Abstract
The concept of actuarial senescence (defined here as the increase in mortality hazards with age) is often confounded with life span duration, which obscures the relative role of age-dependent and age-independent processes in shaping the variation in life span. We use the opportunity afforded by the Species360 database, a collection of individual life span records in captivity, to analyze age-specific mortality patterns in relation to variation in life span. We report evidence of actuarial senescence across 96 mammal species. We identify the life stage (juvenile, prime-age, or senescent) that contributes the most to the observed variation in life span across species. Actuarial senescence only accounted for 35%–50% of the variance in life span across species, depending on the body mass category. We computed the sensitivity and elasticity of life span to five parameters that represent the three stages of the age-specific mortality curve—namely, the duration of the juvenile stage, the mean juvenile mortality, the prime-age (i.e., minimum) adult mortality, the age at the onset of actuarial senescence, and the rate of actuarial senescence. Next, we computed the between-species variance in these five parameters. Combining the two steps, we computed the relative contribution of each of the five parameters to the variance in life span across species. Variation in life span was increasingly driven by the intensity of actuarial senescence and decreasingly driven by prime-age adult mortality from small to large species because of changes in the elasticity of life span to these parameters, even if all the adult survival parameters consistently exhibited a canalization pattern of weaker variability among long-lived species than among short-lived ones. Our work unambiguously demonstrates that life span cannot be used to measure the strength of actuarial senescence, because a substantial and variable proportion of life span variation across mammals is not related to actuarial senescence metrics.
Highlights
The extreme range of variation in animal life span has puzzled biologists for a very long time [1,2,3,4,5]
Variability in the way mortality increased with age never accounted for more than half of the variance in life span across 96 mammal species, which sampled a large array of life history strategies from short-lived tree shrews to long-lived hippopotamuses
We demonstrate that using life span metrics, such as mean or maximum longevity, to quantify actuarial senescence is not reliable and should be discouraged
Summary
The extreme range of variation in animal life span has puzzled biologists for a very long time [1,2,3,4,5]. Decomposition of the variance in life span actuarial senescence (usually defined as the observed increase in mortality hazards with age) [11,12,13,14]. This practice implies that variation in life span is mostly caused by variation in the intensity of actuarial senescence across species. With the recent increase in long-term individual-based studies [15], we have empirical evidence that life span is not a good proxy for actuarial senescence across individuals in a range of species [16,17,18,19,20,21]. To the best of our knowledge, these hypotheses have never been tested empirically, and the relative contributions of the successive life stages to variation in life span across species have never been quantified
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