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GENETIC CONSIDERATIONS IN BIOLOGICAL
PEST CONTROL
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The Natural Population at its Origin
Improving
Fitness of Natural Enemies
Improving Tolerance to Pesticides
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Overview According to past records, about
80% of the natural enemies introduced into a new environment for biological control
in the United States have failed (Clausen 1956); 42% of the Canadian projects
have failed between 1929-1955 (Turnbull & Chant 1961); and 90% have
failed worldwide (Turnbull 1967). There is an apparent modern trend toward
more failures (Hall & Ehler 1979, Ehler & Andres 1983). Many of these
failures involved natural enemies that were poorly adapted to the host
species against which they were introduced, or were handled inefficiently,
released in inadequate numbers and under improper circumstances. Adverse
environmental conditions at the time of liberation are cited as principal
causes for failure. These include unavailable hosts or host plants, scarcity
of food, water or shelter, severe competition with analogous organisms,
adverse toxic effects of chemicals; adverse cultural practices; diapause
problems (Legner 1979b ); and host-parasitoid asynchrony. Researchers are often
able to minimize most of these obstacles or at least recognize their presence
so that establishment trials may be repeated during favorable intervals; but
the genetic make-up of the colonized natural enemies is usually
unknown (Hoy 1976; Mackauer 1972, 1976; Messenger & van den Bosch 1971;
Myers & Sabath 1980; Rousch 1979). In a recent review, Whitten &
Hoy (1996) emphasized that biological control should be favored in terms of
cost effectiveness, environmental acceptability and the safety record which
is overwhelming. They based their conclusion on the numerous examples of pest
reduction with this method. However they reported that biological control has
been attempted for less than 5% of the 5000 or so arthropod pests (Rosen
1985) and probably for an even smaller percentage of nematodes (van Gunday
1985), weeds (Charudattan 1985, Bernays 1985), and plant pathogens (Baker
1985, Schroth & hancock 1985, Lindow 1985, Martin et al. 1985). Genetic studies of beneficial
arthropods reveal great complexities, which cause hesitation to experiment
with improvement at the applied level. However, researchers overlook probable
field examples of genetic improvement, and there is a tendency to devote an
inordinate amount of time viewing limited genetic diversity through
electrophoretic analysis. Genetic considerations are
important to biological control by suggesting improved strategies for the
acquisition of new natural enemies from abroad, in their breeding for
introduction programs, and in their mass release for direct control (Levins
1969, Lucan 1969, Mackauer 1976, 1980; Myers & Sabath 1980; Remington
1968, Whitten 1970). Biological control traditionally
involves the permanent transfer of natural enemies from one geographic area
to another. These natural enemies, or colonizers, after leaving their source
population, are faced with problems not encountered previously. While
searching in the new environment, they invariably confront situations
completely different from those prevailing at their points of origin. Due to
the comparatively small numbers of individuals in the colonizing flock with
respect to the point of origin, intraspecific competition is relaxed,
enabling less fit genotypes to survive, reproduce and interact. Thus, a high
genetic variability develops which may eventually give rise to a new
genotype. Such a process was apparently recorded in England by Ford &
Ford (1930) with the colonial checker-spot butterfly, Euphydryas aurinia
(Rottenburg). Furthermore, if the colonizer originates from a marginal
population, it may more successfully exploit its genetic opportunity because
of a smaller genetic load and a possible lower inversion heterozygosity
(Force 1967, Remington 1968). A group of colonizers is an
atypical isolate of the source population. In the new area to which it is
introduced it no longer is subjected to the diluting effect of gene flow from
the main body of the population. A change in gene frequencies occurs which is
called the Founder Principle. However,
relaxation from intraspecific competition may be accompanied by an increased
interspecific competition to which the colonizer may not be preadapted; and
new environmental conditions may make such competition impossible. When the
environmental resistance is in the form of already established natural
enemies, the introduction of superior species may be difficult or impossible
(Ehler & Andres 1983). When a colonizer encounters
related species in the new environment, the outcome of such encounters
depends on the perfection of the prezygotic barriers to hybridization and
upon the relative fitness of the hybrid and the parental species (Remington
1968). Callan
(1969) offered a list of three major genetic groups of entomophagous
colonizers: (1) colonizers with built-in success which become rapidly
established, (2) colonizers with delayed success and (3) colonizers which are
predestined to fail. Remington (1968) and Lucas (1969) presented opposite
views of the genetic make-up of populations and what should be sought in
biological control. However, Myers & Sabbath (1980) suggest that Lucas failed
to distinguish between probable marginal and central populations. The Natural
Population at its Origin.--The
size of the population at its origin determines its genetic variability due to
mutation (including chromosomal aberrations), outcrossing (the larger the
population the higher the outcrossing rate), and genetic drift, which
endangers very small populations by the loss of genes. The original
population may be either continuous and numerous, continuous and rare,
subdivided into semi-isolated segments or demes, and subdivided into wholly
isolated demes (Remington 1968). The central portion of the source
population dwells in the ecologically optimal region of the species, while
marginal portions are found near the ecological boundaries of the species.
Data for central and marginal insect populations comes principally from Drosophila
studies conducted in the Western Hemisphere by Carson (1955, 1959, 1965),
Dobshansky (1956), Prakash (1973), and Townsend (1952), and for insects and
vertebrates (Nevo 1978). Compared to marginal populations,
central populations are subjected to greater heteroselection, they are larger
and outbreeding, they have increased concealed genetic variability and carry
a higher genetic load. They may show increased inversion heterozygosity and,
therefore, may not be as evolutionarily plastic. Central populations are
adapted to the average environment. Marginal populations may be
subjected to greater homoselection and are small and inbreeding. They have
less alleles per locus and increased homozygosity in Drosophila. There
is a lesser genetic load, but they may be endangered by genetic drift. They
may show less heterozygosity for inversions and, therefore, higher
evolutionary plasticity. Marginal populations are adapted to narrower niches.
Remington (1968) and Messenger & van den Bosch (1971) discussed in
greater detail the characteristics of these two major types of populations.
Nevo (1978) showed electrophoretic data which suggest opposite allelic
characteristics from those described by Remington (1969) from a study of both
vertebrates and invertebrates. Myers & Sabath (1980) concluded that
generalizations about central and marginal populations are not valid and
cannot be used as a basis for decisions on where to collect biological
control agents. But this conclusion seems to weigh the electrophoretic data
more heavily than the cytological evidence from Drosophila. The fact
that most of the alleles marked in electrophoresis are probably neutral (99%
as believed by some), casts doubt on conclusions referring to
"expressed" hetero- or homozygosity. Futuyma (1979) discussed
further limitations of electrophoretic data, and especially emphasized the
possible role of regulator genes, which cannot be assessed biochemically. Cultured parasitic Hymenoptera
show low levels of enzyme polymorphism (Crozier 1971, 1977; Kawooya 1983,
Metcalf et al. 1975), suggesting that more introductions that involved
culturing probably were also deficient in allelic variability. Thus, such
cultures may have conformed closely to the description of the marginal
population given by Remington (1968). Natural Enemy Introductions.--The existence of races in natural enemies is widely known,
but in foreign exploration genetic variability is usually not clearly
expressed. Thus, the stress has been to introduced natural enemies from
varied areas whenever possible to gain greater genetic heterogeneity (Whitten
1970). When natural enemies are first
introduced to new environments, the pace of genetic drift is accelerated and
quick evolution anticipated. The introduced organism, by virtue of both
having been sampled from the original population and then passed
through the bottleneck of culture,
theoretically contains but a small fraction of the original gene pool. Many
of the lost alleles may have been essential for fitness, and a marked trend
for greater homozygosity exists (Legner 1979a, Unruh et al. 1983). Most natural enemy introduction
attempts fall naturally into two or three phases. The first phase
involves an initial search for natural enemies where little is known about
what species exist or their potential for biological control (Zwolfer et al.
1976). Restricted financial support usually dictates a less than thorough
sample of the indigenous area. The second phase is taken after
repeated search has turned up a few natural enemy species, but initial colonization
has failed. Additional information is available since the first attempt.
Continued searching is carried out, or previously discovered species are
tried again in the quest for greater genetic diversity. A final phase
may be entered by researchers cognizant of the importance of genetic make-up,
and involves the acquisition of seasonal and geographic strains of an
initially colonized species. New species are often discovered in this phase
whose activity may be confined to certain seasons. However, the numerous
steps outlined by Mackauer (1980) to assure genetic stability in laboratory
stocks can rarely be taken. Improving Fitness of Natural
Enemies.--Fitness of a
given natural enemy to a target environment may be improved generally in two
ways: (1) by artificial selection, in which a stock of the organism is
created by selection in the laboratory to enable it to cope with some
limiting environmental factor, such as temperature of insecticide treatment
(Hoy 1976, 1979), and (2) by increasing genetic diversity through
hybridization or by colonization of a greater number of individuals from the
source population. A more plastic or diverse stock is created which, after
colonization, will have an increased chance for improvement through natural selection.
A third possibility, genetic engineering, has not yet been attempted with
parasitoids and predators, but has found application with pathogens (e.g., Bacillus
thuringiensis Berliner). Examples of artificial selection
were few prior to 1970, and its practicality in continued improved biological
control was doubtful. Difficulties included a lack of knowledge concerning
the genetic basis for inheritance of the desired characteristics. There is
also usually little information about the amount of genetic diversity on
which to base selection. The possibility of unintentional co-selection for
detrimental qualities is always present (Ashley et al. 1973). Nevertheless, there have been numerous
attempts to select adaptive features for beneficial organisms. One of the
most common efforts involves the improvement of climatic tolerance. Wilkes
(1947) attempted this with Dahlbominus fuscipennis
(Zetterstedt), and DeBach & Hagen (1964) and White et al. (1970) reported
on work with Aphytis lingnanensis Compere. Improvements in the sex ratio to
favor females were sought by Wilkes (1947) with Dahlbominus fuscipennis
and Simmonds (1947) with Aenoplex carpocapsae (Cushman). Host-finding
ability was improved in Trichogramma minutum Riley by Urquijo
(1951); and a change of host preference was induced in Horogenes molestae
(Urchida) by Allen (1954, 1958), and Chrysopa carnea Stephens
by Meyer & Meyer (1946). Resistance to DDT was produced in Macrocentrus
ancylivorous Rohwer by Pielou & Glasser (1952), while in predatory
mites resistance was developed to organophosphate insecticides (Croft 1970,
croft & Brown 1975), to permethrin (Hoy & Knop 1981, Hot et al.
1982), and to sulfur (Hoy & Standow 1982). Interspecific crosses between two
species of Spalangia parasitoids of synanthropic flies in Australia
yielded a field hybrid with improved fecundity and longevity (Handschin 1932,
1934). Intraspecific crosses (crosses
between strains) have resulted in improved host preference behavior in the
tachinid Paratheresia claripalpis (Box 1956), in increased
laboratory productivity in the braconid Apanteles melanoscelus
(Ratzeburg) (Hoy 1975) and in improved fecundity and longevity with Spalangia
and Muscidifurax parasitoids of synanthropic flies (Legner 1972 , 1987a. 1987b, 1988, 1989, 1993). In the latter
case, the reproductive potential was utilized, which gave a strong measure of
fitness, probably influenced by many polymorphic genes. True fitness in the
field, of course, is also influenced by other behavioral traits, such as
habitat selection (see Hoy 1976). However, the process of intraspecific
hybridization and heterosis is probably natural, causing the hybrids to be
more vigorous and better able to withstand environmental resistance, and to
extend their range in all niches a population has mastered (Carson 1959). The
selection of appropriate strains for intraspecific crosses is critical, as
detrimental outcomes due to negative heterosis (hybrid dysgenesis) may occur
(Croft 1970, Mahr & McMurtry 1979, Legner 1972). Hoy (1976) and Whitten & Foster (1975) discuss
genetic improvement further. Experimental field demonstrations
of natural enemy improvement through heterosis apparently exist. The mite
predator, Phytoseiulus persimilis Athias-Henriot, which was
initially established in California from a culture obtained in Chile,
improved its effectiveness following the subsequent introduction of another
strain from Italy (McMurtry et al. 1978). A triple hybrid of Apanteles
melanoscelus gave good inundative release effects, although the final
degree of host parasitism was not higher than that rendered by nonhybrids
(Hoy 1975). Nevertheless, field establishment might not have been successful
with either of the single strains available at the time. Fitness of parasitic insects can
also be improved physiologically without any apparent genetic change, as
evidenced by experimental cold storage treatments (Guzman & Petersen
1986, Legner 1976). There
have been relatively more recent attempts to genetically improve pathogens of
arthropods (Faulkner & Boucias 1985, Luthy 1986, Aizawa 1987, Yoder et al.
1987), nematodes (Gaugler 1987), plant pathogens (Lindow et al. 1989, Napoli
& Staskawitz 1985). Improving Tolerance
to Pesticides.--By 1975 pesticide resistance was found to have
developed under field conditions in some natural enemies, including the
predatory mites Metaseiulus occidentalis, Typhlodromus caudiglans,
Typhlodromus pyri, Amblyseius fallacis, A.
hibisci, the coccinellid Coleomegilla maculata, the
predatory filth fly Ophyra leucostoma, and the braconids Macrocentrus
ancylivorus and Bracon mellitor (Croft & Brown
1975). Croft & Meyer (1973) increased resistance to azinphosmethyl
300-fold in A. fallacis by experimental treatment of a Michigan
apple orchard with 5-7 annual applications over a four-year period. Croft
(1972) expressed pessimism about the efficacy of laboratory selection and
argued in favor of concentrating effort in the field where the experiment
could be conducted under more natural conditions and on a scale not possible
in the laboratory. High levels of resistance to organophosphates and
carbamates and limited response to synthetic pyrethroids were obtained (Croft
& Meyer 1973, Strickler & Croft 1981). The wider benefits of laboratory
selection for improved performance was demonstrated in several ways by Hoy (Whitten
& Hoy 1996). First, the range of natural enemies subjected to artificial
selection was extended to include the parasitoids Aphytis melinus
DeBach and Trioxys pallidus Haliday (Rosenheim & Hoy 1988,
Hoy & Cave 1988) and the common green lacewing Chrysoperla carnea
(Stephens), a generalist predator (Grafton-Cardwell & Hoy 1986).
Secondly, the combined benefits of laboratory and field selection were
optimized (Whitten & Hoy 1996). Previous workers had recognized increased
pesticide resistance among field populations of parasitoids, including A.
melinus, A. africanus and Comperiella bifasciata
(Hoy 1987a), however, where attempts were made to increase resistance levels
in natural enemies by laboratory selection, insufficient attention was given
to the source populations, which were often derived from few individuals or
had been inbred in the laboratory for extended periods. This produced strains
that failed to respond to selection or strains with very low levels of
resistance (Hoy 1987a). With this in mind, intraspecific variation in levels
of pesticide resistance in field populations of M. occidentalis,
C. carnea, A. melinus and T. pallidus
were surveyed, and field material was used to found populations for
laboratory selection (Hoy & Knop 1979, Grafton-Cardwell & Hoy 1985,
Rosenheim & Hoy 1986, Hoy & Cave 1988). This approach provided an
indication of the genetic variability relating to the character under
selection and therefore could be a measure of the likelihood of response to
selection. It also maximized the change of capturing useful genes of major
effect in the founding colonies. An important quality of the
artificial selection program developed by Hoy and her colleagues was the
range of pesticides covered in the selection program, and the successful
incorporation of several into multiple-resistant strains (Hoy 1984, 1985a,
Whitten & Hoy 1996). An economic analysis of the program in terms of
reduced pesticide usage suggested a potential annual return on the cumulative
research investment in the range of 280-370% each year if the program becomes
widely adopted by almond industry (Headley & Hoy 1987). The benefits are
in reality being accrued, as surveys indicate that ca. 60% of the almond
acreage in California relies on resistant M. occidentalis. The
many considerations necessary for effectively employing pesticide resistant
natural enemies, including polygenic vs. single gene systems, are thoroughly
discussed by Whitten & Hoy (1996). Genetic Engineering.--Whenever
genes responsible for a phenotypic shift are known and have been
biochemically characterized, it may be possible to consider transferring such
a desirable gene directly from one insect species to another, thereby
avoiding a labor-intensive and sometimes futile classical selection program.
It is important to have a general method of transferring genes from one
species to another. A method for this is at present (Jan 1991) unavailable,
but there is every reasons to believe the possibility will develop shortly,
and attention ought to be given to identifying suitable genes for transfer
and which organisms should be involved in proposed genetic engineering
projects. Specific genes may not be isolated, propagated in a bacterial
system and studied in a new environment if they have coupled to an
appropriate promoter segment which permits expression. Cloned genes have been
reintroduced into the genome of Drosophila melanogaster. A
preferred technique for such transformations uses a segment of DNA from D.
melanogaster called a transposable P-element which encodes a
transposase enzyme whose function is to facilitate integration of detached
genes back into a chromosome (Whitten & Hoy 1996). Transformation of D.
melanogaster with genes from that of other species is not a routine
procedure in some laboratories. Presnail & Hoy (1992) have developed a
microinjection technique which resulted in the stable transformation of the
western predatory mite Metaseiulus occidentalis. Early
preblastoderm eggs within gravid females were microinjected, the needle being
inserted through the cuticle of gravid females into the egg, or the tissue
immediately surrounding the egg. This maternal injection resulted in
relatively high levels of survival and transformation. Transformation was achieved
without the aid of any transposase-producing helper plasmid. The predatory
mite was transformed with a plasmid containing the Escherichia coli
Beta-galactosidase gene (lacZ) regulated by the Drosophila hsp70
heat-shock promoter. Putatively transformed lines were isolated based on
beta-galactosidase activity in 1st generation larvae. Transformation was
confirmed in the 6th generation by polymerase chain reaction amplification of
a region spanning the Drosophila/E. coli sequences. Other variations of the P-element
system from Drosophila are being evaluated as the basis for a general
gene transfer technology. Preliminary results seem good, but no practical
system has yet developed (Cockburn et al. 1984. Beckendorf & Hoy 1985,
Whitten 1986, Hoy 1987). The technology will probably entail manipulation of
eggs or early embryonic stages, and the development of micro-injection
procedures. Therefore, its application to specific natural enemies might be
difficult, especially for endoparasitoids. Whitten & Hoy (1996) pointed
out that in practical terms we have to choose genes for which specific
mutation will cause a desirable shift in the phenotype, but unfortunately we
usually only determine such an effect after the event. The set of genes we
could therefore be interested in is indeterminate and often indeterminable.
The molecular biologist must modify the genotype in the hope that the
phenotype will shift only in the desired direction, and not in any unintended
direction as well because of pleiotropy. This may be difficult to achieve
especially where the immediate gene product is only distantly connected to
the phenotypic shift. Where the phenotype is directly determined by the
protein product of the gene, there is less of a problem. Similarly, in a
beneficial arthropod, if the gene product is an enzyme highly effective at
metabolizing a pesticide, the phenotypic shift could be significant, stable
and beneficial. However, for most desirable shifts in arthropod natural
enemies, even if the gene transfer capabilities are adequate, the likelihood
of achieving the intended phenotypic shift, as well as excluding unintended
adverse effects on the phenotype, seems remote at the present time (Whitten
& Hoy 1996). These difficulties are probably
less for pesticide resistance and may not apply to microbial natural enemies.
The opportunities to genetically engineer viruses, bacteria and fungi seem
considerable and only limited by the ingenuity of the pathologist. Hence, the
objective is to cause a foreign gene to express in a host causing its
premature death. The task is to develop a practical delivery system (Whitten
& Hoy 1996). It was also emphasized by Whitten & Hoy (1996) that one
obvious risk in genetically engineering beneficial insects, and particularly microbial
pathogens, emanates from the community perceptions of such procedures. It is
not unreal to suggest that the intelligent layman cannot adequately
comprehend the complex way biological knowledge is encoded in DNA and
accessed during the life cycle of an organism to regulate its development and
behavior. "Indeed many biologists do not have sufficient understanding
of the interface between genotype and phenotype to quantify the biological
ramifications and risk of such manipulations. Consequently, there is a
distinct prospect that community demand for fail-safe procedures and
comprehensive environmental impact statements could create serious obstacles
for the genetic engineer of natural enemies. Of increased concern would be
the spillover of these concerns into areas of classical biological control
with the increased risk of otherwise safe and effective natural enemies never
being released because the residual doubts concerning safety could not be
quashed." "The inability of biological control experts to guarantee
in advance successful control of a pest by a natural enemy illustrates that
the discipline is still partly 'art.' As such, we could be sorely pressed if
genetic engineering of natural enemies became the rationale for a community
demand that biological control become an exact science before approval could
normally be given for importation of additional natural enemies. Van Driesche & Bellows (1996)
noted that genetically-modified microorganisms may play an important role
biological control. Government policy on the testing, registration, and use
of these organisms influences the extent and speed of the development of such
agents. Central to these policies are the development of concepts and
procedures for assessing the risks from recombinant microorganisms. Studies
of norirecombinant agents in current use may be belpftil in forming such
policies (Fuxa 1989; Wilson & Lindow 1993). Similar issues arise with
genetically-modified arthropods or other multicellular species (Hoy 1992). Prolonged Culture.--The
problem in culture is to judge whether the stock material is genetically
changed as time goes on. Some commercial insectaries in California have
maintained sustained cultures of beneficial arthropods for over 50 years
without knowingly changing their stock or its effectiveness. In many cases a
beneficial species becomes established from cultures started with very few
founders (Mackauer 1972, Simmonds 1964); and DeBach (1965) found no
correlation between the number of individuals liberated and the probability
of establishment. Studies of three parasitic
species, Muscidifurax raptor Girault & Sanders, M. zaraptor
Kogan & Legner (Legner 1979a), and Aphidius
ervi Haliday (Unruh et al. 1983) show that cultures are indeed changed
genetically with time. In the former two species, cultures maintained for
over 100 generations (25 days allowed for one generation) were compared to
those gathered from the field just one or three generations earlier. An
examination of their reproductive potentials indicated an immediate loss of
wild alleles during the first couple of generations in culture. However,
considerable heterogeneity (and presumably heterozygosity) was retained in culture
over the 100 generations (Legner 1979a ). Declines in
allozyme variability in laboratory populations of A. ervi
(Unruh et al. 1983) support the initial loss of heterozygosity in cultures of
arrhenotokous Hymenoptera. There is no clear agreement,
however, on how to retain heterozygosity. Unruh et al. (1983) believed that
the only way to prevent genetic drift in laboratory culture is to keep
population sizes large. Wright (1951) recommended subdividing the population
into several smaller subpopulations (stepping stones) among which gene fly
may occur. A compromise suggested by studies with Muscidifurax species
(Legner 1979a, 218. ) might be
considered as follows: Initial acquisitions of field
cultures could be converted to a series of inbred lines, maintained without
gene flow among them to guarantee their separate characteristics and
the retention of a greater number of alleles with respect to all lines
cultured. This is possible with some hymenopterous species because genetic
decay is uncommon or unknown (Crozier 1970, Legner 1979a ). The number of individuals in each line could be held
relatively low with the heterozygosity among lines retained by having a large
number of such separate lines. The more lines initially established from
individuals acquired in the field, the greater the chances for the presence
of genetic variability. Because gene flow is eliminated between lines, there
would be a reduced tendency for certain genotypes to dominate as in a single
large culture. The total number of individuals of a species thus cultured
might not be much greater than that recommended by advocates of the large
populations. The greatest increase in labor would be that associated with the
maintenance of separate units. The technique might have to be
modified for Hymenoptera possessing the Whiting single locus multiple allele
scheme of sex determination (Crozier 1971, Whiting 1943). Also, variability
in the stock of inbred lines would probably not reconstitute the original
sampled population (Wright 1980). Admittedly, duplicating the structure of
the original population is impossible. However, the inbred isolated line
approach would offer a further step in the direction of increasing
heterozygosity. Not employing the technique certainly guarantees losing
heterozygosity. For example, in the Muscidifurax study (Legner 1979a ), contrary to expectations, traits for both high and low
reproductive potential were lost in prolonged culture. Such traits, along
with other unknown attributes of fitness, such as high searching capacity,
might have been preserved had original genomes been isolated. Thus, although
Unruh et al. (1983) believed that inbred lines do not presently represent a
practical alternative for maintaining genetic variability in biological
control importations, it seems that they may be an expedient way to retain
greater heterozygosity than is now usually the case. It was emphasized by Luck et al.
(1992) that inbreeding when coupled with the haplo-diploid genetic system,
has consequences for the maintenance of parasitoid cultures in addition to
those associated with the occurrence of diploid males. The genome of a
parasitoid can be classified into three functional parts: (1) genes that code
for traits expressed in both males and females, (2) genes that code for
traits expressed only in females and (3) genes that code for traits expressed
only in males (Luck et al. 1992). Because of haplo-diploidy the three groups
of genes are exposed to different selection regimes. Those traits expressed
only in males are exposed to selection each generation in the hemizygous
male. Since more mutations are deleterious, such a selection regime will
rapidly eliminate these alleles from the genome. A portion of the alleles
expressed in both males and females will be exposed to selection and each
generation in the male offspring but the rest will remain hidden in the
diploid female as heterozygotes. Thus, the elimination of these alleles
occurs more slowly, especially if they are recessives. In contrast
deleterious recessive alleles expressed only the females may remain hidden
within the genome at low frequencies for long periods. Such alleles are
subjected to selection only when they are homozygous. The number of hidden,
deleterious alleles maintained within the female genome is referred to as the
genetic load. The male-limited genome evinces a higher genetic load than that
expressed in the females because of the single set of chromosomes possessed
by the male. The genome expressed in both males and females lies somewhere in
between depending on the percentage of males. Thus, initially females should
be affected more than males by inbreeding when the increased homozygosity
arising from inbreeding exposes the recessive, deleterious alleles (Luck et
al. 1992). Estimates of the percentage of the
genome expressed in both males and females, in males only or in females only
are difficult to obtain. Of 99, mainly morphological characters assayed in Bracon
hebetor, 4.3% were expressed only in males, 21.2% in the females and
75% in both males and females (Smith & Borstel 1950). Kerr (1975) found
that 14.3% of visible alleles in Apis mellifera, 35.9% of the
sterility genes in Nasonia vitripennis, 21.2% of such genes in B.
hebetor and 45.7% of the genome governing quantitative traits in Aphis
mellifera were limited in their expression to females. These figures
suggest that a sizeable proportion of loci are expressed only in the female.
However, Crozier's (1976) calculations suggest that this genome is a rather
small percentage of the total genome. If 1% of the loci are sex limited in
their expression, about 56% of the lethal alleles detected through inbreeding
are limited in their expression in females. Estimates of the percentage of
the genome that is sex-limited using lethal and visual mutations expressed
only in females may be highly biased. These mutations likely involve female
specific behavior and are, thus, more difficult to detect than lethal or
visual mutations (Luck et al. 1992). In cultures subject to inbreeding
such as those used in biological control the genetic load hidden in the
female-limited genome potentially influences the sex ratio by affecting the
production of female offspring. The potential for such an effect depends on
whether the species typically outbreeds, the size of the breeding population,
and the level and diversity of genes present in the initial population (Luck
et al. 1992). Females of species that typically outbreed usually manifest sex
ratios of 1:1. Deleterious alleles expressed as sex limited traits, e.g.,
those affecting egg fertilization or mating success, potentially increase the
proportion of males in a culture by affecting fertilization. Unfertilized
eggs give rise to males. Thus inbreeding leads to homozygosity in female
lethals and sterility traits which effects egg viability or the number of
eggs that are fertilized. For example, only 49% of the eggs of inbred Bracon
hebetor hatched compared with an 80% hatch of the eggs of outbred
females. In the diplo-diploid species Drosophila simulans a
clear depression occurred after six generations of sibling matings in the
percentage of females that were mated after a one hour exposure to a sibling
male (Ringo et al. 1987). In Hymenoptera such a change should lead to a
higher percentage of males in the culture. This along with the occurrence of
diploid males may explain the low percentage of female progeny reported in
laboratory cultures of several Ichneumonidae and Braconidae (Bradley &
Burgess 1934, Simmonds 1947, Flanders & Oatman 1982, Oatman & Platner
1974). In addition to genetic load, the
single-locus and multiple-locus models for sex determination (see ENT229.10)
predict that rearing arrhenotokous species confined as small populations will
produce diploid males at increasing frequencies because of inbreeding and
homozygosity at the sex-determining loci. The rapidity with which this
happens depends primarily on (1) the amount of genetic diversity among the
individuals used to initiate the culture, (2) the effective population size,
and (3) the number of gender-determining loci involved. Depending on the
species, diploid males can either be fertile or infertile. If fertile,
diploid males are capable of mating with females but the fertilized eggs are
usually sterile. The few females that occasionally develop from these eggs
are triploid and also usually sterile. Thus a decreasing number of females
because of genetic reasons, and an increasing number of diploid males and
those arising from unfertilized eggs, characterize such inbred populations.
The consequence is the likely extinction of the culture (Luck et al. 1992). Chalcidoidea seem much less affect
by inbreeding. The generality of the single-locus and multiple-locus models
can be tested by continued inbreeding and testing for diploid males. However,
long term inbreeding experiments failed to reveal diploid males in either Nasonia
vitripennis or Mellitobia (Schmieder & Whiting 1947).
However, it can always be argued that the inbreeding has not been long enough
to create complete homozygosity at all sex loci or that homozygous sex
alleles are lethal (Crozier 1971). Indirect evidence suggests otherwise.
Smith (1941) was the first to call attention to the high homozygosity of many
thelytokous species. In such species normal meiosis occurs and diploidy is
restored by the fusion of two of the meiotic products. With many of these
cytogenetic mechanisms the homozygosity of individuals increases over time
and should lead to complete homozygosity. Under such circumstances diploid
males are expected if the single-locus or multiple-locus models apply.
Diploidy is restored in the thelytokous species Diplolepis rosae
by gamete duplication leading to complete homozygosity in one generation
(Stille & Davring 1980). Similar mechanisms appear to allow restoration
of diploidy in Muscidifurax uniraptor (Legner 1985b) and several Trichogramma spp. (Luck et al. 1992).
Because these thelytokous forms produce females generation after generation,
the sex locus models do not appear to be a general explanation for sex
determination in Hymenoptera (see ENT229.10). Although males should suffer no
negative effects from inbreeding, some unexpected results have been reported
in the drones of inbred honeybees, A. mellifera. At relatively
low (25-50%) levels of inbreeding, males appeared to suffer substantial
inbreeding depression in the number of sperm produced, flight performance and
several physiological and biochemical characters (Luck et al. 1992). We must also consider whether
heterozygosity in our imported biological control organisms is indeed
necessary. Introductions from marginal homozygous populations may yield
organisms with the capacity for rapid change in the new environment (Remington
1968). Because, as mentioned earlier, conditions at the place of introduction
always differ to some degree from the place of origin, the colonizer
invariably is faced with differences which may require it to modify its
genotype in order to be maximally successful. Thus, organisms with greater
homozygosity may be better candidates for introduction because they have a
better capacity for evolving into new superiorly adapted types (Remington
1968). In biological control, which aims at reducing pest densities, this has
important implications. Liberations of the previously described inbred lines
in different geographic portions of the introduction area offers a means for
testing this hypothesis. Some support for its validity is the evidence of
many successful biological control introductions having obviously involved
highly inbred, homozygous lines of natural enemies (Mackauer 1972). In this section we briefly
illustrated the complexities involved in genetic considerations of natural
enemy introduction, which leaves some researchers perplexed when considering
practical solutions. This was again made obvious in a recent statement by
Unruh et al. (1983) that "Genetic drift, as well as inbreeding and
selection occurring in founder colonies, transport, quarantine and culture of
natural enemies, will deter us from reaching our goals until we grasp the
nature of variation within and among populations." However, achievements
in the improvement of fitness are common to entomologists and plant scientists
alike (Hoy 1976). Since laboratory techniques for creating apparently better
adapted strains are available, and field demonstrations are known (Hoy 1976,
1982a, 1982b; McMurtry et al. 1978, White et al. 1970), there is no reason
why we cannot proceed with other planned attempts. Exercise 9.1--According
to Charles Remington's hypothesis, a foreign explorer should collect natural
enemies from what portion(s) of their home range? Exercise 9.2--How
may natural enemies be improved to produce greater impact on a target
host population? Exercise 9.3--Of
what theoretical value is a knowledge of population genetics in biological
control? Exercise 9.4--Discuss
some important genetic characteristics for a colonizer. Exercise 9.5--How
might heterozygotes differ from homozygotes in meiosis? Of what evolutionary
significance are such differences? Exercise 9.6--What
is required for the persistence of a pesticide-resistant strain of natural
enemy in the environment? Exercise 9.7--Discuss
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