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OCR for page 157
Pesticide Resistance: Strategies and Tactics for Management.
1986. National Academy Press, Washington, D.C.
Factors :Influencing the
Evolution of Resistance
GEORGE P. GEORGHIOU and CHARLES E. TAYLOR
Any attempt to devise management strategies for delaying or fore-
stalling the evolution of pesticide resistance requires a thorough
understanding of the parameters influencing the selection process.
The parameters known to influence this process in pest populations
are presented systematically under three categories genetic, bio-
logicallecological, and operational and their relative importance
is discussed with reference to available case histories.
INTRODUCTION
More than 447 species of arthropods have now developed resistance to
insecticides (Georghiou, this volume). The main weapon for countering this
resistance has been the use of alternative chemicals with structures that are
unaffected by cross-resistance. The gradual depletion of available chemicals
as resistance to them developed has revealed the limitations of this practice
and emphasized the need for maximizing the "useful life" of new chemicals
through their application under conditions that delay or prevent the devel-
opment of resistance. To achieve this goal it is essential to understand the
parameters influencing the selection process.
It is well established that resistance does not evolve at the same rate for
all organisms that come under selection pressure. Resistance may develop
rapidly in one species, more slowly in another, and not at all in a third. For
example, despite enormous selection pressure during many years of intensive
DOT treatment in the corn belt of the United States, the corn borer showed
no evidence of resistance. Yet house flies in many areas developed resistance
157
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158
POPULATION BIOLOGY OF PESTICIDE RESISTANCE
TABLE 1 Known or Suggested Factors Influencing the
Selection of Resistance to Insecticides in Field
Populations
A. Genetic
a. Frequency of R alleles
b. Number of R alleles
c. Dominance of R alleles
d. Penetrance, expressivity, interactions of ~ alleles
e. Past selection by other chemicals
f. Extent of integration of R genome with fitness factors
B. Biological/Ecological
1. Biotic
a. Generation turnover
b. Offspring per generation
c. Monogamy/polygamy, parthenogenesis
2. Behavioral/Ecological
a. Isolation, mobility, migration
b. Monophagy/polyphagy
c. Fortuitous survival, refugia
Operational
1. The chemical
a. Chemical nature of pesticide
b. Relationship to earlier-used chemicals
c. Persistence of residues, formulation
2. The application
a. Application threshold
b. Selection threshold
c. Life stage(s) selected
d. Mode of application
e. Space-limited selection
f. Alternating selection
SOURCE: Adapted from Georghiou and Taylor (1976).
within two to three years under selection pressure by this insecticide. Even
within a species, resistance may develop more rapidly in one population than
in another. The Colorado potato beetle, for example, showed far greater
propensity for resistance on Long Island than on the mainland (Forgash,
1981, 1984).
There are many factors that can influence the rate at which this evolution
proceeds. One effort to systematize them is shown in Table 1, modified
slightly from a classification we proposed and discussed earlier (Georghiou
and Taylor, 1976, 1977a,b). The factors are grouped into three categories,
depending on whether they concern the genetics of resistance, the biology/
ecology of the pest, or the control operations used. Most factors in the first
two categories cannot be controlled, and the importance of some may not
even be determined until resistance has already developed. Only through
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THE EVOLUTION OF RESISTANCE
159
hindsight, for example, can one obtain any idea about the initial frequency
of the alleles conferring resistance. Nor is it usually possible to measure
dominance until one isolates such alleles and makes the appropriate crosses.
In some cases these issues may be addressed in laboratory studies where
resistant strains can be developed by selection on large, recently colonized
populations. Nonetheless, some factors that influence the evolution of resis-
tance are under man's control, especially those related to the timing and dose
of insecticide application (Operational Factors, Table 11. The problem is to
identify them and determine how their manipulation under the existing genetic
and biological/ecological constraints may retard the evolution of resistance.
During the past few years, important contributions have been made by
workers in a handful of laboratories, mainly in the United States, the United
Kingdom, and Australia (Coming, 1977a,b, 1979a,b; Georghiou and Taylor,
1977a,b; Haile and Weidhaas, 1977; Curtis et al., 1978; Conway and Comins,
1979; Sutherst and Comins, 1979; Sutherst et al., 1979; Taylor and Geor-
ghiou, 1979, 1982; Gressel and Segel, 1982; Muggleton, 1982; Tabashnik
and Croft, 1982; Levy et al., 1983; McPhee and Nestmann, 1983; Taylor et
al., 1983; Wood and Cook, 1983; Knipling and Klassen, 1984; Mani and
Wood, 1984; McKenzie and Whitten, 19841. Some of these contributions
are examined in other papers in this symposium. We shall confine ourselves
to a discussion of how, in a historical perspective, the accumulated knowledge
on the occurrence and dynamics of resistance leads to the recognition of
these factors (Table 1) as important.
GENETIC FACTORS IN RESISTANCE
Evolutionists frequently assume that organisms have the capacity to evolve
nearly any type of resistance. From this follow many of the "optimization"
arguments and the "adaptationist program" (Lewontin and Gould, 1979~.
This assumption is not warranted for insecticide resistance. Some populations
obviously do not have the capacity to come up with the necessary resistant
alleles in the first place, despite what would seem to be an obvious advantage
for doing so. The corn borer is one species that did not. The paucity of cases
of resistance to arsenicals in insects and to copper fungicides in plant path-
ogens are other examples. It has been speculated that herbivorous species,
which have frequently evolved the capacity to deal with plant alkaloids, are
in some sense preadapted to dealing with the problems posed by dangerous
chemicals in their environment (Croft and Brown, 19751.
Related to this is the fact that there may be many ways to achieve resis-
tance-by detoxifying the chemicals, altering site specificity, reducing pen-
etration, behavioral avoidance of residues, to name a few. When more avenues
are open it would be expected that resistance would evolve more easily.
Once alleles conferring resistance are present in the population, the fre
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160
POPULATION BIOLOGY OF PESTICIDE RESISTANCE
quency at which they occur may be important. There are several reasons for
this. Obviously if the initial frequency is higher, then resistance has a head
start. There may, however, be an Allee effect, so if the population is reduced
to a sufficiently low level, the resulting population size is too small to sustain
positive growth, perhaps by failure to find mates. More important, the se-
lection pressures and immigration rates may impose an unstable equilibrium
of gene frequencies, below which resistance alleles decrease in fitness and
above which they increase (Haldane, 19301. In this case the initial frequency
is especially important.
In practice the importance of many factors for resistance seems related to
this unstable equilibrium. In the simplest instance this equilibrium depends
largely on initial gene frequency, dominance, and immigration. These factors
in turn may depend on others. Imagine a population with resistant allele, R.
at a low frequency. Homozygous RR individuals may occur if the population
is large enough, but will be very few in number. If the resistance is recessive
or can be made recessive by application of an appropriately high dose of
insecticide (Taylor and Georghiou, 1979), then following insecticide use all
of the susceptible homozygotes (SS) and heterozygotes (RS) will be elimi-
nated, leaving only the very few RR. If now there is an inflow of largely
susceptible migrants, then those few RR will mate with SS homozygote
immigrants, and the offspring for the next generation will be almost all SS
and RS. These can be killed with another application of insecticide, keeping
the population under control. It is possible to study this result mathematically
and describe precisely when it should be observed (Coming, 1977a; Curtis
et al., 1978; Taylor and Georghiou, 1979~.
It is generally thought that resistance alleles are mildly deleterious prior
to insecticide use, so that they are present initially at some sort of mutation-
selection balance. This would typically be at an allele frequency of 10-2 to
10-4, with the RR homozygotes present at 10-4 to 10-~. Of course if two
loci are required or if more than one nucleotide change is necessary then the
frequency may be substantially less (Whitten and McKenzie, 19821.
McDonald (1959) proposed that dieldrin resistance, being more dominant
than DDT resistance in Anopheline mosquitoes, would evolve at a faster
rate. In theory there should be little difference between rates of evolution of
dominant and recessive alleles in the absence of immigrants. But, in fact,
McDonald's prediction has been more-or-less realized. The reason for this
is probably related to the unstable equilibrium described above, which exists
only when the resistant allele is recessive.
Dominance typically depends on the dose applied. Figure 1 shows the
dosage-response curves for three genotypes of a mosquito, Culex quinque-
fasciatus, exposed to a pyrethroid insecticide. When a small dose, Ds, is
applied, the heterozygotes survive, but with a larger dose, Do, they do not.
Thus, with Ds, the resistance is functionally dominant, but with Do, it is
- ~ --r r
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THE EVOLUTION OF RESISTANCE
98
95
90
80
70
60
50
40
30
20
0
.ooo 1 .001 .o 1
CONC. NRDC 167 (ppm)
2
~-
/ 't/
/+ /
/ l
- / Ds / DL /
, , , , , , , , 1 , , , a, , , , 1 , , , , , , , ,41 , , , . , , , i] 3
.1
1.
7
6
an
5 m
0
tar
4
161
FIGURE 1 Dosage-response lines for larvae of Culex quinquefasciatus susceptible, het-
erozygous, and resistant tested with permethrin. The dominance is seen to depend on
dose: with a small dose (Ds), resistance is functionally dominant, whereas with a large
dose (D~) it is functionally recessive.
functionally recessive. Modifier genes are known to change the location of
the heterozygote line, typically moving it to the right.
Modifier genes may be important in other ways as well, most notably by
helping to integrate the resistance allele into the rest of the genome to produce
a "harmoniously coadapted genome" in the sense of Mayr (1963) or Dob-
zhansky (19701. There may be many pleiotropic effects from the substitution
of a resistant allele for its wild-type alternative. Many of these are likely to
be detrimental, so the resistant allele is initially mildly deleterious (Ferrari
and Georghiou, 19811. Later, when there has been an opportunity for the
modifiers to be selected and the pleiotropic side effects have been compen-
sated for, such a disadvantage diminishes or disappears.
With few exceptions resistant populations demonstrate lower fitness than
their susceptible counterparts. Continued selection may improve fitness through
coadaptation of the resistant genome, resulting in more stable resistance. A
dramatic illustration of this is a laboratory experiment of Abedi and Brown
(19601. They selected for resistance, then released selection, then selected,
and so forth. After several cycles resistance evolved much more rapidly and
was more stable than initially. Almost certainly, modifier genes were the
cause.
Instability of resistance may not necessarily be due entirely to differences
in fitness, however. For example, genes for resistance to an organophosphate
(temephos), a pyrethroid (permethrin), and a carbamate (propoxur) were
introduced into a susceptible strain of Culex quinquefasciatus through a
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162
POPULATION BIOLOGY OF PESTICIDE RESISTANCE
system of backcrosses. The resulting synthetic was subsequently divided into
substrains and selected by these insecticides. Tests showed that the stability
of resistance in each strain differed considerably: Organophosphate resistance
regressed rapidly, pyrethroid resistance moderately, but resistance to the
carbamate showed considerable persistence (Georghiou et al., 19831. It is,
therefore, likely that the mechanism of resistance involved in each case may
influence its persistence in populations.
Past selection by insecticides may facilitate evolution of resistance to new
insecticides because of cross-resistance. Certain mechanisms of resistance
have been found to confer resistance not only within an insecticide class but
across classes as well. A classic example of this is the kdr gene. Both DDT
and pyrethroids interfere with sodium gates along the axons of nerve cells.
The kdr allele, by altering properties of the axonal membrane, makes it less
receptive to binding. Thus, it confers resistance to pyrethroids in populations
that had been selected earlier by DDT and vice versa (Priester and Georghiou,
1978; Omer et al., 19801.
Recently, Sawicki et al. (1984) showed that an esterase, E.0.33, selected
in house flies by the organophosphates malathion and trichlorphon, confers
mild cross-resistance to pyrethroids as well. By itself the esterase is of no
consequence in the control of house flies with pyrethroids because the doses
used in practice are strong enough to overcome the mild resistance it confers.
In some populations, however, kdr is also present, albeit at low frequencies,
probably as a result of previous use of DDT for control of flies. In these
populations the introduction of pyrethroids led to the simultaneous selection
of kdr, as well as the esterase, and to rapid control failure of pyrethroids.
Thus, the earlier, sequential use of two different groups of insecticides,
organophosphates and DDT, contributed to the rapid failure of a third group
of compounds, the pyrethroids, through the selection of common resistance
mechanisms.
The Colorado potato beetle also provides a pertinent example. On Long
Island the population of this species required seven years to develop resistance
to DDT, the first synthetic insecticide with which it was selected. The same
population has required progressively less time to develop resistance to the
subsequently used chemicals: five years for resistance to azinphosmethyl,
two for carbofuran, two for pyrethroids, and one for pyrethroids with a
synergist (Georghiou, this volume).
BIOLOGICAL/ENVIRONMENTAL FACTORS IN RESISTANCE
Ecology and life histories may dramatically alter the responsiveness to the
selection that leads to resistance. Most obvious, of course, is that the larger
the number of generations per year, the faster the evolution of resistance.
The fruit tree mite Panonychus ulmi, which has as many as 10 generations
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THE EVOLUTION OF RESISTANCE
5
4
3
L`J
1~ 2
(n
Ad
0 1
lo]
Z 0.5
loll
Be\
I I I
3 4 5 6 8 10 20
YRS TO APPEARANCE OF RESISTANCE
FIGURE 2 Relationship between generations per year and appearance of resistance in
species selected by soil applications of aldrin/dieldrin.
m.\
\v ~
CZAR
imp
,. , , ,1 , ,
163
I ~ /ly/emyo sp.
~ J /ly/emyo sp.
m Conoderus fo//i
I]Z D/obrol~co /ong/corn/s
LIZ Amph/mo//on majo//s
AT Popi///c' japon/ca
IBM Me/onolus tomsuyens/s
per year, has developed resistance rapidly to many groups of insecticides.
But another fruit tree mite Bryobia rubrioculus, which has only two gen-
erations per year, has yet to be reported as resistant (Georghiou, 19811.
Figure 2 illustrates the relation between generation turnover in various
soil-inhabiting pest species and the number of years it has taken them to
manifest resistance to soil applications of aldrin/dieldrin (Georghiou, 19801.
It can be seen that root maggots (Hylemya spp.), which complete three to
four generations per year, evolved resistance after five years of exposure,
while Conoderus fall), with two generations per year, evolved resistance in
six years. Diabrotica longicornis, Amphimallon majalis, and Popillia ja-
ponica, each with one generation per year, have required 8 to 14 years for
resistance development, while the sugarcane wireworm (Melanotus tamsuy-
ensis) in Taiwan, with a two-year life cycle, has taken 20 years to develop
resistance. A similar correlation between generation turnover and rate of
evolution of resistance is reported for apple tree pests by Tabashnik and Croft
(1985~.
All else being equal, populations with a higher reproductive potential are
able to withstand a higher substitutional load, that is, they can tolerate a
higher intensity of selection. Consequently one would expect to see a positive
correlation between the rate of evolution of resistance and fertility. We are
not aware of generalizations regarding this, however; nor are we aware of
generalizations regarding monogamy/polygamy or mode of reproduction.
Because of the unstable equilibrium discussed above, immigration may have
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164
POPULATION BIOLOGY OF PESTICIDE RESISTANCE
a decisive role in retarding evolution. It is essential, however, that the few
surviving RR homozygotes mate with SS immigrants. One might then expect
polygamous species to evolve more slowly. Related to this is the importance
of sexual selection and evolution of sex. It is thought that the principal
advantage conferred by sexual systems over asexual ones is the ability to
respond to environmental challenges, especially if the challenges are of-
fered in rapid succession (the red queen hypothesis, as detailed in May-
nard-Smith, 1978~. There is clearly an opportunity for much interesting
research here.
Polyphagous insect pests tend to develop resistance more slowly than
monophagous ones. Two factors may contribute to this: A smaller part of
polyphagous species are likely to be exposed, hence the selection is less
intense on these species; because some of the insects would be in untreated
refugia, they would provide a reservoir from which untreated, susceptible
migrants could come. This may be the reason that resistance in ticks of
livestock in South Africa appeared first in one-host species and only later in
species that attack two or three hosts (Whitehead and Baker, 1961; Wharton
and Roulston, 19701. Similarly, among aphids the spotted alfalfa aphid in
California was one of the first to develop resistance, but the lettuce aphid,
which moves to poplars during part of the year, has been controlled without
evidence of resistance.
It is interesting that on strictly biochemical criteria polyphagy may enhance
the potential of a species to develop resistance. Krieger et al. (1971) have
provided evidence that in lepidopterous larvae the insecticide-metabolizing
activity of microsomal oxidases is higher in polyphagous than in monopha-
gous species. It is possible that a similar mechanism is involved in the
tendency of plant-feeding insects to evolve resistance before their parasitoids
do (Croft, 1972; Georghiou, 1972), although it should be apparent that the
parasitoids can survive only after their hosts have become resistant, giving
an evident bias in sampling.
We have suggested that one of the most important features of an insect's
ecology, insofar as resistance is concerned, is the amount of immigration of
susceptible individuals (Georghiou and Taylor, 1977a). After treatment with
insecticides only a few RR individuals will usually survive (if a large enough
dose, Do, is used to make the resistance functionally recessive). If, then,
enough SS immigrants arrive and mate with them, for all practical purposes
the offspring will consist only of RS heterozygotes and SS homozygotes,
both of which can be killed with subsequent treatment. If, however, there
are no immigrants, or if they are too few, then substantial numbers of RR
individuals will be produced and the population will be on its way to evolving
resistance. This gives the unstable equilibrium alluded to above. The critical
issues here are the numbers of RR survivors and SS immigrants. Low pop-
ulation densities contribute to fewer RRs, and immigration rates, refugia,
polyphagy, and polygamy all contribute to this process.
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THE EVOLUTION OF RESISTANCE
165
As an illustration of the adverse effect of isolation, or absence of immi-
gration, it may be noted that the highest resistance of house flies in California
was found in populations breeding inside poultry houses. These houses had
been screened, ostensibly for the purpose of excluding flies from entering.
Ironically, prevention of immigrants has probably contributed to even higher
levels of resistance.
In normal pest control all surviving individuals have not necessarily been
reached by chemical treatment. Depending on the biological and behavioral
characteristics of a species, a proportion may be present in refugia at the
time of treatment, thus escaping selection. Refugia may consist of plant
tissues, distorted foliage, growth buds, erineum, and the like, or they may
represent a physiological state of lower susceptibility, such as diapause or
pupation in soil. Whatever the reason, such refugia may be very important
in providing a source of susceptible immigrants, thus retarding evolution
(Georghiou and Taylor, 19761. The eriophyid mite Aceria sheldoni, which
inhabits citrus buds, has been controlled for several years with chlorobenzilate
and has yet to develop resistance. The citrus rust mite, however, also an
eriophyid but feeding on leaf surfaces, has been reported as resistant.
Refugia may often be an important mechanism for delaying the buildup
of resistance. Relative to the inward flux of migrants from the outside, they
are less subject to the vagaries of weather, breeding sites, and other factors
that may influence the timing or intensity of immigration from the outside.
Further, we have suggested that refugia may be created artificially by inten-
tionally excluding from treatment some segment of the population and it can
thus be an operational factor in resistance management (Georghiou and Tay-
lor, 1977b). Even with refugia, however, some inflow of migrants is nec-
essary for an unstable equilibrium to exist.
OPERATIONAL FACTORS IN RESISTANCE
Operational factors in resistance are those related to the application of
pesticides and are thought of as being under man's control. Most obviously
these include the timing, dose, and formulation of pesticides used. But, in
a way, effective dominance, refugia, and immigration may also be under
some degree of control if conditions of application are made more-or-less
favorable to them. For example, as indicated above refugia may be created
by deliberately excluding some part of the population from treatment. The
efficacy of this has been explored by Denholm et al. (1983), using house
flies that had already been partially selected for resistance to a long-residual,
synthetic pyrethroid, permethrin. Within three weeks after a single application
of this persistent insecticide, to which virtually all flies were exposed, they
became very resistant. But when a closely related pesticide, bioresmethrin,
was applied as a space spray at two-week intervals, no buildup of resistance
was observed. This difference was attributed to the fact that bioresmethrin
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
exerted only an immediate toxic effect on the adult flies directly exposed to
it. The many flies not in the adult stage, and thus in refugia, became part
of the breeding population when they later emerged.
Timing of insecticide use may often be important. For an unstable equi-
librium to exist there must be very few RR survivors following the initial
treatment. This will occur if the R allele frequency is low, and also when
the total population size is low. All else being equal, it is desirable to treat
the population before its numbers become too large.
Pesticide dosage has been discussed above as an important determinant of
dominance. Related to this are the formulation and rate of pesticide decay.
After initial application the concentration of pesticide effectively decreases,
because of breakdown, dilution and so forth. If this occurs rapidly then the
population can be thought of as effectively receiving either a large dose, Do,
or none at all. With a persistent pesticide this occurs slowly, however, and
for some time there is an effectively small dose, Ds, that may be very
favorable for resistance development. A persistent pesticide may also kill
susceptible immigrants and thus effectively prevent immigration.
Computer simulations have indicated that the timing and economic thresh-
olds- of application make little difference in the absence of migration. This
is because selection is usually so intense that the selection coefficients are
virtually the same in all these circumstances.
Of course the choice of insecticide is very important. Usually there is
some degree of cross-resistance to other pesticides within the same class.
Depending on the mechanism of resistance, there may also be cross-resistance
among classes. Especially notable are cross-resistance between DDT and
pyrethroids due to the gene kdr and between carbamates and organophos-
phates due to selection of "insensitive" acetylcholinesterase (Hama, 19831.
Whether insecticides are best used in combinations or sequentially is at
present unclear. There are some suggestions that combinations may be more
effective if there is much dominance and immigration in the system (Man),
in press; C. F. Curtis, London School of Hygiene and Tropical Medicine,
personal communication, 19851. Our simulations, using quantitative genetic
models, indicate that there is little difference if one works under the constraint
of a constant selection differential. The available experimental evidence also
suggests that there is little difference. Georghiou et al. (1983) selected mos-
quitoes by various combinations or sequences of temephos, permethrin, and
propoxur, representatives of the three major classes of insecticides. The
populations responded more-or-less the same. They observed, however, that
there was some negative cross-resistance, in that strains that were more
resistant to the organophosphate tended to be more susceptible to the pyr-
ethroid. Just how this can be put to best use in an operational sense is still
unclear. There is certainly a need for more Experimental and theoretical work
on this important problem.
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THE EVOLUTION OF RESISTANCE
167
CONCLUSION
Because insecticide resistance has become such a serious problem in recent
years, it is abundantly clear that merely switching to new insecticides when
the current one is no longer effective cannot continue. Integrated pest man-
agement, which will almost always involve some use of pesticides, is now
regarded as essential. Recognizing and manipulating those factors that may
help retard resistance should be an integral part of any such program. Throughout
the preceding discussion we have emphasized the effects of pesticides on the
target population alone. No mention has been made of the effects on com-
petitors, parasites, or predators. These should be a part of the deliberation
of which strategy to use, especially when considering the use of several
insecticides in combinations. In any practical problem there are bound to be
many unknowns, even surprises. There is a need for better knowledge of the
factors influencing the evolution of resistance, enabling us to better assess
the risk of resistance developing in each individual case and thus to formulate
more realistic management practices for delaying or forestalling its evolution.
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POPULATION BIOLOGY OF PESTICIDE RESISTANCE
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Representative terms from entire chapter:
insecticide resistance
