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Pesticide Resistance: Strategies and Tactics for Management. 1986. National Academy Press, Washington, D.C. Pleiotropy and the Evolution of Genetic Systems Confernng Resistance to Pesticides MARCY K. UYENOYAMA The evolution of pesticide detoxification is portrayed as the re- sponse to extreme selection pressures by a genetic network of ca- tabolic enzymes and their regulators. Empirical and theoretical studies necessary for the assessment of this view and the exploration of its implications are described. INTRODUCTION Effective strategies designed to oppose the evolution of pesticide resistance must address the problem of preventing or retarding the development of the full expression of resistance, as well as the problem of controlling the density of highly resistant individuals. Most of the extensive mathematical and nu- merical models reviewed by Taylor (1983) investigate only the latter question, the control of quantitative aspects of resistance, including the rate of increase of highly effective mechanisms of resistance within and among populations. In this paper I consider the evolutionary process at the earlier stage, in which qualitative improvement of the expression of resistance arises as an adaptation both to the pesticide and to natural selection. In this discussion I consider pesticide resistance as an expression of an entire genetic system and examine the implications of this multilocus per- spective with respect to the optimal conditions for its evolution. Pesticide resistance in insects and novel metabolic capabilities in microorganisms rep- resent adaptations to selection of extreme intensity that are fashioned from elements of normal metabolism. Sewall Wright's shifting balance theory, which addresses the significance of population structure to the evolution of 207

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208 POPULATION BIOLOGY OF PESTICIDE RESISTANCE genetic networks, provides the theoretical framework of this discussion, which seeks to convey some sense of why answers to such questions are essential from an evolutionary perspective. EVOLUTION OF NEW FUNCTION IN MICROORGANISMS Biochemical and genetic analyses of new catabolic pathways in laboratory populations of bacteria have yielded a wealth of information on the assembly and integration of genetic networks (Clarke, 1978; Mortlock, 1982; Hall, 1983~. The processes of adaptation occurring in microbes in the laboratory and in pests of commercial crops in the field share two characteristics: the extraordinary intensity of selection imposed and the sophistication of the genetic mechanisms for the coordinated induction and repression of catabolic enzymes that respond. Responses of modern microbes to laboratory selection may in fact reveal more about the evolution of pesticide resistance than the evolution of primitive microorganisms. Selection Procedures Two major strategies for selecting mutants that possess extended metabolic capabilities have been adopted: one approach challenges populations to sub- sist on a novel substrate and the other requires the restoration of a known function by strains in which the structural locus that normally performs the function has been deleted. Investigators using the first approach focus on the identification of the regulatory and structural loci that participate in the new pathways. For example, Klebsiella and Escherichia populations presented with sugars one or several biochemical steps removed from the normal sub- strates constructed new metabolic pathways by borrowing enzymes from existing pathways (Mortlock, 1982~. Clarke (1978) reviews experiments on Pseudomonas that used a variant of this first approach: altered regulation and activity of a specific amidase was selected by challenging populations with analogues of the normal substrate (acetamide). Investigators using the second approach focus on the execution of a specific task by a specific operon; they study the re-evolution of a key link in a known pathway rather than the formation of entire pathways. Selection has been imposed on Escherichia cold strains carrying deletions of the lacZ (,B-galactosidase) gene from the lac operon to obtain lines in which ~B-galactosidase activity has been restored. The mutations of the regulatory and structural loci of the EBG (evolved ,B- galactosidase) operon, from which a well-regulated, high-activity response was eventually fashioned, are reviewed by Hall (19831. On the molecular level the appearance de novo of a new functional locus, with appropriate sequences for initiating transcription, directing the pro- cessing of the mRNA, initiating translation, and terminating translation,

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PLEIOTROPY AND GENETIC SYSTEMS CONFERRING RESISTANCE 209 represents an extraordinary macromutation. In every case the response that permitted survival involved existing enzymes having the fortuitous ability to metabolize the substrate. Regulatory mutations that induced the production of these enzymes in the absence of their normal substrates played key roles. Hall and Hartl (1974) obtained mutants characterized by hyperinducibility of the EBG operon by lactose, as well as constitutive mutants. In other experiments the key catabolic enzyme was induced by a substance in the selective medium (Clarke, 1978~. Costs Associated with Pleiotropy If the modification of normal regulation or specificity of the key enzyme favored under artificial selection interferes with its original function, then the mutant form may suffer a disadvantage relative to the wild type in the absence of artificial selection. This disadvantage under natural selection may be regarded as the cost of pleiotropy. The EBG operon, possibly "an evo- lutionary remnant" (Clarke, 1978) of a relict lactose utilization pathway, may represent an exception to this generalization because it does not appear to perform any essential metabolic function in wild-type cells. Even in this case constitutive synthesis may reduce fitness under natural selection through wasteful overproduction of an enzyme (Hall, 1983; Clarke, 19781. Further, metabolism of possibly toxic analogues of the new substrate may inhibit the growth of organisms with nonspecific induction mechanisms (Hall, 19831. Disruption of normal regulation may contribute to pleiotropic costs through imbalances of catabolites and catabolic repression (Mortlock, 19821. Clarke (1978, Table III) lists a number of amides whose catabolism can provide carbon and nitrogen but inhibits growth. Scangos and Reiner (1978) dem- onstrated that the inhibition (by compounds to which the wild type was insensitive) of E. cold strains capable of growing on the novel substrate (xylitol) was due to the activity of an enzyme whose derepression permitted use of xylitol. Further, inhibition by the novel substrate itself was relieved only at the expense of the ability to metabolize the normal substrate. Further evolution of microbial populations with extended metabolic ca- pabilities likely involves improved effectiveness and specificity of the re- sponse to the substrate (Mortlock, 1982; Hall, 19831. Wu et al. (1968) obtained a structural locus mutation that improved the rate of catalysis of xylitol and halved the doubling time of constitutive Klebsiella populations. A second mutation improved xylitol uptake and permitted another 50 percent reduction in doubling time. A sequence of four mutations in the regulatory and structural loci of the EBG operon was required for the formation of a well-regulated lactose utilization operon, in which lactose induced the syn- thesis of a modified EBG enzyme whose catalytic activity converted lactose into an inducer of the lactose transport system.

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210 POPULATION BIOLOGY OF PESTICIDE RESISTANCE These examples support the view that prolonged selection in the new environment results in the refinement of the response that permits survival in that environment. Inducibility, higher rates of activity, greater specificity, and even modification of the catalyzed conversion improve the operation of the new pathway. Further, if the population repeatedly encounters both the original and the novel environments, then adaptation entails the ability to respond to both selection regimes (Clarke, 1978; Mortlock, 1982~. Indepen- dent regulation of the old and new functions, which permits the expression of genetic loci primarily in response to the selective regime under which they evolved, requires the release of the elements of the new pathway from the control of the old pathway (Mortlock, 1982~. Reduction in pleiotropic costs associated with new functions permits adaptation by the population to both environments. MECHANISMS OF PESTICIDE RESISTANCE The effective, highly evolved mechanisms for tolerating or detoxifying pesticides possessed by laboratory strains derived from resistant populations are not very likely to be representative of the rudimentary resistance mech- anisms that were marshaled on initial exposure to the pesticides. Inferences regarding aspects of the resistance mechanism (including its specificity, the type of mutations involved, and the magnitude of pleiotropic costs) made on the basis of comparisons among inbred laboratory strains are relevant to questions surrounding the initial stages of the evolution of resistance only to the extent that differences among such strains reflect variation that was present in the natural populations in which resistance evolved. This caveat applies with particular force to the assessment of pleiotropic costs, because such costs may themselves evolve toward lower values as regulation of the resis- tance mechanism and its integration into the genome proceeds. In this section I draw analogies between the microbial evolution experiments and the evo- lution of pesticide resistance, while recognizing that any interpretations are open to question. Specificity of the Response Detoxification of certain classes of pesticides involves catabolic enzymes of low substrate specificity (Plapp and Wang, 19831. The primary function of the mixed-function oxidases that detoxify carbamate and organophosphate pesticides in the house fly and other insects appears to lie in normal metab- olism (Georghiou, 19721. Resistant strains produce unusually high concen- trations of microsomal oxidases that differ from the oxidases of susceptible strains with respect to substrate specificity and other properties (Plapp, 1976~. Resistance to juvenile hormone analogues may also involve these broad

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PLE!OTROPY AND GENETIC SYSTEMS CONFERRING RESISTANCE 211 spectrum oxidases (Plapp, 1976; Tsukamoto, 19831. Nonspecific resistance to a variety of pesticides may involve mechanical rather than catabolic de- fenses. A reduction in rates of absorption of pesticides contributes to resis- tance in diverse organisms (Georghiou, 1972; Plapp, 19761. Such mechanisms of reduced penetration confer limited resistance and are most effective in combination with detoxification. Specific structural changes have also been implicated in mechanisms of resistance. The shift in substrate specificity of certain mixed-function oxi- dases cited above indicates that structural as well as regulatory mutations are involved. Plapp (1976) describes qualitative differences in acetylcholines- terase and carboxylesterase activity that improve tolerance to or detoxification of organophosphate and carbamate insecticides. Loci controlling specific modifications of acetylcholinesterase and sensitivity of neurons to DDT reside on chromosomes II and III in the house fly (Tsukamoto, 19831. The Evolution of Pleiotropic Costs Crow (1957) demonstrated that the chromosomes contribute nonepistati- cally to the survival rate of Drosophila melanogaster exposed to DDT. He hypothesized that epistatic networks can evolve under close inbreeding or asexual reproduction, but that selection in outcrossing, genetically hetero- geneous populations produces nonepistatic mechanisms of resistance. If ele- ments of rudimentary resistance mechanisms evolving in nature contribute nonepistatically to fitness in both treated and untreated environments, then the characterization of resistance as the response of a genetic network is inappropriate. No direct evidence on this point is available; Keiding (1967) has suggested that reversion may be caused by elements whose deleterious effects reflect a lack of integration with the genetic background rather than inherent harmfulness. Crow (1957) has discussed the potential for erroneously attributing cor- relations between resistance and other traits to pleiotropy in cases where those traits simply reflect differences between the particular strains repre- senting the resistant and susceptible phenotypes. Lines et al. (1984) examined the F2 progeny of resistant and susceptible strains in order to distinguish between effects due to strain differences per se and effects due to resistance loci (or closely linked loci). The question of pleiotropy is particularly sensitive to the general problem of choosing an appropriate control (susceptible) strain, because pleiotropic costs may evolve. With respect to the early stages of the evolution of resistance, the proper control should represent susceptible in- dividuals of the same population, because it is in this context that the initial rudimentary resistance mechanisms must be refined. Apparent reversion of resistance during periods in which use of the pes- ticide had been suspended has been observed in field populations (Keiding,

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212 POPULATION BIOLOGY OF PESTICIDE RESISTANCE 1967; Georghiou, 1972~. Curtis et al. (1978) estimated the pleiotropic costs associated with resistance by monitoring the decline of resistance in popu- lations of Anopheles; they caution that such field studies may wrongly at- tribute declines due to migration of susceptibles to reversion. Perhaps the best demonstration that characters influencing fitness in the absence of in- secticides evolve in treated populations comes from the work of McKenzie et al. (1982) on diazinon resistance in natural populations of the blow fly, Lucilia cuprina. In 1969-1970, population experiments indicated lower fit- ness in resistant flies relative to flies from a standard reference strain (McKenzie et al., 1982~. In contrast resistant lines derived from a field population in 1979 suffered no disadvantage relative to the control strain, either in labo- ratory population cages or in field viability tests. Results resembling the earlier observations were obtained following placement of the major resis- tance gene on the control background by backcrossing. These results indicate that regardless of the appropriateness of the standard reference strain as a susceptible control, continued pesticide treatment in the field has modified characters that contribute to fitness in the absence of the pesticide: the pleio- tropic costs have undergone evolution. Evolution of Epistatic Resistance The question of fashioning resistance to pesticides from the components of normal metabolism centers on the evolutionary process by which an in- tegrated genetic network controlling normal metabolism transforms into an- other genetic network capable of responding to both treated and untreated environments. Known single-locus determinants of resistance may represent highly evolved mechanisms, the products of the evolutionary process dis- cussed here. The evolutionary process under which genetic systems evolve differs fundamentally from the processes involving the independent evolution of single characters (Wright, 19601. Analysis of the process of the evolution of genetic networks may contribute toward the control of pesticide resistance by suggesting some means of retarding the development of effective mech- anisms of resistance. THE SHIFTING BALANCE THEORY Genetic Systems as Sets of interacting Loci A complex developmental process integrating a myriad of internal and external influences is interposed between genes and characters of selective importance (Wright, 1934, 1960, 19681. Substitution of an allele at a given locus by another allele of different effect alters the entire developmental network, thereby inducing a response in several characters. Wright based

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PLE!OTROPY AND GENETIC SYSTEMS CONFERRING RESISTANCE 213 this principle of "universal pleiotropy" (1968, Chapter V) on his extensive studies of inheritance in laboratory populations of guinea pigs, whose ex- traordinary diversity of morphology, vigor, and temperament derived from the interaction between various genetic factors and particular backgrounds (Wright, 1978~. Shifts Among Peaks in the Adaptive Topography Wright (1932) characterized the possible genetic states of an individual as points in a gene frequency space whose dimensions correspond to loci, and associated with each point the adaptive value of individuals carrying the corresponding array of genes. Under pleiotropy and epistasis certain genetic combinations confer particularly high fitness, corresponding to peaks of this adaptive topography, and others confer low fitness, corresponding to valleys. In the imagery of the adaptive topography, populations ascend toward peaks. Having once attained a peak the population undergoes no further improvement except insofar as new mutations elevate the peak at which it resides or otherwise modifies the surrounding topography (Wright, 19421. Sustained advance requires some means of momentary release from convergence toward a peak to permit the population to explore other regions of the topography. Continual shifts to higher peaks constitute the essence of the shifting balance process. Among the several mechanisms enumerated by Wright (1931, 1932, 1940, 1948, 1955, 1959) that can modulate the selective process that compels populations to proceed up gradients in the adaptive topography are genetic drift and qualitative changes in selection pressure. Genetic drift introduces an element of stochasticity into evolutionary changes in gene frequency and permits the nonadaptive passage of populations into and even through valleys of the adaptive topography. Variable selection pressures, especially in cases in which the direction of evolution undergoes periodic reversals, can trigger peak shifts (Wright, 1932, 1935, 1940, 1942, 1956~. In the imagery of the adaptive topography, valleys may be temporarily uplifted, permitting the population to wander into the domain of attraction of a new peak by means of a wholly adaptive process. THE EVOLUTION OF PESTICIDE RESISTANCE In its simplest form the evolution of a rudimentary resistance mechanism and the reduction of pleiotropic costs through the separation of incipient detoxification pathways from metabolic pathways represents a peak shift under fluctuating selection. Alternation of treated and untreated generations requires the maintenance of adaptations to both selective regimes. Moderate

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214 POPULATION BIOLOGY OF PESTICIDE RESISTANCE levels of migration between treated and untreated populations may promote peak shifts in both regions. Multiple Peaks in the Adaptive Topography Upon initial exposure to the pesticide, rare individuals survive by virtue of regulatory mutations that induce sufficient production of an enzyme having the fortuitous ability to detoxify the compound in the absence of its normal substrate. All individuals possess the bifunctional structural locus; the sole genetic difference between susceptible and resistant individuals at this stage lies at the regulatory locus. Temporary suspension of pesticide treatments tends to reduce the level of resistance in the population by restoring the original selective regime, which favors a lower rate of production. Distinct modifier loci contribute to the resistance mechanism by releasing the key enzyme from its original metabolic pathway. Such mutations are likely to induce deleterious effects in the absence of the pesticide by inter- fering with the regulation of the original metabolic pathway. Under pesticide treatment these mutations are favored by directional selection because any degree of separation between the two pathways permits the detoxification pathway to operate more efficiently. Selection by pesticides favors maximal synthesis of the key enzyme and maximal separation of the pathways. Natural selection in the absence of the pesticide either favors moderate levels of synthesis of the enzyme if the pathways are not separated or is insensitive to the rate of synthesis if the pathways are entirely separated. Only one combination, maximal synthesis of the key enzyme and complete separation of the pathways, confers high fitness under both selective regimes. In the absence of the pesticide, however, this optimal combination is separated from the current position of the pop- ulation by the disadvantage of incompletely separated pathways. The transfer of the population from its original state to the optimal state through the alternation of the two selective regimes represents a peak shift. Effects of Migration Between Treated and Untreated Areas Migration of susceptible individuals into areas under treatment by pesti- cides can delay the increase in density of individuals carrying well-developed, single-locus resistance mechanisms by inflating the frequency of the suscep- tible allele and ensuring that most resistance alleles are carried by hetero- zygotes (Georghiou and Taylor, 1977; Comins, 1977; Tabashnik and Croft, 19821. Comins (1977) showed that intermediate levels of migration promote the optimal balance between its positive effect (increasing the frequency of the susceptible allele in the treated deme) and its negative effect (increasing the frequency of the resistant allele in the untreated deme). If the untreated

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PLEIOTROPY AND GENETIC SYSTEMS CONFERRING RESISTANCE 215

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216 POPULATION BIOLOGY OF PESTICIDE RESISTANCE metabolism and evolve resistance without bearing the pleiotropic costs that opposed the rise of resistance in the first population. A CALL FOR EMPIRICAL AND THEORETICAL WORK This discussion and its conclusions draw upon a number of suppositions and assumptions: primitive resistance mechanisms redirect the activity of enzymes that normally participate in metabolism toward detoxification; such redirection entails pleiotropic costs that, in the absence of pesticide treatment, lower the fitness of resistant individuals relative to susceptible individuals; pleiotropic costs can be reduced through adaptation by a genetic network of modifiers; peak shifts of this kind occur under alternation of treated and untreated generations; and migration from treated areas promotes peak shifts that may form the basis of preadaptations to the pesticide. An informed assessment of this argument and the validity of any control strategies it may suggest requires empirical and theoretical investigation. Empirical Studies of Rudimentary Resistance Analysis of the genetic structure of primitive mechanisms of resistance and the direct assessment of pleiotropic costs associated with such mecha- nisms would provide empirical information of crucial importance for the prevention or retardation of the evolution of resistance. The highly successful strategy of the microbial evolution experiments could be modified for the study of rudimentary resistance mechanisms either by challenging organisms in the laboratory with new pesticides to which effective resistance has not yet evolved or by deleting a locus of major effect on resistance and monitoring the restoration of its function. The objectives would include (1) classification of the key mutations with respect to regulatory or structural function, (2) estimation of the relative importance of regulatory mutations causing constitutivity and hyperinducibility, and (3) assessment of the effects of the key mutations on normal metabolism. Direct estimates of pleiotropic costs associated with poorly formed resis- tance mechanisms could be obtained by comparing the levels of additive genetic variance in fitness in experimental populations before and after ex- posure to a novel pesticide. Fitness in the absence of the pesticide may be regarded as a character which is correlated with the character of resistance and which is disrupted by the selection imposed by the pesticide (Falconer, 1953, 1981~. Before pesticide application, the additive genetic variance of characters closely associated with fitness is expected to be low (Fisher, 1958; Falconer, 1981~. After exposure the surviving individuals are likely to differ in a variety of characters from individuals that succumbed. If certain of those characters contribute to fitness in the absence of the pesticide, then the

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PLEIOTROPY AND GENETIC SYSTEMS CONFERRING RESISTANCE TABLE 1 Relative Fitnesses in the Absence of Pesticide Treatment (Regime 1) BB Bb bb AA w1 w1 - s t Aa w2 w2- s t aa w3 w3 - s t 217 additive genetic variance in fitness is expected to increase after treatment. The magnitude of change in additive genetic variance in fitness reflects the magnitude of the pleiotropic costs associated with resistance. It is this com- ponent of variance that determines the rate of reversion of resistance in the absence of pesticide treatment (Falconer, 1981~. A Model of Epistatic Resistance In its simplest form the peak shift required for the evolution of resistance mechanisms that incur low pleiotropic costs entails genetic changes at two loci: the regulatory locus controlling the level of synthesis at the key structural locus and a modifier locus permitting separation of the two pathways. The effects of migration and population size on the refinement of resistance in a population that exchanges migrants with untreated populations could be in- vestigated through the analysis of the two-locus model described in this section. In the absence of pesticide treatment, genetic variation at the regulatory locus is maintained by heterosis in fitness and the modifier locus is mono- morphic. The introduction by mutation or migration of a new allele at the modifier locus results in the production of heterozygotes that suffer a re- duction in fitness due to interference between the detoxification pathway and normal metabolism. In homozygotes for the new allele the pathways are independent, rendering variation at the regulatory locus, which now controls the production of an enzyme involved only in detoxification, selectively neutral. Regime 1 corresponds to natural selection in the absence of treatment by the pesticide. Table 1 presents the fitness matrix associated with Regime 1. Locus A represents the regulatory locus at which variation is maintained by heterosis (W2 ~ We, Why. Locus B represents the modifier locus at which the heter- ozygote detracts from fitness (s > 0) and the homozygote improves fitness by causing the separation of the pathways (t > Wi - S for all i). Because the new allele (b) at the modifier locus causes underdominance in fitness in combination with all genotypes at the regulatory locus, its introduction is uniformly opposed by natural selection. Exposure to the pesticide favors maximal rates of synthesis of the key

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218 POPULATION BIOLOGY OF PESTICIDE RESISTANCE TABLE 2 Relative Fitnesses Under Treatment by Pesticides (Regime 2) BB Bb bb AA x1 x1 + u x1 + v Aa x2 x2 + U x2 + V aa x3 x3+u x3+v enzyme and any reduction in the interdependence of the two pathways. Table 2 presents the fitness matrix associated with Regime 2, which corresponds to pesticide treatment. Selection at locus A, which was balancing under Regime 1, now becomes directional (x' > x2 > X34. Selection at locus B. which was underdominant under Regime 1, now also becomes directional, favoring the new allele (v > u > 01. In treated areas Regime 1 alternates with Regime 2 at a frequency deter- mined by the generation time of the pest relative to the interval between treatments. Evolution in untreated populations is governed solely by Regime 1. Migration is represented by an exchange of genes between the treated population and one or more unexposed populations. The key objectives of the theoretical analysis of this system include the description of evolution in treated and untreated regions separately and the influence of migration between these regions. Such studies should explore the effect of relative population sizes in treated and untreated areas, the migration rate, the frequency of treatment, and the intensity of selection on the rate of introduction of the new allele (b) and the probability and rate of fixation of the optimal combination in treated populations. Numerical and mathematical analyses of the model could be used to explore the process of formation of preadaptations to the pesticide in untreated areas by studying the effect of migration rate and population size on the rate of introduction of the new modifier allele (b) through the barrier of underdominance in fitness. CONCLUSION The central concern of this discussion has been to suggest that empirical and theoretical investigation be directed toward the elucidation of the process under which primitive responses to pesticides develop into highly effective mechanisms of resistance. The bifunctionality of components of primitive resistance mechanisms suggests that in the early evolutionary stages the defense against pesticides involves some disruption of normal physiological processes. Direct empirical investigations of primitive responses to new pes- ticides would provide crucial evidence to support or refute the hypothesis that primitive mechanisms of resistance incur substantial pleiotropic costs.

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PLEIOTROPY AND GENETIC SYSTEMS CONFERRING RESISTANCE 219 The evolution of genetic systems entails changes at several genetic loc under epistatic selection. Taylor (1983) cites only one paper (Plapp et al. 1979) that addresses multilocus models of resistance. The multilocus ap- proach permits the study of qualitatively new phenomena which have no representation in one-locus models: epistasis deriving from pleiotropy, the central issue of this discussion, requires a multilocus approach. In the pre- ceding section, a simple two-locus model was proposed that incorporates migration within subdivided populations and loci that contribute to both detoxification and normal metabolism. Of particular relevance to the devel- opment of effective control policies is the question of whether migration between treated and untreated regions promotes the reduction of pleiotropic costs and the rate of preadaptation to the pesticide by untreated populations. The confrontation of theoretical population genetics with the practical problems of the control of pesticide resistance enriches both fields by re- vealing new perspectives on old problems and by provoking the development of new questions. While the establishment of improved channels for dialogue can hardly be expected to produce panaceas, the clear necessity of effective policies governing the control and management of pest populations demands the best efforts of a variety of disciplines. ACKNOWLEDGMENTS I thank Bruce E. Tabashnik and Richard T. Roush whose insight and knowledge of the literature served as my introduction to the study of pesticide resistance. John A. McKenzie, on very short notice, graciously forwarded preprints and offered suggestions that improved the paper. This study was supported by PHS Grant HD-17925. REFERENCES Bengtsson, B. O., and W. F. Bodmer. 1976. On the increase of chromosome mutations under random mating. Theor. Popul. Biol. 9:260-281. Clarke, P. H. 1978. Experiments in microbial evolution. Pp. 137-218 in The Bacteria, T. C. Gunsalos, ed. New York: Academic Press. Comins, H. N. 1977. The development of insecticide resistance in the presence of migration. J. Theor. Biol. 64:177-197. Crow, J. F. 1957. Genetics of insect resistance to chemicals. Annul Rev. Entomol. 2:227-246. 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. Falconer, D. S. 1953. Selection for large and small size in mice. J. Genet. 51:470-501. Falconer, D. S. 1981. Introduction to Quantitative Genetics, 2nd ed. London: Longman. Fisher, R. A. 1958. The Genetical Theory of Natural Selection, 2nd ed. New York: Dover. Georghiou, G. P. 1972. The evolution of resistance to pesticides. Annul Rev. Ecol. Syst. 3:133- 168.

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220 POPULATION BIOLOGY OF PESTICIDE RESISTANCE Georghiou, G. P., and C. E. Taylor. 1977. Operational influences in the evolution of insecticide resistance. J. Econ. Entomol. 70:653-658. Hall, B. G. 1983. Evolution of new metabolic functions in laboratory organisms. Pp. 234-257 in Evolution of Genes and Proteins, M. Nei and R. K. Koehn, eds. Sunderland, England: Sinauer. Hall, B. G., and D. L. Hartl. 1974. Regulation of newly evolved enzymes. I. Selection of a novel lactase regulated by lactose in Escherichia coli. Genetics 76:391-400. Keiding, J. 1967. Persistence of resistant populations after the relaxation of the selection pressure. World Rev. Pest Control 6:115-130. Lande, R. 1979. Effective deme sizes during long-term evolution estimated from rates of chro- mosomal rearrangement. Evolution 33:234-251. Lines, J. D., M. A. E. Ahmed, and C. F. Curtis. 1984. Genetic studies of malathion resistance in Anopheles arabiensis. Bull. Entomol. Res. 74:317-325. McKenzie, J. A., M. J. Whitten, and M. A. Adena. 1982. The effect of genetic background on the fitness of the diazinon resistance genotypes of the Australian sheep blowfly, Lucilia cuprina. Heredity 49:1-9. Mortlock, R. P. 1982. Regulatory mutations and the development of new metabolic pathways by bacteria. Evol. Biol. 14:205-268. Plapp, F. W., Jr. 1976. Biochemical genetics of insecticide resistance. Annul Rev. Entomol. 21: 179- 197. Plapp, F. W., Jr., C. R. Browning, and P. J. H. Sharpe. 1979. Analysis of rate of development of insecticide resistance based on simulation of a genetic model. Environ. Entomol. 8:494-500. Plapp, F. W., Jr. and T. C. Wang. 1983. Genetic origins of insecticide resistance. Pp. 47-70 in Pest Resistance to Pesticides, G. P. Georghiou and T. Saito, eds. New York: Plenum. Scangos, G. A., and A. M. Reiner. 1978. Acquisition of ability to utilize xylitol: Disadvantages of a constitutive catabolic pathway in Escherichia coli. J. Bacterial. 134:501-505. Tabashnik, B. E., and B. A. Croft. 1982. Managing pesticide resistance in crop-arthropod complexes: Interactions between biological and operational factors. Environ. Entomol. 11:1137-1144. Taylor, C. E. 1983. Evolution of resistance to insecticides: The role of mathematical models and computer simulations. Pp. 163-173 in Pest Resistance to Pesticides, G. P. Georghiou and T. Saito, eds. New York: Plenum. Taylor, C. E., and G. P. Georghiou. 1979. Suppression of insecticide resistance by alteration of gene dominance and migration. J. Econ. Entomol. 72:105-109. Tsukamoto, M. 1983. Methods of genetic analysis of insecticide resistance. Pp. 71-98 in Pest Resistance to Pesticides, G. P. Georghiou and T. Saito, eds. New York: Plenum. Walsh, J. B. 1982. Rate of accumulation of reproductive isolation by chromosomal rearrangements. Am. Nat. 120:510-532. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:97-159. Wright, S. 1932. The roles of mutation, inbreeding, crossbreeding, and selection in evolution. Proc. 6th Int. Congr. Genet. 1:356-366. Wright, S. 1934. Physiological and evolutionary theories of dominance. Am. Nat. 68:24-53. Wright, S. 1935. Evolution in populations in approximate equilibrium. J. Genet. 30:257-266. Wright, S. 1940. The statistical consequences of Mendelian heredity in relation to speciation. Pp. 161-183 in The New Systematics, J. Huxley, ed. Oxford: Clarendon. Wright, S. 1941. On the probability of fixation of reciprocal translocations. Am. Nat. 75:513-522. Wright, S. 1942. Statistical genetics and evolution. Bull. Am. Math. Soc. 48:223-246. Wright, S. 1948. On the roles of directed and random changes in gene frequency in the genetics of populations. Evolution 2:279-294. Wright, S. 1955. Classification of the factors of evolution. Cold Spring Harbor Symp. Quant. Biol. 20: 16-24. Wright, S. 1956. Modes of selection. Am. Nat. 90:5-24. Wright, S. 1959. Physiological genetics, ecology of populations, and natural selection. Perspect. Biol. Med. 3:107-151.

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PLEIOTROPY AND GENETIC SYSTEMS CONFERRING RESISTANCE 221 Wright, S. 1960. Genetics and twentieth century Darwinism: A review and discussion. Am. J. Hum. Genet. 12:365-372. Wright, S. 1968. Evolution and the Genetics of Populations. Genetic and Biometric Foundations, Vol. I. Chicago, Ill.: University of Chicago Press. Wright, S. 1978. The relation of livestock breeding to theories of evolution. J. Anim. Sci. 46:1192- 1200. Wu, T. T., E. C. C. Lin, and S. Tanaka. 1968. Mutants of Aerobacter aerogenes capable of utilizing xylitol as a novel carbon. J. Bacterial. 96:447-456.