Selective adaptation to noxious foods

feeding by herbivorous insects. Some of these noxious compounds are both unpalatable and toxic, while others are merely unpalatable or toxic (Bernays and Chapman, 1987; Chapman and Sword, 1994; Glendinning, 1996; Harley and Thorsteinson, 1967). Because many plants concentrate noxious compounds in their most nutritious tissues (McKey, 1979), herbivores would benefit from an ability to adapt to foods containing these compounds. Indeed, there are many reports of herbivorous insects adapting to foods containing noxious plant compounds following 1–4 days of chronic exposure (e.g. Blaney and Simmonds, 1987; Blaney et al., 1986; Glendinning and Gonzalez, 1995; Jermy et al., 1982; Raffa and Frazier, 1988; Schoonhoven, 1969; Snyder and Glendinning, 1996; Usher et al., 1988; Glendinning et al., 2001). There are also reports, however, of herbivorous insects failing to adapt to foods containing noxious plant compounds (Yamamoto and Fraenkel, 1960; Chapman and Sword, 1994; Jermy et al., 1987). In some cases, the failure to adapt was so absolute that the insects starved to death rather than eat the noxious food (e.g. Peterson et al., 1993). Insects have both gustatory and post-ingestive mechanisms for adapting to noxious compounds in foods. Repeated sampling of noxious foods can (i) desensitize the peripheral or central gustatory mechanisms that mediate the aversive response (e.g. Simmonds and Blaney, 1983; Glendinning et al., 1999a; Glendinning et al., 2001), (ii) activate post-ingestive adaptation mechanisms that reduce an insect’s toxic sensitivity to the noxious compound (e.g. induction of P450 detoxification enzymes in the midgut; Snyder and Glendinning, 1996) or (iii) engage both gustatory and post-ingestive adaptation mechanisms (Szentesi and Bernays, 1984). Given all these adaptation mechanisms, why do insects nevertheless fail to adapt to some noxious plant tissues? We hypothesized that insects have more difficulty adapting to compounds that are both unpalatable (e.g. bitter) and toxic than to compounds that are merely unpalatable. To test this hypothesis, we developed several ways to dissociate the contribution of gustatory versus toxicity effects to the physiological adaptation process. Our model system consisted of the tobacco hornworm caterpillar (Manduca sexta; Sphingidae) and two plant compounds, salicin (a phenolic glycoside) and aristolochic acid (an aromatic nitro derivative). Both these compounds taste bitter to humans and inhibit feeding in M. sexta through a gustatory mechanism during 2 min feeding tests (Glendinning et al., 1999b). Salicin and aristolochic acid may also inhibit 3355 The Journal of Experimental Biology 204, 3355–3367 (2001) Printed in Great Britain © The Company of Biologists Limited 2001 JEB3634