ReviewMutations and their use in insect control
Introduction
Insect pests continue to pose a major threat to man, his animals and his crops despite the best efforts of entomologists to develop effective control strategies. Killing insect pests with chemicals has been the traditional approach to confronting this threat and this is likely to be the main line of defense for some time to come. Over the past few decades, there has been a continuous improvement in the effectiveness of the different active molecules both in specificity and in the mode of delivery, which has culminated in the now wide-spread use of transgenic plants that produce an insect toxin [1]. The prevalent use of chemical poisons on large populations of insects over space and time quickly demonstrated the direct relevance of the mutation process to insect control with the rapid development of insecticide resistance. Insects very quickly evolved heritable, stable, qualitative or quantitative changes in their genomes that rendered many chemicals largely ineffective [2], [3], [4], [5]. Other approaches to insect management include the use of other living organisms as a form of biological control [6] or manipulation of insect behavior using semio-chemicals [7]. These approaches are far less damaging to the environment, but now even classical biological control is not escaping criticism due to the sometimes unpredictable consequences of introducing a natural enemy into a new ecosystem [8]. The vast majority of current insect control techniques can be seen as variations on these major themes accompanied by constant attempts to improve specificity and efficiency and to reduce any detrimental effects on the environment.
An increasingly common principle heard in insect control is the use of the area-wide approach. This recognizes the importance of taking into account the spatial and temporal distribution of the total pest population when implementing insect management field programs. It often enables a proactive approach to be taken instead of reacting when pest populations reach threatening levels and in certain situations, it can lead to the eradication of pest insects from large areas. A recent book describes in detail the theory and practice of the use of this approach [9]. The use of gene and/or chromosome mutations as components of rational insect intervention strategies represents an additional weapon in the fight against insect pests.
In the late 1930s, Knipling suggested (see [10]) that if a way could be found to genetically sterilize male insects, without affecting their ability to mate, then following their release and mating with wild female insects, population fertility could be reduced leading to suppression or even eradication of the target population. Even though geneticists were aware for some time that X-rays could in fact sterilize insects [11], [12], it was not until 1950 that the first experiments were carried out to evaluate this procedure on an insect pest namely, the New World screw-worm, Cochliomyia hominivorax [13]. The demonstration that sterility could indeed be induced by X-rays in this species was the first small step on the way to the eradication of this serious livestock pest from the southern states of America and now from most countries of Central America [14]. This long-term and hugely successful program (Fig. 1) has demonstrated the important role that radiation-induced mutations can play in developing environmentally acceptable, area-wide, pest intervention strategies.
During the first field trials of sterile screw-worms in Curacao, the genetic basis of the induced sterility was poorly understood, as was knowledge of the genetics of the screw-worm, leading to the comment by Bushland that “we eradicated screw-worms from Curucao and the southeastern United States without knowing how many chromosomes it had” (quote in [15]). It was, however, realized very early on that the induced sterility was a result of the induction of dominant lethal mutations in the irradiated sperm [13] and the application of this principle for insect control became known as the sterile insect technique (SIT). This first powerful demonstration of the role that mutations could play in insect control technology led to a re-assessment of many other well known genetic phenomena [16], [17], [18], [19], [20]. More recently, the ability to introduce genes into the germ-line of many insect pests [21], [22], [23], [24], [25], [26], [27], [28], [29], [30], [31], [32] has opened up new possibilities and excited the imagination of insect molecular biologists who are now proposing radical new approaches to the way we look at insect control. This review will aim to put into perspective the opportunities presented by the different types of “mutation” in order to develop more efficient and acceptable methods for insect control. Table 1 shows a chronology of the key events that have played a role in developing the use of mutations in insect control. Several of these key events will be discussed in detail in the following sections.
Section snippets
Dominant lethal mutations and the sterile insect technique
The unique opportunity that mutations provide to the field of insect control is exemplified by the use of radiation-induced dominant lethal mutations in the SIT. Dominant lethality occurs when a haploid nucleus has been altered in such a way that when combined with a normal haploid nucleus the resulting zygote dies at the moment when the genetic information required for normal development is absent or incorrect [12]. A very early convincing demonstration of dominant lethal induction was
Genetically derived sterility
Individuals carrying different types of structural chromosomal mutation can produce a variety of gametes, some of which carry unbalanced genetic material that can lead to zygotic death following fertilization. Serebrovskii [67] described the use of chromosomal translocations for insect control based on the production of unbalanced gametes from individuals carrying translocations in the heterozygous condition. He also noted that together with the unbalanced gametes segregating from the
Developing improved strains for sit
An examination of the principles on which SIT is based reveals that it is only the sterile male insects that are required in the field as they transfer sperm carrying the dominant lethal mutations to wild females. Females however have to be reared, irradiated and released, with their associated costs, even though they do not contribute to the overall effectiveness of the technology. If females could be removed from the production and release procedures then considerable economic advantages
Transformation and beneficial mutations
The successful demonstration of transformation in Drosophila melanogaster [184] encouraged the development of similar systems in other insects, including important pest species. A review by Handler [185] provides a comprehensive historical account of the development of trangenesis for pest insects and, as indicated in the introduction, this has now been largely successful in wide variety of species. Looking at the speed of development of the technology it is likely that most insects will be
Conclusion
For some time conventional insecticides will continue to be very important components of pest control strategies, however, increasing public concerns relating to food safety and the increasing demand for organically grown agricultural products will put further constraints on their use. The use of transgenic plants to express insecticidal proteins does not appear to address these two issues in any significant way and in itself will probably lead to the development of resistance, a process that
References (203)
- et al.
Transposable elements and gene transformation in non-drosophilid insects
Insect. Biochem. Mol. Biol.
(1996) A study of the causes underlying the differences in radiosensitivity between mature spermatozoa and late spermatids in Drosophila
Mutat. Res.
(1969)- et al.
Insect radiosensitivity: dose curves and dose fractionation studies of dominant lethal mutations in the mature sperm of four insect species
Mutat. Res.
(1984) - et al.
Radiation sterilization of Aedes aegypti in nitrogen and implications for sterile male technique
Nature
(1973) - et al.
Radiation repair of chromosome breaks as effected by constituents of nucleic acids
Rad. Botany
(1967) - et al.
Theoretical studies on the use of translocations for the control of tsetse flies and other disease vectors
Theoret. Pop. Biol.
(1971) Transgenic host plant resistance to insects—some reservations
Ann. Entomol. Soc. Am.
(1999)Insecticide resistance, a problem in applied biology
Sci. Prog. Oxf.
(1975)- et al.
Genetic and biological influences in the evolution of insecticide resistance
J. Econ. Entomol.
(1977) - et al.
Operational influences in the evolution of insecticide resistance
J. Econ. Entomol.
(1977)
Gene amplification and insecticide resistance
Ann. Rev. Entomol.
Environmental impacts of classical biological control
Ann. Rev. Entomol.
The use of gamma for control or eradication of the screw-worm
J. Econ. Entomol.
Effects of roentgen rays on the tobacco or cigarette beetle and the results of an experiment with a new roentgen tube
J. Agric. Res.
Artificial transmutation of the gene
Science
Experiments with screw-worm flies sterilized by X-rays
J. Econ. Entomol.
Insect control by genetic manipulation of natural populations
Science
Control of insect populations through genetic manipulations
Ann. Entomol. Soc. Am.
Genetic control of insect populations
Science
Field studies of genetic control systems for mosquitoes
Ann. Rev. Entomol.
Genetic control of insect pests: growth industry or lead balloon
Biol. J. Linnean Soc.
Prospects for the genetic transformation of arthropods
Insect. Mol. Biol.
Stable transformation of the yellow fever mosquito, Aedes aegypti, with the Hermes element from the housefly
Proc. Natl. Acad. Sci. U.S.A.
Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti
Proc. Natl. Acad. Sci. U.S.A.
The Lepidopteran transposon vector, piggyBac, mediates germ-line transformation in the Mediterranean fruitfly
Proc. Natl. Acad. Sci. U.S.A.
Building a better bug
Sci. Am.
Genetic transformation of non-drosophilid insects by transposable elements
Ann. Entomol. Soc. Am.
Stable germ-line transformation of the malaria mosquito Anopheles stephensi
Nature
Germ-line transformation of pink boll-worm (Lepidoptera: Gelechidae) mediated by the piggyBactransposable element
Insect. Mol. Biol.
Transformation of Stomoxys calcitrans with a Hermes gene vector
Insect. Mol. Biol.
Successful transformation of the housefly, Musca domestica (Diptera: Muscidae) with the transposable element, mariner
Appl. Entomol. Zool.
The piggyBac transposon mediates germ-line transformation in the Oriental fruitfly and closely related elements exist in its genome
Insect. Mol. Biol.
Production of dominant lethal genetic effects by X-radiation of sperm in Habrobracon
Science
Population control by release of irradiated males
Science
The dosage response curve from radiation-induced dominant lethal mutations in the honeybee
Genetics
Effects of gamma irradiation on longevity and oviposition of the codling moth
J. Econ. Entomol.
Effect of irradiation on adult fecundity and longevity of the Mediterranean fruitfly Ceratitis capitata Wiedemann in Egypt (Diptera: Tephritidae)
Zeit. Ang. Entomol.
Sterilization of boll weevil pupae with fractionated doses of gamma irradiation
Entomol. Exp. Et. Appl.
Sterilization of screw-worm flies (Diptera: Calliphoridae) with gamma rays: restudy after two decades
J. Med. Entomol.
The rate of induction of dominant lethals in Drosophilia melanogaster sperm by X-rays
J. Genet.
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