Sex-specific effects of protein and carbohydrate intake on reproduction but not lifespan in Drosophila melanogaster

Abstract

Modest dietary restriction extends lifespan (LS) in a diverse range of taxa and typically has a larger effect in females than males. Traditionally, this has been attributed to a stronger trade-off between LS and reproduction in females than in males that is mediated by the intake of calories. Recent studies, however, suggest that it is the intake of specific nutrients that extends LS and mediates this trade-off. Here, we used the geometric framework (GF) to examine the sex-specific effects of protein (P) and carbohydrate (C) intake on LS and reproduction in Drosophila melanogaster. We found that LS was maximized at a high intake of C and a low intake of P in both sexes, whereas nutrient intake had divergent effects on reproduction. Male offspring production rate and LS were maximized at the same intake of nutrients, whereas female egg production rate was maximized at a high intake of diets with a P:C ratio of 1:2. This resulted in larger differences in nutrient-dependent optima for LS and reproduction in females than in males, as well as an optimal intake of nutrients for lifetime reproduction that differed between the sexes. Under dietary choice, the sexes followed similar feeding trajectories regulated around a P:C ratio of 1:4. Consequently, neither sex reached their nutritional optimum for lifetime reproduction, suggesting intralocus sexual conflict over nutrient optimization. Our study shows clear sex differences in the nutritional requirements of reproduction in D. melanogaster and joins the growing list of studies challenging the role of caloric restriction in extending LS.

Keywords: caloric restriction; fitness; geometric framework; lifespan; nutrient regulation; reproduction.

Fig 1

Nonparametric thin-plate spline contour visualizations of the responses surfaces describing the effects of protein and carbohydrate intake on (A) male lifespan (LS), (B) female LS, (C) male offspring production rate, (D) female egg production rate, (E) lifetime offspring production in males, and (F) lifetime egg production in females in Drosophila melanogaster. Individual flies were allowed to feed ad libitum from one of the 29 liquid foods across their adult LS. Open black circles represent the intake of protein and carbohydrates along each of the seven nutritional rails by individual flies. The regulated intake point (±SE) for flies given the choice between alternate diets (Experiment 2) is mapped on each landscape (in white), after being converted to a daily intake. On each landscape, the gray dashed line represents an ‘isocaloric line’ across the nutritional landscape where a given intake of nutrients yields equal calories. As protein and carbohydrates contain approximately the same amount of energy per unit ingested (∼4 calories per gram), the slope of the isocaloric line is −1.

Fig 2

Age-dependent reproduction in relation to protein and carbohydrate intake. Male offspring production (in competition with a 3-day-old Krüppel male with a visible eye mutation) in relation to age and the intake of protein (A) and carbohydrate (C). Female egg production in relation to age and the intake of protein (B) and carbohydrate (D).

Fig 3

Age-specific trajectories of egg production in females (A) and offspring production in males (B) for cohorts of flies with different lifespans (indicated as numbers next to the trajectory curves).

Fig 4

Cumulative intake of protein and carbohydrates (mean ± SE) by male (closed symbols) and female (open symbols) Drosophila melanogaster over the first 15 days of adulthood when given the choice between five different diet pairs: (A) diet pair 1: diet 7 vs. diet 27; (B) diet pair 2: diet 7 vs. diet 28; (C) diet pair 3: diet 8 vs. diet 27; (D) diet pair 4: diet 8 vs. diet 28; and (E) diet pair 5: diet 12 vs. diet 28 (see Table S1 for diet compositions). (F) The average cumulative intake of protein and carbohydrates across all diet pairs. The terminal feeding points in (F) represent the regulated intake point for each sex. The P:C ratio of the two diets in each diet pair are provided above the axes, and a black dashed line is provided for the diet that does not have a P:C ratio of 0:1 (which occurs on the y axis). The area between these two P:C ratios represents the region in nutrient space that flies are able to occupy through dietary choice. The red dashed line represents the cumulative intake of nutrients if flies consumed these nutrients in a P:C ratio of 1:4.