Having it all: historical energy intakes do not generate the anticipated trade-offs in fecundity

Abstract

An axiom of life-history theory, and fundamental to our understanding of ageing, is that animals must trade-off their allocation of resources since energy and nutrients are limited. Therefore, animals cannot "have it all"--combine high rates of fecundity with extended lifespans. The idea of life-history trade-offs was recently challenged by the discovery that ageing may be governed by a small subset of molecular processes independent of fitness. We tested the "trade-off" and "having it all" theories by examining the fecundities of C57BL/6J mice placed onto four different dietary treatments that generated caloric intakes from -21 to +8.6% of controls. We predicted body fat would be deposited in relation to caloric intake. Excessive body fat is known to cause co-morbidities that shorten lifespan, while caloric restriction enhances somatic protection and increases longevity. The trade-off model predicts that increased fat would be tolerated because reproductive gain offsets shortened longevity, while animals on a restricted intake would sacrifice reproduction for lifespan extension. The responses of body fat to treatments followed our expectations, however, there was a negative relationship between reproductive performance (fecundity, litter mass) and historical intake/body fat. Our dietary restricted animals had lower protein oxidative damage and appeared able to combine life-history traits in a manner contrary to traditional expectations by having increased fecundity with the potential to have extended lifespans.

Figure 1

Body mass of female C57BL/6J mice that received standard laboratory chow then after week zero either an ad libitum supply of control (10% kcal fat; n=35), medium fat (45% kcal fat; n=40) or high-fat diet (60% kcal fat, n=40) or a daily ration of 75% of ad libitum intake of control diet (n=37). Ten animals from each group (open symbols) were culled at week 16 and tissues were analysed for protein carbonyl content. Breeding animals were removed from treatment at week 11 so breeding would not be directly affected. Some animals were maintained on the original diet (open symbols). Error bars represent standard error of the means.

Figure 2

Body composition of female C57BL/6J mice was measured once during a 30 day period ca 10 days after pups from the pre-treatment test mating had been weaned (21 days after birth) and again when females were six months of age after nine weeks of treatment (restricted, n=37; control, n=35; medium fat, n=40; high fat, n=40). (a) LM and (b) fat mass were estimated by DXA then corrected using an equation developed specifically for our machine. Error bars represent standard error of the means and columns without a common letter are significantly different (p<0.05, ANOVA with post hoc t-tests).

Figure 3

Post-treatment body mass of females that gave birth to live pups and weaned litters 21 days after birth (restricted, n=27; control, n=18; medium fat, n=16; high fat, n=12). Error bars represent standard error of the means and columns without a common letter differ (p<0.05, ANOVA with post hoc t-tests).

Figure 4

The differences between litter mass from the pre-treatment and post-treatment matings at the time of (a) birth and (b) at weaning 21 days after birth (restricted, n=27; control, n=18; medium fat, n=16; high fat, n=12). Error bars represent standard error of the means and columns without a common letter differ (p<0.05, ANOVA with post hoc t-tests).

Figure 5

The differences between the number of pups per litter from the pre-treatment and post-treatment matings at the time of birth and weaning 21 days after birth (restricted, n=27; control, n=18; medium fat, n=16; high fat, n=12). Error bars represent standard error of the means and columns without a common letter differ (p<0.05, ANOVA with post hoc t-tests).

Figure 6

Protein carbonyl content of liver and gastrocnemius muscle of animals post-treatment (n=10 per treatment). Error bars represent standard error of the means and columns without a common letter differ by p<0.05 (ANOVA with post hoc t-tests).