Abstract
Biological species have evolved characteristic patterns of age-specific mortality across their life spans. If these mortality profiles are shaped by natural selection they should reflect underlying variation in the fitness effect of mortality with age. Direct fitness models, however, do not accurately predict the mortality profiles of many species. For several species, including humans, mortality rates vary considerably before and after reproductive ages, during life-stages when no variation in direct fitness is possible. Variation in mortality rates at these ages may reflect indirect effects of natural selection acting through kin. To test this possibility we developed a new two-variable measure of inclusive fitness, which we term the extended genomic output or EGO. Using EGO, we estimate the inclusive fitness effect of mortality at different ages in a small hunter-gatherer population with a typical human mortality profile. EGO in this population predicts 90% of the variation in age-specific mortality. This result represents the first empirical measurement of inclusive fitness of a trait in any species. It shows that the pattern of human survival can largely be explained by variation in the inclusive fitness cost of mortality at different ages. More generally, our approach can be used to estimate the inclusive fitness of any trait or genotype from population data on birth dates and relatedness.
Highlights
Patterns of mortality vary greatly among biological species [1]
The general trend of increasing mortality is reversed and mortality rate either declines during some life stages or continuously throughout life. This variation presents a challenge for evolutionary theories of aging [3,4,5]. These theories were developed to explain the apparent paradox of aging—how natural selection, acting to maximize direct fitness, can cause mortality rates to increase across the life span
The mortality profile observed in both Agta and UN populations is characterised by relatively high mortality rates in infancy, which rapidly decline to a minimum at adolescence and remain low until the age of sexual maturity, after which mortality rises gradually with age (Fig. 1a)
Summary
Patterns of mortality vary greatly among biological species [1]. In many species there is a general increase in the rate of mortality with age [1]. The general trend of increasing mortality is reversed and mortality rate either declines during some life stages (e.g., the alpine swift Apus melba [1]) or continuously throughout life (e.g., the desert tortoise Gohoerus agissizii and the white mangrove Avicennia marina [1, 2]) This variation presents a challenge for evolutionary theories of aging [3,4,5]. These theories were developed to explain the apparent paradox of aging—how natural selection, acting to maximize direct fitness, can cause mortality rates to increase across the life span. They are based on Fisher’s initial proposal that the Malthusian parameter (m), estimated by the Euler-Lotka equation (ELe) [6, 7], is a measure of the average individual fitness in a PLOS ONE | DOI:10.1371/journal.pone.0117019 January 21, 2015
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