Fertility/longevity trade-offs under limiting-male conditions in mating populations of Caenorhabditis elegans

Abstract

Evolutionary theories of aging suggest that trade-offs between longevity and fitness should be found under certain conditions. In C. elegans, there is little evidence for the existence of such trade-offs. We asked if fertility/longevity trade-offs exist in populations of randomly mating males and hermaphrodites. We set up a large population of young males and 5-day-old hermaphrodites that were no longer self-fertile. We then allowed them to mate for one day with an equal number young males and then separated hermaphrodites to individual plates and determined daily fertility of individual hermaphrodites. There was a significant negative relationship between late-life fertility and individual longevity.

Fig. 1. Lifespans and daily progeny production of mated and unmated wild-type hermaphrodites (N2CGCb)

Individual hermaphrodites were separated at the fourth larval stage. About half were never mated with males, while the other half were mated with five males on the first day of adulthood, which we called day 0. (A–C) Graphs of individual experiments. Daily progeny production of each individual hermaphrodite is shown on a different horizontal line, using different colors to depict progeny production on each day. Mated animals live significantly shorter lives (P < 0.0001) and produce significantly more progeny (P < 0.0001) than unmated. (D) Scatterplots and linear fit of the data from Figures 1A–C, with lifespan (x axis) plotted against progeny production (y axis). Regression coefficient between lifespan and progeny production of each group are as follows: (A) Experiment 1, unmated: beta = −0.82, p = 0.62; mated: beta = 35.98, p = 0.01; both: beta = −38.36, p = 0. (B) Experiment 2, unmated: beta = 2.43, p = 0.22; mated: beta = 7.74, p = 0.42; both: beta = −28.19, p = 0. (C) Experiment 3, unmated: beta =1.71, p = 0.17; mated: beta = 15.18, p = 0.2; both: beta = −18.05, p = 0. All unmated (beta = 1.28, p = 0.13), all mated (beta = 39.05, p = 0), both (beta = −25.99, p = 0).

Fig. 2. Total number of progeny, mated or unmated, as a function of adult age

The mating scheme was five males to one hermaphrodite, mating starts at the first day of adulthood. (A) Summary of total fertility, all experiments with N2CGCb hermaphrodites. (B-D) Number of progeny per day for N2CGCb, age-1(hx546) and daf-2(e137). P values are shown.

Fig. 3. Relationship between cross-progeny production and lifespan

In a mass mating (89 males and 89 hermaphrodites, N2CGCb), animals were allowed to mate for 24 hours (large NGM, OP50). (A) Horizontal bar graph of lifespans (x axis) of individual worms (y axis). Different colors indicate number of progeny produced per day for each individual. (B) Scatterplot of individual animal lifespans (x axis) and progeny production (y axis). There is a negative correlation between progeny production and lifespan (p < 0.0001).

Fig. 4. Lifespan and progeny production of mated and unmated individual hermaphrodites

(Mating as in Figure 2). Horizontal bar graph of lifespans (x axis) of individual worms (y axis). Different colors indicate number of progeny produced per day for each individual. (A) age-1(hx546). (B) daf-2(e137). In both, animals that are mated live significantly shorter lives (P < 0.0001) and produce significantly more progeny (P < 0.0001).