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            GENETIC CONSIDERATIONS IN BIOLOGICAL

 

                                   PEST CONTROL

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Overview

The Natural Population at its Origin

Natural Enemy Introductions

Improving Fitness of Natural Enemies

Improving Tolerance to Pesticides

Genetic Engineering

Prolonged Culture

Exercises

References

[Please refer also to Selected Reviews #1, #2  &  Detailed Research ]

 

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 were 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 norecombinant agents in current use may be helpful 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.

Exercises:

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 genetically engineering desirable traits into natural enemies.

 

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