The evolution of insecticide resistance: Have the insects won?

While insecticides have greatly improved human health and agricultural production worldwide, their utility has been limited by the evolution of resistance in many major pests, including some that became pests only as a result of insecticide use. Insecticide resistance is both an interesting example of the adaptability of insect pests, and, in the design of resistance management programmes, a useful application of evolutionary biology. Pest susceptibility is a valuable natural resource that has been squandered; at the same time, it is becoming increasingly expensive to develop new insecticides. Pest control tactics should therefore take account of the possibility of resistance evolution. One of the best ways to retard resistance evolution is to use insecticides only when control by natural enemies fails to limit economic damage. This review summarizes the recent literature on insecticide resistance as an example of adaptation, and demonstrates how population genetics and ecology can be used to manage the resistance problem.     

迁移对害虫抗性演化的影响

利用抗性群体遗传模型研究了迁移对害虫抗性演化的影响。模拟结果表明,迁入比例对害虫种群抗性演化的影响存在一定的阈值。若迁入个体全为敏感(SS)纯合子,而其比例又在阈值以下时,这种迁入对抗性演化无延缓作用;迁入比例在阈值以上时,随比例加大,对抗性延缓作用逐渐增强,加大到某一值时,抗性演化可完全被阻止;若迁入个体携有R基因,则迁入比例在阈值以下时,会促进迁入区害虫种群的抗性演化;在阈值以上时,可延缓或完全阻止害虫种群的抗性演化。处理区害虫种群原有个体的迁出,可加强SS个体迁入对害虫种群抗性演化的影响,而使携R基因的个体的迁入影响减弱。以小菜蛾Plutella xylostella为模型昆虫所作的试验结果表明,模型模拟与验证试验的结果具有较好的一致性,说明抗性模拟模型可用于害虫种群的抗性演化预测和分析。     

Delayed action insecticides and their role in mosquito and malaria control

There is considerable interest in the management of insecticide resistance in mosquitoes. One possible approach to slowing down the evolution of resistance is to use late-life-acting (LLA) insecticides that selectively kill only the old mosquitoes that transmit malaria, thereby reducing selection pressure favoring resistance. In this paper we consider an age-structured compartmental model for malaria with two mosquito strains that differ in resistance to insecticide, using an SEI approach to model malaria in the mosquitoes and thereby incorporating the parasite developmental times for the two strains. The human population is modeled using an SEI approach. We consider both conventional insecticides that target all adult mosquitoes, and LLA insecticides that target only old mosquitoes. According to linearised theory the potency of the insecticide affects mainly the speed of evolution of resistance. Mutations that confer resistance can also affect other parameters such as mean adult life span and parasite developmental time. For both conventional and LLA insecticides the stability of the malaria-free equilibrium, with only the resistant mosquito strain present, depends mainly on these other parameters. This suggests that the main long term role of an insecticide could be to induce genetic changes that have a desirable effect on a vital parameter such as adult life span. However, when this equilibrium is unstable, numerical simulations suggest that a potent LLA insecticide can slow down the spread of malaria in humans but that the timing of its action is very important.     

Multiple Resistances and Complex Mechanisms of Anopheles sinensis Mosquito: A Major Obstacle to Mosquito-Borne Diseases Control and Elimination in China

Malaria, dengue fever, and filariasis are three of the most common mosquito-borne diseases worldwide. Malaria and lymphatic filariasis can occur as concomitant human infections while also sharing common mosquito vectors. The overall prevalence and health significance of malaria and filariasis have made them top priorities for global elimination and control programmes. Pyrethroid resistance in anopheline mosquito vectors represents a highly significant problem to malaria control worldwide. Several methods have been proposed to mitigate insecticide resistance, including rotational use of insecticides with different modes of action. Anopheles sinensis, an important malaria and filariasis vector in Southeast Asia, represents an interesting mosquito species for examining the consequences of long-term insecticide rotation use on resistance. We examined insecticide resistance in two An. Sinensis populations from central and southern China against pyrethroids, organochlorines, organophosphates, and carbamates, which are the major classes of insecticides recommended for indoor residual spray. We found that the mosquito populations were highly resistant to the four classes of insecticides. High frequency of kdr mutation was revealed in the central population, whereas no kdr mutation was detected in the southern population. The frequency of G119S mutation in the ace-1 gene was moderate in both populations. The classification and regression trees (CART) statistical analysis found that metabolic detoxification was the most important resistance mechanism, whereas target site insensitivity of L1014 kdr mutation played a less important role. Our results indicate that metabolic detoxification was the dominant mechanism of resistance compared to target site insensitivity, and suggests that long-term rotational use of various insecticides has led An. sinensis to evolve a high insecticide resistance. This study highlights the complex network of mechanisms conferring multiple resistances to chemical insecticides in mosquito vectors and it has important implication for designing and implementing vector resistance management strategies.     

天敌昆虫抗药性研究进展

天敌昆虫抗药性研究在协调害虫化学防治和生物防治中有着重要的理论和现实意义,其研究的最终目的在于更好地推进抗性天敌在害虫综合治理(IPM)中的应用。抗药性天敌昆虫具有潜在的巨大价值。鉴于此,本文系统地综述了天敌昆虫抗药性最新研究进展,包括杀虫剂对天敌昆虫的影响、天敌昆虫抗药性现状、抗药性机理和限制天敌昆虫抗药性发展因素等。文章最后还对抗药性天敌昆虫的应用前景进行了展望。     

Evolution of insecticide resistance in non-target black flies (Diptera: Simuliidae) from Argentina

Black flies, a non-target species of the insecticides used in fruit production, represent a severe medical and veterinary problem. Large increases in the level of resistance to the pyrethroids fenvalerate (more than 355-fold) and deltamethrin (162-fold) and a small increase in resistance to the organophosphate azinphos methyl (2-fold) were observed between 1996-2008 in black fly larvae under insecticide pressure. Eventually, no change or a slight variation in insecticide resistance was followed by a subsequent increase in resistance. The evolution of pesticide resistance in a field population is a complex and stepwise process that is influenced by several factors, the most significant of which is the insecticide selection pressure, such as the dose and frequency of application. The variation in insecticide susceptibility within a black fly population in the productive area may be related to changes in fruit-pest control. The frequency of individuals with esterase activities higher than the maximum value determined in the susceptible population increased consistently over the sampling period. However, the insecticide resistance was not attributed to glutathione S-transferase activity. In conclusion, esterase activity in black flies from the productive area is one mechanism underlying the high levels of resistance to pyrethroids, which have been recently used infrequently. These enzymes may be reselected by currently used pesticides and enhance the resistance to these insecticides.     

昆虫抗药性产生机制

杀虫剂是害虫防治的有效途径之一,但随着杀虫剂长期和广泛的使用,昆虫种群对各种杀虫剂的敏感性降低,产生了抗药性,如何克服昆虫的抗药性是害虫综合治理的重要问题。近年来,借助基因组测序和遗传操作技术的发展,对昆虫抗药性的研究已经深入到细胞水平和分子水平,取得诸多重要的突破,为害虫抗性的控制奠定了理论基础。本文从常见杀虫剂的历史沿革及作用机理切入,从靶标抗性、代谢抗性和穿透抗性3个方面阐述了杀虫剂抗性产生的机制:杀虫剂作用位点的突变降低了靶标与杀虫剂的亲和力,细胞色素P450酶系和谷胱甘肽转移酶系的激活增加了杀虫剂的降解,表皮结构成分的变化和ABC转运蛋白的增加有效阻挡了杀虫剂的渗入。利用基因操作手段或抑制剂,对上述3种抗性机制的关键步骤进行调控可能成为未来杀虫剂抗性控制的新策略。     

The importance of modelling the spread of insecticide resistance in a heterogeneous environment: the example of adding synergists to bed nets

ABSTRACT: BACKGROUND: Insecticides are an effective and practical tool for reducing malaria transmission but the development of resistance to the insecticides can potentially compromise controls efforts. In this study a mathematical model was developed to explore the effects on mosquito populations of spatial heterogeneous deployment of insecticides. This model was used to identify important parameters in the evolution of insecticide resistance and to examine the contribution of new generation long-lasting insecticidal bed nets, that incorporate a chemical synergist on the roof panel, in delaying insecticide resistance. METHODS: A genetic model was developed to predict changes in mosquito fitness and resistance allele frequency. Parameters describing insecticide selection, fitness cost and the additional use of synergist were incorporated. Uncertainty and sensitivity analysis were performed followed by investigation of the evolution of resistance under scenarios of fully effective or ineffective synergists. RESULTS: The spread of resistance was most sensitive to selection coefficients, fitness cost and dominance coefficients while mean fitness was most affected by baseline fitness levels. Using a synergist delayed the spread of resistance but could, in specific circumstances that were thoroughly investigated, actually increase the rate of spread. Different spread dynamics were observed, with simulations leading to fixation, loss and most interestingly, equilibrium (without explicit overdominance) of the resistance allele. CONCLUSIONS: This strategy has the potential to delay the spread of resistance but note that in an heterogeneous environment it can also lead to the opposite effect, i.e., increasing the rate of spread. This clearly emphasizes that selection pressure acting inside the house cannot be treated in isolation but must be placed in context of overall insecticide use in an heterogeneous environment.     

The impact of insecticide resistance in the currant-lettuce aphid, Nasonovia ribisnigri, on pest management in lettuce

Abstract 1 This paper reports on experiments to determine how two different insecticide resistance phenotypes in the aphid Nasonovia ribisnigri (Mosley), which is a major pest of lettuce, change its susceptibility to pyrethroid insecticides and the carbamate pirimicarb. 2 A novel statistical approach determined how the effectiveness of different insecticides was changed by the two resistance phenotypes. This compared the between‐plant distribution of aphid numbers, as opposed to the mean number of aphids per plant. 3 Results from field cage experiments showed that the effect of the resistances differed. Pyrethroid resistance resulted in lower mortality immediately after application of pyrethroids, whereas resistance to pirimicarb shortened the time over which the chemical was effective. 4 The results of laboratory bioassays suggested that these two resistances were not found together in N. ribisnigri. However, the results reported here contradict this assertion. 5 Experiments with insecticide residues showed that reproduction of resistant N. ribisnigri was greater than that of susceptible N. ribisnigri on plants with ageing insecticide residues, even in circumstances where mortality of resistant and susceptible clones of N. ribisnigri were similar. 6 If more than a few aphids are found on a plant then a whole consignment can be rejected for processing. The results reported here suggest that the effect of both insecticide resistances in N. ribsinigri will be to increase the proportion of lettuce heads with an unacceptable number of aphids on them, leading to increased rejection of plants for processing.     

Combining zooprophylaxis and insecticide spraying: a malaria-control strategy limiting the development of insecticide resistance in vector mosquitoes

Strategies to eradicate the vector-borne infectious diseases (e.g. malaria and Japanese encephalitis) are often directed at controlling vectors with insecticides. Spraying insecticide, however, opens the way for the development of insecticide resistance in vectors, which may lead to the failure of disease control. In this paper, we examine whether the combined use of insecticide spray and zooprophylaxis can limit the development of insecticide resistance in mosquitoes. Zooprophylaxis refers to the control of vector-borne diseases by attracting vectors to domestic animals in which the pathogen cannot amplify (a dead-end host). The human malaria parasite Plasmodium spp. has a closed transmission cycle between humans and mosquitoes, and hence cattle can serve as a dead-end host. Our model reveals that, by a suitable choice of insecticide spraying rate and cattle density and location, malaria can, in some situations, be controlled without mosquitoes developing insecticide resistance.     

杀虫剂使用失当是甜菜夜蛾大发生的重要原因

近年来,甜菜夜蛾Spodoptera exigua(H櫣bner)在我国的危害面积越来越广,造成的损失越来越大。为了更好地了解甜菜夜蛾的发生和成灾规律,改善和提高预测与防治技术,文章就杀虫剂对甜菜夜蛾及其天敌的影响进行了分析。结果表明,杀虫剂使用失当是甜菜夜蛾大发生的重要原因。甜菜夜蛾对杀虫剂的抗药性水平超过天敌,而天敌的飞行、搜索、攻击和产卵等行为,以及生长、发育、生殖和寿命等又容易受杀虫剂的干扰,产生负面影响,从而降低天敌对甜菜夜蛾的控制能力。因此,如何合理使用杀虫剂,在有效控制甜菜夜蛾种群的同时,达到保护天敌的目的,将是我们面临的新课题。     

Insecticide resistance in populations of Tuta absoluta (Lepidoptera: Gelechiidae)

1 Control failures of insecticides used against the tomato leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Brazil led to the investigation of the possible occurrence of resistance of this insect pest to abamectin, cartap, methamidophos and permethrin. 2 The insect populations were collected from seven sites in the states of Minas Gerais, Rio de Janeiro, and São Paulo. These populations were subjected to concentration–mortality bioassays using insecticide‐impregnated filter papers. 3 We were unable to obtain a single population which provided a susceptibility standard for all insecticides tested. Therefore, the resistance levels were estimated in relation to the most susceptible population to each insecticide. Resistance to abamectin and cartap were observed in all populations when compared with the susceptible standard population, with resistance ratios ranging from 5.2‐ to 9.4‐fold and from 2.2‐ to 21.9‐fold for abamectin and cartap, respectively. Resistance to permethrin was observed in five populations with resistance ratios ranging from 1.9‐ to 6.6‐fold, whereas resistance to methamidophos was observed in four populations with resistance ratios ranging from 2.6‐ to 4.2‐fold. 4 The long period and high frequency of use of these insecticides against this insect pest suggest that the evolution of insecticide resistance on them has been relatively slow. Alternatively, the phenomenon might be widespread among Brazilian populations of T. absoluta making the finding of suitable standard susceptible populations difficult and leading to an underestimation of the insecticide resistance levels in this pest. 5 Higher levels of resistance to abamectin, cartap and permethrin are correlated with greater use of these compounds by growers. This finding suggests that local variation in insecticide use was an important cause of variation in susceptibility.     

害虫抗药性的显性水平与抗性进化

对杀虫剂的代谢抗性和主要靶标抗性的显性水平作了理论解释,其中包括昆虫对Bt抗性的显性水平的解释。并对抗性显性具有的多变性作了阐述。分析抗性显性水平与抗药性进化的关系,认为在抗性进化早期抗性表现为显性的基因频率上升快于抗性表现为隐性时;但在抗性等位基因频率较高且出现抗性纯合子个体时,抗性表现为隐性的基因频率上升显著快于抗性表现为显性时。最后论述抗性显性在抗性治理中的应用。     

Monitoring and mechanisms of organophosphate resistance in San Jose scale,Diaspidiotus perniciosus (Hemiptera: Diaspididae)

San Jose scale, Diaspidiotus perniciosus (Comstock), is a serious pest in Chilean apple tree orchards, and a number of organophosphate insecticides were used to control them for decades. Recently, control failures with these insecticides were reported and linked to insecticide resistance development. In this study, 40 San Jose scale field populations were collected and their susceptibility to two commonly used organophosphate insecticides, that is chlorpyrifos and methidathion, was assessed. The obtained bioassay data suggest moderate levels of resistance to both insecticides when compared to a reference susceptible strain. The highest resistance ratio (RR) detected for chlorpyrifos and methidathion was 31‐fold and 11‐fold, respectively. The bioassay results suggest the occurrence of a significant cross‐resistance between both compounds. Biochemical measurements revealed a role for esterases in conferring resistance to organophosphates, but not modified acetylcholinesterase. The spatial spread and extend of insecticide resistance were also evaluated. Our result shows that no autocorrelation can be assumed, and then, insecticide resistance is caused by random factors.     

Evaluation of organic insecticides for management of spotted‐wing drosophila (Drosophila suzukii) in berry crops

Spotted‐wing drosophila, Drosophila suzukii (Matsumura), is an invasive pest affecting fruit production in many regions of the world. Insecticides are the primary tactic for controlling D. suzukii in organic as well as conventional production systems. Organic growers have a greater challenge because fewer insecticides are approved for use in organic agriculture. The most effective organically approved product is spinosad, but alternatives are needed because of label restrictions limiting the number of applications per year, toxicity to beneficial arthropods and the risk of developing resistance. We evaluated several organically approved insecticides against D. suzukii in laboratory assays and field trials conducted on organic blueberry and raspberry farms. Spinosad was consistently the most effective insecticide, but a few other insecticides such as azadirachtin + pyrethrins, Chromobacterium subtsugae and sabadilla alkaloids showed moderate activity. None of the treatments had long residual activity. Mortality started to decline by 3 days after treatment, and by 5 days after application, the treatments were not different from the controls. These products may be useful in rotation programmes, necessary for reducing reliance on spinosad and mitigating resistance. Cultural and biological control approaches are needed in fruit production for D. suzukii management, but insecticides will likely continue to be the dominant management tactic while these other approaches are being optimized and adopted.     

Characterization of mosquito larval habitats and assessment of insecticide-resistance status of Anopheles gambiae senso lato in urban areas in southwestern Ghana

The study was carried out to characterize potential larval habitats in the city of Sekondi with the aim of assessing the relative importance of anthropogenic and natural water bodies as larval habitats. Insecticide-resistance status of Anopheles gambiae senso lato in the southwestern part of the coastal savannah zone in Ghana was also assessed against four different classes of insecticides. Larval surveys were carried out in two communities that are separated by a lagoon. Although the lagoon was a potential mosquito larval habitat, we showed that it was not an important mosquito breeding site. The major larval habitats were anthropogenic, resulting from human behavior. Some of the organically polluted breeding sites were inhabited by both An. gambiae s.l. and Culex quinquefasciatus larvae. The data also showed that An. gambiae s.l. has currently developed a strong resistance to DDT and pyrethroid insecticides in southwestern Ghana, where the species was reported to be susceptible about a decade ago. The use of insecticides in households was implicated as a possible cause of the development of resistance among An. gambiae s.l. populations in the area. The management of insecticide resistance among malaria vectors needs urgent attention if insecticide-treated materials can continue to be used for malaria control.     

小菜蛾对杀虫剂的敏感性与其抗药性的相关性

在开展云南省通海县小菜蛾Plutella xylostella(L.)种群对11种杀虫剂的敏感性的同时,对小菜蛾抗药性进行了测定,并分析二者之间的相关性,结果表明:小菜蛾对杀虫剂的敏感性与其抗药性总体上呈现负相关,即随着抗药性的增加,小菜蛾对杀虫剂的敏感性呈下降趋势,但相关性并不显著。如在无抗性至高抗性的杀虫剂之间,其敏感性并无明显的变化,处理间无差异,只有对其极高抗性的阿维菌素、虫酰肼和高效氯氰菊酯才表现出明显的下降趋势。因此,在实际生产过程中,一种药剂是否因抗药性增加而不能使用,还应该参照田间防治效果。     

寄生蜂抗药性研究进展

植物-植食性昆虫-寄生蜂三级营养结构之间由于长期相互适应和协同进化,产生了一系列独特的相互关系。选择压力将对害虫和寄生蜂的抗药性演化产生影响,但由于寄生蜂具有与植食性昆虫不同的生物学及生态学特性,选择压力对害虫和寄生蜂抗药性演化的影响作用也是不同的。研究结果表明,除体外杀虫剂对寄生蜂的直接汰选因素外,进入寄主昆虫体内的杀虫剂成分、寄主昆虫取食不同植物的特有成分以及气候因子等均会对寄生蜂的抗药性演化产生影响。     

The impact of secondary pests on Bacillus thuringiensis (Bt) crops

The intensification of agriculture and the development of synthetic insecticides enabled worldwide grain production to more than double in the last third of the 20th century. However, the heavy dependence and, in some cases, overuse of insecticides has been responsible for negative environmental and ecological impacts across the globe, such as a reduction in biodiversity, insect resistance to insecticides, negative effects on nontarget species (e.g. natural enemies) and the development of secondary pests. The use of recombinant DNA technology to develop genetically engineered insect‐resistant crops could mitigate many of the negative side effects of insecticides. One such genetic alteration enables crops to express toxic crystalline (Cry) proteins from the soil bacteria Bacillus thuringiensis (Bt). Despite the widespread adoption of Bt crops, there are still a range of unanswered questions concerning longer term agro‐ecosystem interactions. For instance, insect species that are not susceptible to the expressed toxin can develop into secondary pests and cause significant damage to the crop. Here, we review the main causes surrounding secondary pest dynamics in Bt crops and the impact of such outbreaks. Regardless of the causes, if nonsusceptible secondary pest populations exceed economic thresholds, insecticide spraying could become the immediate solution at farmers’ disposal, and the sustainable use of this genetic modification technology may be in jeopardy. Based on the literature, recommendations for future research are outlined that will help to improve the knowledge of the possible long‐term ecological trophic interactions of employing this technology.     

DDT, pyrethrins, pyrethroids and insect sodium channels

The long term use of many insecticides is continually threatened by the ability of insects to evolve resistance mechanisms that render the chemicals ineffective. Such resistance poses a serious threat to insect pest control both in the UK and worldwide. Resistance may result from either an increase in the ability of the insect to detoxify the insecticide or by changes in the target protein with which the insecticide interacts. DDT, the pyrethrins and the synthetic pyrethroids (the latter currently accounting for around 17% of the world insecticide market), act on the voltage-gated sodium channel proteins found in insect nerve cell membranes. The correct functioning of these channels is essential for normal transmission of nerve impulses and this process is disrupted by binding of the insecticides, leading to paralysis and eventual death. Some insect pest populations have evolved modifications of the sodium channel protein which prevent the binding of the insecticide and result in the insect developing resistance. Here we review some of the work (done at Rothamsted Research and elsewhere) that has led to the identification of specific residues on the sodium channel that may constitute the DDT and pyrethroid binding sites.