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

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.

Female reproductive senescence across mammals: A high diversity of patterns modulated by life history and mating traits

“…Despite these reports of contrasted patterns of age-specific decline in reproductive performance with increasing age, there has been so far no attempt to quantify the occurrence and the variation in reproductive senescence across a wide range of species, or to identify the ecological and biological factors underlying the diversity of patterns. This contrasts with the increasing number of comparative analyses that focused on actuarial senescence (Bronikowski et al, 2011;Lemaître et al, 2020c;Péron et al, 2019b;Ricklefs, 1998Ricklefs, , 2006Ricklefs and Scheuerlein, 2001), which have notably revealed that life-history strategies (e.g. Garratt et al, 2013;Ricklefs, 2010) and environmental conditions (Colchero et al, 2019;Tidière et al, 2016) modulate both the onset and the rate of actuarial senescence.…”

Sex differences in adult lifespan and aging rates of mortality across wild mammals

“…this variation (20). Therefore, while the above-mentioned evolutionary hypotheses (i.e., heterogametic sex and mother's curse) could influence the evolution of sex differences in lifespan, they are not necessarily associated with the evolution of sex differences in the rate of aging.…”

The hidden ageing costs of sperm competition

“…Soulsbury, 2010 in mammals) would provide complementary insights on the role played by sperm competition in shaping lifespan and actuarial senescence patterns in males. In addition, analyses performed at the population level will enable tests of whether these long‐term survival costs are a consequence of an earlier age at the onset of ageing, an increased rate of ageing or both (Péron et al ., 2019).…”

“…Although the exact physiological pathways linking sexual selection to the degradation of the ‘organismal somatic state’ are likely to be complex and probably involve a complex role of androgens (Brooks and Garratt, 2017; Metcalf et al ., 2020), several empirical studies have evidenced an ageing cost of male allocation to sexual competition (see Table 1). Most of these studies have expressed this survival cost in terms of lifespan reduction, which may not directly translate into an ageing cost in the strict sense (Péron et al ., 2019). However, a few studies have also considered possible consequences in terms of ageing per se .…”