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OCR for page 143
Population Biology of Pesticide
Resistance: Bridging the Gap Between
Theory and Practical Applications
WERE THE EVOLUTION OF PESTICIDE RESISTANCE not of grave concern
to human health and well-being, it would have still been important
as a major example of the power and potential of adaptive evo-
lution. Surprisingly, population geneticists and ecologists have paid little
attention to it. Similarly, relatively few investigators involved in management
of resistance have directly applied the tools and theoretical concepts of ac-
ademic population biology.
In this chapter we describe current attempts at bridging the gap between
academic and applied population biology, discuss aspects of the genetics
and population biology of resistance critical to developing resistance man-
agement programs, recommend future work needed in this area, and de-
scribe major impediments to developing and implementing programs to
manage resistance.
A HEURISTIC MODEL OF MANAGING RESISTANCE
We present here a simplistic, idealized model of the resistance cycle re-
sulting from pesticide use, solely for heuristic purposes (as a "thought ex-
periment"), not as a realistic model for the long-term management of resistance.
The model assumes that resistant genotypes arise in the pest population and,
as a result of selection imposed by pesticide use, field control fails because
these genotypes attain high frequencies. The model assumes that stopping
use of the pesticide will result in a continuous decline in the frequency of
resistant genotypes and, in a reasonable amount of time, the frequency of
susceptible genotypes will become sufficiently high for the population to be
143
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144
POPULATION BIOLOGY OF PESTICIDE RESISTANCE
effectively controlled by that pesticide once again (see Figure 11. Neither
assumption is a necessary outcome.
The time period between initial use of the pesticide and control failure is
the resistance onset interval, TR(i). Stopping treatment with pesticide i results
in relaxation of selection pressure for resistance to i and a decline in the
frequency of resistant genotypes. The time between the end of treatment with
i and a decline in the frequency of resistant genotypes low enough to resume
effective control with compound i is the susceptibility recovery interval,
TS(i).
In theory, pest control is possible indefinitely by cycling through an array
of compounds, as long as resistance to each of them is independent of
resistance to every other. The total number of pesticides required for this
cycling depends solely on the lengths of the resistance onset and susceptibility
recovery intervals (Figure 11.
In this model, the goal of resistance management is to maximize the
resistance onset intervals and minimize the susceptibility recovery intervals.
The effect of this strategy would be to minimize the number of independent
compounds needed for effective long-term control.
USE OF POPULATION BIOLOGY THEORY AND
CONCEPTS IN RESISTANCE MANAGEMENT
To date, population biology theory has contributed to resistance manage-
ment primarily in identifying the factors contributing to the rise of resistance,
and to some extent in interpreting factors responsible for resistance in specific
populations. We are unaware of any pesticide-use programs that have been
entirely planned and executed in a manner prescribed from theoretical and
empirical considerations of population genetics of resistance and the ecology
of the organisms and ecosystem under treatment.
Elements of population biology theory have, however, been applied to
some aspects of pest management. For example, the theory of the population
biology of infectious disease played a role in the development of the suc-
cessful multiline cultivar procedure used to reduce fungicide use in barley
cultivation (Wolfe and Barrett, this volume). This theory has also been useful
in a retrospective manner. Analyses of resistance cycles are generally con-
sistent with those anticipated from population biology theory and laboratory
experiments (Gutierrez et al., 1976; Comins, 1977b; Taylor et al., 1983;
Tabashnik, this volume).
Nevertheless, we are unaware of any cases where a high-dose regime or
any other tactic has been actually put into practice based solely upon con-
siderations of population genetic theory, even though several theoretical
investigations are directly relevant. For example, MacDonald (1959) noted
that resistance would develop more slowly if it was recessive. Davidson and
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
.
·
. . . .
TR3 TS3 j
1
~TR,
it' TSC
. . .
TR2 TS2 '
.. .
TR1 ~TS1
_1
_
C
~_\
C-1 3
· ~
145
FIGURE 1 The Pesticide Resistance Cycle. Tit(i) is the time period from the first use
of a pesticide, i, to the time resistance precludes its use, the resistance onset interval.
TS(i) is the time period between termination of use of compound i to the time the frequency
of resistant pests is sufficiently low to maintain effective population control with that
compound, the susceptibility recovery interval. C is the total number of compounds
required for indefinite control.
Pollard (1958) found that higher doses of gamma-BHC (lindane) would kill
heterozygotes and indicated that this would slow resistance development.
More recently, the high-dose approach has been the subject of much theo-
retical work (Tabashnik and Croft, 1982~. By and large, management of
resistance to pesticides has made little direct use of population and community
ecology theory. Earlier recognition by pesticide users of the "Volterra"
principle (when predators and their prey are both killed, prey populations
will increase) would have highlighted the danger of indiscriminate use of
pesticides on populations where some control of prey species (pests) was
achieved by natural enemies (predators).
GENETIC AND ECOLOGICAL INFORMATION REQUIRED FOR
MODELS OF THE POPULATION BIOLOGY OF RESISTANCE
Even though specific resistance management programs should be designed
on a case-by-case basis, the following general classes of information are
required to develop realistic models of the population biology of pesticide
resistance, and thus to design resistance management programs:
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
· Mode of Inheritance. Knowing the mode of inheritance of the resistant
phenotype is critical to developing any model of pesticide resistance. Al-
though it sounds formidable, a relatively modest amount of genetic infor-
mation would actually be needed for models of the population genetics of
resistance. Particularly critical for these models is whether resistance is in-
herited as a discrete character (involving one or two major genes) or acts as
a continuously distributed (quantitative, or polygenic) character, because
different classes of theoretical models are applicable to single-gene and po-
lygenic resistance (Via, Uyenoyama, this volume). In the former we must
know the number of alleles at the resistance-determining loci and the dom-
inance relationship among these alleles (as a function of pesticide concen-
tration) (Curtis et al., 19781. It would also be valuable to know the nature
of the interactions (epistasis) between the genes determining resistance as
well as other, modifying loci (Uyenoyama, this volume). Where resistance
acts as a quantitative character, it is particularly critical to know the mean
levels of resistance, the phenotypic variances, the additive and nonadditive
genetic variance in these levels of resistance, and the genetic covariance in
the tolerances to different pesticides (Via, this volume). We recognize that
these cannot be known until resistance has evolved, but some generalities
on inheritance of resistance are emerging (Chapter 2~.
· Fitness Relationships. Estimating genotypic fitness is difficult, even in
a well-controlled experiment. Nevertheless, at least rough estimates of the
relative reproductive and survival rates of resistant and susceptible genotypes
are necessary to consider their rates of increase, frequencies after pesticide
treatment, and rate of decline when treatment is stopped (i.e., when selection
is relaxed). It is not sufficient to assume that fitness is simply a matter of
the kill rate or that resistant genotypes will have a selective disadvantage in
the absence of pesticides. These fitness estimates have to be obtained for
resistant and susceptible genotypes as functions of stage in the life cycle and
concentrations of pesticides. Fitness should not be assumed to be a constant.
In obtaining these estimates, it is necessary to control for a variety of other
environmental and genetic factors such as temperature, season, physiological
state, population density, and genetic background. Again, this information
is not available until after resistance has evolved. In the case of insects and
rodents, behavioral considerations should also be taken into account (Gould,
1984).
· Population Structure. Some details of intrinsic genetic structure of the
target population and its spatial and temporal distribution are critical to
developing a realistic model, especially: (1) whether generations are discrete
or overlapping, (2) the nature of the alternation of haploid and diploid phases
of the life cycle, (3) the relative lengths of sexual and asexual stages, and
(4) the duration of the whole life cycle and its various stages. The lengths
of both the resistance onset and susceptibility recovery intervals depend in
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
147
part on how isolated the treated population is. A high rate of migration (gene
flow) from susceptible populations would both delay an increase in the pro-
portion of resistant genotypes and increase their rate of decline when treatment
is stopped. Migrants from resistant populations, rather than independent
mutants, could be the primary reason for the spread of resistance. To de-
termine this physical component of population structure, the nature and timing
of migration, as well as its absolute rate, should be considered. When con-
sidering gene flow, the frequency of resistant genotypes in the untreated
population may also be important if that reservoir population is relatively
small. In studying migration, an attempt should be made to estimate the
genetically effective component, not just movement (Comins 1977b; Roush
and Croft, May and Dobson, this volume).
· Population Regulation. Pest population growth is not necessarily ex-
ponential and unregulated in the absence of treatment. Interspecific and
intraspecific competition, predation, and parasitism may help limit the rate
of growth and densities of pest populations. The nature and importance of
the population-regulating mechanisms have to be known and considered in
the population biology of resistance. The Volterra principle suggests that
pesticide use could exacerbate situations where the pest population is nor-
mally limited by parasites or predators that are susceptible to the controlling
pesticide. The intensity of selection for and against resistant genotypes could
be greatly affected by the nature of the trade-off between density-dependent
and density-independent mortality and morbidity factors. Where there is
substantial intraspecific competition, sublethal doses of a pesticide could
have a strong selection effect by weakening the competitive abilities of
susceptible individuals, even when it does not control the density of the
population (McKenzie et al., 19821.
· Refuges. Reservoirs of susceptible genotypes within the treated area
could result from pesticide dose variation in space or time. As is the case
for weed seeds, these refuges could be quite substantial and play a sig-
nificant role in augmenting the resistance onset interval (Gressel and Segel,
1978).
GENERAL AND SPECIFIC MODELS
It is possible to construct general models of the population biology of
resistance with few possibly no data from natural sources. Models of this
type have been used to identify the factors contributing to the rise of resistance
and evaluate their relative importance (Coming, 1977a; Taylor, 1983; May
and Dobson, this volume). These general models may be the only ones that
can be constructed when little population biology information is available,
and they can have considerable value. Finally, these models can be used to
distinguish between the factors that are really important and those that play
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
minor roles in the rise of resistance, thus playing a critical role in deciding
which empirical studies should be conducted.
Where extensive information is available, more detailed applied models
can be constructed and analyzed with analytical and computer simulation
procedures (Tabashnik, this volume). Although more specific models can
provide more quantitatively accurate predictions than general models, we see
no justification to postpone developing resistance management programs
based on models until all the data are available.
SOURCE OF DATA FOR MODEL CONSTRUCTION AND EVALUATION
· The Roles of Laboratory and Field Studies. Studies with pesticide-
resistant mutants generated in the laboratory and fitness experiments per-
formed with laboratory-selected strains may provide some information about
the nature of the alleles conferring resistance and their anticipated fate in
populations. Whenever possible, however, these investigations should use
susceptible and resistant genotypes isolated from natural sources and perform
fitness studies under natural conditions. The genetics of resistance in natural
populations are probably different from those generated in the laboratory,
because, for example, selection pressure under natural conditions might be
different from that in short-term laboratory studies (McKenzie et al., 1982;
Uyenoyama, this volume). Laboratory studies indicate that fitness differences
are likely to exist in natural situations but do not provide accurate estimates
of fitness differentials in the field. On the other hand, laboratory studies
could provide reliable estimates of toxicological dominance, if they were
performed under conditions that approximate field exposure to pesticides.
· Extrapolating from Existing Genetic Information and Molecular Pro-
cedures. To a great extent the high rate of progress in academic genetics can
be attributed to the common use of relatively few species (model systems)
that are particularly convenient to study. Unfortunately, real pest organisms
are seldom ideal experimental organisms, so genetic information often has
to be acquired by extrapolation from related organisms.
Using DNA and RNA probes to determine the physical location of genes
and to ascertain whether homologous genes are responsible for the same
phenotype in different species considerably broadens the range of organisms
amenable to genetic analysis. Only limited use has been made of in vitro
genetic procedures to investigate the genetics of pesticide resistance (see
Georgopoulos, Gressel, Hardy, Hammock and Soderlund, MacNicoll, Plapp,
Chapter 2, this volume). Obtaining DNA and RNA probes is not easy when
the gene product is not known or known and present in low quantities, or
when the physical location on the gene of the model organisms is not known,
but molecular techniques should be considered for determining modes of
inheritance for population studies of pesticide resistance.
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
149
It is both convenient and traditional to focus on phenotypes that are (or
seem to be) discrete characters determined by one of two genes, but it is
critical to consider that specific cases of resistance may be determined by
multiple alleles and that resistance behaves as a quantitative character. There
are well-developed procedures to analyze inheritance of quantitative char-
acters and model the behavior of these characters under selection (Via, this
volume).
EVALUATING MODELS AND PROGRAMS FOR
PESTICIDE RESISTANCE MANAGEMENT
While we may believe that existing studies of the fit between theory and
empirical observation justify the use of population biology theory to develop
pesticide use and resistance management programs, a final demonstration of
their utility remains necessary. In order to demonstrate the utility of math-
ematical and numerical modeling, the programs developed using them must:
(1) maintain the required level of pest control, (2) be economically com-
petitive, (3) yield lower levels of resistance than would be anticipated for
alternative programs employing the same compounders), and (4) be safe from
both an environmental and health perspective.
While not sufficient in a formal sense, the a posterior) fit between obser-
vation and prediction should certainly be considered partial demonstration
of the validity of models. Properly controlled pilot studies could provide
further evidence, if they were run under field conditions using a few "model"
systems with properties similar to those of the intended target species and
communities. In cases where the pesticide is already in use, field data could
serve as control. These studies should make the evaluation in the minimum
time possible, and some acceleration could be achieved by using procedures
to detect resistant organisms when they are rare and possibly heterozygous
(for one- or two-gene resistance), or when resistance levels are low (for
polygenic resistance).
The models and data will be quantitative, but fit will have to be evaluated
somewhat qualitatively. The extraordinary number of interactions between
the biotic and physical factors in a field study cannot all be controlled. On
the other hand, if a program is effective, one would anticipate the desired
level of pest control and significantly lower rates of increase of resistant
genotypes in the experimental populations.
FOLKLORE, DOGMA, AND AD HOC PRACTICES
There are a number of current pesticide use practices and assumptions
about their consequences for resistance management that seem to have little
or no base in population biology theory.
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
· Return to Pesticide Susceptibility. While only occasionally stated ex-
plicitly, there seems to be a general belief that a decline in the frequency of
resistant genotypes will necessarily follow when use of a compound is stopped.
While we expect this to be true in the long run, the length of the susceptibility
recovery interval may be effectively indefinite in many cases. In the absence
of pesticide use, the selective differential between susceptible and resistant
genotypes may be quite small. Even if the original resistant genotypes had
a marked disadvantage in the absence of the pesticide, there may be selection
for modifier genes that improve the fitness of resistant genotypes.
The limited empirical results on the fate of alleles conferring resistance
following termination of pesticide use support a mixed view of the fate of
resistance genotypes in the absence of pesticide selection. In some cases,
the frequencies of alleles conferring resistance declined relatively rapidly
(Greaves et al., 1977; Partridge, 1979; McKenzie et al., 1982; also see
Greaves, Georgopoulos, this volume). In other cases, there was little change
in the frequency of these alleles following the relaxation of selection (White-
head et al., 1985; Georgopoulos, Roush and Croft, this volume).
Even in cases where the resistant genotypes have a clear selective dis-
advantage relative to sensitive genotypes, the intervals for susceptibility re-
covery will still be substantially longer than for the corresponding resistance
onset. The intensity of selection favoring resistance during pesticide use will
certainly be much greater than that favoring susceptibility following the
termination of treatment. For a pesticide to be biologically effective for a
period as long as that during its first use, the frequency of resistant genotypes
in the recovered population would have to be similar to that prior to first use
(see May and Dobson, this volume).
This conclusion has a number of immediate implications. First, the sim-
plistic scheme depicted in our heuristic model is unlikely to be a realistic
long-term solution to the problem of pesticide resistance. The recovery period
following the rise of resistance could be extremely long and, for practical
purposes, too long for individual pesticides to be used more than once. Thus,
long-term control by pesticides alone would require an almost infinite supply
of independent compounds. In a short-term view, the factors affecting ev-
olutionary rates also illustrate the utility of (1) terminating pesticide use
before the frequency of resistance is high; (2) developing procedures that
increase the selection pressures favoring susceptible genotypes; and (3) programs
that increase rates of gene flow from sensitive populations.
· Pesticide Mixing and Cycling. A current controversy is whether pesti-
cides should be in rotations or mixtures before their target pesos) become
resistant. The answer is equivocal. Models can be constructed in which
pesticide cycling or mixing either increases or decreases the resistance onset
interval. The outcome depends critically on the way the different pesticides
interact in determining the fitness of resistant and sensitive genotypes. Also
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
151
important are: modes of inheritance of resistance; frequency of mutations for
resistance; rates of recombination between the loci involved; and population
dynamics of pest growth, refuges, migration and pesticide action.
These qualifications emphasize the need for considering tactics on a
case by case basis with validation prior to implementation. The population
biology of each type of pesticide use regime can be readily modeled, and
the relative merits and liabilities of these pesticide use regimes can be
. . ~
assessed a prlorl.
· Directed Evolution of Resistance. A fundamental premise of evolution-
ary theory is that mutations occur at random; their incidence and nature are
independent of specific selection pressure. Starting with the classical fluc-
tuation test experiment of Luria and Delbruck (1943), there have been a
number of lines of evidence in support of this interpretation (Crow, 19571.
There have been suggestions, nevertheless, that pesticides will promote the
generation of resistant organisms (as well as select for increase in their
frequency) or that resistance to one compound will increase the rate of
mutation to a second compound (Wallace and MacSwiney, 19761.
While it may be easy to discount these (or any) neolamarckian interpre-
tations, we believe that the hypothesis that the rate and nature of mutation
is influenced by selection for that mutation is interesting from both an aca-
demic and applied perspective and certainly worth testing. We can speculate
on mechanisms that make mutations appear to be directed. In nonlethal doses,
pesticides could cause "genomic shocks" that increase frequencies of trans-
position of chromosome pieces. If pesticide resistance is the result of inserting
movable elements of chromosomes, then conceivably the initial transposition
could increase the future rates of transposition. In cases where resistance to
specific pesticides requires two mutations, one in a gene that is common to
resistances to different compounds and one that is unique to each, mutation
could appear to be directed.
IMPEDIMENTS
Implicit in this discussion is the assumption that the pesticide resistance
problem is amenable to a technical solution. There is some justification for
this assumption; for specific agricultural or clinical situations, programs using
combinations of chemical and biological agents could be developed to prolong
the useful life of compounds. On the other hand, we see little justification
in maintaining the polite fiction that pesticide resistance is solely a technical
problem and therefore solvable with the right tools. The design, execution,
monitoring, and evaluation of pesticide-use programs and their ultimate im-
plementation are major endeavors, even for single agricultural or clinical
situations. Development and testing require cooperation of investigators in
a variety of fields: chemistry, genetics, population biology, toxicology, bot
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
any, microbiology, zoology, epidemiology, and medicine. These activities
have to be coordinated with people actually running and monitoring the
program in the field or clinic. Pesticide-producing companies, primary users
of these compounds (growers, physicians, veterinarians, and public health
personnel) and government agencies regulating their use will have to partic-
ipate.
· The Dilemma of Interdisciplinary Programs. Pesticide-use programs
are interdisciplinary, yet universities, research institutes, and funding orga-
nizations responsible for their development and support are rigidly structured
along traditional, disciplinary lines. In universities in the United States,
academic and applied biology departments are almost always separate, both
geographically and administratively, and have been maintained that way for
50 years or more. Most evolutionary geneticists, ecologists, and population
biologists are in academic departments while biologists directly involved in
pesticide use and management are in agricultural, clinical, and other more
applied departments. Academic and applied biologists primarily publish in
different journals and receive funding from different sources. As a result,
there is relatively little intellectual intercourse between investigators in these
two types of biology departments and often considerable xenophobia. While
there are many situations where these administrative and geographic barriers
have been breached (e.g., a number of papers in the bibliographies of the
population biology papers in this volume and cited here), these are rare
exceptions. More extensive breakdown of the traditional separation between
applied and academic biology would be a major step toward the solution to
the pesticide resistance problem as well as other biological-technical prob-
lems.
We see no easy general solution to this problem. While lip service is
frequently given to the value of interdisciplinary programs, their active de-
velopment has been limited at best, and this situation is likely to persist as
long as universities, research institutes, and funding agencies are adminis-
tratively partitioned into academic and applied areas. As long as these separate
administrative units have primary control over personal rewards (salary,
promotion, tenure), and as long as the kudos (invitations, travel, awards,
and other recognition) are generated along disciplinary lines, from a purely
careerist perspective, there is little positive incentive for individuals to engage
in interdisciplinary projects; in some cases, there is pressure to avoid doing
so. Funding may well be the greatest impediment to jointly applied and
theoretical research. As long as research is funded either explicitly or im-
plicitly (via the peer review system) along disciplinary lines, interdisciplinary
projects will be at a disadvantage.
In the long run academic and applied biology could be somewhat unified,
despite existing administrative barricades, with a more ecumenical approach
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
153
to teaching. The genetics and population biology of pesticide resistance are
certainly interesting applied problems that merit investigation even from the
perspective of the most basic biology. Many other applied examples could
replace more traditional model systems or natural populations used as ex-
amples in genetics and population biology courses.
RECOMMENDATIONS
RECOMMENDATION 1. Pesticide use practices based on considerations of
the population biology of pesticide resistance should be developed and im-
plemented.
Although the theory and observations of academic population biology have
been used to explain past resistance episodes, at this juncture there have not
been significant pesticide use programs developed and implemented from con-
siderations of the principles of population biology.
RECOMMENDATION 2. General models of the population biology of resis-
tance can be used to develop pesticide-use practices, as long as the basic
premises of these models can be empirically justified.
While it may be a long-term goal to develop precise analogs of specific
pesticide-use situations, population biology theory may be applied to develop
pesticide-use regimes before specific models are developed. The fact that general
population biology theory has been successful in a retrospective manner, by
providing mechanistic explanations for past resistance episodes, justifies the use
of this theory in a prospective manner.
RECOMMENDATION 3. While general models may have broad utility, it
remains necessary to gather the genetic and ecological information needed
to construct specific models.
In cases where general models prove inadequate, it will be necessary to employ
specific and precise analogs of the populations and pesticides under considera-
tion.
RECOMMENDATION 4. The continuous monitoring of resistance frequencies
should be an integral part of all programs to manage resistance.
If the models are realistic analogs of the effects of the pesticide use regime
on the genetic structure of the target population, there should be a good corre-
spondence between the observed and predicted resistance frequencies and changes
in those frequencies.
RECOMMENDATION 5. Population biology theory should be used to examine
current pesticide-use practices and controversies.
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
There are a variety of ad hoc pesticide-use practices, e.g., alternating and
mixing pesticides to extend the useful life of compounds, which may or may
not be justifiable. Mathematical models of the population biology of pesticide
use represent an efficient way to evaluate these practices in a prospective
manner.
RECOMMENDATION 6. An extensive effort should be made to encourage
both research on pesticide use and resistance by academic biologists and
the study of the population biology by applied biologists involved in pesticide
use.
Pesticide resistance is a long-term problem that will require the coordinated
efforts of investigators representing several disciplines that currently suffer from
a lack of interdisciplinary communication. While unlikely to be sufficient as a
unique solution to the problem of coordinating efforts, some funds specifically
earmarked for joint basic and applied research on the population biology of
pesticide resistance may help surmount some of the institutional impediments to
this type of interdisciplinary activity.
RECOMMENDATION 7. A considerable effort should be put into developing
pest-control measures that do not rely on the use of chemical pesticides.
The continuous control of pest populations by cycling through novel chemical
pesticides is unlikely to be a viable long-term strategy. There is no biological
or evolutionary justification for the assumptions that (1) pest populations will
return to sensitive states relatively quickly following the termination of the use
of specific pesticides, or (2) an adequate supply of novel and safe pesticides can
be developed and made available continuously to replace compounds that have
lost their effectiveness due to resistance.
ACKNOWLEDGMENT
We would like to thank Ralph V. Evans for his comments on this manu-
scrtpt.
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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
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Davidson, G. and D. G. Pollard. 1958. Effect of simulated field deposits of gamma-BHC and
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Partridge, G. G. 1979. Relative fitness of genotypes in a population of Rattus norvegicus polymorphic
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WORKSHOP PARTICIPANTS
Population Biology of Pesticide Resistance. Bridging the Gap Between Theory
and Practical Applications
BRUCE R. LEv~N (Leader), University of Massachusetts
J. A. BARRETT, Cambridge University
E~NoR C. CRUZE, National Research Council
ANDREW P. DOBSON, Princeton University
FRED Gould, North Carolina State University
JOHN H. GREAVES, Ministry of Agriculture, Fisheries and Food, Great Britain
DAVID HECKEE, Clemson University
ROBERT M. MAY, Princeton University
HAROLD T. REYNOLDS, University of California, Riverside
RICHARD T. ROUSH, Mississippi State University
OCR for page 156
156
POPULATION BIOLOGY OF PESTICIDE RESISTANCE
BRUCE E. TAsAsHN~K, University of Hawaii
MARCY UYENOYAMA, Duke University
SARA VIA, University of Iowa
MAX J. Whirred, Commonwealth Scientific and Industrial Research
Organization
M. S. Wolfe, Plant Breeding Institute, Cambridge
Representative terms from entire chapter:
pesticide resistance
