Late-life mortality-rate plateaus
Mortality rates have been shown to decelerate and ‘plateau’ late in life in a number of organisms, including Drosophila, medflies, waSPS, yeast, nematodes and humans (Greenwood & Irwin, 1939; Comfort, 1964; Carey et al., 1992; Curtsinger et al., 1992; Fukui et al., 1993; Brooks et al., 1994; Curtsinger et al., 1995; Charlesworth & Partridge, 1997; Vaupel et al., 1998; Drapeau et al., 2000; Rose et al., 2002; Miyo & Charlesworth, 2004). When mortality-rate plateaus were first definitively demonstrated (Carey et al., 1992; Curtsinger et al., 1992), they challenged theories of aging that predicted an exponential increase in age-specific mortality rates (Finch, 1990). The plateauing of cohort mortality rates late in life suggested that, in an infinite population, some organisms could theoretically live forever. Although there is currently no widely accepted explanation for mortality-rate plateaus, many theories have been proposed (Abrams & Ludwig, 1995; Mueller & Rose, 1996; Charlesworth & Partridge, 1997; Pletcher & Curtsinger, 1998; Wachter, 1999; Demetrius, 2001; Gavrilov & Gavrilova, 2001; Weitz & Fraser, 2001). Among these theories, two types have received the most attention: evolutionary and demographic.
The demographic theories of late-life mortality suggest that mortality rates plateau because of lifelong differences in individual robustness (Vaupel et al., 1979; Vaupel, 1988,1990; Pletcher & Curtsinger, 2000). This effect only results in mortality-rate plateaus when heterogeneity in robustness is extreme and sustained throughout life (Service, 2000a). However, heterogeneity this extreme and this consistent has yet to be found experimentally (Curtsinger et al., 1992; Fukui et al., 1996; Brooks et al., 1994; Vaupel et al., 1994; Khazaeli et al., 1998; Drapeau et al., 2000; but see Service, 2000b; Mueller et al., 2000).
One evolutionary theory of late-life mortality is based on the plateau, at or near zero, in the age-specific force of natural selection after the end of reproduction (Mueller & Rose, 1996; Rose & Mueller, 2000; Charlesworth, 2001; see Pletcher & Curtsinger, 1998 for caveats). This theory has been experimentally corroborated by the result that the onset of mortality-rate plateaus evolutionarily fluctuates with the age at which reproduction ends (Rose et al., 2002).
As with mortality, the force of natural selection acting on fecundity should decline with age until the last age of survival in the environment in which a population evolves (Hamilton, 1966). The force of natural selection acting on age-specific fecundity scales according to s’(x) = e−rxlx, where x is the age of a genetic effect on fecundity, r is the Malthusian parameter for the population and lx is survivorship to age x (Fig. 1). After the last age at which individuals survive in the population's evolutionary history (say d, which is not necessarily the last age of cohort survival under protected conditions) s′(x) converges on and remains at zero thereafter.
According to this evolutionary theory, fecundity should mimic the age-specific force of natural selection. That is, fecundity should decline in mid-life and plateau at very late ages, in a fashion analogous to mortality rates, after the last age of survival. We have already experimentally demonstrated that population fecundity indeed plateaus at late ages in three large cohorts of Drosophila melanogaster (Rauser et al., 2003) and that the occurrence of late-life fecundity plateaus is not affected by nutrition or mate age (Rauser et al., 2005).
This evolutionary theory not only implies that population fecundity should plateau at late ages, but that these plateaus should evolve according to the last age of survival in the population's evolutionary history. In this study, we test this prediction by comparing the onset of population fecundity plateaus in populations that have long had different last ages of survival. If fecundity plateaus in late life and evolves according to the evolutionary theory, then our results will support the evolutionary theory.
Late-life offspring viability
Offspring viability generally declines with parental age in Drosophila (Price & Hansen, 1998; Hercus & Hoffmann, 2000), except in later reproducing lines (Kern et al., 2001). Thus, it may be important to include reproductive factors, such as viability, in the evolutionary theory of aging because it is conceivable that the same genetic mechanisms that affect age-specific mortality and fecundity rates could similarly affect offspring viability.
In this study, we determined egg-to-adult viability for offspring from mid-and late-life parental ages in early and late-reproducing populations. Our objective was to test the effects of parental age on the evolution of offspring viability, and to determine whether eggs laid in late life are viable and how that viability compares to eggs laid in mid life.
Antagonistic pleiotropy and fecundity
Antagonistic pleiotropy occurs when genes that are beneficial early in life are deleterious later in life (Williams, 1957; Rose, 1985; Charlesworth, 1994). Late-acting deleterious genes that cause reproductive senescence late in life can persist in a population because these same genes enhance reproduction, or other fitness characters, at earlier ages when the force of natural selection is much stronger.
Because the start of late-life fecundity plateaus depends on the timing in the drop in the force of natural selection, we predict that switching to a selection regime with an earlier last age of reproduction should lead to an earlier age for the onset of fecundity plateaus if antagonistic pleiotropy is a genetic mechanism underlying late-life fecundity patterns. In this study we subject late-reproducing populations to an evolutionary reversion to earlier ages of reproduction (cf. Rose et al., 2002, 2004) and statistically test whether these newly derived early reproducing populations have an earlier plateau onset compared to the late-reproducing populations from which they were derived. Antagonistic pleiotropy is distinguished from mutation accumulation and genetic drift in this experiment by selecting for an earlier age of reproduction for only 24 generations, which is too little evolutionary time for mutation accumulation or drift to have a significant effect at the population sizes we employ.
In this paper, we experimentally test the predictions of the evolutionary theory for late life based on the declining force of natural selection, using D. melanogaster populations having different last ages of survival. We predict that all of these populations should show plateauing in late-life population fecundity, and have corresponding differences in the age at which fecundity stops declining and plateaus. Viability of eggs laid in mid- and late-life is also analysed. Lastly, we test a population genetic mechanism that may shape the evolution of late-life fecundity: antagonistic pleiotropy.