Effects of high-fat diet on feeding and performance in the tobacco hornworm, Manduca sexta

Abstract

Nutritionally balanced diets are important for overall fitness. For insects, fat is vital for development due to its high-energy value. Little is known about how insects regulate dietary fat for storage, but research has shown conflicting results on how altering fat impacts development and performance. In this study, we sought to investigate how high-fat diets affect developing insects. To determine how insects respond to variation in dietary fat content, we reared Manduca sexta of different larval stages on diets containing varying concentrations of linseed oil in high (5.6%), medium (3.4%) or low (0.4%) fat. Young larvae reared on high-fat diets had 80% mortality and 43% lower body mass compared to those reared on medium- or low-fat diets. Older larvae showed no difference in mortality with increasing dietary fat content, but they were smaller than controls, suggesting a developmental shift in lipid metabolism. We measured mRNA expression of Apolipoprotein I and II (APO1 and 2), proteins responsible for transporting lipids, as a possible explanation of increased survival in older larvae. Levels of APO1 and 2 mRNA did not differ with dietary fat content. We then tested the hypothesis that the high-fat diet altered feeding, resulting in the observed decrease in body size. Caterpillars fed a high-fat diet indeed ate less, as indicated by a decrease in food consumption and the number and mass of fecal pellets produced. These results suggest that increased fat disrupted feeding and may indicate that there is a threshold for lipid storage, but further studies are needed to understand the underlying mechanism.

Keywords: Anorexia; Development; Fat body; Growth; High-fat diet; Insect; Juvenile; Lipid content; Nutrition.

Fig. 1.

Body masses of caterpillars placed on HF (black triangles), MF (gray squares), or LF (open circles) diets in the first (A) and fourth instars (B). First instar caterpillars were tested on diets made with linseed oil (A). Caterpillars fed HF diets starting in the fourth (B) instar had better survival, but in all cases, HF diets resulted in lower body mass over time.

Fig. 2.

Body mass (A, B) and daily growth rates (C, D) of caterpillars fed HF (black triangles), MF (gray squares), or LF (open circles) diets from the first day of the fifth instar in experiment 1 (A, C) and 2 (B, D). Asterisk indicates a significant difference between growth rates of caterpillars on HF (gray, hatched box) and LF (open box) diets.

Fig. 3.

Absolute food consumption (A) and mass-specific food consumption (B) of fifth instar M. sexta reared on HF (black triangles), MF (gray squares), or LF (open circles) diets. Asterisk represents significant difference between HF and LF diet-fed caterpillars.

Fig. 4.

Mass-specific total protein consumption versus (A) mass-specific total carbohydrate consumption and (B) mass-specific total lipid consumption of fifth instar M. sexta reared on HF (black triangles), MF (gray squares), or LF (open circles) diets.

Fig. 5.

Mass-specific expression of Apolipoprotein I & II mRNA from fat bodies of M. sexta on the second, third, and fourth days of the fifth instar after feeding on either HF (black triangles), MF (gray squares), or LF (open circles) diets.

Fig. 6.

Effects of dietary fat content on wet and dry mass of fifth instar M. sexta fat body mass (A) and lipid content relative to fat body mass (B).

Fig. 7.

Lipid content of fecal pellets of fifth instar M. sexta fed HF (black triangles), MF (gray squares), and LF (open circles) diets (A), relative to the dry mass of fecal pellets (B), and relative to body mass (C).

Fig. 8.

Approximate digestibility of each diet by day of the fifth instar in M. sexta. Asterisks indicate a significant difference between HF (gray, hatches box) and LF (open box) diets.