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OCR for page 207
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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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.
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Representative terms from entire chapter:
pesticide resistance
