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Altered dietary nutrient intake maintains metabolic homeostasis in parasitized larvae of the insect Manduca sexta L.

S. N. Thompson^*, R. A. Redak and L.-W. Wang

Analytical Chemistry Instrumentation Facility and Department of Entomology, University of California, Riverside, California 92521, USA

View larger version (15K): [in a new window]   Fig. 1. Effects of parasitism by Cotesia congregata on diet consumption and growth of the host Manduca sexta given a dietary choice. Nutrient consumption is shown as a bivariate plot of protein and carbohydrate consumption. Values are means ± least-squares S.E.M.; horizontal bars refer to protein diet and vertical bars to carbohydrate diet. Values followed by different letters are statistically different for protein diet or carbohydrate diet, indicated by the directional error bar. Triangles and lower case letters refer to Experiment 1, where larvae were fed for 2 days. Circles and upper case letters refer to Experiment 2, where larvae were fed for 3 days. Growth for the two experiments is shown in the accompanying bar graph. Newly moulted normal (filled bars) and parasitized (open bars) fifth-instar larvae were given a choice of two synthetic artificial diets, one containing sucrose without casein, and the other, casein without sucrose, both nutrients at 120 g l–1. All values are g wet mass. Data were analyzed by ANCOVA with initial mass as the covariate. For a statistical summary, see Table 1.

View larger version (22K): [in a new window]   Fig. 2. Effects of dietary conditioning (A) and parasitism (B) by Cotesia congregata on diet consumption and growth of the host Manduca sexta, when given a dietary choice. Nutrient consumption is shown as a bivariate plot of protein diet and carbohydrate diet consumption. Values are indicated by mean ± least-squares S.E.M.; horizontal bars refer to protein diet and vertical bars to carbohydrate diet. Values followed by different letters are statistically different for the protein diet or carbohydrate diet, indicated by the directional error bar. Triangles and lower case letters, and circles and upper case letters, refer to the duplicate Experiments (Exp.) 1 and 2, respectively. Newly moulted normal and parasitized fifth-instar larvae were conditioned for 1 day on a synthetic artificial diet containing sucrose without casein, or casein without sucrose (both nutrients at 120 g l–1), and subsequently given a choice of the two diets for an additional 2 days. The effects of conditioning and parasitism on growth are shown in the insets. All values are g wet mass. Data were analyzed by two-way ANCOVA with initial mass as the covariate. No significant interaction between conditioning and parasitism was evident. For a statistical summary, see Table 2.

View larger version (25K): [in a new window]   Fig. 3. Size-mediated effects of dietary conditioning and parasitism by Cotesia congregata on consumption of a protein diet and a carbohydrate diet by the host Manduca sexta given a dietary choice. Results for individual larvae are shown with regression lines depicting the relationships between size and consumption for each treatment level. (A) Effects of conditioning on carbohydrate consumption. For larvae conditioned on the protein diet (triangles), consumption=0.2091xfinal mass; for larvae conditioned on the carbohydrate diet (circles), consumption=0.6820xfinal mass. (B) Effects of conditioning on protein consumption. For larvae conditioned on the protein diet (triangles), consumption=1.3072xfinal mass; for larvae conditioned on the carbohydrate diet (circles), consumption=0.9861xfinal mass. (C) Effects of parasitism on carbohydrate consumption. For parasitized animals (triangles), consumption=0.2091xfinal mass; for normal animals (circles), consumption=0.9405xfinal mass. (D) Effects of parasitism on protein consumption. For parasitized animals (triangles), consumption=1.3072xfinal mass; for normal animals (circles), consumption=2.3149 (final mass). The results of the ANCOVAs are shown in Table 3.

View larger version (22K): [in a new window]   Fig. 4. Short-term dietary selection by the host Manduca sexta. Newly moulted fifth-instar larvae were conditioned for 1 day on a synthetic artificial diet containing sucrose without casein, or casein without sucrose (both nutrients at 120 g l–1), and subsequently given a choice of the two diets. (A,B) The percentage of normal larvae (A) and parasitized larvae (B) choosing the protein (squares) and carbohydrate (triangles) diets following conditioning on the protein diet. (C,D) The percentage of normal (C) and parasitized (D) larvae choosing the protein and carbohydrate diets following conditioning on the carbohydrate diet. Each graph shows the distribution of 20 larvae.

View larger version (19K): [in a new window]   Fig. 5. Effect of dietary protein/carbohydrate ratio on the numbers and mass of Cotesia congregata developing in the host Manduca sexta. (A) Effect of dietary nutrient ratio on total parasite number. Values are means ± S.E.M. Values followed by different letters are statistically different at =0.05 as determined by the Nemenyi multiple-range test. (B) Effect of dietary nutrient ratio on total (squares) and individual (triangles) parasite biomass. Values are means ± S.E.M. Values followed by different letters are statistically different at =0.05 from those in the same data set, as determined by the Ryan–Einot–Gabriel–Welsch multiple-range test. All diets were isocaloric and contained an equivalent total amount of casein and sucrose.

View larger version (61K): [in a new window]   Fig. 6. The relationship between dietary protein and carbohydrate consumption and the numbers of Cotesia congregata developing in the host Manduca sexta. (A) Three-dimensional representation. (B) Topographical representation of A. The diagonal line shows the predicted relationship for the 1:1 diet containing an equivalent amount of casein and sucrose, based on actual experimental values as shown.

View larger version (17K): [in a new window]   Fig. 7. Typical 13C NMR spectrum of perchloric acid extracts of haemolymph from fifth-instar M. sexta larvae given a dietary choice for 48 h and administered [2-13C]pyruvate. (A) Spectrum in the region –5.0 p.p.m. to 210 p.p.m. showing enrichments for alanine, trehalose and C5 of glutamate and glutamine. (B) Partial spectrum in the region 14–96 p.p.m. showing 13C-enrichments for C2 and C3 of alanine and Glx. (C) Partial spectrum in the region 59–96 p.p.m. showing the selective 13C-enrichment in trehalose, as well as other metabolites, including glycerol and glycerol phosphate with the same or similar chemical shifts. Haemolymph was collected 3.5 h post-injection. The spectrum was generated from 4000 data acquisitions and is shown with 3 Hz line broadening. See text for explanation of the metabolic derivation of 13C-enrichments.

View larger version (19K): [in a new window]   Fig. 8. Metabolism of [2-13C]pyruvate by fifth-instar M. sexta larvae, illustrating the derivation of 13C-enrichment in glycolytic and gluconeogenic intermediates, and in haemolymph trehalose. Principal metabolic derivations are shown with different symbols. Circles, 13C enrichments derived directly following carboxylation of the original 13C in [2-13C]pyruvate, as administered to larvae; *13C-enrichments derived from [2-13C]pyruvate, but following carboxylation and randomization at the fumarase-catalyzed step of the TCA cycle; 13C-enrichments also derived from [2-13C]pyruvate following decarboxylation to acetyl-coenzyme A, condensation with oxaloacetate and subsequent synthesis of Glx. The metabolic effects of pentose cycling are not shown.