Fitness costs associated with insecticide ... - Wiley Online Library

Mini-review Received: 16 December 2011

Revised: 13 July 2012

Accepted article published: 6 August 2012

Published online in Wiley Online Library: 4 September 2012

(wileyonlinelibrary.com) DOI 10.1002/ps.3395

Fitness costs associated with insecticide resistance Adi Kliot and Murad Ghanim∗ Abstract Insects are exposed to a variety of stress factors in their environment, and, in many cases for insect pests to agriculture, those factors include toxic chemical insecticides. Coping with the toxicity of insecticides can be costly and requires energy and resource allocation for adaptation and survival. Several behavioural, physiological and genetic mechanisms are used by insects to handle toxic insecticides, sometimes leading to resistance by constitutive overexpression of detoxification enzymes or inducing mutations in the target sites. Such actions are costly and may affect reproduction, impair dispersal ability and have several other effects on the insect’s fitness. Fitness costs resulting from resistance to insecticides has been reported in many insects from different orders, and several examples are given in this mini-review. c 2012 Society of Chemical Industry Keywords: fitness cost; insecticide resistance; selection; pest

1

INTRODUCTION

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Fitness costs associated with resistance to insecticides have been reported in insects belonging to different orders. Identifying fitness costs as a result of resistance to any insecticide can be an advantage in designing an integrated pest management (IPM) programme for limiting the spread of the resistant population. The higher the fitness cost, the longer it is likely to take for resistant individuals to spread in the population, thus adding an important factor for an IPM programme among a resistant population. Here, a review is given of known cases of fitness costs as a result of resistance to insecticides in insects that belong to different orders, with emphasis placed on the consequences that result from these costs for the insect’s life history (Table 1).

2 HEMIPTERA This order includes many important insect pests to agriculture, such as aphids, whiteflies and psyllids. They directly feed on the plant’s vascular system with their piercing-sucking mouth parts, and serve as vectors for many important plant viruses. One of the major classes of insecticide used against hemipterans is the neonicotinoids. Neonicotinoids target the nicotinic acetylcholine receptor, exhibit low toxicity to mammals and can be applied systemically with irrigation. These features have made them an important group in many IPM programmes for the past 20 years. Although neonicotinoids exhibit exceptional toxicity against their target pests, many resistance cases in a range of insects have been reported.4 For example, in the brown planthopper, Nilaparvata lugens Stål., the most important rice pest in Southeast Asia, very high levels of resistance to imidacloprid were observed in many regions, and the reason was believed to be a case of

∗

Correspondence to: Murad Ghanim, Department of Entomology, the Volcani Centre, Bet Dagan 50250, Israel. E-mail: [email protected] Department of Entomology, the Volcani Centre, Bet Dagan, Israel

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c 2012 Society of Chemical Industry

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Fitness costs associated with insecticide resistance are where the development of resistance to an insecticide is accompanied with high energetic cost or significant disadvantage that diminishes the insect’s fitness compared with its susceptible counterparts in the population. One significant outcome is that genes conferring resistance to insecticides rarely become fixed in natural populations. A common hypothesis that supports this observation is that a fitness cost is apparent not only in relation to insecticide resistance but whenever an organism adapts to a new environment, combating many environmental stressors such as adaptation to new plants and their toxic secondary metabolites. Because the phenotype of an organism is defined by various selection pressures to suit its environment, strong phenotypic change is expected to be deleterious when the organism returns to its old environment.1 To date, three main mechanisms of insecticide resistance have been defined: (1) metabolic detoxification through the overexpression of metabolic genes; (2) target-site modification; (3) reduced penetration/increased excretion. Overexpression of a resistance-conferring gene is thought to result in a fitness cost because of a resource and energy reallocation at the expense of metabolic and developmental processes. A constitutive lowexpression and target-site modification can result in a fitness cost when the target-site substitution or the low-expressed gene are essential for the viability of the insect, or when this change results in a near loss of function. Any molecular alteration may also have pleiotropic effects on other traits, causing a morphological and possibly a behavioural change impairing the resistant individual’s survival and/or reproductive success in the natural population. A fitness cost in resistant heterozygotes is considered more important than a fitness cost in resistant homozygotes, because the heterozygotes will be more common at the early stages of insecticide selection, and also because the dominance of any possible pleiotropic effects of the resistance can be better studied in these heterozygous individuals.2,3

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Table 1.

A Kliot, M Ghanim

Reported fitness costs associated with insecticide resistance

Order

Species

Insecticide group

Resistance mechanism

Fitness effects found in resistant strains

Hemiptera

Nilaparvata lugens

Neonicotinoids

Metabolic

Hemiptera

Bemisia tabaci

Neonicotinoids

Not tested

Hemiptera

Myzus persicae

Pyrethroids, DDT

Target site, metabolic

Diptera

Culex pipiens

OPs

Target site, metabolic

Diptera Diptera Lepidoptera Lepidoptera

Culex quinquefasciatus Musca domestica Several species Plutella xylostella

OPs OPs, DDT Bt toxins Tebufenozide

Target site, metabolic Target site Target site Not tested

Lepidoptera

Cydia pomonella

Pyrethroids, benzoylurea

Not tested

Lepidoptera Coleoptera

Choristoneura rosaceana Leptinotarsa decemlineata

OPs Bt toxins

Not tested Not tested

Coleoptera Coleoptera Coleoptera

Leptinotarsa decemlineata Tribolium castaneum Sitophilus zeamais

OPs, pyrethroids OPs OPs, pyrethroids, DDT

Not tested Not tested

Larval survival rate, adult emergence rate, copulation rate, fecundity and hatchability5 Adult fecundity and longevity, developmental time of the nymphal stages, size of instars and pupae7 Overwintering survival,13 response to the aphid alarm pheromone, vulnerability to parasitioids9 – 16 Survival rates during winter time, ability to avoid predation, mating cost, fecundity, wing span, pre-imaginal development, fat stores26 – 29 Inhibition of the vectored parasite’s development3 Preference along a temperature gradient30 Survival, developmental time, body mass32 Survival rate, copulation rate, fecundity, hatchability33 Fecundity, larval development, body mass of instars, adult male longevity34 Pheromone production, calling time for mating35 Larval development and weight, oviposition period, egg size, fecundity, sexual competitiveness, population growth rate, overwintering mortality36,39 Fecundity and fertility2 Fecundity, copulation ability40,42 Fat body mass, respiration rates, morphology of the fat body cells43

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point mutation in the nicotinic acetylcholine receptor that was selected in a laboratory population; however, it was recently linked to overexpression of cytochrome P450 enzymes and metabolic breakdown.5 A laboratory strain selected for resistance to neonicotoniods showed that the development of resistance was uneven between selected and unselected populations over many generations. While the unselected population developed much faster as the generations progressed, the selected population suffered great fitness cost: their larval survival rate, adult emergence rate, copulation rate, fecundity and hatchability were all significantly lower, and the relative fitness of the resistant planthoppers decreased with further generations.6 Although effects on fitness were observed in these laboratory experiments, it was uncertain whether the resistance was conferred by overexpression of cytochrome P450 enzymes. Planthoppers resistant to neonicotinoids are common in rice fields, suggesting the presence of other unknown factors that determine the level of the fitness cost associated with the resistance. The existence of fitness costs as a result of resistance to neonicotinoids was also examined in the sweetpotato whitefly Bemisia tabaci. A B. tabaci B-biotype strain was selected for resistance to thiamethoxam through several generations, while comparing several life history traits between selected and unselected strains.7 Fecundity and adult longevity of the resistant individuals were significantly lower than those of the susceptible unselected strain. Conversely, the developmental time of the nympal stages was longer in the resistant strain. The resistant strain further exhibited phenotypical differences: all instars and pupae were smaller than those of the susceptible strain; however, these differences in size did not persist in the adult stage.7

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A major hemipteran that was extensively studied in relation to resistance to insecticides is the peach potato aphid Myzus persicae (Sulzer). Several mechanisms for resistance have been reported from M. persicae, including overexpression of carboxylesterases conferring resistance to organophophates (OPs) and pyrethroids, target-site mutation in acetylcholine esterases conferring resistance to the dimethylcarbamate and pirimicarb, a single point mutation in the nicotinic acetylcholine receptor that conferred strong resistance to neonicotinoids8 and other target-site mutations linked to resistance to pyrethroids and dichlorodiphenyltrichloroethane (DDT).9 Recently, the overexpression of cytochrome P450 genes in M. persicae was shown to be responsible for low resistance to neonicotinoids.10 An extensive survey of M. persicae in the United Kingdom was conducted, and it was found that in the autumn, towards the end of the field crop season, populations of M. persicae comprise more OPresistant aphids.9,11,12 As a consequence of fitness cost associated with the resistance, resistant individuals are less able to overwinter and survive the low temperatures, thus lowering their potential to establish large populations in the following season.13 The inability to establish large populations was later linked to the slow movement of resistant forms from senescing leaves owing to a behavioural disadvantage that could be linked to a poor response to the aphids’ alarm pheromone.14 The low response to the alarm pheromone is severe in the resistant population and was highly correlated with the presence of extreme carboxylesterase resistance and the knockdown resistance mutation (kdr) conferring DDT and pyrethroid resistance. The kdr gene was shown to be in linkage disequilibrium with the genes conferring OP and pirimicarb resistance, and thus it was persistent in the population. Furthermore, resistant individuals were found to be more


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Fitness cost and insecticide resistance

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vulnerable to attack from their primary endoparasitoid wasp at different spatial scales, and more susceptible aphids than resistant ones moved from their inoculation leaves to other leaves on the same plant after exposure to parasitoids. These findings implied that natural enemies can influence the evolution and dynamics of insecticide resistance by influencing important behavioural traits.15,16 This was the first time a fitness cost associated with insecticide resistance was shown to be imposed by another trophic level.

3

DIPTERA

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Many dipterans or true flies are agricultural pests, but they are also vectors of human and animal diseases, including mosquitoes, sand flies and tsetse flies.17 DDT was the first chemical compound used for efficient control of this group of insects in the 1950s. However, once resistance against DDT arose, other groups of chemicals were introduced, including classical OPs, carbamates and pyrethroids, and subsequently other chemistries that had to be very efficient against these pests, but safe for humans and other mammals.18 Research on fitness cost effects on DDT-resistant mosquitoes was conducted back in 1948. Several studies showed higher fitness traits in resistant strains compared with susceptible ones, and most notably a longer time for larval stages to reach pupation in the resistant strain.19 In many cases, resistance to insecticides was fixed in the populations, mostly owing to the overuse of a single insecticide because of the lack of other effective ones. Furthermore, after the resistance was fixed, no apparent fitness cost characteristics were identified in the resistant population. An example is the resistance of the sheep blowfly (SBF) Lucilia cuprina to OPs. Diazinon, an OP, was largely used to control SBF in Australia, and, as it was the only effective compound used for 15 successive years, even after resistance was reported in field populations in 1967. A lack of fitness cost as a result of the resistance to diazinon was shown among resistant SBF, although 10 years earlier a fitness cost was observed.20 The lack of fitness cost among resistant populations and their equal vitality compared with the susceptible strains was postulated to be a result of the presence and expression of a modifier gene located in the SBF genome which has an important role in the fly’s physiology.21 – 23 The expression of the modifier gene enabled the diazinon-resistant insects to be as fecund and fit as the susceptible ones. The modifier was mapped to the Scalloped wings (Scl) locus, a homologue of the Drosophila melanogaster Notch gene. No molecular data were gathered on the activity of the modifier gene, but the hypothesis was that the change in substrate specificity of the esterase gene Rop-1 conferring diazinon resistance also impaired its interaction with other genes and its role in cell adhesion, which is critical for proper tissue development via the Scl signalling pathway. The modified Scl allele, namely the modifier gene, corrects this and enables proper signalling and development in insects with the resistant Rop-1 gene.23 A fitness cost as a consequence of the resistance to OPs was further studied in the mosquito Culex pipiens. By monitoring laboratory and field populations in the southern part of France, it was found that three loci are involved in the resistance to OPs. Two tightly linked loci, Est-2 and Est-3, encode detoxifying esterases A and B and confer resistance to OPs through overexpression. This is achieved by the modification of gene regulation or by gene amplification.24 The third locus, Ace, encodes the target site of OPs, acetylcholinesterase. Variants of this locus are insensitive

to the inhibitory action of OPs. Studies on populations with these different loci conferring resistance to OPs found that they suffer different fitness cost effects and selection pressures. For example, some variants in the Ace locus showed differential survival rates during winter time, indicating their impaired ability to avoid predation and other selection pressures to which the overwintering females are exposed.24 It was observed that susceptible females migrate to overwintering caves earlier than resistant ones, although one alternative hypothesis to this result is that the selection pressure of the applied insecticides drives the earlier migration of susceptible females. Before and during winter, events of migration from one, unfit, overwintering site to an alternative one occur. In these cases, a fitness cost is most obvious; the mosquitoes arriving at the new site were found to have a low frequency of resistant genes. The reason for this fitness cost is yet unknown.25 Fitness costs found in the three possible resistant loci include a mating cost in the resistant males compared with susceptible ones, lower fecundity in the females, a predation cost, shorter wing span (possibly associated with the low fecundity due to the low body size) in the resistant individuals and longer pre-imaginal developmental time in the field.26 – 28 These studies were partially done on field populations and in part on isogenic laboratory strains. A physiological examination of the energetic reserves of four isogenic strains, three containing OP-resistance-conferring loci, found that the resistant strains had significantly fewer energy reserves than the susceptible ones. Indeed, recent work carried out on C. pipiens has shown that a hyperactivation of the nervous system results in a depletion of fat stores by increasing metabolic rates and decreasing fatty acid synthesis.29 The gap between the strains was especially apparent in the adult stage after the depletion of the energy resources during the pupation stage. The researchers’ hypothesis was that, in the field, where food is scarce, the difference will be noticeable in the larval stage, resulting in larval death and longer developmental time of resistant individuals. It was also hypothesised that, even though insecticide resistance increases the number of surviving mosquitoes, the resistant trait may change their physiology in a manner that lowers their ability to harbour parasites and serve as disease vectors. Researchers examined lines of OP-resistant Culex quinquefasciatus collected from Sri Lanka and exposed them to further OP selection pressure under laboratory conditions. These lines expressed high levels of esterases in the midgut, subcuticular layer, Malpighian tubules and salivary glands, resulting in an increase in the redox potential in the cells compared with their susceptible counterparts. Those specific tissues are all possible transfer routes that the parasites transmitted by the mosquito must cross in its life cycle. C. quinquefasciatus is the vector of the parasitic worm Wuchereria bancrofti causing periodic lymphatic filariasis, a disease endemic to Sri Lanka. This study showed that the parasite’s development was indeed hindered in the midguts of resistant mosquitoes compared with those of susceptible ones.3 The inhibition of the parasite’s development is severe enough that no mature worm stages were found in the midguts of resistant female mosquitoes.3 Although very few effective insecticides are available against pests of this order and resistance rates are high and common in the field, a decline in the transmissibility of parasites by the resistant individuals is possible, a fact that shows one positive outcome resulting from the resistance to insecticides, and the possible fitness costs associated with this resistance. A final example from the Diptera is the housefly Musca domestica, in which it was shown that kdr targetsite resistant flies to pyrethroids and DDT exhibit behavioural

www.soci.org differences in comparison with susceptible insects. The resistant individuals showed no preference along a temperature gradient, while susceptible genotypes exhibited a strong preference for warmer temperatures.30

4

LEPIDOPTERA

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Lepidoptera consists of many important agricultural pests, primarily moths. The damaging stage of this order is predominantly the larvae owing to herbivory on leaves, flowering parts and fruits. Insecticidal toxins of the Cry1A family produced by strains of the bacterium Bacillus thuringiensis (Bt) are very efficient against many lepidopterans but non-toxic to most other animal species. High concentrations of the toxins result in the insects’ death, and low concentrations inhibit larval growth and feeding. Since 1996 these toxins have been used in genetically modified crops to control mainly lepidopterans. The binding targets are critical in determining the range of species on which the toxins are active, and reduction or loss of binding is an important mechanism of genetically based resistance in the target pest species.31 Resistant strains were selected and maintained mainly in laboratory experiments, but cases of relative resistance to Bt were also recorded in the field.32 The main strategy applied in order to preserve the susceptibility to Bt is the use of temporal and/or spatial refuge in which Bt-susceptible individuals can reproduce and where the Bt-resistant individuals suffer the highest fitness costs so that their proliferation in the population, and the spread of their resistance alleles, is minimal. Insecticide resistance is mostly recessive, thus allowing the creation of heterogenic progeny carrying both susceptible and resistant alleles but presenting no apparent fitness cost. In the case of the use of Bt, the assumption is that the concentration of the toxin in the genetically modified plants is high enough to eliminate all but the resistant homozygous individuals, those that are the least likely to survive and procreate in the refuge areas, and in this way to eradicate the evolution of Bt resistance. There have been many investigations aimed at testing a possible fitness cost as a result of Bt resistance, mainly in moths but also on insects of other orders.32 The deduction from an overview of these studies that, on average, resistance ratios decreased by a factor of 10 for each seven generations without exposure to Bt toxins confirmed their ‘handicap’ on the insect’s fitness. The analyses also suggested that, the higher the level of resistance caused by a mutation or other mechanism, the higher was the fitness cost. This suggests another benefit to genetically modified crops with high concentrations of Bt toxins: in addition to the refuge advantage, the higher the insect’s resistance developed on these crops, the higher its cost will be. With regard to measuring the various fitness cost effects, results showed that the magnitude of the fitness cost varied significantly among the three major components analysed, with costs highest for survival, intermediate for development time and lowest for mass.32 Other insecticides, apart from Bt toxins, are used in the control of lepidopteran pests; some are generalist insecticides, such as benzoylureas and pyrethriods, and others are aimed specifically at Lepidoptera, such as tebufenozide. Tebufenozide is an insect growth regulator with an unknown mode of action. It kills larvae by inducing a premature moulting, and its toxicity varies in different lepidopteran species. This compound was developed in 1988 and was commercialised many years later. No resistance cases against the compound have been reported in field populations, although laboratory strains with high resistance levels were generated


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through artificial selection in many species. Possible fitness cost effects were examined in a laboratory-generated tebufenozideresistant strain of the diamondback moth Plutella xylostella.33 The results showed that the resistant strain had a relative fitness of only 0.3-fold compared with its susceptible ancestral line; the resistant individuals had a development rate similar to that of the susceptible insects, but their survival rate was lower in all preadult life stages.33 The copulation rate and effective fecundity of adults and the hatchability of eggs of the resistant-strain insects were also significantly lower. These results indicate a low probability for resistance development against tebufenozide under a proper pest control regime. A study that compared fitness parameters of two resistant strains of the codling moth Cydia pomonella (L.) to a susceptible strain showed high fitness costs in both resistant lines owing to low female fecundity, longer larval developmental times, smaller body mass of resistant instars and shorter adult lifespan of resistant males.34 Further comparisons intriguingly found that the difference in female fecundity was derived from the fact that the resistant females laid eggs for only 1 week, while the susceptible females continued laying eggs for at least another week. During that first week, the resistant females laid the same amount of eggs as the susceptible ones.34 The resistant lines used in this study displayed resistance to deltamethrin (a pyrethroid ester) and diflubenzuron (a benzamide) and were collected in fields in France where reports of pest control failure had been received. The two lines do not share a genetic background either between each other or between them and the susceptible line. This fact dilutes the impact of the results, such that it is not clear whether the fitness cost observed is derived from resistance and its pleiotropic effects, from other deleterious genetic traits or from an interaction between the two. Pheromone-based communications are a very important aspect in many insects, especially in moths, where it plays a key role in the ability of a male to locate a female for mating and reproduction. Studies on the fitness cost effects of insecticide resistance on pheromone production and male reproducibility in the obliquebanded leafroller Choristoneura rosaceana, using the OP azinphosmethyl-resistant strain, showed a significant reduction in pheromone production in the females and shorter calling times.35 On the other hand, no apparent fitness cost was found in males; males of the resistant line had no trouble finding a mate and their spermatophores were not significantly smaller than those of the susceptible males.35

5 COLEOPTERA This is a very large order, but it does not contain as many agricultural pest species as the Lepidoptera and the Hemiptera. Nevertheless, pests of this order cause grave damage to agriculture and forestry during both the larval and adult life stages. Larvae can feed on roots, leaves and flowering parts, tree bark and fruits. Many are storage pests, damaging dry silos of grains and other seeds or dried plant tissue. The Colorado potato beetle (CPB), Leptinotarsa decemlineata, is one of the major pests defoliating potato crops around the world,36 and it has been the subject of many resistance and fitness studies throughout the years. Strains of CPB with resistance to OPs and pyrethroids were found in the field in various parts of the world.2 Furthermore, laboratory strains were selected for resistance to Bt Cry toxins. Genetically modified potato plants producing Bt Cry3A toxin were commercially used against the CPB from 1996 until 2001. No cases


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Pest Manag Sci 2012; 68: 1431–1437

was compared with two pyrethroid-resistant strains collected in two different sites in Brazil. One strain was also DDT resistant, and the other OP resistant. The OP- and pyrethroid-resistant strain exhibited poor fitness compared with the susceptible strain in the field, while the DDT- and pyrethroid-resistant strain had fitness similar to that of the susceptible strains.43 The results also showed that the insecticide-susceptible strain of S. zeamais harboured smaller fat body cells than the resistant strains. The cells from resistant insects also had more vacuoles, proteins and carbohydrates than cells from susceptible insects.43 The DDT- and pyrethroid-resistant strain had a body mass greater than that of both the susceptible and the OP- and pyrethroid-resistant strain, and also showed the highest respiratory rate. It is postulated that the insecticide-resistant strains have modified the morphology of their fat body cells to favour higher stored energy reserves, leading to larger cells. The resistant insects require higher respiratory rates to support a higher energetic need in order to maintain their resistance abilities. It should be mentioned that the resistant strains used in this study were collected in distant regions of Brazil, while the susceptible strain was derived from a population grown in isolation under laboratory conditions for many generations. Therefore, it is highly possible that the physiological differences between the three lines are not entirely fitness cost related but a consequence of the varied genetic backgrounds.

6 CONCLUSIONS A fitness cost is a phenomenon that appears in organisms facing a niche change and adapting to new environments. If the evolutionary pressure persists for many generations it is likely that further genetic changes will occur to alleviate the deleterious effects caused by the initial adaptation, and refine it so that no fitness costs will be detected. Such environmental changes requiring special adaptation include the use of a certain insecticide against an insect pest population. This review has presented many examples, collected worldwide and over many years, in which insects newly adapted to insecticides suffer a fitness cost derived from this new trait, either from a pleiotrophic genetic effect or from a physiological effect. It has also presented cases, such as in the sheep blowfly L. cuprina and the red flour beetle T. castaneum, where the use of the insecticide, even after the development of resistance, eliminated all fitness costs by the development of a modifier and thus fixed the resistance trait in the population, making the insecticide ineffective against the insect pest. Several biological and physiological life history traits can be measured for examining the existence of fitness costs in an insect population; however, it is not always possible to measure these traits easily. Generally, there is also no unison in the populations chosen when comparing resistant and susceptible strains. If possible, the use of isogenic laboratory strains differing only in the resistance trait would be the most accurate way to characterise resistance trait fitness costs; this situation eliminates the possibility that the observed differences between two strains are derived from genetic variance rather than resistance ability. On the other hand, such strains are not always available and do not always truthfully represent the resistance in the field. Additionally, fitness costs are not always imposed by the resistance itself but by the genetic background of the resistance genes. In some cases, the association between resistance and fitness costs can be disrupted, for example by sexual reproduction and subsequent recombination; however, it cannot be disrupted in asexual lineages or species such as aphids when they are reproducing parthenogenetically.



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of field resistance were reported owing to the high dose/refuge policy used to reduce the spread of resistance alleles in the population; however, after 2001, these potatoes were taken out of commercial use as a result of public pressure opposing the use of transgenic plants and the success in controlling CPB using neonicotinoids.37 Experiments conducted on laboratory-selected strains of CPB with Bt resistance showed a high fitness cost in the resistant lines compared with their susceptible counterparts. However, the resistance levels dropped significantly after merely five generations without selection pressure.38 Another study showed that the selection for resistance resulted in prolonged larval development, reduced larval weight, shortened oviposition period, reduced egg mass size and reduced fecundity.39 Yet another study conducted on different laboratory-selected Btresistant strains showed reduced sexual competitiveness of males, reduced population growth rate and increased overwintering mortality.36 The above examples show the cost of becoming a resistant insect against Bt toxins, and all effects seem to be negative. The results further demonstrate the relevance of the refuge strategy, in which the fitness cost of the resistance prevents the dispersal of the pest in the population. A previous study compared the fitness of a field-derived strain of CPB collected in Massachusetts (United States) that carried resistance to both OP and pyrethroids with that of a susceptible laboratory strain.2 In order to avoid possible fitness differences originating from different genetic backgrounds rather than from the resistance trait, two strains, each with a different resistance mechanism (either to OPs or to pyrethroids), were created by backcrossing the field strain with the susceptible line and selecting the offspring on the specific insecticides. It was found that the field-derived strain suffered very high fitness cost in comparison with the susceptible strain: the susceptible strain produced significantly more eggs and larvae, resulting in more than twice as many adult females. Heterozygous offspring from crossing the two strains showed no fitness cost. A similar fitness cost was observed in the laboratory-selected OP-resistant strain. Although all observations met the expectations, in the laboratoryselected pyrethroid-resistant strain, no fitness cost was observed. This result might be attributed to the fact that this strain was exposed to a pyrethroid insecticide for only four generations, which is a short time for a modifier gene to act or evolve. A similar intriguing case of a resistant fitness cost was recently recorded in the red flour beetle (RFB) Tribolium castaneum. Malathion (OP insecticide) has been used intensively in grain silos since the late 1950s, and resistance in this beetle was first documented in 1961 in Kenya. Field surveys conducted between the 1960s and the 1990s showed that about 90% of the RFB populations tested were malathion resistant. Malathion is still in use nowadays to control other storage pests, thus creating a continuous selection pressure against malathion-susceptible individuals of RFB.40 Other studies showed that no fitness cost could be detected in a resistant strain of RFB compared with a susceptible one,41 and that not only did the resistant line suffer from no fitness cost, it showed higher fecundity than the susceptible strain.42 Female progenies contained a higher percentage of resistant individuals, and resistant males had similar or higher rates of last-male copulations.40 A study conducted on the maize weevil, Sitophilus zeamais, which damages stocks of dried corn grains and also corn crops, examined fitness costs in resistant strains of this pest not via life history traits but by measuring the mass of the fat body and the insects’ respiration rates.43 A susceptible laboratory strain

www.soci.org Measurements for testing the existence of fitness costs performed in laboratory conditions can be useful when evaluating specific traits, but often do not correspond to the environment and conditions the insects face in the wild, where they are under some form of environmental stress, and hence costs may be missed under optimal laboratory conditions. There are certain aspects of the fitness that can only be seen outside laboratory conditions, such as survival during overwintering studies like those performed on the peach-potato aphid M. persicae and the mosquito C. pipiens. Other aspects present outside laboratory conditions that can affect fitness are the host plant and its defence chemicals and the presence of entomopathogens and natural enemies. Finally, more studies are needed on changes in insect behaviour that are associated with the evolution of resistance, as insecticides tend to target the insect nervous system where mutations conferring resistance can have pleiotropic effects on nerve function and insect behaviour. These effects on behaviour may lead to changes in the insects’ success under natural conditions, thus imposing indirect fitness costs caused by insecticide resistance.

REFERENCES

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1 Coustau C, Chevillon C and ffrench-Constant R, Resistance to xenobiotics and parasites: can we count the cost?. Tree 15:379–383 (2000). 2 Argentine JA, Marshall CJ and Ferro DN, Relative fitness of insecticide-resistant Colorado potato beetle strains (Coleoptera: Chrysomelidae). Environ Entomol 18:705–710 (1989). 3 McCarroll L and Hemingway J, Can insecticide resistance status affect parasite transmission in mosquitoes?. Insect Biochem Mol Biol 32:1345–1351 (2002). 4 Nauen R and Denholm I, Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. ArchInsectBiochem Physiol 58:200–215 (2005). 5 Puinean AM, Denholm I, Millar NS, Nauen R and Williamson MS, Characterisation of imidacloprid resistance mechanisms in the brown planthopper, Nilaparvata lugens Stål. (Hemiptera: Delphacidae). Pestic Biochem Physiol 97:129–132 (2010). 6 Liu Z and Han Z, Fitness costs of laboratory-selected imidacloprid resistance in the brown planthopper, Nilaparvata lugens Stål. Pest Manag Sci 62:279–282 (2006). 7 Feng YT, Wu QJ, Xu BY, Wang SL, Chang XL, Xie W, et al, Fitness costs and morphological change of laboratory-selected thiamethoxam resistance in the B-type Bemisia tabaci (Hemiptera: Aleyrodidae). J Appl Entomol 133:466–472 (2009). 8 Bass C, Puinean AM, Andrews M, Cutler P, Daniels M, Elias J, et al, Mutation of a nicotinic acetylcholine receptor β subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC Neurosci 12:51 (2011). 9 Foster SP, Denholm I and Devonshire AL, The ups and downs of insecticide resistance in peach-potato aphids (Myzus persicae) in the UK. Crop Prot 19:873–879 (2000). 10 Puinean AM, Foster SP, Oliphant L, Denholm I, Field LM, Millar NS, et al, Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. Plos Gen 6:e1000999 (2010). 11 Foster SP, Woodcock CM, Williamson MS, Devonshire AL, Denholm I and Thompson I, Reduced alarm response by peach-potato aphids, Myzus persicae (Hemiptera: Aphididae), with knock-down resistance to insecticides (kdr) may impose a fitness cost through increased vulnerability to natural enemies. Bull Ent Res 89:133–138 (1999). 12 Foster SP, Denholm I, Thompson R, Poppy GM and Powell W, Reduced response of insecticide-resistant aphids and attraction of parasitoids to aphid alarm pheromone; a potential fitness trade-off. Bull Ent Res 95:37–46 (2005). 13 Foster SP, Harrington R, Devonshire AL, Denholm I, Devine GJ, Kenward MG, et al, Comparative survival of insecticide-susceptible and resistant peach-potato aphids, Myzus persicae (Sulzer) (Hemiptera: Aphididae), in low temperature field trials. Bull Entomol Res 86:17–27 (1996).


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14 Foster SP, Harrington R, Devonshire AL, Denholm I, Clark SJ and Mugglestone MA, Evidence for a possible fitness trade-off between insecticide resistance and the low temperature movement that is essential for survival of UK populations of Myzuspersicae (Hemiptera: Aphididae). Bull Entomol Res 87:573–579 (1997). 15 Foster SP, Tomiczek M, Thompson R, Denholm I, Poppy G, Kraaijeveld AR, et al, Behavioural side-effects of insecticide resistance in aphids increase their vulnerability to parasitoid attack. Anim Behav 74:621–632 (2007). 16 Foster SP, Denholm I, Poppy GM, Thompson R and Powell W, Fitness trade-off in peach-potato aphids (Myzus persicae) between insecticide resistance and vulnerability to parasitoid attack at several spatial scales. Bull Entomol Res 101:659–666 (2011). 17 Lawrence PA, The Making of a Fly: the Genetics of Animal Design. Blackwell Scientific, Oxford, UK (1992). 18 Hemingway J and Ranson H, Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45:371–391 (2000). 19 Pimentel D, Dewey JE and Schwardt HH, An increase in the duration of the life cycle of DDT-resistant strains of the house fly. J Econ Entomol 44:477–481 (1951). 20 McKenzie JA, Whitten MJ and Adena MA, The effect of genetic background on the fitness of DIAZINON resistance genotypes of the australian sheep blowfly, Lucilia cuprina. Heredity 49:1–9 (1982). 21 McKenzie JA and Game AY, Diazinon resistance in Lucilia cuprina; mapping of a fitness modifier. Heredity 59:371–381 (1987). 22 McKenzie JA and Clarke GM, Diazinon resistance, fluctuating asymmetry and fitness in the Australian sheep blowfly, Lucilia cuprina. Genetics 140:213–220 (1988). 23 Davies AG, Game AY, Chen Z, Williams TJ, Goodall S, Yen JL, et al, Scalloped wings is the Lucilia cuprim Notch homologue and a candidate for the modifier of fitness and asymmetry of diazinon resistance. Genetics 143:1321–1337 (1996). 24 Chevilon C, Bourguet D, Rousset FO, Pasteur N and Raymond M, Pleiotropy of adaptive changes in populations: comparisons among insecticide resistance genes in Culex pipiens. Genet Res Camb 70:195–204 (1997). 25 Gazave E, Chevillon C, Lenormand T, Marquine M and Raymond M, Dissecting the cost of insecticide resistance genes during the overwintering period of the mosquito Culex pipiens. Heredity 87:441–448 (2001). 26 Berticat C, Boquien G, Raymond M and Chevillon C, Insecticide resistance genes induce a mating competititon cost in Culex pipiens mosquitoes. Genet Res Camb 79:41–47 (2002). 27 Berticat C, Duron O, Heyse D and Raymond M, Insecticide resistance genes confer a predation cost on mosquitoes, Culex pipiens. Genet Res Camb 83:189–196 (2004). 28 Bourguet D, Guillemaud C, Chevilon C and Raymond M, Fitness costs of insecticide resistance in natural breeding sites of the mosquito Culex pipiens. Evolution 58:128–135 (2004). 29 Rivero A, Magaud A, Nicot A and Vezilier J, Energetic cost of insecticide resistance in Culex pipiens mosquitoes. J Med Entomol 48:694–700 (2011). 30 Foster SP, Young S, Williamson MS, Duce I, Denholm I and Devine GJ, Analogous pleiotropic effects of insecticide resistance genotypes in peach-potato aphids and houseflies. Heredity 91:98–106 (2003). 31 Gahan LJ, Pauchet Y, Vogel H and Heckel DG, An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PloS Genet 6:e1001248 (2010). 32 Gassmann AJ, Carriere Y and Tabashnik BE, Fitness costs of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 54:147–163 (2009). 33 Cao G and Han Z, Tebufenozide resistance selected in Plutella xylostella and its cross-resistance and fitness cost. Pest Manag Sci 62:746–751 (2006). 34 Boivin T, Chabert dHieres C, Bouvier JC, Beslay D and Sauphanor B, Pleiotropy of insecticide resistance in the codling moth, Cydia pomonella. Ent Exp Appl 99:381–386 (2001). 35 Delisle J and Vincent C, Modified pheromone communication associated with insecticidal resistance in the obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera: Tortricidae). Chemoecology 12:47–51 (2002). 36 Alyokhin A and Ferro DN, Relative fitness of Colorado potato beetle (Coleoptera: Chrysomelidae) resistant and susceptible to the Bacillus thuringiensis Cry3A toxin. J Econ Entomol 92:510–515 (1999).


Pest Manag Sci 2012; 68: 1431–1437


www.soci.org

37 Shelton AM, Zhao JZ and Roush RT, Economic, ecological, food safety and social consequences of the deployment of Bt transgenic plants. Ann Rev Entomol 47:845–881 (2002). 38 Rahardja U and Whalon ME, Inheritance of resistance to Bacillus thuringiensis subsp. Tenebrionis CryllIA o-endotoxin in Colorado potato beetle (Coleoptera: Chrysomelidae). J Econ Entomol 88:21–26 (1995). 39 Trisyonoi A and Whalon ME, Fitness costs of resistance to Bacillus thuringiensis in Colorado potato beetle (Coleoptera: Chrysomelidae). J Econ Entomol 90:267–271 (1997). 40 Arnaud L and Haubruge E, Insecticide resistance enhances male reproductive success in a beetle. Evolution 56:2435–2444 (2002).

41 Beeman RW and Nanis SM, Malathion resistance alleles and their fitness in the red flour beetle (Coleoptera: Tenebrionidae). J Econ Entomol 79:580–587 (1986). 42 Haubruge E and Arnaud L, Fitness consequences of malathion-specific resistance in red flour beetle (Coleoptera: Tenebrionidae) and selection for resistance in the absence of malathion. J Econ Entomol 94:552–557 (2001). 43 Guedes RNC, Oliveira EE, Guedes NMP, Ribeiro B and Serrao JE, Cost and mitigation of insecticide resistance in the maize weevil, Sitophilus zeamais. Physiol Entomol 31:30–38 (2006).

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Pest Manag Sci 2012; 68: 1431–1437

