Reproduction regulates Drosophila nutrient intake through independent effects of egg production and sex peptide: Implications for aging

Abstract

BACKGROUND: The ratio of protein to carbohydrate (P:C) consumed influences reproduction and lifespan, outcomes that are often maximized by different P:C intake. OBJECTIVE: Determine if reproduction in female Drosophila drives elevated P:C intake. Distinguish whether such a preference is driven by egg production or from male-derived sex peptides in seminal fluid. METHODS: Intake of protein and carbohydrate was measured in a diet-choice assay. Macronutrient intake was calculated for mated and unmated fertile females, mated and unmated sterile females, and both types of female when mated to wildtype males and to males lacking sex peptide. RESULTS: Mated females have high P:C intake relative to unmated females and mated, sterile females. Fertile females mated to wildtype males and to males lacking sex peptide have high P:C intake, but sterile females have similar, low P:C intake when unmated and when mated to males lacking sex peptide. CONCLUSIONS: The metabolic demands of egg production and sex peptides are individually sufficient to drive elevated P:C intake in adult female Drosophila. Reproductive state can thus modulate how animals consume macronutrients, which in turn can impact their health and aging.

Keywords: Drosophila; Nutrients; aging; reproduction; sex peptide.

Fig.1

Wildtype (fertile) and sterile (OvoD, Bam) females. Mean cumulative protein and carbohydrate intake consumed by females with daily point estimate standard deviation, plotted across two weeks in CAFE assay. Cumulative intake trajectories with 2-day census intervals, and best-fit linear (solid line) or quadratic (dash line) functions. P:C ratios at legend were estimated from linear regression.

Fig.2

Wildtype fertile females (A) and sterile OvoD females (B) when unmated (virgin), once-mated (at eclosion), or twice mated (at eclosion and remated at day 7). Cumulative intake trajectories with daily point estimate standard deviation, using daily census intervals, and best fit linear (solid line) or quadratic (dash line) functions, with P:C ratios (at legend) estimated from linear regression.

Fig.3

Wildtype fertile females (A), sterile OvoD females (B), sterile Bam females when unmated (virgin), or once-mated (at eclosion) to wildtype males (control) or to males lacking sex peptide SP⁰ (mutant) (C). Cumulative intake trajectories with daily point estimate standard deviation, using 2-day census intervals, and best-fit linear function, with P:C ratios (at legend) estimated from linear regression.

Fig.4

Box-whisker plots for eggs laid in CAFE vials by wildtype females once mated to wildtype males (control) or to males lacking sex peptide (sex peptide mutant), or when unmated (virgin). Points represent total number of deposited eggs in the first three days of the CAFE trial. Means among the mated females did not significantly differ, while means of both mated female groups differed from that of unmated females (Dunnett’s multiple comparison with α= 0.05).