Senescence is more important in the natural lives of long- than short-lived mammals

Abstract

Background: Senescence has been widely detected among mammals, but its importance to fitness in wild populations remains controversial. According to evolutionary theories, senescence occurs at an age when selection is relatively weak, which in mammals can be predicted by adult survival rates. However, a recent analysis of senescence rates found more age-dependent mortalities in natural populations of longer lived mammal species. This has important implications to ageing research and for understanding the ecological relevance of senescence, yet so far these have not been widely appreciated. We re-address this question by comparing the mean and maximum life span of 125 mammal species. Specifically, we test the hypothesis that senescence occurs at a younger age relative to the mean natural life span in longer lived species.

Methodology/principal findings: We show, using phylogenetically-informed generalised least squares models, a significant log-log relationship between mean life span, as calculated from estimates of adult survival for natural populations, and maximum recorded life span among mammals (R2=0.57, p<0.0001). This provides further support for a key prediction of evolutionary theories of ageing. The slope of this relationship (0.353+/-0.052 s.e.m.), however, indicated that mammals with higher survival rates have a mean life span representing a greater fraction of their potential maximum life span: the ratio of maximum to mean life span decreased significantly from >10 in short-lived to approximately 1.5 in long-lived mammal species.

Conclusions/significance: We interpret the ratio of maximum to mean life span to be an index of the likelihood an individual will experience senescence, which largely determines maximum life span. Our results suggest that senescence occurs at an earlier age relative to the mean life span, and therefore is experienced by more individuals and remains under selection pressure, in long- compared to short-lived mammals. A minimum rate of somatic degradation may ultimately limit the natural life span of mammals. Our results also indicate that senescence and modulating factors like oxidative stress are increasingly important to the fitness of longer lived mammals (and vice versa).

Figure 1. Mean and maximum life span of mammals.

(A) Maximum recorded life span of 125 mammal species (square: humans) plotted as a function of their mean natural life span, calculated from estimates of annual survival. The observed slope of this relationship (solid line; 0.353±0.052) computed from phylogenetically informed generalized least squares (PGLS) differs significantly (t = 12.43, P<0.0001) from an average constant ratio between these two variables (dashed line). The maximum likelihood estimate of Pagel's λ in PGLS was 0.82 indicating a strong phylogenetic signal in maximum longevity among mammals. The deviation between predicted (dashed line) and observed maximum life spans (data points) was confirmed by a significant Runs test (Standardized Runs Statistic = −2.5248; P = 0.011) applied to the differences of these measures ordered along their means. (B) The same data plotted again to illustrate the pronounced decrease in the ratio of maximum to mean life span with increasing mean life span. The regression line (solid line; log10 ratio = 0.966−0.646× log10 mean life span) was computed using PGLS. The dashed line shows the prediction assuming an average constant ratio (maximum = 7.2× mean life span). A negative correlation is statistically expected when plotting a ratio as a function of its denominator using random, independent pairs of data . For example, the dotted line shows the decrease in the ratio assuming a constant average maximum life span for all species (that is, if maximum life span was entirely independent of mean life span). This fact does not diminish the biological significance of relationships in empirical data , for which there is no mathematical or biological reason to exclude the alternative of no association (indeed this is the predicted relationship here).

Figure 2. Schematic of the age of senescence and maximum life span in short- versus long-lived species.

Schematic representation of survival curves for populations in the wild and in captivity or protected environments. For short-lived mammal species, senescence (shown as red shading) and therefore maximum life span occur at an age when most individuals in wild populations have succumbed to environmental mortalities; whereas, for long-lived species, senescence occurs at an earlier age relative to survival in the wild and hence at an age when selection pressure could remain high.

Figure 3. Schematic of mean life span in short- versus long-lived species.

Schematic representation of the mean life span of wild populations as a function of potential reproductive and maximum life span (as exhibited in captive or protected populations) for short- and long-lived species.