1 Introduction

Aphids (Hemiptera: Aphididae) are a diverse group of plant-feeding insects that have undergone rapid adaptive radiation, particularly during the Late Cretaceous period (Julca et al., 2019). This rapid diversification has resulted in a complex phylogenetic structure that has been challenging to resolve using traditional morphological methods alone (Ortiz-Rivas and Martínez-Torres, 2010; Owen and Miller, 2022). Aphids are known for their significant impact on agriculture, both as direct pests and as vectors of plant diseases, making them a critical focus of entomological and agricultural research (Simon and Peccoud, 2018).

Understanding the phylogenetic relationships among aphid lineages is crucial for several reasons. Firstly, it provides insights into the evolutionary history and adaptive mechanisms of these insects, which are essential for developing effective pest management strategies (Loxdale et al., 2020). Secondly, phylogenetic studies can help clarify taxonomic ambiguities that arise due to the morphological plasticity and phenotypic convergence observed in aphids (Nováková et al., 2013; D’acier et al., 2014). Finally, a robust phylogenetic framework can facilitate the identification of key genetic and molecular traits that contribute to the ecological success and pest status of aphids (Ren et al., 2017; Song et al., 2019).

This study synthesizes current knowledge on the phylogenetic relationships among major aphid lineages by integrating molecular and morphological data. This study provides a comprehensive overview of the latest findings from phylogenomic studies, highlights the challenges posed by gene tree discordance and introgression, and discusses the implications of these findings for aphid taxonomy and evolutionary biology. Additionally, this study seeks to identify gaps in the current understanding and propose directions for future research to further elucidate the complex phylogeny of aphids.

2 Overview of Aphid Diversity

2.1 Major aphid families

Aphids, belonging to the family Aphididae, are a diverse group of plant-feeding insects known for their complex life cycles and significant agricultural impact. Aphididae, the primary family within the superfamily Aphidoidea, is divided into several subfamilies and tribes. Recent phylogenetic studies have identified three main lineages within Aphididae: A+D, E+T, and L. The A+D lineage includes subfamilies such as Aphidinae, Calaphidinae, Chaitophorinae, Drepanosiphinae, and Pterocommatinae. The E+T lineage comprises Anoeciinae, Eriosomatinae, Hormaphidinae, Mindarinae, and Thelaxinae, while the L lineage is represented solely by the subfamily Lachninae (Ortiz-Rivas and Martínez-Torres, 2010; Owen and Miller, 2022).

2.2 Key morphological traits

Aphids exhibit a range of morphological traits that are influenced by both biotic and abiotic factors. These traits include the presence of siphunculi (cornicles), which are tubular structures on the abdomen, and variations in wing morphology. The tribe Eriosomatini, for example, is known for inducing leaf galls on their primary host plants, such as Ulmus and Zelkova, with gall morphology ranging from leaf-roll types to completely enclosed pouch types (Sano and Akimoto, 2011). Additionally, the extinct family Oviparosiphidae, characterized by the presence of both ovipositor and siphunculi, highlights the morphological diversity and evolutionary history of aphids (Żyła et al., 2017).

2.3 Geographic distribution

Aphids are predominantly found in temperate regions, with their distribution closely tied to the availability of host plants. The biogeographic origins and diversification of aphids are linked to their host plants, with major divergences occurring during the Middle to Late Tertiary. For instance, the tribe Aphidini, which includes the genus Aphis, shows a biogeographic separation into Nearctic, Western Palearctic, and Eastern Palearctic regions (Kim et al., 2011). The Rhus gall aphids, part of the subtribe Melaphidina, exhibit an intercontinental distribution between eastern Asia and North America, with evolutionary relationships suggesting a divergence around the early Paleocene (Ren et al., 2017; Ren et al., 2019). In summary, the diversity of aphids is reflected in their complex phylogenetic relationships, varied morphological traits, and widespread geographic distribution. Understanding these aspects is crucial for comprehending the evolutionary history and ecological significance of this group of insects.

3 Molecular Phylogenetics

3.1 DNA sequencing techniques

DNA sequencing techniques have been pivotal in elucidating the phylogenetic relationships among aphid lineages. Various methods, including Sanger sequencing and next-generation sequencing (NGS) technologies, have been employed to generate comprehensive molecular data. For instance, the study by Bai et al. (2010) utilized both Roche-454 and Illumina GA-II platforms to develop extensive transcriptomic and genomic resources for the invasive soybean aphid, Aphis glycines. Similarly, Owen and Miller (2022) leveraged genome and transcriptome data to estimate phylogenomic relationships among aphid subfamilies, highlighting the utility of NGS in resolving complex phylogenetic questions.

3.2 Molecular markers used in aphid studies

Molecular markers such as mitochondrial genes and nuclear sequences have been extensively used in aphid phylogenetic studies. The mitochondrial cytochrome oxidase I (COI) gene is a commonly used marker due to its high variability and ease of amplification, as demonstrated by Abdulla Agha et al. (2023), who used COI gene sequencing to infer relationships among aphid species in Kurdistan. Additionally, Ortiz-Rivas and Martínez-Torres (2010) employed nuclear sequences like the long-wavelength opsin gene and elongation factor 1 alpha gene, along with mitochondrial genes, to analyze the phylogeny of major aphid taxa. These markers provide robust data for constructing phylogenetic trees and understanding evolutionary relationships.

3.3 Phylogenetic tree construction

Data collection for phylogenetic studies involves the extraction and sequencing of DNA from various aphid species. For example, Nováková et al. (2019) analyzed 255 Buchnera gene sequences from 70 host aphid species to compare symbiont-derived phylogenies with those obtained from aphid sequences. The preparation of these sequences often includes alignment and comparison with existing databases, such as NCBI GenBank, to ensure accuracy and completeness.

Phylogenetic inference methods include Bayesian inference (BI), Maximum Likelihood (ML), and parsimony analyses. These methods are used to construct phylogenetic trees and infer evolutionary relationships. For instance, Chen et al. (2017) utilized multiple data sets and model-based methods to perform phylogenetic inferences, resulting in well-supported backbone relationships for major aphid lineages. Similarly, Ren et al. (2017) employed BI, ML, and parsimony analyses of mitochondrial genome data to examine the evolutionary relationships within Melaphidina aphids.

Selecting appropriate models and validating phylogenetic trees are crucial steps in ensuring the reliability of phylogenetic inferences. Studies often compare different models and partitioning schemes to identify the best fit for their data. For example, Wei et al. (2019) used both BI and ML analyses to validate their phylogenetic findings, while Zhang et al. (2022) provided comparative genomic analyses to investigate the evolution of unique features in aphid mitogenomes . These approaches help in refining phylogenetic hypotheses and improving the accuracy of evolutionary interpretations.

4 Morphological Phylogenetics

4.1 Morphological character selection

Morphological character selection is a critical step in constructing phylogenetic trees, especially for groups like aphids where rapid diversification has led to significant morphological variation. In the study of gall-forming aphids of the tribe Eriosomatini, 52 morphological characters were selected to infer phylogenetic relationships, highlighting the importance of detailed morphological data in understanding evolutionary changes in aphid-host associations and gall morphology (Sano and Akimoto, 2011). Similarly, the analysis of extinct aphid taxa, such as the family Oviparosiphidae, utilized morphological data to challenge the presumed monophyly of this group, demonstrating the necessity of careful character selection to resolve phylogenetic relationships (Żyła et al., 2017).

4.2 Comparative morphology

Comparative morphology involves analyzing and comparing the morphological traits of different species to infer their evolutionary relationships. For instance, the study on European species of the genus Aphidius used geometric morphometrics to explore morphological divergences in forewing size, finding significant differences in mean wing shape between species (Mitrovski-Bogdanović et al., 2021). This approach helps in identifying phylogenetically informative characters and understanding the morphological evolution within a group. Additionally, the phylogeny of drepanosiphine aphids was reconstructed using a combination of molecular and 64 morphological and biological characteristics, providing a comprehensive view of their evolutionary relationships (Du et al., 2021).

4.3 Integrating morphological data

Integrating morphological data with molecular data can enhance the resolution and robustness of phylogenetic trees. The study on the phylogeny of drepanosiphine aphids combined four molecular genes with morphological data, resulting in well-supported phylogenetic inferences that clarified the taxonomic status of various subfamilies (Du et al., 2021). Similarly, the phylogenetic analysis of gall-forming aphids integrated morphological characters with molecular data, supporting the monophyly of the Eriosomatini and providing insights into the evolution of aphid-host associations. These examples underscore the value of integrating multiple data types to achieve a more accurate and comprehensive understanding of phylogenetic relationships.

5 Combined Analysis of Molecular and Morphological Data

5.1 Advantages of combined approaches

Combining molecular and morphological data in phylogenetic studies offers several advantages. Firstly, it allows for a more comprehensive understanding of evolutionary relationships by integrating different types of information (Lagos et al., 2014). Molecular data, such as DNA sequences, provide insights into genetic relationships and evolutionary history that may not be evident from morphology alone. Conversely, morphological data can offer context and validation for molecular findings, especially in cases where molecular data might be limited or ambiguous. For instance, the study by Ortiz-Rivas and Martínez-Torres (2010) demonstrated that combining nuclear and mitochondrial sequences helped to confirm the existence of three main lineages in aphid phylogeny, which was consistent with previous morphological classifications. Similarly, Du et al. (2021) showed that integrating molecular genes and morphological characteristics clarified the phylogenetic relationships among drepanosiphine aphids, supporting their classification at the subfamily level.

5.2 Case studies

Several case studies highlight the effectiveness of combined approaches in aphid phylogenetics. The research by Ren et al. (2019) on Melaphidina aphids used both nuclear and mitochondrial DNA data alongside morphological traits to resolve phylogenetic relationships, resulting in well-supported topologies and taxonomic revisions (Figure 1). Another example is the study by Mitrovski-Bogdanović et al. (2021), which analyzed molecular and morphological variation among European species of the genus Aphidius. This study found significant congruence between molecular phylogenies and morphological divergences, particularly in well-resolved groups, demonstrating the utility of combined data in resolving phylogenetic relationships. Additionally, Żyła et al. (2017) utilized morphological data from extinct aphid taxa to complement molecular analyses, revealing the polyphyly of the extinct family Oviparosiphidae and providing insights into early aphid evolution.

The phylogenetic tree illustrates the evolutionary relationships among Melaphidina aphids using a combined dataset of mitochondrial and nuclear gene sequences. The tree is rooted with Baizongia pistaciae as the outgroup. The nodes marked with stars indicate high support, showing Bayesian posterior probabilities (PP) of 1.00 and bootstrap values (BS) of 100%, highlighting strong confidence in these branching points. The tree demonstrates distinct clades within Melaphidina, with species like Melaphis rhois, Floraphis choui, and others forming separate branches. The Kaburagia rhusicola species complex appears closely related, indicating recent diversification. The tree structure suggests that certain morphological and ecological traits have evolved within specific lineages, as reflected by the images of aphids and their associated host plants. This phylogenetic analysis provides insights into the genetic diversity and evolutionary history of Melaphidina aphids, underscoring the role of both mitochondrial and nuclear genes in resolving their evolutionary relationships.

5.3 Challenges and limitations

Despite the advantages, there are challenges and limitations to combining molecular and morphological data. One major challenge is the potential for incongruence between molecular and morphological phylogenies, which can complicate the interpretation of results. For example, Owen and Miller (2022) highlighted issues of gene tree discordance and introgression, which can obscure phylogenetic relationships even when using extensive genomic data. Another limitation is the difficulty in obtaining comprehensive morphological data for all taxa, particularly for extinct or poorly preserved specimens. The study by Chen et al. (2017) on mitochondrial genome sequences noted that while molecular data provided robust phylogenetic frameworks, the lack of corresponding morphological data for some taxa limited the overall resolution. Additionally, Agha et al. (2023) pointed out that hybridization and introgression events can lead to low resolution in molecular phylogenies, necessitating careful consideration of both data types to avoid misleading conclusions.

6 Phylogenetic Insights and Evolutionary Patterns

6.1 Divergence times and evolutionary rates

The divergence times of aphid lineages have been a focal point in understanding their evolutionary history. Most generic divergences in the tribe Aphidini occurred in the Middle Tertiary, with species-level divergences happening between the Middle and Late Tertiary. This period coincides with the diversification of their primary hosts, mainly in the Rosaceae family, and the emergence of secondary hosts such as Poaceae (Kim et al., 2011). Similarly, the subfamily Hormaphidinae experienced tribal diversification during the Late Cretaceous, aligning with the appearance of their primary host plants (Huang et al., 2012). These findings suggest that the evolutionary rates of aphids are closely tied to the availability and diversification of their host plants.

6.2 Biogeographical patterns

The biogeographical origins and patterns of aphid lineages reveal significant insights into their evolutionary trajectories. The major lineages within Aphidina likely separated into Nearctic, Western Palearctic, and Eastern Palearctic regions (Kim et al., 2011). The Rhus gall aphids, for instance, show a clear biogeographical split between North American and Eastern Asian species, with the North American Melaphis diverging from its closest Asian relatives around the early Paleocene (Ren et al., 2017). This intercontinental biogeographical pattern highlights the historical dispersal and subsequent isolation of aphid lineages.

6.3 Co-evolution with host plants

Aphids exhibit a complex co-evolutionary relationship with their host plants, which has significantly influenced their diversification. Host plants impose considerable selective pressure on aphids, leading to strong evolutionary commitments in host plant choice (Peccoud et al., 2010). For example, the Aphis gossypii group shows evidence of primary host shifts and hybridization between sympatric species, indicating ecological specialization through host-associated speciation (Lee et al., 2021). Additionally, the phylogenetic congruence between aphids and their endosymbionts, such as Buchnera, supports the parallel evolution of these organisms, further emphasizing the role of host plants in shaping aphid evolution (Liu et al., 2013; Nováková et al., 2013). The diversification of Japanese Stomaphis aphids, primarily driven by host plant shifts, occasionally occurred between distantly related host plant taxa, underscoring the adaptability and evolutionary plasticity of aphids in response to their host plants  (Yamamoto et al., 2020).

7 Applications of Phylogenetic Studies

7.1 Implications for pest management

Phylogenetic studies of aphids have significant implications for pest management strategies. By understanding the evolutionary relationships among aphid species, researchers can develop more targeted and effective pest control methods. For instance, the identification of genetic similarities among pest species can lead to the development of broad-spectrum pesticides that are effective against multiple aphid pests. Additionally, phylogenetic insights can help in predicting the spread of pest species and their potential impact on agriculture. For example, the study of the mitochondrial genome of the soybean aphid (Aphis glycines) provides valuable information on its genetic makeup, which can be used to develop specific pest management strategies (Song et al., 2019). Similarly, the diversity and phylogenetic relationships of aphid pests in Bangladesh highlight the need for integrated pest management programs that consider the genetic relatedness of different aphid species (Af, 2016).

7.2 Conservation strategies

Phylogenetic studies also play a crucial role in conservation strategies for aphids and their associated ecosystems. By understanding the evolutionary history and relationships of aphid species, conservationists can identify key species and lineages that are critical for maintaining biodiversity. For example, the phylogenetic analysis of aphids using mitochondrial genome sequences has revealed deep branching events and the evolutionary significance of certain subfamilies, such as Mindarinae and Eriosomatinae (Chen et al., 2017). This information can be used to prioritize conservation efforts for these subfamilies and their habitats. Additionally, the study of extinct aphid families, such as Oviparosiphidae, provides insights into the historical diversity of aphids and the impact of past environmental changes on their evolution (Żyła et al., 2017). Such knowledge is essential for developing conservation strategies that aim to preserve the evolutionary potential of aphid species in the face of ongoing environmental changes.

7.3 Future Research Directions

Future research in aphid phylogenetics should focus on several key areas to further enhance our understanding of their evolutionary relationships and applications. First, there is a need for more comprehensive phylogenetic studies that incorporate both molecular and morphological data. The integration of these data types can provide a more robust and accurate picture of aphid evolution, as demonstrated by studies that combine genome and transcriptome data and those that use both nuclear and mitochondrial sequences.

The researchers should explore the role of symbiotic bacteria, such as Buchnera aphidicola, in aphid evolution. Studies of Nováková et al. (2013) have shown that symbiont-derived phylogenies can provide valuable insights into aphid phylogeny and evolution. Finally, future research should investigate the functional significance of unique genetic features, such as the repeat regions in aphid mitochondrial genomes. Understanding the evolution and function of these regions can shed light on the genetic mechanisms underlying aphid diversification and adaptation.

Acknowledgments

Sincerely thank the two anonymous peer reviewers for their feedback on 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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