

Molecular Entomology, 2024, Vol. 15, No. 4 doi: 10.5376/me.2024.15.0016
Received: 16 May, 2024 Accepted: 24 Jun., 2024 Published: 08 Jul., 2024
Xu J., and Xu Q.B., 2024, Developmental biology and pest management: insights from cotton aphids, Molecular Entomology, 15(4): 129-137 (doi: 10.5376/me.2024.15.0016)
Cotton aphids (Aphis gossypii) represent a significant threat to global cotton production, necessitating effective pest management strategies. Understanding the developmental biology of cotton aphids is crucial for improving control measures. This study explores the life cycle, reproductive strategies, and genetic factors influencing the development of cotton aphids, alongside the impact of environmental conditions, and examines various pest management strategies, including chemical, biological, and integrated pest management (IPM) approaches, and their effectiveness at different developmental stages of the aphid. Advances in molecular techniques, such as genomic and transcriptomic approaches, RNA interference (RNAi), and CRISPR-Cas9 gene editing, are discussed in relation to their potential for enhancing pest control strategies. A case study demonstrates the application of developmental biology insights in real-world pest management scenarios, highlighting successes and areas for future research. This study aims to emphasize the importance of integrating developmental biology with pest management to address current challenges and advance cotton aphid control.
1 Introduction
Cotton aphids, Aphis gossypii, are significant agricultural pests that affect a wide range of crops, including cotton. These pests are known for their ability to cause direct damage to plants by feeding on their sap, which can lead to reduced plant vigor and yield. Additionally, cotton aphids are vectors for various plant viruses, further exacerbating their impact on crop health and productivity (Lagos-Kutz et al., 2021).
The management of cotton aphids has been challenging due to their rapid reproduction rates and the development of resistance to multiple insecticides (Chen et al., 2020). This resistance has necessitated the exploration of alternative pest management strategies, including biological control and cultural practices (Eid et al., 2018).
Understanding the developmental biology of cotton aphids is crucial for developing effective pest management strategies. The life cycle of A. gossypii, including its reproductive behavior and physiological adaptations, plays a significant role in its ability to infest and damage crops. For instance, the expression of specific genes, such as those in the Cytochrome P450 family, is linked to the aphid's ability to detoxify plant defenses and insecticides, thereby influencing its survival and fecundity (Gao et al., 2022).
Additionally, environmental factors such as rising atmospheric CO2 levels can affect the growth, development, and host-selection behavior of cotton aphids, potentially increasing their pest status under future climate conditions (Dai et al., 2018). By studying these biological and environmental interactions, researchers can identify vulnerabilities in the aphid's life cycle that can be targeted for more sustainable pest control methods.
This study reviews the current understanding of the developmental biology of cotton aphids and its implications for pest management. This includes examining the behavioral and physiological responses of A. gossypii to various environmental factors and control strategies. This study highlights the importance of integrating biological insights into pest management practices to develop more effective and sustainable approaches for controlling cotton aphid populations.
2 Developmental Biology of Cotton Aphids
2.1 Life cycle and reproductive strategies
Cotton aphids (Aphis gossypii) exhibit a complex life cycle characterized by both asexual and sexual reproduction, a phenomenon known as reproductive polyphenism. During favorable conditions, aphids reproduce asexually through viviparous parthenogenesis, allowing rapid population growth. However, in response to environmental cues such as shorter photoperiods in autumn, they switch to sexual reproduction, producing males and oviparous females that mate and lay overwintering eggs (Liu et al., 2014). This switch is regulated by changes in gene expression and hormonal signaling, particularly involving juvenile hormone (JH) (Trionnaire et al., 2012).
2.2 Morphological and physiological development
The development of cotton aphids includes distinct morphological changes, particularly in response to environmental conditions. Aphids can develop into winged or wingless morphs depending on factors such as population density, temperature, and host plant conditions. Winged morphs are typically produced under stressful conditions to facilitate dispersal and colonization of new plants (Ogawa and Miura, 2013). Physiologically, aphids adapt to their environment through changes in body weight, glycogen, body fat, and amino acid content, which are influenced by factors like atmospheric CO2 levels (Dai et al., 2018).
2.3 Genetic factors influencing development
Genetic factors play a crucial role in the development and adaptability of cotton aphids. The draft genome of A. gossypii has revealed insights into the genetic basis of their complex life cycle and adaptability. Key genes involved in detoxification, steroid biosynthesis, and ethylbenzene degradation have been identified, which are crucial for their survival and reproduction under varying environmental conditions (Quan et al., 2019). Additionally, differential gene expression studies have highlighted the role of odorant binding proteins (OBPs) and chemosensory proteins (CSPs) in host location and environmental interaction (Gu et al., 2013).
2.4 Impact of environmental conditions on development
Environmental conditions significantly impact the development and life history traits of cotton aphids. Rising atmospheric CO2 levels, for instance, enhance aphid activity and host selection ability, leading to increased body weight and energy reserves. Temperature fluctuations also affect aphid fitness, with extreme temperatures negatively impacting their survival and fecundity (Gao et al., 2018). These environmental factors not only influence the immediate physiological state of aphids but also drive evolutionary changes in their reproductive strategies and genetic architecture (Sandrock et al., 2011).
3 Pest Management Strategies Targeting Cotton Aphids
3.1 Chemical control methods
Chemical control methods have historically been a primary strategy for managing cotton aphids. In the Australian cotton industry, for example, aphids were effectively controlled using compounds targeted at other pests like Helicoverpa spp., as well as specific applications of dimethoate/omethoate and pirimicarb. However, prolonged use led to resistance in cotton aphids to these chemicals, necessitating the development of insecticide resistance management (IRM) strategies. These strategies included rotating insecticide modes of action and limiting the number of applications to manage resistance effectively (Herron and Wilson, 2017).
3.2 Biological control agents
Biological control plays a significant role in managing cotton aphids. In China, nearly 500 species of natural enemies have been reported in cotton systems, including arthropod predators, parasitoids, and microbial agents like fungi, bacteria, and viruses. Specific biological control agents such as Trichogramma spp., Microplitis mediator, and Bacillus thuringiensis have been mass-reared and commercially produced for use in cotton pest management. The implementation of Bt cotton has also contributed to reducing insecticide sprays, thereby increasing the abundance of natural enemies and preventing aphid outbreaks (Luo et al., 2014).
3.3 Integrated pest management (ipm) approaches
Integrated Pest Management (IPM) combines multiple strategies to manage pest populations effectively. In the context of cotton aphids, IPM strategies include the use of biological control, chemical control, and cultural practices. For instance, in Australia, an IPM strategy was developed that incorporated farm hygiene to reduce overwintering hosts for resistant aphids, conservation of natural enemies, and effective pest sampling and thresholds. This approach has been successful in recovering susceptibility to certain insecticides and managing resistance. Additionally, IPM strategies in China have been implemented across various regions, combining cultural, biological, physical, and chemical controls to manage cotton pests effectively.
3.4 Role of cultural practices in pest management
Cultural practices are essential components of pest management strategies. These practices include crop rotation, farm hygiene, and the use of resistant plant varieties. For example, in Australia, farm hygiene practices were incorporated into the IPM strategy to reduce overwintering hosts for resistant aphids, thereby minimizing the risk of aphid outbreaks. Moreover, cultural methods can support synergies between biological control and other pest management techniques, enhancing the overall effectiveness of pest management programs (Gurr and Kvedaras, 2010). In China, cultural practices have been integrated into IPM strategies to manage cotton pests, contributing to the overall success of pest management efforts.
4 Interaction between Developmental Biology and Pest Management
4.1 Influence of developmental stages on control efficacy
The developmental stages of cotton aphids significantly influence the efficacy of pest control measures. For instance, the early-stage defense mechanisms of cotton aphids against fungal infections involve up-regulation of immune responses and molting hormones, which can affect the success of biological control methods like entomopathogenic fungi (Figure 1) (Im et al., 2022). Additionally, the overexpression of certain genes, such as UDP-glycosyltransferases (UGTs), in different developmental stages can enhance detoxification processes, thereby increasing resistance to various insecticides (Chen et al., 2020). Understanding these developmental responses is crucial for optimizing the timing and type of pest control interventions.
Figure 1 Expression of insect hormone-related genes (Adopted from Im et al., 2022) Image caption: (A) Enriched insect hormone biosynthesis pathway; (B) Heatmap of insect hormone-related genes with expression level, and (C) Molting response in JEF-544-infected aphid as a defense behavior (Adopted from Im et al., 2022) |
The study of Im et al. (2022) illustrates the role of insect hormone-related genes in the molting process of aphids, particularly in response to infection by Beauveria bassiana (JEF-544). The pathway involved in ecdysone biosynthesis is highlighted, showing the critical enzymes and hormones that regulate molting. The heatmap indicates differential expression of key genes related to insect hormones, suggesting their involvement in the defense mechanism of the aphid during fungal infection. The diagram further demonstrates how the molting process is triggered as a protective response, showcasing the intricate hormonal signaling that underpins this adaptive behavior in aphids.
4.2 Timing of pest management interventions
The timing of pest management interventions is critical for maximizing their effectiveness. For example, the resistance management strategy for cotton aphids in Australian cotton fields emphasized the rotation of insecticide modes of action and limited the number of applications to prevent resistance buildup (Herron and Wilson, 2017). Similarly, rapid bioassays have been developed to quickly determine resistance levels, allowing for timely adjustments in pest management strategies (Ulusoy, 2023). Effective timing also involves considering the seasonal migration and life cycle of aphids, which can lead to rapid genetic diversity and resistance development.
4.3 Resistance development and management strategies
Resistance development in cotton aphids is a significant challenge that requires comprehensive management strategies. The overexpression of chemosensory proteins (CSPs) and UGTs has been linked to increased resistance to multiple insecticides, suggesting that these proteins could be targeted for developing new pest control methods (Li et al., 2021). Additionally, fitness costs associated with resistance, such as those observed with pirimicarb resistance, can be leveraged in resistance management. For instance, maintaining a population of susceptible aphids can help manage resistance by ensuring that resistant individuals face competitive disadvantages (Tieu et al., 2017). Integrated pest management (IPM) strategies that combine chemical, biological, and cultural controls are essential for sustainable resistance management (Erdős et al., 2021).
5 Advances in Molecular Techniques for Studying Cotton Aphid Development
5.1 Genomic and transcriptomic approaches
Recent advancements in genomic and transcriptomic techniques have significantly enhanced our understanding of cotton aphid development and their interaction with host plants. For instance, the identification and functional analysis of long non-coding RNAs (lncRNAs) in cotton under sap-sucking insect infestation have revealed critical insights. A study compared the transcriptome profiles of resistant and susceptible cotton cultivars under whitefly infestation, identifying 6,651 lncRNAs and 606 differentially expressed lncRNAs. This research highlighted the role of lncRNAs in modulating development and resistance to stimuli, providing a novel perspective on the cotton defense system against pests (Zhang et al., 2022).
5.2 Use of RNA interference (RNAi) in pest management
RNA interference (RNAi) has emerged as a promising tool for pest management, particularly in targeting specific genes in cotton aphids. Various studies have demonstrated the efficacy of RNAi in reducing aphid populations and increasing their susceptibility to insecticides. For example, RNAi targeting the CYP6CY3 gene in Aphis gossypii using a nanocarrier-based transdermal delivery system resulted in significant gene silencing and increased mortality rates. This approach also delayed developmental duration and reduced reproductive rates, indicating the potential of RNAi for controlling aphid populations (Linyu et al., 2021). Additionally, plant-mediated RNAi has been explored, where transgenic plants expressing dsRNA targeting essential aphid genes resulted in reduced progeny and increased aphid mortality (Pitino et al., 2011; Yu et al., 2016).
5.3 CRISPR-Cas9 and gene editing applications
CRISPR-Cas9 technology has revolutionized functional genomics by enabling precise gene editing. Although its application in aphids presents challenges due to their unique reproductive cycles, significant progress has been made. A protocol for targeted mutagenesis in the pea aphid, Acyrthosiphon pisum, involved microinjection of CRISPR-Cas9 components into fertilized eggs, resulting in stable mutant lineages. This method demonstrated a mutation rate of 70%~80% before diapause and a germline transmission rate of around 35%, paving the way for functional studies through genome editing in aphids (Trionnaire et al., 2019). Furthermore, CRISPR-Cas9 has been used to knock out lncRNAs in cotton, revealing their role in the jasmonic acid-mediated signaling pathway and plant defense against aphid infestation (Figure 2).
Figure 2 Study on insect resistance of T1 transgenic lines (Adopted from Zhang et al., 2022) Image caption: (A) Statistics on the results of aphids in each line of lncD09 gene and picture of aphid infestations. (B) Statistics on the results of aphids in each line of lncA07 gene and picture of aphid infestations; Error bars represent the standard deviation of three biological replicates; **Represents p < 0.01, *represents 0.01<p<0.05 (Adopted from Zhang et al., 2022) |
The study of Zhang et al. (2022) presents a study on insect resistance in T1 transgenic lines by comparing aphid infestation between knockout plants and control plants. The bar charts indicate that the transgenic knockout lines (lncD09 and lncA07) exhibit significantly higher aphid infestations compared to the control Jin668 line. The accompanying photos visually confirm the increased susceptibility of the knockout plants to aphids. This suggests that the targeted lncD09 and lncA07 genes play a crucial role in conferring resistance to aphids, with the loss of these genes leading to higher vulnerability in the plants.
These molecular techniques collectively offer powerful tools for studying cotton aphid development and devising effective pest management strategies. By leveraging genomic, transcriptomic, RNAi, and CRISPR-Cas9 technologies, researchers can gain deeper insights into aphid biology and develop innovative approaches to mitigate their impact on cotton production.
6 Case Study
6.1 Overview of the case study
The cotton aphid is a significant agricultural pest affecting a variety of crops, including cotton. This case study explores the application of developmental biology insights to manage this pest effectively. The focus is on understanding the genetic, biochemical, and ecological aspects of A. gossypii to develop sustainable pest management strategies.
6.2 Application of developmental biology insights in pest management
Recent advancements in the genomic and transcriptomic analysis of A. gossypii have provided valuable insights into its biology and adaptation mechanisms. The draft genome of A. gossypii has revealed key pathways involved in detoxification and steroid biosynthesis, which are crucial for its survival and adaptation to various host plants (Quan et al., 2019). Additionally, the identification of specific cytochrome P450 genes, such as AgoCYP6CY19, has highlighted their role in detoxifying plant toxins, offering potential targets for pest control (Gao et al., 2022).
Behavioral studies have shown that A. gossypii responds differently to volatile organic compounds (VOCs) emitted by infested and uninfested cotton plants. This knowledge can be leveraged to develop pest management strategies that manipulate these chemical cues to deter aphid infestation. Furthermore, the use of entomopathogenic fungi, such as Beauveria bassiana and Lecanicillium attenuatum, has been explored as a biological control method. These fungi infect and kill aphids, providing an environmentally friendly alternative to chemical insecticides (Im et al., 2022).
6.3 Outcomes and lessons learned
The integration of genomic data with pest management practices has led to several promising outcomes. For instance, the silencing of the AgoCYP6CY19 gene in A. gossypii resulted in increased mortality and reduced fecundity, demonstrating the potential of targeting specific genes for pest control. The use of VOCs to manipulate aphid behavior has shown that infested plants emit compounds that can repel aphids, suggesting a novel approach to pest deterrence (Hegde et al., 2011).
However, the application of chemical insecticides, such as thiacloprid and deltamethrin, has raised concerns due to their negative impact on beneficial parasitoids like Aphidius flaviventris . This highlights the need for careful consideration of the ecological balance when implementing pest management strategies (Majidpour et al., 2020). The use of entomopathogenic fungi has shown varying levels of effectiveness depending on the developmental stage of the aphids, indicating that timing and application methods are critical for success (Kim and Roberts, 2012).
6.4 Implications for future research and practice
The insights gained from developmental biology and genomic studies of A. gossypii have significant implications for future research and pest management practices. Future research should focus on further elucidating the molecular mechanisms underlying aphid adaptation and resistance to both chemical and biological control methods. This could lead to the development of more targeted and sustainable pest management strategies. Additionally, the integration of chemical ecology with pest management practices offers a promising avenue for reducing aphid infestations without relying heavily on chemical insecticides. The use of VOCs and other semiochemicals to manipulate pest behavior could be further explored and optimized for field applications.
7 Challenges and Future Directions
7.1 Current challenges in cotton aphid management
Managing cotton aphids presents several significant challenges. One of the primary issues is the development of resistance to multiple insecticides, including neonicotinoids, pyrethroids, and organophosphates, which has been documented in various regions (Koo et al., 2014). This resistance complicates control efforts and necessitates the continuous development of new management strategies. Additionally, the use of insecticides can have unintended consequences on non-target organisms, such as beneficial predators like lady beetles (Cycloneda sanguinea) and parasitoids (Aphidius flaviventris), which are crucial for natural pest control (Majidpour et al., 2020). The ecological interactions between aphids, their host plants, and natural enemies are complex and can be disrupted by chemical treatments, leading to further challenges in integrated pest management (IPM) (Pachú et al., 2021).
7.2 Potential for emerging technologies
Emerging technologies offer promising avenues for improving cotton aphid management. Genomic and transcriptomic studies have provided valuable insights into the genetic basis of aphid resistance and adaptation, which can inform the development of targeted control methods (Li et al., 2013; Quan et al., 2019). For instance, the draft genome of A. gossypii has revealed key pathways involved in detoxification and resistance, such as UDP-glycosyltransferases and cytochrome P450 enzymes, which could be potential targets for novel insecticides or genetic interventions (Chen et al., 2020). Additionally, the use of entomopathogenic fungi, such as Beauveria bassiana, has shown potential as an environmentally friendly alternative to chemical insecticides, although further research is needed to optimize their application and understand their interactions with aphid physiology (Im et al., 2022).
7.3 Future research priorities in developmental biology and pest management
Future research in developmental biology and pest management should focus on several key areas. First, there is a need to further elucidate the molecular mechanisms underlying aphid resistance and adaptation to different host plants and environmental conditions. This includes studying the genetic and epigenetic factors that contribute to resistance and exploring the potential for gene editing technologies to disrupt these mechanisms (Zhang et al., 2021). Second, research should aim to develop and refine IPM strategies that integrate biological control agents, such as parasitoids and predators, with reduced-risk insecticides and cultural practices to minimize resistance development and environmental impact (Herron and Wilson, 2017). Finally, there is a need to investigate the ecological interactions between aphids, their host plants, and natural enemies in greater detail to understand how these relationships can be leveraged to enhance pest control while preserving ecosystem health (Cunha et al., 2022). By addressing these research priorities, we can develop more sustainable and effective approaches to managing cotton aphids and other agricultural pests.
Acknowledgments
Thanks to the reviewers for their feedback on the manuscript; their valuable suggestions have enhanced the quality of the article.
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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