Review
Mutations and their use in insect control

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Abstract

Traditional chemically based methods for insect control have been shown to have serious limitations, and many alternative approaches have been developed and evaluated, including those based on the use of different types of mutation. The mutagenic action of ionizing radiation was well known in the field of genetics long before it was realized by entomologists that it might be used to induce dominant lethal mutations in insects, which, when released, could sterilize wild female insects. The use of radiation to induce dominant lethal mutations in the sterile insect technique (SIT) is now a major component of many large and successful programs for pest suppression and eradication. Adult insects, and their different developmental stages, differ in their sensitivity to the induction of dominant lethal mutations, and care has to be taken to identify the appropriate dose of radiation that produces the required level of sterility without impairing the overall fitness of the released insect. Sterility can also be introduced into populations through genetic mechanisms, including translocations, hybrid incompatibility, and inherited sterility in Lepidoptera. The latter phenomenon is due to the fact that this group of insects has holokinetic chromosomes. Specific types of mutations can also be used to make improvements to the SIT, especially for the development of strains for the production of only male insects for sterilization and release. These strains utilize male translocations and a variety of selectable mutations, either conditional or visible, so that at some stage of development, the males can be separated from the females. In one major insect pest, Ceratitis capitata, these strains are used routinely in large operational programs. This review summarizes these developments, including the possible future use of transgenic technology in pest 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

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