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Special Issue "The Evolution of Pesticide Resistance"

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A special issue of Insects (ISSN 2075-4450). This special issue belongs to the section "Insect Pest and Vector Management".

Deadline for manuscript submissions: closed (31 March 2023) | Viewed by 13178

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Special Issue Editors

Dr. Qiang Xu

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Guest Editor

Department of Biology, Abilene Christian University, Abilene, TX 79699, USA
Interests: molecular mechanisms of pesticide resistance; functional genomics; proteomics; gene expression and regulation; antibody specificity; RNAi; CRISPR Therapeutics

Dr. Fang (Rose) Zhu

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Guest Editor

Department of Entomology, Pennsylvania State University, University Park, PA 16802, USA
Interests: xenobiotic adaptation; arthropod structural biology; functional genomics; insect toxicogenomics; insect molecular biophysics; enzyme chemistry

Dr. Ting Li

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Guest Editor

Department of Biological Sciences, Alabama State University, Montgomery, AL 36104, USA
Interests: organism adaption to environmental changes; insecticide resistance; insect toxicology and physiology; insect-plant interaction
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Arthropod pests cause substantial economic loss in agricultural and urban systems and could threaten food safety, nutrition, and human health. Pesticide application plays a critical role in the control of agricultural pests and disease vector populations. However, extensive application of pesticides accelerates the accumulation of resistance-associated genes in survivors. The development of pesticide resistance is a dynamic and complex process, depending on genetic, physiological, behavioral, and ecological factors, as well as operational factors, including the application timing, rate, coverage, and method. Additionally, increased usage of pesticides consequently damages ecological systems and non-target organisms. With the advance of genomic and post-genomic technologies, studies uncovering the genes, pathways, mechanisms, and ecological factors responsible for the evolution of pesticide resistance become promising. Further research on pesticide adaptation is of theoretical and applied importance in understanding the evolution of resistance and helping the development of more sustainable pest control strategies in the future.

Dr. Qiang Xu
Dr. Fang (Rose) Zhu
Dr. Ting Li
Guest Editors

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Keywords

insecticides
miticides
fungicides
herbicides
biopesticides
resistance mechanisms
target-site insensitivity
detoxification
plant allelochemicals
xenobiotic adaptation
symbionts
pollutants
circadian rhythms
climate change

Published Papers (12 papers)

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Research

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Open AccessArticle

Insecticide Resistance of Cimex lectularius L. Populations and the Performance of Selected Neonicotinoid-Pyrethroid Mixture Sprays and an Inorganic Dust

Jin-Jia Yu

Sabita Ranabhat

and

Changlu Wang

Insects 2023, 14(2), 133; https://doi.org/10.3390/insects14020133 - 27 Jan 2023

Viewed by 711

Abstract

Insecticide resistance is one of the factors contributing to the resurgence of the common bed bug, Cimex lectularius L. This study aimed to profile the resistance levels of field-collected C. lectularius populations to two neonicotinoids and one pyrethroid insecticide and the performance of selected insecticide sprays and an inorganic dust. The susceptibility of 13 field-collected C. lectularius populations from the United States to acetamiprid, imidacloprid, and deltamethrin was assessed by topical application using a discriminating dose (10 × LD₉₀ of the respective chemical against a laboratory strain). The RR₅₀ based on KT₅₀ values for acetamiprid and imidacloprid ranged from 1.0–4.7 except for the Linden 2019 population which had RR₅₀ of ≥ 76.9. Seven populations had RR₅₀ values of > 160 for deltamethrin. The performance of three insecticide mixture sprays and an inorganic dust were evaluated against three C. lectularius field populations. The performance ratio of Transport GHP (acetamiprid + bifenthrin), Temprid SC (imidacloprid + β-cyfluthrin), and Tandem (thiamethoxam + λ-cyhalothrin) based on LC₉₀ were 900–2017, 55–129, and 100–196, respectively. Five minute exposure to CimeXa (92.1% amorphous silica) caused > 95% mortality to all populations at 72 h post-treatment. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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Open AccessFeature PaperArticle

Fitness Cost of the Field-Evolved Resistance to Sulfoxaflor and Multi-Insecticide Resistance of the Wheat Aphid Sitobion miscanthi (Takahashi)

and

Insects 2023, 14(1), 75; https://doi.org/10.3390/insects14010075 - 12 Jan 2023

Viewed by 629

Abstract

Sulfoxaflor belongs to a new class of insecticides that is effective against many sap-feeding pests. In this study on Sitobion miscanthi (Takahashi) (i.e., the predominant wheat pest), a highly sulfoxaflor-resistant (SulR) population was obtained from a field. Its resistance to the other seven insecticides and its biological fitness were analyzed using a leaf-dip method and a two-sex life table approach, respectively. Compared with the relatively susceptible (SS) population, the SulR population was highly resistant to sulfoxaflor, with a relative insecticide resistance ratio (RR) of 199.8 and was moderately resistant to beta-cypermethrin (RR = 14.5) and bifenthrin (RR = 42.1) but exhibited low resistance to chlorpyrifos (RR = 5.7). Additionally, the SulR population had a relative fitness of 0.73, with a significantly prolonged developmental period as well as a lower survival rate and poorer reproductive performance than the SS population. In conclusion, our results suggest that S. miscanthi populations that are highly resistant to sulfoxaflor exist in the field. The possibility that insects may develop multi-resistance between sulfoxaflor and pyrethroids is a concern. Furthermore, the high sulfoxaflor resistance of S. miscanthi was accompanied by a considerable fitness cost. The study data may be useful for improving the rational use of insecticides and for exploring novel insecticide resistance mechanisms. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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Open AccessFeature PaperEditor’s ChoiceArticle

Cuticle Modifications and Over-Expression of the Chitin-Synthase Gene in Diflubenzuron-Resistant Phenotype

Valentina Lucchesi

Lorenzo Grimaldi

Valentina Mastrantonio

Daniele Porretta

Letizia Di Bella

Tania Ruspandini

Martino Luigi Di Salvo

and

Insects 2022, 13(12), 1109; https://doi.org/10.3390/insects13121109 - 30 Nov 2022

Viewed by 813

Abstract

Insecticide resistance is a major threat challenging the control of harmful insect species. The study of resistant phenotypes is, therefore, pivotal to understand molecular mechanisms underpinning insecticide resistance and plan effective control and resistance management strategies. Here, we further analysed the diflubenzuron (DFB)-resistant phenotype due to the point-mutation I1043M in the chitin-synthase 1 gene (chs1) in the mosquito Culex pipiens. By comparing susceptible and resistant strains of Cx. pipiens through DFB bioassays, molecular analyses and scanning electron microscopy, we showed that the I1043M-resistant mosquitoes have: (i) a striking level of DFB resistance (i.e., resistance ratio: 9006); (ii) a constitutive 11-fold over-expression of the chs1 gene; (iii) enhanced cuticle thickness and cuticular chitin content. Culex pipiens is one of the most important vector species in Europe and the rapid spread of DFB resistance can threaten its control. Our results, by adding new data about the DFB-resistant phenotype, provide important information for the control and management of insecticide resistance. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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Open AccessArticle

Detection of Chitin Synthase Mutations in Lufenuron-Resistant Spodoptera frugiperda in China

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Insects 2022, 13(10), 963; https://doi.org/10.3390/insects13100963 - 20 Oct 2022

Cited by 1 | Viewed by 927

Abstract

Spodoptera frugiperda (J. E. Smith), is commonly known as fall armyworm, native to tropical and subtropical regions of America, is an important migratory agricultural pest. It is important to understand the resistance and internal mechanism of action of S. frugiperda against lufenuron in China. Lufenuron is one of the main insecticides recommended for field use in China and has a broad prospect in the future. We conducted a bioassay using the diet-overlay method and found that the current S. frugiperda in China are still at a low level of resistance to lufenuron. Secondly, we examined whether the mutation I1040M (I1042M in Plutella xylostella), associated with lufenuron resistance, was produced in the field. And then we tested the expression of chitin synthase SfCHSA and SfCHSB in different tissues, and the changes of these two genes after lufenuron induction. The results showed that there is still no mutation generation in China and there is a significant change in the expression of SfCHSA under the effect of lufenuron. In conclusion, our study suggests that field S. frugiperda populations in 2019 and 2020 were less resistant to lufenuron. In fall armyworm, chitin synthases included SfCHSA and SfCHSB genes, and after induction treatment with lufenuron, the expression of the SfCHSA gene was significantly increased. In SfCHSA, no mutation has been detected in the site associated with lufenuron resistance. Secondly, in S. frugiperda larvae, the SfCHSA gene was the highest in the head of the larvae, followed by the integument; while the SfCHSB gene was mainly concentrated in the midgut. Therefore, we believe that the SfCHSA gene plays a greater role in the resistance of S. frugiperda to lufenuron than the SfCHSB gene. It is worth noting that understanding the level of resistance to lufenuron in China, the main mechanism of action of lufenuron on larvae, and the mechanism of resistance to lufenuron in S. frugiperda will help in crop protection as well as in extending the life span of this insecticide. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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Open AccessArticle

Sublethal and Transgenerational Toxicities of Chlorfenapyr on Biological Traits and Enzyme Activities of Paracoccus marginatus (Hemiptera: Pseudococcidae)

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Insects 2022, 13(10), 874; https://doi.org/10.3390/insects13100874 - 26 Sep 2022

Cited by 1 | Viewed by 829

Abstract

Papaya mealybug, Paracoccus marginatus Williams and Granara de Willink (Hemiptera: Pseudococcidae), is an economically important, invasive insect that is now distributed worldwide. Chlorfenapyr has been demonstrated to have a significant control effect on P. marginatus. In order to evaluate the sublethal and transgenerational effects of chlorfenapyr on P. marginatus, the life table data of three consecutive generations were collected and analyzed by the age stage, two-sex life table method, and the enzyme activities were assayed using a spectrophotometer. The results showed that exposure to the insecticide had significant effects on the biological traits of subsequent generations of P. marginatus, and a higher intrinsic rate of increase (r), finite rate of increase (λ), net reproductive rate (R₀), and a shorter mean generation time (T) were observed in the chlorfenapyr-treated F₁ mealybugs. Enzyme activity assays showed that chlorfenapyr significantly inhibited the activities of catalase (CAT) and peroxidase (POD) while activating the activities of superoxide dismutase (SOD), which suggested that SOD, CAT, and POD may play an important role in the self-defense of P. marginatus against chlorfenapyr. These results conclusively demonstrated that exposure of P. marginatus to sublethal concentrations of chlorfenapyr induced hormetic effects on the F₁ generation while having negative effects on the F₀ and F₃ generations. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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Open AccessArticle

Sensitivity Differences and Biochemical Characteristics of Laodelphax striatellus (Fallén) to Seven Insecticides in Different Areas of Shandong, China

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Insects 2022, 13(9), 780; https://doi.org/10.3390/insects13090780 - 29 Aug 2022

Cited by 2 | Viewed by 875

Abstract

Laodelphax striatellus Fallén is one of the main pests that can severely harm rice, corn, and wheat. Insecticides acting on the nicotinic acetylcholine receptor (nAChR) are the main type of pesticides used for the control of L. striatellus in Shandong Province, a major grain-producing region in China. In this study, the rice seedling dipping method was used to determine the sensitivities of six field L. striatellus populations in Shandong to seven insecticides acting on nAChR. The results showed that all the field populations were sensitive to clothianidin, nitenpyram, and triflumezopyrim, and the Jiaxiang population exhibited the lowest resistance ratio (RR) to imidacloprid, dinotefuran, sulfoxaflor, and thiamethoxam. The Donggang population showed a medium-level resistance to imidacloprid, with the highest RR of 17.48-fold. The Yutai population showed low-level resistance to imidacloprid and thiamethoxam, with RRs of 7.23- and 7.02-fold, respectively. The contents of cytochrome P450 monooxygenase (P450s), carboxylesterase (CarE), and glutathione S-transferase (GST) were the highest in the Donggang population and the lowest in the Jiaxiang population. The P450 gene CYP314A1 and the CarE gene LsCarE12 were highly up-regulated in all populations. No mutations of V62I, R81T, and K265E in the nAChR β1 subunit were found in any of the populations. These results provide valuable information for the strategies of resistance management of L. striatellus in the field. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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Open AccessArticle

Pyrethroids in an AlphaFold2 Model of the Insect Sodium Channel

Boris S. Zhorov

and

Ke Dong

Insects 2022, 13(8), 745; https://doi.org/10.3390/insects13080745 - 18 Aug 2022

Cited by 3 | Viewed by 1105

Abstract

Pyrethroid insecticides stabilize the open state of insect sodium channels. Previous mutational, electrophysiological, and computational analyses led to the development of homology models predicting two pyrethroid receptor sites, PyR1 and PyR2. Many of the naturally occurring sodium channel mutations, which confer knockdown resistance (kdr) to pyrethroids, are located within or close to these receptor sites, indicating that these mutations impair pyrethroid binding. However, the mechanism of the state-dependent action of pyrethroids and the mechanisms by which kdr mutations beyond the receptor sites confer resistance remain unclear. Recent advances in protein structure prediction using the AlphaFold2 (AF2) neural network allowed us to generate a new model of the mosquito sodium channel AaNav1-1, with the activated voltage-sensing domains (VSMs) and the presumably inactivated pore domain (PM). We further employed Monte Carlo energy minimizations to open PM and deactivate VSM-I and VSM-II to generate additional models. The docking of a Type II pyrethroid deltamethrin in the models predicted its interactions with many known pyrethroid-sensing residues in the PyR1 and PyR2 sites and revealed ligand-channel interactions that stabilized the open PM and activated VSMs. Our study confirms the predicted two pyrethroid receptor sites, explains the state-dependent action of pyrethroids, and proposes the mechanisms of the allosteric effects of various kdr mutations on pyrethroid action. The AF2-based models may assist in the structure-based design of new insecticides. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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Open AccessArticle

Large-Scale Monitoring of the Frequency of Ryanodine Receptor Target-Site Mutations Conferring Diamide Resistance in Brazilian Field Populations of Fall Armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae)

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Insects 2022, 13(7), 626; https://doi.org/10.3390/insects13070626 - 13 Jul 2022

Cited by 3 | Viewed by 1320

Abstract

Fall armyworm (FAW), Spodoptera frugiperda, is an important lepidopteran pest in the Americas, and recently invaded the Eastern Hemisphere. In Brazil, FAW is considered the most destructive pest of corn and cotton. FAW has evolved resistance to many insecticides and Bacillus thuringiensis (Bt) proteins. Here, a large-scale monitoring was performed between 2019 and 2021 to assess diamide insecticide susceptibility in more than 65 FAW populations sampled in corn and cotton. We did not detect a significant shift in FAW susceptibility to flubendiamide, but a few populations were less affected by a discriminating rate. F2 screen results of 31 selected FAW populations across regions confirmed that the frequency of diamide resistance alleles remained rather stable. Two laboratory-selected strains exhibited high resistance ratios against flubendiamide, and cross-resistance to anthranilic diamides. Reciprocal crosses indicated that resistance is autosomal and (incompletely) recessive in both strains. F1 backcrosses suggested monogenic resistance, supported by the identification of an I4734M/K target-site mutation in the ryanodine receptor (RyR). Subsequent genotyping of field-collected samples employing a TaqMan-based allelic discrimination assay, revealed a low frequency of RyR I4790M/K mutations significantly correlated with phenotypic diamide resistance. Our findings will help to sustainably employ diamides in FAW resistance management strategies across crops. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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Open AccessArticle

Characterization of Insecticide Response-Associated Transcripts in the Colorado Potato Beetle: Relevance of Selected Cytochrome P450s and Clothianidin

Raed Bouafoura

Pierre Bastarache

Brigitte Christelle Ouédraogo

and

Insects 2022, 13(6), 505; https://doi.org/10.3390/insects13060505 - 26 May 2022

Cited by 1 | Viewed by 1252

Abstract

The Colorado potato beetle (Leptinotarsa decemlineata (Say)) is known for its capacity to cause significant damages to potato crops worldwide. Multiple approaches have been considered to limit its spread including the use of a diverse arsenal of insecticides. Unfortunately, this insect frequently develops resistance towards these compounds. Investigating the molecular bases underlying the response of L. decemlineata against insecticides is of strong interest to ultimately devise novel and targeted approaches aimed at this pest. This work aimed to characterize, via qRT-PCR, the expression status of targets with relevance to insecticide response, including ones coding for cytochrome P450s, glutathione s-transferases, and cuticular proteins, in L. decemlineata exposed to four insecticides; chlorantraniliprole, clothianidin, imidacloprid, and spinosad. Modulation of levels associated with transcripts coding for selected cytochrome P450s was reported in insects treated with three of the four insecticides studied. Clothianidin treatment yielded the most variations in transcript levels, leading to significant changes in transcripts coding for CYP4c1, CYP4g15, CYP6a13, CYP9e2, GST, and GST-1-Like. Injection of dsRNA targeting CYP4c1 and CYP9e2 was associated with a substantial decrease in expression levels and was, in the case of the latter target, linked to a greater susceptibility of L. decemlineata towards this neonicotinoid, supporting a potential role for this target in clothianidin response. Overall, this data further highlights the differential expression of transcripts with potential relevance in insecticide response, as well as generating specific targets that warrant investigation as novel dsRNA-based approaches are developed against this insect pest. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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Open AccessArticle

Knockdown Resistance Mutations in the Voltage-Gated Sodium Channel of Aedes aegypti (Diptera: Culicidae) in Myanmar

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Insects 2022, 13(4), 322; https://doi.org/10.3390/insects13040322 - 25 Mar 2022

Cited by 2 | Viewed by 1485

Abstract

Aedes aegypti is an important mosquito vector transmitting diverse arboviral diseases in Myanmar. Pyrethroid insecticides have been widely used in Myanmar as the key mosquito control measure, but the efforts are constrained by increasing resistance. Knockdown resistance (kdr) mutations in the voltage-gated sodium channel (VGSC) are related to pyrethroid resistance in Ae. aegypti. We analyzed the patterns and distributions of the kdr mutations in Ae. aegypti in the Mandalay area of Myanmar. The segment 6 regions of domains II and III of vgsc were separately amplified from individual Ae. aegypti genomic DNA via polymerase chain reaction. The amplified gene fragments were sequenced. High proportions of three major kdr mutations, including S989P (54.8%), V1016G (73.6%), and F1534C (69.5%), were detected in the vgsc of Ae. aegypti from all studied areas. Other kdr mutations, T1520I and F1534L, were also found. These kdr mutations represent 11 distinct haplotypes of the vgsc population. The S989P/V1016G/F1534C was the most prevalent, followed by S989P/V1016V and V1016G/F1534C. A quadruple mutation, S989P/V1016G/T1520I/F1534C, was also identified. High frequencies of concurrent kdr mutations were observed in vgsc of Myanmar Ae. aegypti, suggesting a high level of pyrethroid resistance in the population. These findings underscore the need for an effective vector control program in Myanmar. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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Review

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Open AccessReview

Dynamic Roles of Insect Carboxyl/Cholinesterases in Chemical Adaptation

Casey Cruse

Timothy Walter Moural

and

Fang Zhu

Insects 2023, 14(2), 194; https://doi.org/10.3390/insects14020194 - 16 Feb 2023

Cited by 1 | Viewed by 693

Abstract

Insects have evolved several intricate defense mechanisms to adapt to their chemical environment. Due to their versatile capabilities in hydrolytic biotransformation, insect carboxyl/cholinesterases (CCEs) play vital roles in the development of pesticide resistance, facilitating the adaptation of insects to their host plants, and manipulating insect behaviors through the olfaction system. CCEs confer insecticide resistance through the mechanisms of qualitative or quantitative changes of CCE-mediated enhanced metabolism or target-site insensitivity, and may contribute to the host plant adaptation. CCEs represent the first odorant-degrading enzymes (ODEs) discovered to degrade insect pheromones and plant odors and remain the most promising ODE candidates. Here, we summarize insect CCE classification, currently characterized insect CCE protein structure characteristics, and the dynamic roles of insect CCEs in chemical adaptation. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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Open AccessReview

Insights into the Use of Eco-Friendly Synergists in Resistance Management of Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

Rana Muhammad Kaleem Ullah

and

Muhammad Nadir Naqqash

Insects 2022, 13(9), 846; https://doi.org/10.3390/insects13090846 - 16 Sep 2022

Cited by 1 | Viewed by 1197

Abstract

The Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say), is the most notorious insect pest of potato globally. Injudicious use of insecticides for management of this pest has resulted in resistance to all major groups of insecticides along with many human, animal health, and environmental concerns. Additionally, the input cost of insecticide development/discovery is markedly increasing because each year thousands of chemicals are produced and tested for their insecticidal properties, requiring billions of dollars. For the management of resistance in insect pests, synergists can play a pivotal role by reducing the application dose of most insecticides. These eco-friendly synergists can be classified into two types: plant-based synergists and RNAi-based synergists. The use of plant-based and RNAi-based synergists in resistance management of insect pests can give promising results with lesser environmental side effects. This review summarizes the resistance status of CPB and discusses the potential advantage of plant-based and RNAi-based synergists for CPB resistance management. It will motivate researchers to further investigate the techniques of using plant- and RNAi-based synergists in combination with insecticides. Full article

(This article belongs to the Special Issue The Evolution of Pesticide Resistance)

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