Sex-specific effects of protein and carbohydrate intake on reproduction but not lifespan inDrosophila 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.

Effects of macronutrient intake on the lifespan and fecundity of the marula fruit fly, Ceratitis cosyra (Tephritidae): Extreme lifespan in a host specialist

“…Thus, C. cosyra females opted for a protein and carbohydrate intake promoting strong egg production per day, rather than across their entire lives. The effects of protein and carbohydrate intake on lifespan in our study species were similar to those observed in other studies applying the GF to Tephritidae (Fanson & Taylor, 2012; Fanson et al., 2009), Diptera (Jensen et al., 2015; Lee et al., 2008), and other herbivorous insect orders (Harrison, Raubenheimer, Simpson, Godin, & Bertram, 2014; Maklakov et al., 2008). As in these other studies, we found that lifespan was optimized when flies consumed high quantities of a carbohydrate‐biased diet.…”

“…(2015). Sucrose was used as a source of carbohydrate (C), and a blend of 18 free amino acids (Table S2) was used as a source of protein (P).…”

“…To assess the regulation of nutrient intake in male and female C. cosyra , consumption of carbohydrate and protein was recorded when flies were allowed dietary choice using established methods (Jensen et al., 2015; Maklakov et al., 2008). Flies were maintained as in the no‐choice experiment, the only difference being that instead of one diet, they were given a pair of diets.…”

“…Expression of life‐history traits such as growth (Dussutour, Latty, Beekman, & Simpson, 2010), reproduction, and survival (Jensen, Mcclure, Priest, & Hunt, 2015) all depend on nutrition. The relationship between the ratio of nutrients consumed and life‐history traits can be modeled using the “Geometric Framework” (GF; Simpson & Raubenheimer, 2012).…”

“…For example, female Drosophila melanogaster needs to consume high P:C ratio diets to maximize fertility, but high protein intake reduces female survival (Jensen et al., 2015). In this situation, females cannot maximize fertility and lifespan at the same intake of nutrients, and so they face a trade‐off between these important life‐history traits.…”