Variation in actuarial senescence does not reflect life span variation across mammals

• Published in: PLoS biology 2019-09, Vol.17 (9), p.e3000432-e3000432
• Main Authors: Péron, Guillaume, Lemaître, Jean-François, Ronget, Victor, Tidière, Morgane, Gaillard, Jean-Michel
• Format: Article
• Language: English
• Subjects: Actuarial Analysis; Age; Aging; Analysis; Animals; Biodiversity; Biology and Life Sciences; Biometry; Body mass; Captivity; Computation; Computer and Information Sciences; Developmental stages; Ecology; Elasticity; Female; Growth; Life Sciences; Life span; Life spans (Biology); Longevity; Mammals; Mammals - physiology; Medicine and Health Sciences; Mortality; Mortality patterns; Parameter sensitivity; Physical Sciences; Physiological aspects; Population growth; Populations and Evolution; Senescence; Short Reports; Species; Theory; Variance; Variation
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3000432

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.