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Selective adaptation to noxious foods by a herbivorous insect

John I. Glendinning^*, Stephanie Domdom and Eliza Long

Department of Biological Sciences, Barnard College, Columbia University, 3009 Broadway, NY 10027, USA

View larger version (25K): [in a new window]   Fig. 1. Ingestive responses of caterpillars: (A–C) to the control, aristolochic acid (0.38 mmol kg–1) and salicin (157 mmol kg–1) diets following 48 h of exposure to the control diet (N=30 caterpillars), (D–F) to the control and aristolochic acid (Aristo. acid) diets following 48 h of exposure to the aristolochic acid diet (N=24) and (G–I) to the control and salicin diets following 48 h of exposure to the salicin diet (N=24). We present three measures of ingestive behavior across the 2 min brief-access biting test: total intake, total number of bites and bite size. We compare the median values in each panel (± median absolute deviation) using the Wilcoxon matched-pairs signed-rank test (*P0.025).

View larger version (20K): [in a new window]   Fig. 2. Food consumption (A) and growth (B) in caterpillars maintained for 48 h on the control (N=18), aristolochic acid (Aristo. acid; N=8) or salicin (N=15) diet. The concentrations of aristolochic acid and salicin in the diets are as in Fig. 1. We monitored food consumption indirectly by measuring the total amount of frass (dry mass) produced during each successive 4 h time interval. We monitored growth directly by determining the percentage increase in mass that occurred over the two successive 24 h exposure periods. In A, we compare frass production during the initial 4 h between caterpillars maintained on the aristolochic acid versus control diets (or salicin versus control diets) using the Mann–Whitney U-test (*P0.05). In B, we compare the percentage increase in mass between caterpillars maintained on the aristolochic acid versus control diets (or salicin versus control diets) after 24 and then 48 h of exposure using the Mann–Whitney U-test (*P0.025). All values are medians ± median absolute deviation.

View larger version (17K): [in a new window]   Fig. 3. Growth in caterpillars lacking their lateral, medial and epipharyngeal sensilla on (A) the salicin versus salicin control diets or (B) the aristolochic acid (Aristo. acid) versus aristolochic acid control diets. We monitored growth directly by determining the percentage increase in mass that occurred over two successive 24 h exposure periods. In each panel, we compare the percentage increase in mass between caterpillars maintained on either diet after 24 and then 48 h of exposure using the Mann–Whitney U-test (*P0.025). All values are median ± median absolute deviation (N=10–11 per treatment group). The concentrations of aristolochic acid and salicin in the diets are as in Fig. 1.

View larger version (27K): [in a new window]   Fig. 4. Effects of different periods of exposure (6, 12, 24 or 48 h) to the control (A–C) or salicin (D–F) diet on the ingestive responses of caterpillars to the salicin diet. We used a 157 mmol kg–1 concentration of salicin in both the exposure diet and the diet used to evaluate ingestive responsiveness. We calculated three ingestive parameters across each 2 min biting test: total intake, total number of bites and bite size. We tested all caterpillars both before (open columns) and after (filled columns) exposure to the control or salicin diet. Each caterpillar was exposed either to the control or to the salicin diet over one of the four exposure periods. We made paired comparisons between the ingestive response of caterpillars to the salicin diet before and after an exposure period, separately for each ingestive measure and exposure diet, using the Wilcoxon matched-pairs signed-rank test (*P0.0125). The number of caterpillars tested at each exposure period ranged between 19 and 23 for those exposed to the control diet and between 18 and 27 for those exposed to the salicin diet. All values are median ± median absolute deviation.

View larger version (15K): [in a new window]   Fig. 5. Ingestive responses of individual caterpillars (N=10) to a range of salicin concentrations, both before and after exposure to the 157 mmol kg–1 salicin diet. We calculated three ingestive parameters across each 2 min biting test: total intake, total number of bites and bite size. Within each panel, we determine whether the ingestive responses of the caterpillars decreased significantly with increasing concentration of salicin, both before and then after the exposure period. To this end, we make paired comparisons between the response to the control diet (i.e. 0 mmol kg–1 salicin; open symbol) and that to each successively higher concentration of salicin (filled symbols) using the Wilcoxon matched-pairs signed-rank test (*P0.0125). All values are median ± median absolute deviation.

View larger version (32K): [in a new window]   Fig. 6. Responsiveness of the bitter-sensitive taste cell in epipharyngeal and lateral sensilla to 50 mmol l–1 salicin, both before (i.e. 0 h) and after (i.e. 24 or 48 h) exposure to the control or 157 mmol kg–1 salicin diet. To determine whether the responsiveness of each class of bitter-sensitive taste cell changed significantly over the exposure period, we calculated the percentage of initial response [i.e. (number of spikes s–1 after exposure period/number of spikes s–1 before exposure period)x100]. These calculations were based on the initial 1 s of the response (median responses ± median absolute deviation). The number of caterpillars tested in each treatment group was as follows: exposed to control diet for 24 h (N=10) or 48 h (N=9); exposed to salicin diet for 24 h (N=10) or 48 h (N=9). For each caterpillar, we recorded from the same lateral and epipharyngeal sensillum both before and after the exposure period. We compared the medians within each panel with an expected null model of 100 % (broken line) using a one-sample Wilcoxon matched-pairs signed-rank test (*P<0.05). We also present representative neural responses of an epipharyngeal (E,F) and lateral (G,H) sensillum to 50 mmol l–1 salicin (in 0.1 mol l–1 KCl) both before and after 24 h of exposure to the control or salicin diet. In all traces, a single bitter-sensitive taste cell is firing at a consistent and relatively rapid rate, whereas a salt-sensitive taste cell is firing more slowly and irregularly (in response to the electrolyte); action potentials from the latter taste cell are marked with an arrowhead. Each trace displays the initial 250 ms of the neural response.

View larger version (21K): [in a new window]   Fig. 7. Recovery from adaptation to salicin. At the beginning of the experiment (i.e. time 0 h), we measured the caterpillars’ ingestive response (during the 2 min biting test) to the salicin (157 mmol kg–1) diet. We calculated three ingestive parameters over the 2 min biting test: total intake, total number of bites and bite size. If the caterpillars exhibited an aversive response, we placed them on the salicin diet for 48 h. After this exposure period (i.e. at 48 h), we measured their ingestive response to the salicin diet a second time. If they had adapted to this diet (i.e. did not exhibit an aversive response), we offered them either the salicin diet (A–C) or the control diet (D–F) for an additional 24 h. We called this latter exposure period the ‘recovery phase’. Finally, we measured the caterpillars’ ingestive response to the salicin diet for a third time (i.e. at 72 h). To determine whether the caterpillars’ aversive response to salicin changed during the recovery phase, we made paired comparisons between the ingestive responses at 48 and 72 h using the Wilcoxon matched-pairs signed-rank test (*P0.05).