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A lot has been learned about insecticide resistance in the past 40 years. The problem is more extensive and widespread than could have been predicted. In this review, Richard Roush discusses the genetics and management of resistance to insecticides (especially as related to arthropod vectors of human and animal diseases), with the objective of suggesting future directions.
Resistance to insecticides made from different chemical compounds were studied in 4 strains of Musca domestica collected from 2 poultry farms and 2 cow farms following WHO methodology. A high resistance to malathion was observed (resistance factor values ranging from 102X to 252X), and moderate, to diazinon, fenthion, dichlorvos, DDT, and propoxur. Resistance to the deltametrine and permethrin pyreturins was not observed.
The insecticide resistance status of 4 strains of adult male Blattella germanica, viz M (Malacca), E (England), F (restaurant) and K (cafeteria) against malathion and bendiocarb compared with a reference susceptible strain (S) was determined by using a modified WHO bioassay method. The results indicated that all the 4 strains were resistant to the insecticides albeit in different degrees. Resistance ratios for malathion ranged from 1.85-41.07-fold, whereas that of bendiocarb ranged from 1.68-4.83-fold. The biochemical microplate enzyme assays technique employed indicated that the resistance in M and E strains were attributed to acetylcholinesterase insensitivity. Multiple resistance was not detected in any of the 4 strains. Parameters of the identified resistance mechanism correlated well with the observed level of resistance. Agar gel electrophoresis showed that variations in esterase isoenzymes did not confer organophosphate and carbamate resistance to the 4 strains.
The resistance to various insecticides from 4 major groups (organochlorine, organophosphate, carbamate and pyrethroid) was investigated in a field strain of Culex quinquefasciatus from Baan Suan community, Nonthaburi province, Thailand by using a standard World Health Organization susceptibility test. The Baan Suan strain was completely resistant to DDT and highly resistant to deltamethrin, permethrin, fenitrothion and propoxur but this strain was still found to be highly susceptible to malathion. This strain displayed high resistance to cypermethrin since the result revealed that the resistance ratio of the 50% lethal concentration value (RR50) between the field and the laboratory strains (NIH strain) was 16. The study indicated that mosquitoes were resistant to almost all insecticide tested except malathion and this should be an alternative for Cx. quinquefasciatus control in this area. Moreover, Aedes aegypti, which is a main dengue vector in Baan Suan community was also tested with deltamethrin, permethrin and fenitrothion. The results showed that dengue mosquitoes are clearly resistant to permethrin and tolerant to deltamethrin, but was 100% susceptible to fenitrothion. The cause of insecticide resistance in Cx. quinquefasciatus may be due to the continuous use of insecticide for dengue vector control programme in Baan Suan community.
Insecticide resistance is an increasing problem in many insect vectors of disease. Our knowledge of the basic mechanisms underlying resistance to commonly used insecticides is well established. Molecular techniques have recently allowed us to start and dissect most of these mechanisms at the DNA level. The next major challenge will be to use this molecular understanding of resistance to develop novel strategies with which we can truly manage resistance. State-of-the-art information on resistance in insect vectors of disease is reviewed in this context.
Voltage-gated sodium channels are essential for the generation and propagation of action potentials (i.e., electrical impulses) in excitable cells. Although most of our knowledge about sodium channels is derived from decades of studies of mammalian isoforms, research on insect sodium channels is revealing both common and unique aspects of sodium channel biology. In particular, our understanding of the molecular dynamics and pharmacology of insect sodium channels has advanced greatly in recent years, thanks to successful functional expression of insect sodium channels in Xenopus oocytes and intensive efforts to elucidate the molecular basis of insect resistance to insecticides that target sodium channels. In this review, I discuss recent literature on insect sodium channels with emphases on the prominent role of alternative splicing and RNA editing in the generation of functionally diverse sodium channels in insects and the current understanding of the interactions between insect sodium channels and insecticides.
The malaria situation in Sri Lanka worsened during the 1990s with the emergence and spread of resistance to the drugs and insecticides used for control. Chloroquine resistance has increased rapidly over this period, but adverse changes in malaria transmission are more closely associated with insecticide use rather than drug resistance. Insecticide susceptibility tests were routinely carried out in key anopheline vectors across the country for more than a decade. These sentinel data were combined with data collected by other research programmes and used to map the spatial and temporal trends of insecticide resistance in the main vectors, Anopheles culicifacies and A. subpictus, and to examine the relationship between insecticide resistance, changes in national spraying regimens and malaria prevalence. Both species had widespread resistance to malathion, the insecticide of choice in the early 1990s. Both species were initially susceptible to the organophosphate and pyrethroid insecticides used operationally from 1993, but some resistance has now been selected. The levels of malathion and fenitrothion resistance in A. subpictus were higher in some ecological regions than others, which may be related to the distribution of sibling species, agricultural pesticide exposure and/or environmental factors. The study highlights that the emergence and spread of insecticide resistance is a constant threat and that active surveillance systems are vital in identifying key vectors and evidence of resistance.
Dominance level of insecticide resistance provided by one major gene (an insensitive acetylcholinesterase) in the mosquito Culex pipiens was studied in two distinct environments. Dominance level was found to be very different environments, varying from almost complete dominance to almost recessive when either propoxur (a carbamate insecticide) or chlorpyrifos (an organophosphorus insecticide) was used. To better understand this plastic response, three environmental parameters were manipulated and their interactions studied. For chlorpyrifos, each parameter had a small effect, but when all parameters were changed, the dominance level was greatly affected. For propoxur, one environmental parameter had a large effect by itself. It was further studied to understand the causal relationship of this plasticity. Recessivity of resistance was associated with more demanding environments. These results are discussed in the context of the various theories of the evolution of dominance. It appears that dominance of insecticide resistance cannot be directly predicted by Wright's physiological theory.
Houseflies in poultry ranches in certain areas of California are now resistant to most insecticides licensed for use in these establishments, and this resistance problem appears likely to spread to other areas in the future. The authors have therefore studied the contact and oral toxicity of 19 new compounds that have shown interesting properties against resistant flies. These compounds were selected from among several hundred submitted by various laboratories for evaluation under a co-operative programme sponsored by the World Health Organization.Five compounds were found to be as toxic to three insecticide-resistant strains as to a susceptible strain, and showed strikingly steep log-dosage/probit mortality lines against the resistant strains. The authors suggest that these compounds be further studied for fly control in field trials.
Dose-mortality data from 40 horn fly, Haematobia irritans (L.), populations revealed that susceptibility to permethrin and diazinon was negatively correlated (i.e., as susceptibility to permethrin decreased, toxicity of diazinon increased). Permethrin-resistant horn fly populations exposed for 18 wk to cattle tagged with ear tags impregnated with 20% (AI) diazinon resulted in a 2- to 6-fold reduction in this resistance. These populations also had LC50s for diazinon that were two to five times lower than those of populations susceptible to permethrin. Frequency of homozygous permethrin-resistant individuals decreased as much as 57% after exposure to diazinon during this period.
Gfi-1 is a C(2)H(2)-type zinc finger protein that is a transcriptional repressor in vertebrates and has been implicated in control of CYP6D1 expression in house flies (Musca domestica). A 15 bp insert, which disrupts a putative mdGfi-1 binding site in the CYP6D1v1 promoter has been implicated as a cause of increased expression of CYP6D1, and thus insecticide resistance. Using electrophoretic mobility shift assays we demonstrate that the CYP6D1 promoter from susceptible strains binds mdGfi-1. The 15 bp insert that interrupts the mdGfi-1-binding site in insecticide-resistant strains reduces the amount of mdGfi-1 binding by 9- to 20-fold, consistent with the role of mdGfi-1 in resistance. Partial sequences of mdGfi-1 (spanning the first intron) from individual houseflies from 11 different strains revealed the presence of 23 alleles. There was no consistent difference in the mdGfi-1 alleles between susceptible and CYP6D1-mediated insecticide-resistant strains, indicating that mdGfi-1 alleles were not likely involved in resistance. Polymorphisms were used to map mdGfi-1 to autosome 1. Quantitative real time PCR (qRT-PCR) revealed Gfi-1 expression was higher in the thorax compared to the head and abdomen, and varied between life stages and between strains. However, similar levels of mdGfi-1 were detected in susceptible and resistant adults suggesting that altered levels of mdGfi-1 were not likely a cause of insecticide resistance. The significance of these results to understanding insecticide resistance is discussed.
The spread of insecticide-resistance in the two main vectors of malaria in Java, Anopheles aconitus Dönitz and A. sundaicus Rodenwaldt, has been of concern to workers in the Indonesian malaria eradication programme since DDT-resistance was first detected, in A. sundaicus, in 1954. The history of development of resistance in these two vectors has been summarized in this paper by assembling the available records in chronological order, thus facilitating reference.The picture which emerges is that of somewhat erratic occurrence of DDT-resistance in A. sundaicus and more stable, expanding areas of DDT-resistant A. aconitus. Dieldrin-resistance is more widespread than DDT-resistance in both species and preceded the onset of DDT-resistance in A. aconitus but not in A. sundaicus. These features should not be regarded as species characteristics, however, since selection pressures on the two species have been far from uniform.Malathion appears to be a promising alternative to DDT and dieldrin for the control of the two vectors in the circumstances described.
The developments of insecticide resistance in insects and antimicrobial resistance in bacteria seem to have not too many aspects in common, due to the diverse nature of eukaryotes and prokaryotes cells and organisms. However, there are several approaches, both in the history of ecological systems and in the History of Science, that can successfully be applied to explain aspects of developments shared by both phenomena of resistance. Looking back to a century of discoveries, scientific explanations, industrial, agricultural, and medical practice, the historian is especially well placed for investigating the lessons to be learned and to be exchanged at the boundaries of research on resistant insects and microbes.
A single point mutation within the GABA receptor gene Resistance to dieldrin (Rdl) confers a high level of resistance to cyclodiene insecticides in a wide range of insects. Previous studies have shown partial rescue of the susceptible phenotype via germline transformation of a 36 kb cosmid coding (or all four alternative Rdl splice forms. Here, we describe the construction of two Rdl promoter/cDNA minigenes, each coding for one of the splice forms alone. Single splice forms rescued both the insecticide susceptible and resistant phenotypes associated with the locus as effectively as the complete cosmid. The minigenes also rescue the lethality associated with homozygous re-arrangements disrupting the Rdl gene, and the level of rescue observed is not increased by the addition of more than one splice form. This demonstrates that only a single Rdl splice form is necessary both to confer insecticide sensitivity and also to rescue lethality. Methods by which phenotype rescue could be enhanced and the potential advantages of using Rdl as a selectable marker are discussed.
Intensive chemical treatments have led to the development of a number of insecticide resistance mechanisms in the peach-potato aphid Myzus persicae (Sulzer). Some of these mechanisms are known to be associated with negative pleiotropic effects (resistance costs). Molecular and biochemical methods were used to determine the genotypes or phenotypes associated with four insecticide resistance mechanisms in single aphids from sexually-reproducing populations in southern France. The mechanisms considered were E4 and FE4 carboxylesterase overproduction, modified acetycholinesterase, and kdr and rdl resistance-associated mutations. A new method for determining individual kdr genotypes is presented. Almost all resistant individuals overproduced FE4 carboxylesterase, whereas modified acetylcholinesterase was rare. Both the kdr and rdl resistance mutations were present at high frequencies in French sexually-reproducing populations. The frequencies of insecticide resistance genes were compared before and after sexual reproduction in one peach orchard at Avignon to evaluate the potential impact of selection on the persistence of resistance alleles in the over-wintering phase. The frequencies of the kdr and rdl mutations varied significantly between autumn and spring sampling periods. The frequency of the kdr mutation increased, probably due to pyrethroid treatments at the end of the winter. Conversely, the frequency of the rdl mutation decreased significantly during winter, probably because of a fitness cost associated with this mutation.
Quantitative genetic studies of resistance can provide estimates of genetic parameters not available with other types of genetic analyses. Three methods are discussed for estimating the amount of additive genetic variation in resistance to individual insecticides and subsequent estimation of the heritability (h2) of resistance. Sibling analysis and offspring-parent regression permit direct estimates of h2 by comparing the resistance phenotypes of individuals of known relatedness. Threshold trait analyses, performed on data from selection experiments, provide estimates of realized heritability. Procedures are outlined for predicting changes in resistance to insecticides based on h2 estimates. Quantitative genetic theory is examined as it relates to resistance and resistance as a quantitative trait; quantitative genetic methods also are unique in providing estimates of genetic correlations between traits. Comments are included on estimates of genetic correlation between resistance and phenotypic traits (e.g., development time) and how they may be used to predict changes in the genetic aspects of phenology that result from insecticide applications (i.e., to predict how the reproductive capacity of future generations will differ from that of the treated generation).
Simulations were used to compare evolution of insecticide resistance predicted by a conventional two-allele model with predictions from three- and four-allele models that assume resistance is based on gene amplification. Results were similar between models when insecticide concentration was low or moderate. In contrast, when 10% of the population was not exposed to insecticide each generation, high insecticide concentrations slowed resistance development in the two-allele model, but caused rapid development of high levels of resistance in the three- and four-allele models. The presence of a third allele at an initial frequency as low as 10-7 doubled or tripled the rate of resistance development in some cases. Attempts to slow evolution of resistance by overwhelming it with high concentrations of insecticides are not likely to succeed if gene amplification or other mechanisms generate alleles that confer high levels of resistance.
Cytochrome P-450s, cytochrome b5, P-450 reductase, and four P-450 monooxygenase activities were abundant in proximal intestine (PI), Malpighian tubules (MT), and fat bodies (FB) in the insecticide resistant (LPR) strain of house fly. Insecticide resistance in LPR flies was associated with increases in P-450 monooxygenase activities in nearly all of these tissues relative to an insecticide susceptible strain. Cytochrome P-450lpr was present in all tissues and at higher levels in LPR than in susceptible flies suggesting that the role of P-450lpr in monooxygenase-mediated insecticide resistance is not due to its higher levels in a single tissue. However, it appears that fat bodies may have a major role in resistance due to their relatively large size and the abundance of P-450lpr in this tissue. Total cytochrome P-450s, cytochrome P-450lpr and P-450 monooxygenase activities were generally refractory to phenobarbital (PB) induction in LPR. This contrasts with a previous report in susceptible house flies showing that P-450 monooxygenases were induced by PB. It appears that total P-450s, cytochrome P-450lpr and monooxygenase activities were expressed at constitutive high levels in several tissues of LPR house flies.