Patterns Of Actuarial Senescence Research Articles

Micro-geographic shift between negligible and actuarial senescence in a wild snake.

While it has long been known that species have contrasted life expectancy (pace of mortality) and generation time (pace of reproduction), recent studies have also uncovered that the shape of adult age trajectories of mortality and reproduction can vary remarkably among species along a continuum of senescence ranging from strong deterioration (senescence), insignificant deterioration (negligible senescence) to improvement with advancing age (negative senescence). As for many long-lived ectotherms with asymptotic growth and increasing reproductive output with age, snakes are good candidates for negligible senescence to occur. Yet, intraspecific variation in the pace and shape of actuarial and reproductive senescence across wild populations of these species remains to be explored. Here, we used 37years of mark-recapture data in two nearby habitats inside a meadow viper Vipera ursinii population to quantify life expectancies, generation times and the shape of actuarial and reproductive senescence. Female vipers maintained stable reproductive performances at old ages, even when accounting for the predicted increase of fertility with body size, providing evidence for negligible reproductive senescence in both habitats. Males had a higher adult mortality and a shorter life expectancy on average than females and actuarial senescence shifted from negligible senescence in the optimal habitat to strong senescence in the sub-optimal habitat. Overall, these results demonstrate that micro-geographic environmental variation can generate qualitative shifts in actuarial senescence patterns. This highlights that taking into account the within-species plasticity of age-dependent trajectories could prove useful in better understanding what determines the evolution of life-history age trajectories.

Population position along the fast-slow life-history continuum predicts intraspecific variation in actuarial senescence.

Patterns of actuarial senescence can be highly variable among species. Previous comparative analyses revealed that both age at the onset of senescence and rates of senescence are linked to position of a species along the fast-slow life-history continuum. As there are few long-term datasets of wild populations with known-age individuals, intraspecific (i.e. between-population) variation in senescence is understudied and limited to comparisons of wild and captive populations of the same species, mostly birds and mammals. In this paper, we examined how population position along the fast-slow life-history continuum affects intraspecific variation in senescence in an amphibian, Bombina variegata. We used capture-recapture data collected in four populations with contrasting life-history strategies. Senescence trajectories were analysed using Bayesian capture-recapture models. We show that in populationswith fast life histories the onset of actuarial senescence was earlier and individuals aged at a faster rate than individuals in populationswith slow life histories. Our study provides one of the few empirical examples of among-population variation in actuarial senescence patterns in the wild and confirms that the fast-slow life-history gradient is associated with both macroevolutionary and microevolutionary patterns of actuarial senescence.

Assessing ageing patterns for comparative analyses of mortality curves: Going beyond the use of maximum longevity

Abstract An increasing number of studies have investigated the diversity of actuarial senescence (i.e. the increase of mortality with age) and mortality patterns in the wild. Most of these studies used maximum longevity as a metric, and only some of them were based on the analysis of mortality or survival curves. However, maximum longevity is not a reliable metric to assess mortality patterns. Two types of metrics can be distinguished: the metrics of pace that include biological times and describe how long individuals live and the metrics of shape that are dimensionless and describe the form of mortality patterns for a given pace. We review the use of pace metrics in comparative analyses of mortality curves and actuarial senescence performed so far, with a special focus on longevity metrics. We demonstrate that multiple statistical issues are associated with the use of maximum longevity, although this metric is the most commonly used to analyse actuarial senescence patterns in research fields such as genomics of ageing. We thus argue for using alternative metrics of longevity. We then propose different metrics of shape and point out the relevance of using several metrics in future comparative analyses of mortality. In particular, two shape metrics can be easily computed from observed distributions of ages at death. We illustrate our approach based on both pace and shape metrics by performing a comparative analysis of actuarial senescence and mortality across 30 species of mammals. The results strongly support the relevance of using shape metrics based on the distribution of the ages at death to assess reliably patterns of mortality. In particular, we found that the pace and the shape of ageing, although statistically independent, could be associated in mammals. We conclude that the metrics defined from the distribution of ages at death provide a complementary approach to mortality or survival curve analyses and, by offering straightforward standardization, provide a promising tool for future comparative analyses of actuarial senescence and mortality across the tree of life. A free Plain Language Summary can be found within the Supporting Information of this article.

High reproductive effort is associated with decreasing mortality late in life in captive ruffed lemurs.

Evolutionary theories of senescence predict that a high allocation to reproduction during early life should have long-term deleterious consequences on future reproduction or survival because individuals have to face an energy allocation trade-off between reproductive effort and the maintenance of body condition. Using a high-quality dataset from 1,721 red ruffed lemurs (RRL, Varecia rubra) and 3,637 black and white ruffed lemurs (BWRM, V. variegata) living in captivity, we tested the existence of a trade-off between reproductive effort and late-life survival after accounting for possible confounding effects of natal environmental conditions. We report clear evidence of actuarial senescence (i.e., the decline of annual survival with increasing age) in both sexes and for both species of ruffed lemurs. RRL had a lower baseline mortality and senesced faster than BWRL, resulting in similar distributions of longevities for both species. No between-sex difference was observed in any species. Lastly, a higher reproductive effort was positively associated with an increase of survival late in life, and thereby an increased longevity. These findings indicate that individual quality rather than trade-off drives the association between reproductive success and survival pattern among individual lemurs of both species in the protected environment provided by zoos. Lemurs are among the world's highest conservation priorities and better understanding factors influencing their longevity and actuarial senescence patterns should improve their conservation.

Age-specific survival in the socially monogamous alpine marmot (Marmota marmota): evidence of senescence

We investigated age-specific variation in survival of dominant individuals in a long-lived and monogamous mammal, the alpine marmot ( Marmota marmota ), from a large dataset collected during a 24-year intensive monitoring of a free-ranging population. We found evidence of actuarial senescence in dominant individuals for both sexes. Survivorship was constant with age until dominant marmots were between 6 and 8 years of age and declined markedly thereafter. No between sex differences occurred in the intensity of actuarial senescence, which might be related to the weak intensity of sexual selection in this socially monogamous mammal. More investigations are needed to know whether cooperative breeding, hibernation, and monogamy, which are key features of the alpine marmot life history, could have shaped the patterns of actuarial senescence we report.

Age‐related variation and temporal patterns in the survival of a long‐lived scavenger

Although senescence has been described for various fitness components in a wide range of animal species, few studies have studied senescence in long‐lived species, and little is known about its interactions with varying environmental conditions. Using a 32 year capture–mark–recapture dataset on the griffon vulture Gyps fulvus, we examined the demographic patterns of actuarial senescence and the patterns of year‐to‐year variation in survival rates. We found a significant, surprisingly late, decrease of annual survival probabilities from the age of 28 years onward and divided individual lifetimes into to three categories (juvenile, mid‐age and senescent birds). In agreement with the environmental canalization hypothesis, our analyses uncovered 1) higher temporal variation of annual survival probabilities in both the juvenile and senescent age classes compared to the mid‐age class and 2) low sensitivity of the population growth rate to the survival of both the juvenile and senescent age classes. Our results further suggested that the temporal variation in the survival of senescent birds might be related to intra‐annual changes in air temperature amplitudes. Finally, using population dynamics modeling, we revealed contrasting effects of the inclusion of the senescent age class on predicted population growth, depending on how survival rates were modeled. Altogether, our results demonstrate the existence of a class of senescent birds that exhibit distinct demographic properties compared to juvenile and mid‐age classes.

Males do not senesce faster in large herbivores with highly seasonal rut

Patterns of actuarial senescence vary among long-lived species. A proposed explanation of the evolution of species-specific senescence patterns is that increased levels of energy allocation to intra-male competition decrease the amount of energy available for somatic maintenance, leading to earlier or faster actuarial senescence. Previous studies did not provide support for such relationships, but did not focus on the intensity of allocation likely to shape inter-specific variation in actuarial senescence in males. Here, by analyzing data from 56 species of captive large herbivores, we tested whether actuarial senescence is more pronounced in species displaying a well-defined ‘rut’ period than in species with year-round reproduction. Using an original quantitative metric of the annual duration of reproductive activity, we demonstrated that the length of the mating season has no detectable effect on actuarial senescence. On the other hand, both diet and body mass are important factors shaping actuarial senescence patterns in male captive herbivores.

Senescence in relation to latitude and migration in birds

Senescence is the age-related deterioration of the phenotype, explained by accumulation of mutations, antagonistic pleiotropy, free radicals or other mechanisms. I investigated patterns of actuarial senescence in a sample of 169 species of birds in relation to latitude and migration, by analysing longevity records adjusted for sampling effort, survival rate and body mass. Senescence might decrease at low latitudes because of elevated adult survival rates and generally slow life histories. Alternatively, the rate of senescence might increase at low latitudes because of the greater impact of biological interactions such as parasitism, predation and competition on fitness through differential effects of age-specific mortality (e.g. because immunologically naïve young individuals and immuno-senescent old individuals might die more frequently than individuals belonging to intermediate age classes). Bird migration entails extensive exercise twice annually, with migrants spending more time in benign environments with little abiotic mortality than residents, migrants having higher adult survival rate and lower annual fecundity than residents, and migrants suffering more from the consequences of oxidative stress than residents. The rate of senescence increased with latitude, as expected because of slow life histories at low latitudes. Independently, rate of senescence decreased with increasing migration distance. These findings were robust to control for potentially confounding effects of body mass, age of first reproduction and phenotypic similarity among species because of common descent.

Actuarial Senescence and Demographic Heterogeneity in the Florida Scrub Jay

Analysis of mortality from a 25—yr sample of 380 Florida Scrub Jays, Aphelocoma c. coerulescens, shows that actuarial senescence (increase in mortality with age) occurs. This refutes the notion that adult mortality is independent of age in birds, and has important implications for evolutionary dynamics. We point to two major factors that may act to mask underlying patterns of actuarial senescence: (1) Selection through time (demographic heterogeneity): because selection inevitably weeds out lower quality individuals first, overall mortality may appear to be constant or even decreasing, despite an increasing force of mortality acting on birds of higher quality. (2) Conflicting processes: one source of mortality may act to decrease mortality over time (e.g., group size effects), while another acts to increase it (e.g., degenerative senescence). Age—specific data, measures of intrinsic quality that are independent of mortality, and exposure of sources of heterogeneity and of conflicting processes allow us to demonstrate a clear pattern of actuarial senescence in an unmanipulated, natural population of long—lived birds. The slow rate of increase in mortality is consistent with the hypothesis that mortality increases more slowly with age in birds than in mammals.