Heterogeneity's ruses: How hidden variation affects population trajectories of age-dependent fecundity in Drosophila melanogaster

Abstract

AbstractBACKGROUNDProgress in understanding senescence requires information about age-dependent changes in individual organisms. However, for experimental systems such as Drosophila melanogaster we usually do not know whether population trajectories are an accurate guide to patterns of individual aging, or are artifacts of population heterogeneity.OBJECTIVEIn experimental cohorts of D. melanogaster, population trajectories of age-specific fecundity typically plateau in old age. Here we ask whether fecundity plateaus can be explained by hidden heterogeneity in reproductive life spans (RLS).METHODSUsing published and original data from five experimental populations, we examined fecundity trajectories in subpopulations stratified by RLS, and in total populations with age expressed relative to RLS for each individual fly. We also executed computer simulations of reproductive senescence in which individuals vary in RLS, and show linear decline in fecundity with increasing age.RESULTSIn subgroups of flies with similar RLS, the senescent decline of fecundity is generally linear. Population trajectories in which age is expressed relative to individual RLS also exhibit linear or slightly accelerated decline. Simulations demonstrate that observed levels of variation in RLS are sufficient to produce plateaus in the mixture trajectories that are very much like those observed in experiments, even though fecundity declines linearly in individuals.CONCLUSIONSLate-life fecundity plateaus in D. melanogaster are artifacts of population heterogeneity in RLS. This conclusion applies to both inbred and outbred populations, and both wild and lab-adapted stocks. For reproductive senescence in this model system, population trajectories are not an accurate guide to individual senescence.1. IntroductionOne goal of biodemography is to understand the forces that shape trajectories of survival and reproduction in laboratory populations of experimental organisms. Here we examine original and published life history data from five populations of the fruit fly Drosophila melanogaster. Our objective is to determine whether population trajectories of age-specific fecundity, which plateau late in life, accurately reflect the pattern of reproductive senescence in individual flies, or whether plateaus are artifacts of population heterogeneity.Examples of population fecundity trajectories are shown in Figure 1. The reproductive chronology starts when females mate, store sperm, and begin laying eggs, one or two days after emergence from the puparium. Flies typically reach peak daily fecundity within the first two weeks of adult life, and then exhibit declining fecundity in old age. At some point in mid- to late-life, the decline moderates and population trajectories inflect upward, producing fecundity plateaus. The plateaus could reflect real biological change in individuals, or they could be an example of heterogeneity's ruses (Vaupel and Yashin 1985). The alternative explanations are analogous to discussions surrounding mortality plateaus, which are well documented in this species (Curtsinger et al. 1992; Vaupel et al. 1998, Khazaeli, Pletcher, and Curtsinger 1998; Wachter 1999; Drapeau et al. 2000; Service 2000; Curtsinger, Gavrilov, and Gavrilova 2006).1.1 The argument for late-life fecundity plateausBased on study of three genetically heterogeneous, lab-adapted populations of D. melanogaster, Rauser et al. (2003; 2005a, 2005b; 2006) argued that reproductive senescence is best understood as a two-stage process: rapid linear decline until a breakday age, followed by a fecundity plateau with low, relatively constant levels late in life. The evidence came primarily from fitting two-stage regression models to complete data on survival and reproduction of individual flies, and also from testing and rejecting a heterogeneity model that involved trade-offs between survival and reproduction (Rauser et al. …