Selective adaptation to noxious foods by a herbivorous insect

Abstract

SUMMARYWhen animals repeatedly sample a noxious food over a period of 1–4 days, they can markedly reduce their aversive behavioral response to the diet’s unpleasant taste (e.g. ‘bitterness’) or toxic effects. This long-term adaptation process is selective, however, permitting insects to adapt physiologically to some but not all noxious foods. We hypothesized (i) that the selective nature of this adaptation process stems from the fact that some unpalatable foods are toxic while others are harmless and (ii) that insects have more difficulty adapting to foods that are both unpalatable and toxic. Our model system consisted of Manduca sexta caterpillars and two compounds that taste bitter to humans and elicit an aversive behavioral response in this insect (salicin and aristolochic acid). We found that 2 days of exposure to a salicin diet completely adapted the aversive response of the caterpillars to salicin, but that exposure to an aristolochic acid diet failed to adapt the aversive response to aristolochic acid. We determined that M. sexta could not adapt to the aristolochic acid diet because it lacked mechanisms for reducing the compound’s toxicity. In contrast, the salicin diet did not produce any apparent toxic effects, and the caterpillars adapted to its aversive taste within 12 h of exposure. We also found that the salicin adaptation phenomenon (i) was mediated by the central gustatory system, (ii) generalized to salicin concentrations that were twice those in the adapting diet and (iii) offset spontaneously when the caterpillar was transferred to a salicin-free diet. We propose that toxicity is a more significant barrier to dietary adaptation than ‘bitterness’ in this insect.