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Pesticide Resistance: Strategies and Tactics for Management. 1986. National Academy Press, Washington, D.C. Factors :Influencing the Evolution of Resistance GEORGE P. GEORGHIOU and CHARLES E. TAYLOR Any attempt to devise management strategies for delaying or fore- stalling the evolution of pesticide resistance requires a thorough understanding of the parameters influencing the selection process. The parameters known to influence this process in pest populations are presented systematically under three categories genetic, bio- logicallecological, and operational and their relative importance is discussed with reference to available case histories. INTRODUCTION More than 447 species of arthropods have now developed resistance to insecticides (Georghiou, this volume). The main weapon for countering this resistance has been the use of alternative chemicals with structures that are unaffected by cross-resistance. The gradual depletion of available chemicals as resistance to them developed has revealed the limitations of this practice and emphasized the need for maximizing the "useful life" of new chemicals through their application under conditions that delay or prevent the devel- opment of resistance. To achieve this goal it is essential to understand the parameters influencing the selection process. It is well established that resistance does not evolve at the same rate for all organisms that come under selection pressure. Resistance may develop rapidly in one species, more slowly in another, and not at all in a third. For example, despite enormous selection pressure during many years of intensive DOT treatment in the corn belt of the United States, the corn borer showed no evidence of resistance. Yet house flies in many areas developed resistance 157

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158 POPULATION BIOLOGY OF PESTICIDE RESISTANCE TABLE 1 Known or Suggested Factors Influencing the Selection of Resistance to Insecticides in Field Populations A. Genetic a. Frequency of R alleles b. Number of R alleles c. Dominance of R alleles d. Penetrance, expressivity, interactions of ~ alleles e. Past selection by other chemicals f. Extent of integration of R genome with fitness factors B. Biological/Ecological 1. Biotic a. Generation turnover b. Offspring per generation c. Monogamy/polygamy, parthenogenesis 2. Behavioral/Ecological a. Isolation, mobility, migration b. Monophagy/polyphagy c. Fortuitous survival, refugia Operational 1. The chemical a. Chemical nature of pesticide b. Relationship to earlier-used chemicals c. Persistence of residues, formulation 2. The application a. Application threshold b. Selection threshold c. Life stage(s) selected d. Mode of application e. Space-limited selection f. Alternating selection SOURCE: Adapted from Georghiou and Taylor (1976). within two to three years under selection pressure by this insecticide. Even within a species, resistance may develop more rapidly in one population than in another. The Colorado potato beetle, for example, showed far greater propensity for resistance on Long Island than on the mainland (Forgash, 1981, 1984). There are many factors that can influence the rate at which this evolution proceeds. One effort to systematize them is shown in Table 1, modified slightly from a classification we proposed and discussed earlier (Georghiou and Taylor, 1976, 1977a,b). The factors are grouped into three categories, depending on whether they concern the genetics of resistance, the biology/ ecology of the pest, or the control operations used. Most factors in the first two categories cannot be controlled, and the importance of some may not even be determined until resistance has already developed. Only through

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THE EVOLUTION OF RESISTANCE 159 hindsight, for example, can one obtain any idea about the initial frequency of the alleles conferring resistance. Nor is it usually possible to measure dominance until one isolates such alleles and makes the appropriate crosses. In some cases these issues may be addressed in laboratory studies where resistant strains can be developed by selection on large, recently colonized populations. Nonetheless, some factors that influence the evolution of resis- tance are under man's control, especially those related to the timing and dose of insecticide application (Operational Factors, Table 11. The problem is to identify them and determine how their manipulation under the existing genetic and biological/ecological constraints may retard the evolution of resistance. During the past few years, important contributions have been made by workers in a handful of laboratories, mainly in the United States, the United Kingdom, and Australia (Coming, 1977a,b, 1979a,b; Georghiou and Taylor, 1977a,b; Haile and Weidhaas, 1977; Curtis et al., 1978; Conway and Comins, 1979; Sutherst and Comins, 1979; Sutherst et al., 1979; Taylor and Geor- ghiou, 1979, 1982; Gressel and Segel, 1982; Muggleton, 1982; Tabashnik and Croft, 1982; Levy et al., 1983; McPhee and Nestmann, 1983; Taylor et al., 1983; Wood and Cook, 1983; Knipling and Klassen, 1984; Mani and Wood, 1984; McKenzie and Whitten, 19841. Some of these contributions are examined in other papers in this symposium. We shall confine ourselves to a discussion of how, in a historical perspective, the accumulated knowledge on the occurrence and dynamics of resistance leads to the recognition of these factors (Table 1) as important. GENETIC FACTORS IN RESISTANCE Evolutionists frequently assume that organisms have the capacity to evolve nearly any type of resistance. From this follow many of the "optimization" arguments and the "adaptationist program" (Lewontin and Gould, 1979~. This assumption is not warranted for insecticide resistance. Some populations obviously do not have the capacity to come up with the necessary resistant alleles in the first place, despite what would seem to be an obvious advantage for doing so. The corn borer is one species that did not. The paucity of cases of resistance to arsenicals in insects and to copper fungicides in plant path- ogens are other examples. It has been speculated that herbivorous species, which have frequently evolved the capacity to deal with plant alkaloids, are in some sense preadapted to dealing with the problems posed by dangerous chemicals in their environment (Croft and Brown, 19751. Related to this is the fact that there may be many ways to achieve resis- tance-by detoxifying the chemicals, altering site specificity, reducing pen- etration, behavioral avoidance of residues, to name a few. When more avenues are open it would be expected that resistance would evolve more easily. Once alleles conferring resistance are present in the population, the fre

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160 POPULATION BIOLOGY OF PESTICIDE RESISTANCE quency at which they occur may be important. There are several reasons for this. Obviously if the initial frequency is higher, then resistance has a head start. There may, however, be an Allee effect, so if the population is reduced to a sufficiently low level, the resulting population size is too small to sustain positive growth, perhaps by failure to find mates. More important, the se- lection pressures and immigration rates may impose an unstable equilibrium of gene frequencies, below which resistance alleles decrease in fitness and above which they increase (Haldane, 19301. In this case the initial frequency is especially important. In practice the importance of many factors for resistance seems related to this unstable equilibrium. In the simplest instance this equilibrium depends largely on initial gene frequency, dominance, and immigration. These factors in turn may depend on others. Imagine a population with resistant allele, R. at a low frequency. Homozygous RR individuals may occur if the population is large enough, but will be very few in number. If the resistance is recessive or can be made recessive by application of an appropriately high dose of insecticide (Taylor and Georghiou, 1979), then following insecticide use all of the susceptible homozygotes (SS) and heterozygotes (RS) will be elimi- nated, leaving only the very few RR. If now there is an inflow of largely susceptible migrants, then those few RR will mate with SS homozygote immigrants, and the offspring for the next generation will be almost all SS and RS. These can be killed with another application of insecticide, keeping the population under control. It is possible to study this result mathematically and describe precisely when it should be observed (Coming, 1977a; Curtis et al., 1978; Taylor and Georghiou, 1979~. It is generally thought that resistance alleles are mildly deleterious prior to insecticide use, so that they are present initially at some sort of mutation- selection balance. This would typically be at an allele frequency of 10-2 to 10-4, with the RR homozygotes present at 10-4 to 10-~. Of course if two loci are required or if more than one nucleotide change is necessary then the frequency may be substantially less (Whitten and McKenzie, 19821. McDonald (1959) proposed that dieldrin resistance, being more dominant than DDT resistance in Anopheline mosquitoes, would evolve at a faster rate. In theory there should be little difference between rates of evolution of dominant and recessive alleles in the absence of immigrants. But, in fact, McDonald's prediction has been more-or-less realized. The reason for this is probably related to the unstable equilibrium described above, which exists only when the resistant allele is recessive. Dominance typically depends on the dose applied. Figure 1 shows the dosage-response curves for three genotypes of a mosquito, Culex quinque- fasciatus, exposed to a pyrethroid insecticide. When a small dose, Ds, is applied, the heterozygotes survive, but with a larger dose, Do, they do not. Thus, with Ds, the resistance is functionally dominant, but with Do, it is - ~ --r r

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THE EVOLUTION OF RESISTANCE 98 95 90 80 70 60 50 40 30 20 0 .ooo 1 .001 .o 1 CONC. NRDC 167 (ppm) 2 ~- / 't/ /+ / / l - / Ds / DL / , , , , , , , , 1 , , , a, , , , 1 , , , , , , , ,41 , , , . , , , i] 3 .1 1. 7 6 an 5 m 0 tar 4 161 FIGURE 1 Dosage-response lines for larvae of Culex quinquefasciatus susceptible, het- erozygous, and resistant tested with permethrin. The dominance is seen to depend on dose: with a small dose (Ds), resistance is functionally dominant, whereas with a large dose (D~) it is functionally recessive. functionally recessive. Modifier genes are known to change the location of the heterozygote line, typically moving it to the right. Modifier genes may be important in other ways as well, most notably by helping to integrate the resistance allele into the rest of the genome to produce a "harmoniously coadapted genome" in the sense of Mayr (1963) or Dob- zhansky (19701. There may be many pleiotropic effects from the substitution of a resistant allele for its wild-type alternative. Many of these are likely to be detrimental, so the resistant allele is initially mildly deleterious (Ferrari and Georghiou, 19811. Later, when there has been an opportunity for the modifiers to be selected and the pleiotropic side effects have been compen- sated for, such a disadvantage diminishes or disappears. With few exceptions resistant populations demonstrate lower fitness than their susceptible counterparts. Continued selection may improve fitness through coadaptation of the resistant genome, resulting in more stable resistance. A dramatic illustration of this is a laboratory experiment of Abedi and Brown (19601. They selected for resistance, then released selection, then selected, and so forth. After several cycles resistance evolved much more rapidly and was more stable than initially. Almost certainly, modifier genes were the cause. Instability of resistance may not necessarily be due entirely to differences in fitness, however. For example, genes for resistance to an organophosphate (temephos), a pyrethroid (permethrin), and a carbamate (propoxur) were introduced into a susceptible strain of Culex quinquefasciatus through a

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162 POPULATION BIOLOGY OF PESTICIDE RESISTANCE system of backcrosses. The resulting synthetic was subsequently divided into substrains and selected by these insecticides. Tests showed that the stability of resistance in each strain differed considerably: Organophosphate resistance regressed rapidly, pyrethroid resistance moderately, but resistance to the carbamate showed considerable persistence (Georghiou et al., 19831. It is, therefore, likely that the mechanism of resistance involved in each case may influence its persistence in populations. Past selection by insecticides may facilitate evolution of resistance to new insecticides because of cross-resistance. Certain mechanisms of resistance have been found to confer resistance not only within an insecticide class but across classes as well. A classic example of this is the kdr gene. Both DDT and pyrethroids interfere with sodium gates along the axons of nerve cells. The kdr allele, by altering properties of the axonal membrane, makes it less receptive to binding. Thus, it confers resistance to pyrethroids in populations that had been selected earlier by DDT and vice versa (Priester and Georghiou, 1978; Omer et al., 19801. Recently, Sawicki et al. (1984) showed that an esterase, E.0.33, selected in house flies by the organophosphates malathion and trichlorphon, confers mild cross-resistance to pyrethroids as well. By itself the esterase is of no consequence in the control of house flies with pyrethroids because the doses used in practice are strong enough to overcome the mild resistance it confers. In some populations, however, kdr is also present, albeit at low frequencies, probably as a result of previous use of DDT for control of flies. In these populations the introduction of pyrethroids led to the simultaneous selection of kdr, as well as the esterase, and to rapid control failure of pyrethroids. Thus, the earlier, sequential use of two different groups of insecticides, organophosphates and DDT, contributed to the rapid failure of a third group of compounds, the pyrethroids, through the selection of common resistance mechanisms. The Colorado potato beetle also provides a pertinent example. On Long Island the population of this species required seven years to develop resistance to DDT, the first synthetic insecticide with which it was selected. The same population has required progressively less time to develop resistance to the subsequently used chemicals: five years for resistance to azinphosmethyl, two for carbofuran, two for pyrethroids, and one for pyrethroids with a synergist (Georghiou, this volume). BIOLOGICAL/ENVIRONMENTAL FACTORS IN RESISTANCE Ecology and life histories may dramatically alter the responsiveness to the selection that leads to resistance. Most obvious, of course, is that the larger the number of generations per year, the faster the evolution of resistance. The fruit tree mite Panonychus ulmi, which has as many as 10 generations

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THE EVOLUTION OF RESISTANCE 5 4 3 L`J 1~ 2 (n Ad 0 1 lo] Z 0.5 loll Be\ I I I 3 4 5 6 8 10 20 YRS TO APPEARANCE OF RESISTANCE FIGURE 2 Relationship between generations per year and appearance of resistance in species selected by soil applications of aldrin/dieldrin. m.\ \v ~ CZAR imp ,. , , ,1 , , 163 I ~ /ly/emyo sp. ~ J /ly/emyo sp. m Conoderus fo//i I]Z D/obrol~co /ong/corn/s LIZ Amph/mo//on majo//s AT Popi///c' japon/ca IBM Me/onolus tomsuyens/s per year, has developed resistance rapidly to many groups of insecticides. But another fruit tree mite Bryobia rubrioculus, which has only two gen- erations per year, has yet to be reported as resistant (Georghiou, 19811. Figure 2 illustrates the relation between generation turnover in various soil-inhabiting pest species and the number of years it has taken them to manifest resistance to soil applications of aldrin/dieldrin (Georghiou, 19801. It can be seen that root maggots (Hylemya spp.), which complete three to four generations per year, evolved resistance after five years of exposure, while Conoderus fall), with two generations per year, evolved resistance in six years. Diabrotica longicornis, Amphimallon majalis, and Popillia ja- ponica, each with one generation per year, have required 8 to 14 years for resistance development, while the sugarcane wireworm (Melanotus tamsuy- ensis) in Taiwan, with a two-year life cycle, has taken 20 years to develop resistance. A similar correlation between generation turnover and rate of evolution of resistance is reported for apple tree pests by Tabashnik and Croft (1985~. All else being equal, populations with a higher reproductive potential are able to withstand a higher substitutional load, that is, they can tolerate a higher intensity of selection. Consequently one would expect to see a positive correlation between the rate of evolution of resistance and fertility. We are not aware of generalizations regarding this, however; nor are we aware of generalizations regarding monogamy/polygamy or mode of reproduction. Because of the unstable equilibrium discussed above, immigration may have

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164 POPULATION BIOLOGY OF PESTICIDE RESISTANCE a decisive role in retarding evolution. It is essential, however, that the few surviving RR homozygotes mate with SS immigrants. One might then expect polygamous species to evolve more slowly. Related to this is the importance of sexual selection and evolution of sex. It is thought that the principal advantage conferred by sexual systems over asexual ones is the ability to respond to environmental challenges, especially if the challenges are of- fered in rapid succession (the red queen hypothesis, as detailed in May- nard-Smith, 1978~. There is clearly an opportunity for much interesting research here. Polyphagous insect pests tend to develop resistance more slowly than monophagous ones. Two factors may contribute to this: A smaller part of polyphagous species are likely to be exposed, hence the selection is less intense on these species; because some of the insects would be in untreated refugia, they would provide a reservoir from which untreated, susceptible migrants could come. This may be the reason that resistance in ticks of livestock in South Africa appeared first in one-host species and only later in species that attack two or three hosts (Whitehead and Baker, 1961; Wharton and Roulston, 19701. Similarly, among aphids the spotted alfalfa aphid in California was one of the first to develop resistance, but the lettuce aphid, which moves to poplars during part of the year, has been controlled without evidence of resistance. It is interesting that on strictly biochemical criteria polyphagy may enhance the potential of a species to develop resistance. Krieger et al. (1971) have provided evidence that in lepidopterous larvae the insecticide-metabolizing activity of microsomal oxidases is higher in polyphagous than in monopha- gous species. It is possible that a similar mechanism is involved in the tendency of plant-feeding insects to evolve resistance before their parasitoids do (Croft, 1972; Georghiou, 1972), although it should be apparent that the parasitoids can survive only after their hosts have become resistant, giving an evident bias in sampling. We have suggested that one of the most important features of an insect's ecology, insofar as resistance is concerned, is the amount of immigration of susceptible individuals (Georghiou and Taylor, 1977a). After treatment with insecticides only a few RR individuals will usually survive (if a large enough dose, Do, is used to make the resistance functionally recessive). If, then, enough SS immigrants arrive and mate with them, for all practical purposes the offspring will consist only of RS heterozygotes and SS homozygotes, both of which can be killed with subsequent treatment. If, however, there are no immigrants, or if they are too few, then substantial numbers of RR individuals will be produced and the population will be on its way to evolving resistance. This gives the unstable equilibrium alluded to above. The critical issues here are the numbers of RR survivors and SS immigrants. Low pop- ulation densities contribute to fewer RRs, and immigration rates, refugia, polyphagy, and polygamy all contribute to this process.

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THE EVOLUTION OF RESISTANCE 165 As an illustration of the adverse effect of isolation, or absence of immi- gration, it may be noted that the highest resistance of house flies in California was found in populations breeding inside poultry houses. These houses had been screened, ostensibly for the purpose of excluding flies from entering. Ironically, prevention of immigrants has probably contributed to even higher levels of resistance. In normal pest control all surviving individuals have not necessarily been reached by chemical treatment. Depending on the biological and behavioral characteristics of a species, a proportion may be present in refugia at the time of treatment, thus escaping selection. Refugia may consist of plant tissues, distorted foliage, growth buds, erineum, and the like, or they may represent a physiological state of lower susceptibility, such as diapause or pupation in soil. Whatever the reason, such refugia may be very important in providing a source of susceptible immigrants, thus retarding evolution (Georghiou and Taylor, 19761. The eriophyid mite Aceria sheldoni, which inhabits citrus buds, has been controlled for several years with chlorobenzilate and has yet to develop resistance. The citrus rust mite, however, also an eriophyid but feeding on leaf surfaces, has been reported as resistant. Refugia may often be an important mechanism for delaying the buildup of resistance. Relative to the inward flux of migrants from the outside, they are less subject to the vagaries of weather, breeding sites, and other factors that may influence the timing or intensity of immigration from the outside. Further, we have suggested that refugia may be created artificially by inten- tionally excluding from treatment some segment of the population and it can thus be an operational factor in resistance management (Georghiou and Tay- lor, 1977b). Even with refugia, however, some inflow of migrants is nec- essary for an unstable equilibrium to exist. OPERATIONAL FACTORS IN RESISTANCE Operational factors in resistance are those related to the application of pesticides and are thought of as being under man's control. Most obviously these include the timing, dose, and formulation of pesticides used. But, in a way, effective dominance, refugia, and immigration may also be under some degree of control if conditions of application are made more-or-less favorable to them. For example, as indicated above refugia may be created by deliberately excluding some part of the population from treatment. The efficacy of this has been explored by Denholm et al. (1983), using house flies that had already been partially selected for resistance to a long-residual, synthetic pyrethroid, permethrin. Within three weeks after a single application of this persistent insecticide, to which virtually all flies were exposed, they became very resistant. But when a closely related pesticide, bioresmethrin, was applied as a space spray at two-week intervals, no buildup of resistance was observed. This difference was attributed to the fact that bioresmethrin

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166 POPULATION BIOLOGY OF PESTICIDE RESISTANCE exerted only an immediate toxic effect on the adult flies directly exposed to it. The many flies not in the adult stage, and thus in refugia, became part of the breeding population when they later emerged. Timing of insecticide use may often be important. For an unstable equi- librium to exist there must be very few RR survivors following the initial treatment. This will occur if the R allele frequency is low, and also when the total population size is low. All else being equal, it is desirable to treat the population before its numbers become too large. Pesticide dosage has been discussed above as an important determinant of dominance. Related to this are the formulation and rate of pesticide decay. After initial application the concentration of pesticide effectively decreases, because of breakdown, dilution and so forth. If this occurs rapidly then the population can be thought of as effectively receiving either a large dose, Do, or none at all. With a persistent pesticide this occurs slowly, however, and for some time there is an effectively small dose, Ds, that may be very favorable for resistance development. A persistent pesticide may also kill susceptible immigrants and thus effectively prevent immigration. Computer simulations have indicated that the timing and economic thresh- olds- of application make little difference in the absence of migration. This is because selection is usually so intense that the selection coefficients are virtually the same in all these circumstances. Of course the choice of insecticide is very important. Usually there is some degree of cross-resistance to other pesticides within the same class. Depending on the mechanism of resistance, there may also be cross-resistance among classes. Especially notable are cross-resistance between DDT and pyrethroids due to the gene kdr and between carbamates and organophos- phates due to selection of "insensitive" acetylcholinesterase (Hama, 19831. Whether insecticides are best used in combinations or sequentially is at present unclear. There are some suggestions that combinations may be more effective if there is much dominance and immigration in the system (Man), in press; C. F. Curtis, London School of Hygiene and Tropical Medicine, personal communication, 19851. Our simulations, using quantitative genetic models, indicate that there is little difference if one works under the constraint of a constant selection differential. The available experimental evidence also suggests that there is little difference. Georghiou et al. (1983) selected mos- quitoes by various combinations or sequences of temephos, permethrin, and propoxur, representatives of the three major classes of insecticides. The populations responded more-or-less the same. They observed, however, that there was some negative cross-resistance, in that strains that were more resistant to the organophosphate tended to be more susceptible to the pyr- ethroid. Just how this can be put to best use in an operational sense is still unclear. There is certainly a need for more Experimental and theoretical work on this important problem.

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THE EVOLUTION OF RESISTANCE 167 CONCLUSION Because insecticide resistance has become such a serious problem in recent years, it is abundantly clear that merely switching to new insecticides when the current one is no longer effective cannot continue. Integrated pest man- agement, which will almost always involve some use of pesticides, is now regarded as essential. Recognizing and manipulating those factors that may help retard resistance should be an integral part of any such program. Throughout the preceding discussion we have emphasized the effects of pesticides on the target population alone. No mention has been made of the effects on com- petitors, parasites, or predators. These should be a part of the deliberation of which strategy to use, especially when considering the use of several insecticides in combinations. In any practical problem there are bound to be many unknowns, even surprises. There is a need for better knowledge of the factors influencing the evolution of resistance, enabling us to better assess the risk of resistance developing in each individual case and thus to formulate more realistic management practices for delaying or forestalling its evolution. REFERENCES Abedi, Z. H., and A. W. A. Brown. 1960. Development and reversion of DDT-resistance in Aedes aegypti. Can. J. Genet. Cytol. 2:252-261. Comins, H. N. 1977a. The development of insecticide resistance in the presence of migration. J. Theor. Biol. 64:177-197. Comins, H. N. 1977b. The management of pesticide resistance. J. Theor. Biol. 65:399-420. Comins, H. N. 1979a. Analytical methods for the management of pesticide resistance. J. Theor. Biol. 77:171-188. Comins, H. N. 1979b. The management of pesticide resistance: Models. Pp. 55-69 in Genetics in Relation to Insect Management, M. A. Hoy and J. J. McKelvey, eds. New York: The Rockefeller Foundation. Conway, G. R., and H. N. Comins. 1979. Resistance to pesticides: Lessons in strategy from mathematical models. Span 22:53-55. Croft, B. A. 1972. Resistant natural enemies in pest management systems. Span 15:19-22. Croft, B. A., and A. W. A. Brown. 1975. Response of arthropod natural enemies to insecticides. Annul Rev. Entomol. 20:285-335. Curtis, C. F., L. M. Cook, and R. J. Wood. 1978. Selection for and against insecticide resistance and possible methods of inhibiting the evolution of resistance in mosquitoes. Ecol. Entomol. 3:273-287. Denholm, I., A. W. Farnham, K. O'Dell, and R. M. Sawicki. 1983. Factors affecting resistance to insecticides in house flies, Musca domestica L. (Diptera: Muscidae). I. Long-term control with bioresmethrin of flies with strong pyrethroid-resistance potential. Bull. Entomol. Res. 73:481- 489. Dobzhansky, T. 1970. Genetics and the Evolutionary Process. New York: Columbia University Press. Ferrari, J. A., and G. P. Georghiou. 1981. Effects of insecticidal selection and treatment on reproductive potential of resistant, susceptible, and heterozygous strains of the southern house mosquito. J. Econ. Entomol. 74:323-327.

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