifying areas of endemism, the study provides a critical framework for biodiversity conservation across the globe.

3.3 Case studies of population structure in different ecosystems

Case studies of earwig populations in various ecosystems provide insights into their population structure and the factors influencing it. In southern Australia, the Anisolabididae family of earwigs shows regional endemism, with distinct clades identifiable by forceps morphology, suggesting that local environmental conditions and historical events have shaped their population structure . Another example is the European earwig, Forficula auricularia, which plays a crucial role in integrated pest management in fruit orchards. Studies have shown that their population densities vary significantly between years and are influenced by factors such as orchard management practices and environmental conditions. These case studies highlight the importance of understanding the specific ecological and environmental contexts in which earwig populations exist to effectively manage them as agricultural pests. In conclusion, the population structure of earwigs is shaped by a combination of genetic diversity, environmental factors, and historical biogeographical events. Understanding these elements is crucial for developing effective pest management strategies and conserving the ecological roles that earwigs play in various ecosystems (Moerkens et al., 2009).

4 Phylogeography of Earwigs

4.1 Historical biogeography and migration patterns

The historical biogeography of earwigs (Dermaptera) is deeply rooted in the breakup of the supercontinent Gondwana. This ancient landmass included present-day Antarctica, South America, Africa, and Madagascar, which were once connected. The highest diversity of earwigs is found in the tropical regions of the southern hemisphere, reflecting their Gondwanan origin. The dispersal of earwigs into the Eurasian plate was significantly influenced by the collision of the Indian subcontinent with Eurasia, which was further constrained by the formation of the Himalayas and colder climatic conditions. These barriers played a crucial role in limiting the northward migration of earwigs from South America to North America (Wang et al., 2023).

4.2 Impact of geographic barriers on gene flow

Geographic barriers have a profound impact on the gene flow of earwig populations. The Himalayan orogenesis and colder temperatures have been significant barriers, preventing the colonization of the northern hemisphere by earwigs. This is consistent with findings in other species where physical barriers such as mountain ranges and climatic conditions have restricted gene flow and led to population divergence. For instance, in the case of the cotton pest Adelphocoris suturalis, geographic barriers in China have led to high levels of genetic differentiation among populations. Similarly, the Appalachian Mountains and the Mississippi River have been identified as major barriers influencing the genetic structure of Podophyllum peltatum in eastern North America (Fattorini, 2022).

4.3 Phylogeographic studies in various regions

In Asia, phylogeographic studies on insects such as the cotton pest Adelphocoris suturalis have revealed significant genetic differentiation between central and peripheral populations in China. This differentiation is attributed to physical barriers and climatic oscillations during the Pleistocene, which have shaped the population structure and distribution of this species (Figure 2) (Zhang et al., 2015)

Figure 2 Map of sampling localities of the Adelphocoris suturalis (Adapted from Zhang et al., 2015) Image caption: Different colors showed three groups defined by SAMOVA based on mitochondrial data (red color represents central group; green color represents peripheral group; blue color represents Hokkaido Japan group) (Adapted from Zhang et al., 2015)

Zhang et al. (2015) found that the mitochondrial data of Adelphocoris suturalis populations show significant genetic differentiation across various geographical regions. Using SAMOVA, they identified three distinct groups, each reflecting unique evolutionary histories and possible barriers to gene flow. The central group exhibits more genetic homogeneity, possibly due to gene flow within a geographically continuous area, whereas the peripheral and Hokkaido groups suggest isolation and limited genetic exchange with the central population. These findings emphasize the role of geographical isolation and environmental factors in shaping genetic structure. Moreover, the differentiation among these groups indicates potential ecological adaptations and local speciation, important for understanding the species' evolutionary trajectory. The study highlights the need for conservation strategies that consider the genetic diversity within and among populations to ensure the long-term survival of the species across its range.

In Europe, the phylogeography of spruce bark beetles, Ips typographus and Dendroctonus micans, has shown that species-specific traits such as dispersal ability and reproductive strategies significantly influence genetic variation. Ips typographus, with its strong dispersal capabilities, exhibits a genetic structure that reflects past climatic changes and geographic barriers, whereas Dendroctonus micans, a poor disperser, shows a more pronounced genetic differentiation due to limited gene flow (Deli et al., 2018).

In North America, the phylogeography of Podophyllum peltatum has been shaped by the Appalachian Mountains and the Mississippi River, which have acted as major barriers to gene flow. The genetic diversity is higher in populations east of the Appalachians, indicating historical refugia and subsequent range expansions during the Pleistocene glacial cycles.

In South America, the phylogeographic structure of seabirds such as Phalacrocorax magellanicus and Phalacrocorax atriceps in Patagonia has been influenced by both physical and non-physical barriers. While both species show genetic divergence among colonies from different coastal regions, the degree of population differentiation is higher in Phalacrocorax magellanicus, which has a more sedentary lifestyle compared to the more migratory Phalacrocorax atriceps (Mayer et al., 2015).

In the Mediterranean, the littoral prawn Palaemon elegans exhibits contrasting phylogeographic patterns between its two genetic types. Type II shows a lack of phylogeographic structure, whereas Type III displays significant population structuring across known gene flow barriers. This suggests that different evolutionary processes, such as larval behavior and historical events, have influenced the genetic diversity and distribution of these types9. Overall, the phylogeographic studies across various regions highlight the complex interplay between historical biogeography, geographic barriers, and species-specific traits in shaping the genetic structure and distribution of earwig populations and other insects (Calderón et al., 2014).

5 Evolutionary Genetics and Adaptation

5.1 Evolutionary dynamics in response to environmental pressures

The study of evolutionary genetics in earwigs (Dermaptera) provides essential insights into how these organisms have adapted to various ecological pressures and environments. Their evolutionary dynamics, genetic adaptations to specific ecological niches, and the role of natural selection have shaped the diversity and population structures observed today. Understanding these processes is critical, not only for comprehending earwig evolution but also for applying this knowledge to agricultural pest management.

Earwig populations exhibit remarkable adaptability in response to a range of environmental pressures, including climate fluctuations, habitat fragmentation, and human-induced changes in the ecosystem. The evolutionary dynamics of earwigs are influenced by both short-term environmental shifts and long-term geological events. For example, the breakup of Gondwana and subsequent climatic events, such as glaciation periods, have had significant impacts on the dispersal and genetic diversity of earwigs. These historical biogeographic events led to population isolation, which promoted speciation and adaptive divergence. In modern environments, earwigs continue to evolve in response to agricultural practices, including the use of pesticides and habitat alteration, demonstrating rapid evolutionary changes at the genetic level.

5.2 Genetic adaptation to ecological niches

The ability of earwigs to occupy diverse ecological niches is a testament to their genetic adaptability. Earwigs have colonized a variety of habitats, from forest floors to agricultural landscapes, exhibiting a wide range of feeding behaviors, reproductive strategies, and survival mechanisms. Genetic studies reveal that earwigs undergo local adaptation, allowing them to thrive in specific environments. For example, species inhabiting arid regions have developed physiological and behavioral adaptations to cope with limited water resources, while those in temperate zones show adaptations for overwintering. These adaptations are often linked to specific genetic markers, such as those related to desiccation resistance, temperature tolerance, and reproductive success in fluctuating environments.

5.3 Role of natural selection in shaping earwig populations

Natural selection plays a pivotal role in shaping the genetic structure of earwig populations. Selective pressures, such as predation, competition, and resource availability, drive evolutionary changes within populations, favoring traits that enhance survival and reproductive success. In agricultural ecosystems, earwigs that possess traits enabling them to resist pesticide exposure or exploit new food sources may have a selective advantage. Over time, these adaptive traits become more prevalent within populations through the process of natural selection. Studies on earwigs in agricultural settings have highlighted the potential for resistance development, emphasizing the need for sustainable pest management strategies that take evolutionary principles into account (Moerkens et al., 2009).

In summary, the evolutionary genetics of earwigs demonstrate their resilience and adaptability to a variety of environmental pressures. Genetic adaptation to specific niches and the action of natural selection have shaped the population structures of earwigs across different ecosystems, providing valuable insights into both their ecological roles and implications for pest management. Further research into the molecular mechanisms driving these adaptations will enhance our understanding of earwig evolution and inform the development of more effective pest control strategies in agricultural systems.

6 Earwigs and Agricultural Pest Management

6.1 Earwig species as agricultural pests

Earwigs, particularly the European earwig (Forficula auricularia), play dual roles in agriculture as both pests and beneficial predators. In stone fruit crops like cherries and peaches, earwigs are considered pests due to their potential to damage the fruit. However, in pome fruit orchards such as apples and pears, they act as beneficial predators by feeding on pests like woolly apple aphids and pear psylla. This dual role necessitates careful management to harness their benefits while mitigating their harmful effects (Bourne et al., 2019).

6.2 Impact of population genetics on pest control strategies

Understanding the population genetics of earwigs is crucial for developing effective pest control strategies. Studies have shown that earwig populations exhibit significant genetic diversity and structure, which can influence their resistance to pesticides and their effectiveness as biocontrol agents. For instance, earwigs from different orchard management systems (organic, conventional, and integrated pest management) show varying levels of gene expression related to detoxification and resistance, indicating that pesticide exposure can drive genetic changes in earwig populations. Additionally, the genetic structure and demographic history of earwig populations can affect their stability and effectiveness in pest control, as seen in the significant population fluctuations observed in earwig populations in fruit orchards (Tang et al., 2022).

6.3 Integrated Pest Management (IPM) approaches utilizing molecular data

Integrated Pest Management (IPM) approaches can benefit significantly from molecular data on earwigs. By understanding the genetic basis of earwig resistance to pesticides and their population dynamics, IPM strategies can be tailored to enhance the effectiveness of earwigs as biocontrol agents. For example, molecular studies have identified specific genes associated with pesticide resistance in earwigs, which can inform the selection of less harmful pesticides and the development of resistance management strategies. Additionally, the use of molecular phylogeography can help identify regions with genetically diverse and stable earwig populations, which can be targeted for conservation and augmentation in IPM programs (Pélissié et al., 2021).

6.4 Challenges and future prospects in agricultural pest control

Despite the potential benefits of using earwigs in pest management, several challenges remain. One major challenge is the instability of earwig populations, which can fluctuate significantly between years, limiting their reliability as biocontrol agents. Additionally, the dual role of earwigs as both pests and predators complicates their management, requiring strategies that maximize their benefits while minimizing their harmful effects. Future research should focus on understanding the ecological and genetic factors that influence earwig population dynamics and resistance to pesticides. Advances in molecular techniques, such as genome sequencing and transcriptomics, offer promising tools for addressing these challenges and improving the sustainability of earwig-based pest management strategies (Hanel et al., 2023).

7 Case Study

7.1 Geographic location and ecosystem of the case study

The case study focuses on the earwig populations in southern Australia, particularly within agricultural production regions. This area is characterized by diverse ecosystems that include both natural habitats and agricultural landscapes. The earwigs in this region belong to the Anisolabididae family, which has shown significant regional endemism.

7.2 Molecular analysis of earwig population structure in the area

Molecular analysis of the earwig populations in southern Australia utilized cox1 barcodes and additional mitochondrial and nuclear gene fragments. The study identified seven morphospecies within the Anisolabididae family (Figure 3), which were corroborated by genetic data showing within-species genetic distances of less than 4% and between-species distances greater than 10%. The molecular phylogenies revealed that the putative genera were not monophyletic, and instead, regional clades were distinguishable by forceps morphology.

Figure 3 Morphometric diagram of male Anisolabididae species genitalia and forceps (Adopted from Stuart et al., 2019) Image caption: (a-n): Photos of male Anisolabididae forceps and parameres. (a,b): Anisolabis sp. 1. (c,d): Anisolabis sp. 2. (e,f): Gonolabis forcipata Burr. (g,h): Gonolabis nr. gilesi Steinmann. (i,j): Gonolabis sp. 1. (k,l): Gonolabis sp. 2. (m,n): Gonolabis sp. 3. (o-s): Diagrams of morphometric measurements taken. (o): Forceps length. (p): forceps width. (q): basal width of forceps. (r): paramere length. (s): paramere width. All scale bars indicate 1 mm. Red arrows indicate location of dorsoventrally oriented teeth (Adopted from Stuart et al., 2019)

Stuart et al. (2019) found that the variation in the male genitalia and forceps morphology of Anisolabididae species plays a significant role in taxonomic differentiation and reproductive success. The study highlights that differences in forceps length, width, and paramere size across species may indicate adaptations to specific mating behaviors or ecological niches. For instance, the presence of dorsoventrally oriented teeth in some species suggests an evolutionary trait that could enhance grip during mating or combat with rivals. These morphological traits are key to understanding the evolutionary trajectory and reproductive strategies of Anisolabididae. By quantifying and comparing these characteristics across species, the research provides insights into how morphological diversity can reflect both environmental adaptation and sexual selection pressures. This work emphasizes the importance of morphometric analysis in resolving taxonomic ambiguities and better understanding the evolutionary dynamics within the family Anisolabididae.

7.3 Phylogeographic patterns and their relevance to pest management

The phylogeographic patterns observed in the earwig populations indicated significant regional endemism, with distinct clades corresponding to different geographic areas. This endemism suggests that earwig populations have limited gene flow between regions, which could be due to physical barriers or ecological factors. Understanding these phylogeographic patterns is crucial for pest management as it highlights the need for region-specific strategies. For instance, the unique genetic makeup of earwig populations in different regions may influence their susceptibility to pesticides and their role in biological control.

7.4 Insights for developing region-specific pest control strategies

The insights gained from the molecular and phylogeographic analyses of earwig populations in southern Australia can inform the development of region-specific pest control strategies. Given the regional endemism and genetic differentiation, pest management programs should consider the local genetic diversity and ecological context. For example, the use of biological control agents, such as predatory earwigs, should be tailored to the specific genetic and ecological characteristics of the target populations. Additionally, the identification of resistance-associated genes in earwigs from different orchard management strategies underscores the importance of monitoring and managing resistance to ensure the effectiveness of biocontrol methods (Fricaux et al., 2023).

8 Concluding Remarks

The research on the molecular ecology and evolutionary genetics of earwigs has provided significant insights into their population structure, phylogeography, and potential for agricultural pest management. Studies have revealed that earwig species, particularly within the Anisolabididae family in Australia, exhibit unique regional endemism and significant genetic diversity, which is crucial for their classification and understanding of their ecological roles. Additionally, European earwigs (Forficula auricularia) have shown potential as biocontrol agents in apple orchards, with varying resistance mechanisms to pesticides depending on the orchard management strategies. The population dynamics of earwigs are influenced by several factors, including density-dependent mechanisms, which are critical for their effective use in integrated pest management. Furthermore, earwigs have demonstrated the ability to reduce populations of pests like Drosophila suzukii, although their effectiveness may vary depending on the timing and environmental conditions.

The findings from these studies have several implications for evolutionary genetics and pest management. The genetic diversity and regional endemism observed in earwig populations suggest that local adaptation plays a significant role in their evolution, which can inform conservation strategies and the development of more targeted pest management practices. The identification of resistance-associated genes in earwigs from different orchard management systems highlights the impact of agricultural practices on the genetic makeup of beneficial insects, emphasizing the need for sustainable pest management approaches that minimize the development of resistance. Understanding the population dynamics and density-dependent factors affecting earwig populations can help optimize their use as biocontrol agents, ensuring stable and effective pest suppression in agricultural settings. The potential of earwigs to control pests like Drosophila suzukii further supports their role in integrated pest management programs, although further research is needed to maximize their efficacy.

Future research should focus on expanding the sampling of earwig populations to include regions outside of agricultural production areas to better understand their genetic diversity and regional endemism. Investigating the molecular mechanisms underlying resistance in earwigs and other beneficial insects can provide insights into how to mitigate the impact of pesticides and enhance the sustainability of pest management practices. Long-term studies on the population dynamics of earwigs in different agricultural landscapes are needed to identify the key factors regulating their populations and develop strategies to prevent population crashes. Additionally, further research on the biocontrol potential of earwigs against a broader range of pests, including their interactions with other natural enemies, can help optimize their use in integrated pest management programs.

Acknowledgments

I am grateful to anonymous reviewers for critically reading the manuscript and providing valuable feedback that improved the clarity of the manuscript.

Conflict of Interest Disclosure

The author affirms 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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