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

Abstract

Although 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.

Figure 1

Event history charts (Carey et al. 1998b) for A. ludens females showing relationship of cohort survival and individual-level reproduction across treatments. The ratios across the top denote the sugar:yeast ratios and the numbers aligned vertically at the right denote the percent concentration of the original stock solution (see Methods). Each horizontal line within a graph denotes a life line for an individual female, the length of which is proportional to her lifespan and with color-coded segments corresponding to age classes. The age-specific egg laying intensity for each individual female corresponds to the shading: green=zero eggs; yellow=1–20 eggs; red=>20 eggs.

Figure 2

Contour graphs showing the response surfaces for restriction level (concentration relative to ad libitum mother stock) and percent yeast in A. ludens— left, middle and right panels shows male life expectancy (days), female life expectancy, and female lifetime egg reproduction, respectively. Local linear fitting techniques (Facer & Müller 2003) were used to produce the numerical values of the response surfaces from the data and DeltaGraph® graphics program was used to generate the contour maps.

Figure 3

Age-specific (net) reproduction functions for the surface transect that connects the coordinates corresponding to the longevity (blue dot) and reproduction (red dot) maxima with three equidistant highlighted locations on the transect line in the female longevity contour graph shown in the inset (from Figure 2b). Colors for each transect location correspond to those for the reproductive schedules. Lifetime egg production for the respective schedules are 295, 463, 663, 872, and 1,086 eggs/female, respectively, and the mean age of reproduction are 37.4, 34.0, 32.4, 31.6 and 29.9 days, respectively.