1 Introduction

Parasitic insects, particularly parasitoid wasps, represent a fascinating and diverse group within the insect world. These insects have evolved complex life strategies that involve parasitizing other organisms (Blaimer et al., 2020), often leading to the eventual death of their hosts (Whitfield, 1998). The parasitoid lifestyle has independently evolved multiple times across different insect orders (Muirhead et al., 2012), making these insects important models for studying evolutionary biology, ecology, and genetics (Kraaijeveld et al., 2018).

Parasitoid wasps, belonging primarily to the order Hymenoptera, are of significant interest due to their role in natural ecosystems and their application in biological control programs (Michel-Salzat and Whitfield, 2004). These wasps are known for their ability to regulate populations of herbivorous pests, thereby contributing to the stability of agricultural systems and natural habitats (Bredlau et al., 2019). The study of parasitoid wasps not only provides insights into the mechanisms of host-parasite interactions but also enhances our understanding of speciation, adaptation, and the evolution of complex life histories (Pennacchio and Strand, 2006).

This study integrates data from various genomic and phylogenetic research to elucidate the evolutionary pathways that have led to the current diversity of parasitoid wasps. It explores the ecological and physiological characteristics of hosts that these insects have successfully exploited, as well as the genetic mechanisms behind their parasitism strategies. The aim is to gain a deeper understanding of the evolutionary drivers of parasitoid wasps and their role within the broader context of parasitic insects.

2 Genetic Evolution of Parasitic Insects

2.1 Overview of genetic changes in parasitic insects

Parasitic insects, particularly parasitoid wasps, exhibit significant genetic changes that have enabled their unique lifestyles. These changes are often driven by interactions with their hosts and the need to overcome host defenses. For instance, the genomes of parasitoid wasps have integrated viral elements that play crucial roles in their parasitic strategies (Coffman and Burke, 2020). Additionally, the rapid evolution of mitochondrial genomes in parasitic wasps, such as those in the genus Nasonia, highlights the dynamic nature of their genetic makeup (Kaltenpoth et al., 2012).

2.2 Evolutionary mechanisms in parasitoid wasps

Parasitoid wasps have evolved through various mechanisms, including horizontal gene transfer (HGT) and the integration of viral genomes. HGT has been a significant driver of genetic innovation in these insects, allowing them to acquire genes that enhance their parasitic capabilities. For example, the integration of polydnavirus DNA into the genomes of parasitoid wasps and their hosts has facilitated the manipulation of host immune responses (Lelio et al., 2019). Additionally, the rapid evolution of mitochondrial genes in parasitoid wasps, driven by directional selection, has contributed to their adaptability and success as parasites (Pennacchio and Strand, 2006).

2.3 Comparative genomic studies

Comparative genomic studies have provided insights into the genetic evolution of parasitoid wasps. The genomes of three closely related Nasonia species have revealed rapid evolution and the presence of unique genetic elements, such as a functional DNA methylation toolkit and hymenopteran-specific genes (Kraaijeveld et al., 2018). Furthermore, the genomic resources developed for parasitoid insects outside the Parasitica clade, such as Goniozus legneri, Aleochara bilineata, and Paykullia maculata, offer valuable data for understanding the generality of findings from Parasitica wasps (Schneider and Thomas, 2014).

2.4 Role of horizontal gene transfer in parasitoid wasps

Horizontal gene transfer (HGT) has played a pivotal role in the genetic evolution of parasitoid wasps. HGT events have allowed these insects to acquire genes from their hosts and other organisms, providing them with new physiological traits and enhancing their parasitic abilities. For instance, the transfer of the Sl gasmin gene from a symbiotic virus of a parasitic wasp to the moth species Spodoptera littoralis has conferred immune advantages to the host (Heisserer et al., 2023). Additionally, the integration of polydnavirus DNA into the genomes of lepidopteran hosts through HGT has been documented in numerous species, highlighting the widespread impact of this mechanism.

3 Morphological Evolution of Parasitic Insects

3.1 Adaptations in morphology due to parasitism

Parasitic insects, particularly parasitoid wasps, exhibit a range of morphological adaptations that facilitate their parasitic lifestyle. These adaptations often include specialized ovipositors for injecting eggs into hosts, modifications in body size and shape to navigate host environments, and the development of structures such as chelae for grasping prey. For instance, the dryinid wasp Gonatopus flavifemur has evolved chelae on its forelegs and venom glands, which are crucial for both predation and parasitism (Blaimer et al., 2020). Additionally, cuckoo wasps have developed chemical mimicry to blend in with their hosts, showcasing the diverse morphological strategies evolved to enhance parasitic efficiency (Branca et al., 2019).

3.2 Evolutionary trends in parasitoid wasps

The evolutionary history of parasitoid wasps is marked by significant diversification and specialization. Phylogenomic analyses of cynipoid wasps reveal that parasitoidism and inquilinism (usurping other species' galls) are ancestral traits, with parasitoidism being a dominant strategy throughout their evolution. Similarly, the Chalcidoidea superfamily, which includes many parasitoid wasps, shows a transition from minute egg parasitoids to larger-bodied parasitoids of other host stages, indicating an evolutionary trend towards increased body size and host range diversification (Bredlau et al., 2019). These trends highlight the adaptive radiation and ecological success of parasitoid wasps over millions of years (Peters et al., 2017).

3.3 Morphological diversification and specialization

Morphological diversification in parasitoid wasps is driven by their interactions with a wide range of hosts. For example, Cotesia congregata has diversified into two incipient species, each adapted to different host species and host foodplants, resulting in reproductive incompatibility and hybrid sterility (Peters et al., 2018). This diversification is often accompanied by changes in gene expression related to parasitism, such as the differential expression of bracovirus genes in C. congregata (Kraaijeveld et al., 2018). The genomic analysis of Goniozus legneri, Aleochara bilineata, and Paykullia maculata, representing independent origins of the parasitoid lifestyle, further underscores the genetic basis of morphological specialization in parasitoid insects (Pauli et al., 2018).

3.4 Influence of host-parasite interactions on morphology

Host-parasite interactions play a crucial role in shaping the morphology of parasitic insects. The genetic structure of Cotesia sesamiae, influenced by host specialization and Wolbachia infections, demonstrates how biotic factors drive morphological and genetic differentiation in parasitoid populations (Coffman and Burke, 2020). Additionally, the presence of endogenous viruses in parasitic wasps, such as polydnaviruses and virus-like particles, has led to the evolution of complex morphological traits that facilitate the transfer of virulence factors to hosts (Drezen et al., 2017).

These interactions highlight the co-evolutionary dynamics between parasitoid wasps and their hosts, driving morphological innovations that enhance parasitic success. In summary, the morphological evolution of parasitic insects, particularly parasitoid wasps, is characterized by a range of adaptations driven by their parasitic lifestyle, evolutionary trends towards diversification and specialization, and the influence of host-parasite interactions. These factors collectively contribute to the remarkable diversity and ecological success of parasitoid wasps (Yang et al., 2021).

Coffman and Burke (2020) conducted a phylogenetic analysis of poxviruses using 16 conserved core genes to explore the evolutionary relationships between insect and vertebrate poxviruses. The study highlights the discovery that Yalta virus, a fly-infecting virus, is the closest known relative to the DlEPV (Diaphragmatic Epithelial Poxvirus), suggesting an evolutionary link between these two viruses.

The maximum likelihood analysis, supported by 1,000 bootstrap iterations, provides robust evidence for the close relationship between Yalta virus and DlEPV, indicating a potential cross-species evolutionary event or a common ancestor shared by these insect and vertebrate poxviruses. This finding expands the understanding of poxvirus evolution, particularly the interactions between insect and vertebrate hosts. The phylogenetic tree constructed in the study illustrates the distinct clustering of insect and vertebrate poxviruses while emphasizing the unique position of Yalta virus within this evolutionary framework.

4 Case Study: Parasitoid Wasps

4.1 Selection of case study species

For this case study, we selected several species of parasitoid wasps that represent diverse evolutionary origins and lifestyles. The species chosen include Goniozus legneri, a parasitoid Hymenopteran, Aleochara bilineata, a Coleopteran parasitoid, and Paykullia maculata, a Dipteran parasitoid (Kraaijeveld et al., 2018). Additionally, we included Diachasmimorpha longicaudata, known for its mutualistic relationship with a poxvirus (Pauli et al., 2018), and Gonatopus flavifemur, a dryinid wasp with unique adaptations for both parasitism and predation (Yang et al., 2021). These species were selected to provide a comprehensive overview of the genetic and morphological adaptations that have evolved in parasitoid wasps.

4.2 Genetic and morphological analysis of the selected species

The genetic analysis of these species revealed significant insights into their evolutionary adaptations (Blaimer et al., 2020). For instance, the genome of Goniozus legneri and other non-Parasitica parasitoids provided a basis for comparative studies with Parasitica wasps, highlighting the fragmented yet complete nature of their genomes. In Diachasmimorpha longicaudata, the presence of an exogenous viral symbiont, Diachasmimorpha longicaudata entomopoxvirus (DlEPV), was identified, which plays a crucial role in the wasp's parasitic lifecycle (Coffman and Burke, 2020). The genome of Gonatopus flavifemur revealed unique venom evolution and dual adaptations for parasitism and predation, with specific expansions in venom-related genes and sex-biased genes contributing to its predatory and reproductive behaviors (Figure 1) (Yang et al., 2021).

Figure 1 Assembly of the genome of G. flavifemur (Adopted from Yang et al., 2021) Image capton: a: A female G. flavifemur attacking its host, the brown planthopper Nilaparvata lugens. B: A winged male G. flavifemur. c: Larvae of G. flavifemur on its host. d: d’ The fore leg and chela of female G. flavifemur. Scale bars: 300 μm. e: An overview of the genome assembly strategy. f: Comparison of assembly contiguity among six hymenopterans. N(x) % graphs show contig or scaffold sizes (y-axis), in which x percent of the assembly consists of contigs/scaffolds of at least that size. g: Comparison of the completeness of genome assemblies, as a percentage of 1367 insect genes from insecta_odb10 (Adopted from Yang et al., 2021)

Yang et al. (2021) conducted a comprehensive study on the genome assembly of Gonatopus flavifemur, a parasitic wasp known for attacking the brown planthopper, Nilaparvata lugens, a significant pest in rice cultivation. The study outlines a detailed genome assembly strategy utilizing both Nanopore long reads and Illumina short reads to achieve a high-quality assembly. The comparison of genome contiguity and completeness with other hymenopterans highlights the effectiveness of their assembly process, positioning G. flavifemur among the more thoroughly assembled genomes within the group. This research not only provides critical insights into the genomic structure of G. flavifemur but also offers valuable resources for further studies on its biology and potential applications in biological control of agricultural pests. The assembly's high completeness in capturing essential insect genes underscores the robustness of their methodology.

4.3 Evolutionary adaptations observed

Several evolutionary adaptations were observed across the selected species. Goniozus legneri and other parasitoids outside the Parasitica clade have developed genomic structures that support their parasitic lifestyle, despite their fragmented genomes. The mutualistic relationship between Diachasmimorpha longicaudata and DlEPV represents a unique adaptation where the virus aids in the wasp's parasitism by producing virus-like particles within the wasp's reproductive tissues. In Gonatopus flavifemur, the evolution of venom and the development of chelae for grasping prey are significant adaptations that enhance its effectiveness as both a predator and a parasitoid (Kraaijeveld et al., 2016).

4.4 Implications for broader insect evolution

The findings from these case studies have broader implications for understanding insect evolution. The repeated evolution of the parasitoid lifestyle in different insect groups suggests a strong selective advantage and highlights the diverse genetic pathways that can lead to similar ecological outcomes. The mutualistic relationships with viruses, as seen in Diachasmimorpha longicaudata, underscore the importance of symbiotic associations in the evolution of parasitism. Additionally, the dual adaptations observed in Gonatopus flavifemur provide insights into the genetic basis of complex behaviors and the evolutionary pressures that drive the development of multifunctional traits. These studies collectively enhance our understanding of the genetic and morphological evolution of parasitic insects and their role in broader ecological and evolutionary contexts (Sevarika et al., 2020).

5 Integration of Genetic and Morphological Data

5.1 Correlating genetic and morphological evolution

The integration of genetic and morphological data is crucial for understanding the evolutionary history and diversification of parasitoid wasps. Combining these data types allows for a more comprehensive view of evolutionary relationships and adaptations, providing insights that might be missed when using a single data type alone. Correlating genetic and morphological evolution in parasitoid wasps has revealed significant insights into their diversification and adaptation strategies.

For instance, the study on chelonine parasitoid wasps utilized both molecular markers and morphological characters to elucidate their evolutionary relationships, highlighting the importance of integrating these data types to resolve phylogenetic uncertainties and propose taxonomic revisions (Werren et al., 2010). Similarly, the phylogenetic reassessment of the Platygastroidea superfamily combined molecular and morphological data to revise familial classifications and understand host group specificity. These studies demonstrate that morphological traits often correlate with genetic data, providing a robust framework for understanding evolutionary patterns (Blaimer et al., 2020).

5.2 Insights from molecular phylogenetics

Molecular phylogenetics has provided profound insights into the evolutionary history of parasitoid wasps. For example, the phylogenomic analysis of cynipoid wasps revealed a complex evolutionary history with significant implications for understanding their life strategies, such as parasitoidism and inquilinism1. Additionally, the phylogenetic analysis of cuckoo wasps using nuclear and mitochondrial genes uncovered artificial classifications at the genus level and provided a clearer understanding of their host associations. These molecular studies are essential for reconstructing evolutionary timelines and identifying key divergence events, as seen in the comprehensive phylogeny of chalcidoid wasps, which traced their diversification back to the late Jurassic (Michel-Salzat and Whitfield, 2004).

5.3 Evolutionary developmental biology (Evo-Devo) perspective

From an Evo-Devo perspective, the study of parasitoid wasps offers unique opportunities to understand the developmental mechanisms underlying their morphological and genetic diversity. The integration of genomic data has revealed how viral symbionts have shaped the evolution of parasitoid wasps, with some lineages incorporating viral elements into their genomes to aid in parasitism. This highlights the role of genetic innovation in the evolution of complex life history traits. Furthermore, the evolutionary history of Hymenoptera, including parasitoid wasps, underscores the transition from phytophagy to parasitoidism, driven by developmental and ecological factors9. These insights emphasize the importance of developmental biology in understanding the evolutionary trajectories of parasitoid wasps (Coffman and Burke, 2020).

5.4 Future research directions

Future research should focus on expanding the integration of genetic and morphological data across a broader range of parasitoid wasp species to refine phylogenetic relationships and uncover new evolutionary patterns. High-throughput sequencing technologies and advanced bioinformatics tools will be instrumental in this endeavor. Additionally, exploring the role of endosymbionts, such as Wolbachia, in shaping the genetic structure and reproductive strategies of parasitoid wasps will provide deeper insights into their evolutionary ecology (Werren and Loehlin, 2009). Investigating the developmental mechanisms underlying morphological adaptations through Evo-Devo approaches will further enhance our understanding of the evolutionary processes driving the diversity of parasitoid wasps (Muirhead et al., 2012).

6 Ecological and Evolutionary Implications

6.1 Impact of evolutionary changes on ecosystems

The evolutionary adaptations of parasitoid wasps have profound impacts on ecosystems. These insects play crucial roles in regulating the populations of their host species, which can significantly influence the structure and dynamics of ecological communities. For instance, the diversification of parasitoid wasps has been linked to the control of pest populations in agricultural settings, thereby maintaining the balance of ecosystems and promoting biodiversity (Bhattacharjee et al., 2023). The evolution of parasitoidism from phytophagy and predation has allowed these wasps to exploit a wide range of ecological niches, further enhancing their role in ecosystem stability (Samuel et al., 2018).

6.2 Co-evolution with host species

Parasitoid wasps and their hosts are engaged in a continuous evolutionary arms race, leading to intricate co-evolutionary dynamics. The genetic and morphological adaptations of parasitoid wasps are often mirrored by counter-adaptations in their hosts. For example, the presence of endosymbiotic bacteria such as Wolbachia in parasitoid wasps can influence host-parasitoid interactions by affecting reproductive compatibility and host specialization (Gabrieli et al., 2021). Additionally, the capture and maintenance of viral machinery by parasitoid wasps, such as Polydnaviruses and Virus-Like particles, highlight the complex co-evolutionary relationships that have evolved to enhance parasitism success (Simões et al., 2018).

6.3 Implications for biological control strategies

The evolutionary traits of parasitoid wasps make them highly effective biological control agents (Wu et al., 2019). Their ability to adapt to various hosts and environments allows for the targeted control of pest species, reducing the need for chemical pesticides and promoting sustainable agricultural practices (Belachew, 2018). The genetic diversity and specialized parasitic strategies of these wasps, such as the use of venom proteins to suppress host immune responses, further enhance their efficacy in biological control programs. Understanding the evolutionary history and genetic basis of these adaptations can inform the development of more effective and environmentally friendly pest management strategies (Altinli et al., 2021).

6.4 Conservation and biodiversity considerations

The conservation of parasitoid wasps is essential for maintaining biodiversity and ecosystem health (Wilke et al., 2020). These insects contribute to the natural regulation of pest populations and support the stability of food webs. However, habitat loss, climate change, and the use of chemical pesticides pose significant threats to their populations (Benelli et al., 2016). Conservation efforts should focus on preserving the habitats of parasitoid wasps and promoting practices that enhance their survival and effectiveness as biological control agents. Additionally, understanding the genetic and ecological factors that influence their diversity and distribution can aid in the development of conservation strategies that protect these vital components of biodiversity (Martinez et al., 2020).

Acknowledgments

We are 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 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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