Behavioural side-effects of insecticide resistance in aphids increase their vulnerability to parasitoid attack

Previous studies using the aphid Myzus persicae have shown that strong heritable variability in a defence behaviour, response to aphid alarm pheromone, is consistently associated with the possession of two insecticide resistance mechanisms. Insecticide-susceptible and -resistant aphids therefore provide the ideal biological material for testing the hypothesis that interactions with the third trophic level (parasitoids) can play a significant inhibitory role in the evolution of adaptive traits at the second trophic level (aphids), based on a fitness trade-off between resistance to insecticides and avoidance of parasitism through defence behaviour. Eight parthenogenetic M. persicae clones, representing different insecticide resistance genotypes, were exposed to alarm pheromone to confirm their level of response. Observations of these clones during periods of exposure to adult female parasitoids, Diaeretiella rapae, were then made in small-scale arenas in the presence and absence of measured amounts of alarm pheromone. Clones showing a consistently high alarm response (insecticide-susceptible forms) displayed a range of behaviours during and after parasitoid attack that were significantly associated with greater survival (avoidance of parasitism) compared with aphids showing a low alarm response (insecticide-resistant forms). Furthermore, this culminated in the latter suffering significantly higher levels of mummification. These data not only provide important empirical evidence that a normal (wild-type) high aphid alarm response reduces vulnerability to parasitoid attack but also represent the first example of insecticide resistance genes having negative pleiotropic effects on fitness by producing maladaptive behaviours in the context of selection imposed by a higher trophic level.