Why is the evolution of resistance to parasitoids in pests under biological control regimes so rare? Obviously, there has to be both genetic variation and a selection pressure in order for any evolution to take place, but these two are not necessar- ily sufficient. An interesting example for this comes from the study of a field pop- ulation of the pea aphid (Acyrtosiphon pisum) and the parasitoid Aphidius ervi.
Henter (1995) and Henter and Via (1995) showed that, despite within-population genetic variation for resistance in the host and substantial attack rates by the par- asitoid, there was no detectable change in resistance in the population during a season. An obvious explanation for this lack of evolution would be the existence of considerable costs of resistance, but on-going work by Ferrari et al.(2001) has so far failed to find such a cost.
At least a pivotal part of the explanation is the existence of costs of resist- ance in the host/pest combined with variation in selection pressure exerted by the parasitoid. Owing to population dynamical processes, parasitoid numbers are more likely to fluctuate than a pesticide concentration. There is growing evidence that resistance mechanisms that rely on a quantitative change in the host, such as an increase in haemocyte numbers, are more likely to bear substantial costs than those that involve a qualitative change, such as a modification of a recognition protein (Cousteau et al., 2000; Rigby et al., 2002). As resistance to parasitoids will usually involve the deployment of an immune system, this suggests that, on average, costs of resistance to parasitoids are likely to be higher than against pes- ticides. However, further empirical work will be needed to confirm this.
Interestingly, Bergelson and Purrington (1996), in a survey of costs of resistance in plants, found that costs of resistance against herbicides have been found more often than costs of resistance against herbivores.
Another potentially important aspect of costs of resistance is the relative magnitude of costs of resistance in the host and costs of counter-resistance in the parasitoid. Sasaki and Godfray (1999) constructed a model to explore this issue.
The model included a genetically variable host and parasitoid population, non- specified costs of resistance and counter-resistance, and allowed the host and par- asitoid population to show population dynamics. One of their main results was that when costs of resistance and counter-resistance are roughly comparable, evolutionary cycles appeared in which hosts alternately experienced selection for and against high resistance. However, when costs of resistance in the host were
176 A.R. Kraaijeveld
relatively high compared with costs of counter-resistance in the parasitoid, the majority of hosts did not invest in resistance but essentially traded off the cost of resistance against the risk of being attacked. Such a scenario may explain, for instance, why D. subobscuradoes not appear to have an immune response to par- asitoid attack, despite suffering from high levels of parasitism at times.
Although this model result of hosts not evolving resistance, despite being under considerable selection pressure to do so, is reminiscent of the situation in many biocontrol projects using parasitoids, it remains to be seen whether this par- ticular aspect of the cost of resistance also plays a role in explaining the rarity of the evolution of resistance in pest insects. However, experimental evolution strongly suggests that costs of resistance play a pivotal role in preventing pest insects from evolving resistance against their biocontrol agents.
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Introduction
Bioengineered transgenic insecticidal crops are among the most significant tech- nological developments in insect pest management since the advent of synthetic insecticides (Persley, 1996; Cannon, 2000; Perlak et al., 2001). Transgenic cotton and maize that produce insecticidal toxins derived from genes transferred from the bacterium Bacillus thuringiensis kurstaki(Btk), for protection against lepidopter- an pests, have been planted widely in selected countries (Cannon, 2000; Fitt, 2000; Pray et al., 2002; Shelton et al., 2002). The planting of transgenic Bt maize is one of the most commonly used methods for suppression of the European corn borer,Ostrinia nubilalis, in maize-growing regions of the USA. Since 1996, the area of Bt cotton planted in the USA has increased nearly 2.5 times, to approx- imately 1.8 million ha (Perlak et al., 2001; Shelton et al., 2002). Transgenic Bacillus thuringiensis tenebrionis(Btt) potatoes created to resist the Colorado potato beetle, Leptinotarsa decemlineata, were grown on relatively small areas in the USA until 2001, when transgenic Bt potatoes were no longer sold (Shelton et al., 2002).
Additional transgenic insecticidal crops have been bioengineered for insect resist- ance using digestive inhibitors, e.g. snowdrop lectin (Galanthus nivalisagglutinin, GNA) and several protease inhibitors (Gatehouse et al.,1996; Michaud, 2000).
The widespread planting of transgenic crops with tissues containing high levels of insecticidal toxins has raised concerns about gene flow, selection for tol- erant pest populations and ecological disruptions of food webs (Rissler and Mellon, 1996; Snow and Palma, 1997; Gould, 1998; Beringer, 2000; Cannon, 2000; Hails, 2000; Poppy, 2000; Watkinson et al., 2000; Wolfenbarger and Phifer,
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