Longevity–fertility trade‐offs in the tephritid fruit fly,Anastrepha ludens, across dietary‐restriction gradients

Abstract

SummaryAlthough it is widely known that dietary restriction (DR) not only extends the longevity of a wide range of species but also reduces their reproductive output, the interrelationship of DR, longevity extension and reproduction is not well understood in any organism. Here we address the question: 'Under what nutritional conditions do the longevity-enhancing effects resulting from food restriction either counteract, complement or reinforce the mortality costs of reproduction? To answer this question we designed a fine-grained DR study involving 4800 individuals of the tephritid fruit fly, Anastrepha ludens , in which we measured sex-specific survival and daily reproduction in females in each of 20 different treatments (sugar : yeast ratios) plus 4 starvation controls. The database generated from this 3-year study consisted of approximately 100 000 life-days for each sex and 750 000 eggs distributed over the reproductive lives of 2400 females. The fertility and longevity-extending responses were used to create contour maps (X-Y grid) that show the demographic responses (Z-axis) across dietary gradients that range from complete starvation to both ad libitum sugar-only and ad libitum standard diet (3 : 1 sugar : yeast). The topographic perspectives reveal demographic equivalencies along nutritional gradients, differences in the graded responses of males and females, egg production costs that are sensitive to the interaction of food amounts and constituents, and orthogonal contours (equivalencies in longevity or reproduction) representing demographic thresholds related to both caloric content and sugar : yeast ratios. In general, the finding that lifespan and reproductive maxima occur at much different nutritional coordinates poses a major challenge for the use of food restriction (or a mimetic) in humans to improve health and extend longevity in humans.

The nature of nutrition: a unifying framework

“…Others reached similar conclusions regarding the importance of the protein to carbohydrate ratio in the diet for longevity in flies (e.g. Carey et al 2008;Skorupa et al 2008;Ja et al 2009;Le Rohellec and Le Bourg 2009;Vigne and Frelin 2010), crickets (Maklakov et al 2008), ants (Dussutour and Simpson 2009;Cook et al 2010) and honey bees (Pirk et al 2010), and the same may well be true for mammals (Orentreich et al 1993;Zimmerman et al 2003;Miller et al 2005;Raubenheimer 2007, 2009). …”

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

“…In the wild, adult tephritids have been recorded acquiring their nutrients from different food sources: fruit juice, nectar, pollen, extrafloral glandular secretions, honeydew, bird feces, and bacteria (Drew, Courtice, & Teakle, 1983; Hendrichs, Lauzon, Cooley, & Prokopy, 1993; Manrakhan & Lux, 2006). 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).…”

The effect of resveratrol on lifespan depends on both gender and dietary nutrient composition in Drosophila melanogaster

“…However, recent reports in several insect species and mice have challenged the effectiveness of this intervention to increase lifespan. Several labs have conducted nutrition geometric studies, which have measured lifespan in several fly species, including Drosophila melanogaster, Queensland fruit fly (Bactrocera tryoni), and the Mexican fruit fly (Mexfly; Anastrepha ludens), under dietary conditions with various amount of sugar and protein (Carey et al 2008;Lee et al 2008;Skorupa et al 2008;Fanson et al 2009;Piper et al 2011). These studies suggest that dietary composition or the ratio of carbohydrate relative to protein is more important than calorie intake in modulating lifespan.…”