Protein:carbohydrate ratios explain life span patterns found in Queensland fruit fly on diets varying in yeast:sugar ratios

Abstract

Dietary restriction extends life span across a vast diversity of taxa, but significant challenges remain in elucidating the underlying mechanisms. Distinguishing between caloric and nutrient effects is an essential step. Recent studies with Drosophila and tephritid fruit flies have reported increased life span as dietary yeastto-sugar ratios decreased and these effects have been attributed to changes in protein-to-carbohydrate (P:C) ratios of the diets rather than calories. However, yeast is a complex mix of macronutrients and micronutrients, and hence changes in yeast content of the diet necessarily alters other nutrients in lockstep. To explicitly test whether studies using yeast are justified in attributing results to diet protein content rather than correlated nutrients, we developed a chemically defined diet allowing manipulation of just the ratio of protein (free amino acids) to carbohydrate (sucrose) levels of diets while holding other nutrients constant. Mated, female Queensland fruit flies (Q-flies) were fed 1 of 18 diets varying in P:C ratios and diet concentration. Diet consumption, egg production, and life span were recorded for each fly. In close concordance with recent studies using yeast diets, flies had increased life span as P:C ratios decreased, and caloric restriction did not extend life span. Similarly, egg production was maximized on high P:C ratios, but lifetime egg production was maximized on intermediate P:C ratios, indicating a life history trade-off between life span and egg production rate. Finally, Q-flies adjusted their diet intake in response to P:C ratios and diet concentration. Our results substantiate recent claims that P:C ratios significantly modulate life span in flies.

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.…”

“…However, compared with other species, optima for LEP and DEP were less protein biased in C. cosyra . For example, LEP and DEP were optimized at a 1:4 and 1:1 P:C ratio in B. tryoni (Fanson & Taylor, 2012), and 1:4 (or 1:2 in Jensen et al., 2015) and 1:2 in D. melanogaster (Jensen et al., 2015; Lee et al., 2008). In addition, even when optimized, DEP in C. cosyra was far lower than in the generalist species B. tryoni , while LEP was similar between unmated females of the two species (Fanson et al., 2009).…”

“…Due to their economic impact on fruit trade, the link between nutrition, reproduction, and lifespan has been relatively well studied in generalist tephritids using dietary manipulations, where hydrolyzed yeast was used as a source of protein (Carey et al., 2008; Fanson, Weldon, Perez‐Staples, Simpson, & Taylor, 2009; Harwood et al., 2013; Liedo, Carey, Ingram, & Zou, 2012; Oviedo et al., 2011). However, as hydrolyzed yeast is a mixture of macro‐ and micronutrients, it is preferable to use protein only (a mixture of amino acids) to ensure that the observed effect can be attributed to the macronutrient and not to the quality of the industrial yeast (Fanson & Taylor, 2012; Piper & Partridge, 2007). To date, the GF has been used to specifically relate macronutrient intake and the lifespan–reproduction trade‐off in only one tephritid fly Bactrocera tryoni , which is a generalist species (Fanson & Taylor, 2012).…”

“…However, as hydrolyzed yeast is a mixture of macro‐ and micronutrients, it is preferable to use protein only (a mixture of amino acids) to ensure that the observed effect can be attributed to the macronutrient and not to the quality of the industrial yeast (Fanson & Taylor, 2012; Piper & Partridge, 2007). To date, the GF has been used to specifically relate macronutrient intake and the lifespan–reproduction trade‐off in only one tephritid fly Bactrocera tryoni , which is a generalist species (Fanson & Taylor, 2012). …”

The nature of nutrition: a unifying framework

“…The results were very similar to those for Drosophila: dietary protein to carbohydrate ratio and not energy intake was strongly associated with lifespan. A subsequent experiment using a chemically defined mixture of amino acids instead of yeast confirmed that protein rather than some other correlated component in yeast was responsible for the life-shortening effect of a high-yeast, low-sugar diet (Fanson and Taylor 2011). Others reached similar conclusions regarding the importance of the protein to carbohydrate ratio in the diet for longevity in flies (e.g.…”