Do age‐specific survival patterns of wild boar fit current evolutionary theories of senescence?

Actuarial senescence is widespread in age‐structured populations. In growing populations, the progressive decline of Hamiltonian forces of selection with age leads to decreasing survival. As actuarial senescence is overcompensated by a high fertility, actuarial senescence should be more intense in species with high reproductive effort, a theoretical prediction that has not been yet explicitly tested across species. Wild boar (Sus scrofa) females have an unusual life‐history strategy among large mammals by associating both early and high reproductive effort with potentially long lifespan. Therefore, wild boar females should show stronger actuarial senescence than similar‐sized related mammals. Moreover, being polygynous and much larger than females, males should display higher senescence rates than females. Using a long‐term monitoring (18 years) of a wild boar population, we tested these predictions. We provided clear evidence of actuarial senescence in both sexes. Wild boar females had earlier but not stronger actuarial senescence than similar‐sized ungulates. Both sexes displayed similar senescence rates. Our study indicates that the timing of senescence, not the rate, is associated with the magnitude of fertility in ungulates. This demonstrates the importance of including the timing of senescence in addition to its rate to understand variation in senescence patterns in wild populations.     

Consequences of mating and predation risk for longevity in a freshwater snail: abstinence makes the heart beat longer

Senescence is not a static property of an individual or population, but rather it is a dynamic process that may be influenced by environmental conditions. This can occur in at least two ways: in the long‐term across multiple generations, and in the short‐term via phenotypic plasticity. The former has attracted a lot of attention, both theoretically and empirically; the latter has lagged behind. To determine whether two important environmental variables (predation risk and mate availability) affect the pattern of actuarial senescence (i.e. the increase in mortality with age), we reared 30 full‐sib families of the simultaneously hermaphroditic freshwater snail Physa acuta under four different environmental conditions and tracked individuals until death. Individuals were reared in a 2×2 factorial experiment that manipulated the nonlethal presence of chemical cues from predatory crayfish (presence/absence) and the opportunity to mate with an unrelated partner (mated/not mated). Snails that receive a partner reproduce by outcrossing, whereas those that remain in isolation can reproduce by self‐fertilization. We compared the cumulative survival curves to test for an effect of predation risk and mating. The hazard ratio (HR) for the predation risk comparison was 1.042 indicating no significant difference between the curves. However, the HR for the mating comparison was 4.021, reflecting a significant reduction in survival probability for mated snails relative to isolated snails. As such, mating resulted in a much shorter lifespan, an outcome that we interpret in terms of shifting resource allocation.     

DOES INCREASED MORTALITY FAVOR THE EVOLUTION OF MORE RAPID SENESCENCE?

It is widely believed (following the 1957 hypothesis of G. C. Williams) that greater rates of “extrinsic” (age- and condition-independent) mortality favor more rapid senescence. However, a recent analysis of mammalian life tables failed to find a significant correlation between minimum adult mortality rate and the rate of senescence. This article presents a simple theoretical analysis of how extrinsic mortality should affect the rate of senescence (i.e., the rate at which probability of mortality increases with age) under different evolutionary and population dynamical assumptions. If population dynamics are density independent, extrinsic mortality should not alter the senescence rate favored by natural selection. If population growth is density dependent and populations are stable, the effect of extrinsic mortality depends on the age specificity of the density dependence and on whether survival or reproduction (or both) are functions of density. It is possible that higher extrinsic mortality will increase the rate of senescence at all ages, decrease the rate at all ages, or increase it at some ages while decreasing it at others. Williams's hypothesis is most likely to be supported when density dependence acts primarily on fertility and does not differentially decrease the fertilities of older individuals. Patterns contrary to Williams's prediction are possible when density dependence acts primarily on the survival or fertility of later ages or when most variation in mortality rates is due to variation in nonextrinsic mortality.     

HUMAN ACTUARIAL AGING INCREASES FASTER WHEN BACKGROUND DEATH RATES ARE LOWER: A CONSEQUENCE OF DIFFERENTIAL HETEROGENEITY?

Many analyses of human populations have found that age-specific mortality rates increase faster across most of adulthood when overall mortality levels decline. This contradicts the relationship often expected from Williams' classic hypothesis about the effects of natural selection on the evolution of senescence. More likely, much of the within-species difference in actuarial aging is not due to variation in senescence, but to the strength of filters on the heterogeneity of frailty in older survivors. A challenge to this differential frailty hypothesis was recently posed by an analysis of life tables from historical European populations and traditional societies that reported variation in actuarial aging consistent with Williams' hypothesis after all. To investigate the challenge, we reconsidered those cases and aging measures. Here we show that the discrepancy depends on Ricklefs' aging rate measure, ω, which decreases as mortality levels drop because it is an index of mortality level itself, not the rate of increase in mortality with age. We also show unappreciated correspondence among the parameters of Gompertz-Makeham and Weibull survival models. Finally, we compare the relationships among mortality parameters of the traditional societies and the historical series, providing further suggestive evidence that differential heterogeneity has strong effects on actuarial aging.     

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.     

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.     

Sex‐Biased Senescence in a Polygynous Bat Species

Bats live substantially longer than any other similar‐sized mammal despite high metabolic rates during flight. The underlying causes for the longevity of bats and the question whether bats exhibit signs of senescence – a progressive deterioration in performance – are still unclear. Here, we describe rates of senescence in individual annual fitness, survival and reproduction using survival and recruitment data collected over an 18‐yr period from 77 males and 81 females in a wild population of Saccopteryx bilineata (greater sac‐winged bat), a polygynous species inhabiting colonies where female groups are defended each by a territorial male. In individuals older than 4 yr of age, individual fitness contribution, survival and recruitment declined with increasing age in males but not in females. Rates of senescence in annual individual fitness and in reproduction of males were at least an order of magnitude higher than those of females. This finding might be explained by the ‘disposable soma theory’ that attributes senescence to an optimal allocation of resources to somatic maintenance and competing traits such as reproduction. The rate of senescence in the survival of males was also significant but of the same order of magnitude as the (non‐significant) rate of females. Unlike many other polygynous mammals, greater sac‐winged bats show little overt male–male competition. As senescence in survival was only weak in males, our results are consistent with the theories for polygynous mammals, which view the trade‐off between male investment in physical traits for intense male–male competition against survival as a major source of the decline of male survival with age. This is the first study to demonstrate sex‐specific senescence rates in a wild population of a small, long‐lived mammalian species.     

The diversity of population responses to environmental change

The current extinction and climate change crises pressure us to predict population dynamics with ever‐greater accuracy. Although predictions rest on the well‐advanced theory of age‐structured populations, two key issues remain poorly explored. Specifically, how the age‐dependency in demographic rates and the year‐to‐year interactions between survival and fecundity affect stochastic population growth rates. We use inference, simulations and mathematical derivations to explore how environmental perturbations determine population growth rates for populations with different age‐specific demographic rates and when ages are reduced to stages. We find that stage‐ vs. age‐based models can produce markedly divergent stochastic population growth rates. The differences are most pronounced when there are survival‐fecundity‐trade‐offs, which reduce the variance in the population growth rate. Finally, the expected value and variance of the stochastic growth rates of populations with different age‐specific demographic rates can diverge to the extent that, while some populations may thrive, others will inevitably go extinct.     

Senescence in the city: exploring ageing patterns of a long‐lived raptor across an urban gradient

In many vertebrates, productivity and survival usually increase with age and then start to decline above a certain age; processes known as reproductive and actuarial senescence. Senescence is widely believed to be driven by the accumulation of somatic damage or mutations. Thus, levels of such cellular damage, and therefore senescence could, in theory, differ between different habitats if they experience different stressors. Urban environments expose animals to a wide range of stressors that pose a challenge to physiological systems and might accelerate the ageing process. We studied productivity and survival of black sparrowhawks across an urban gradient in Cape Town, South Africa. We hypothesise that productivity and survival will first increase with age, but that productivity and survival will then decline above a certain age, due to senescence. Furthermore, we hypothesise that rates of senescence will be accelerated in more urban areas. We used 17 years of data from colour‐ringed individuals. We found no indication of any improvement in productivity with age in early‐life, but we did detect reproductive senescence, with productivity declining above six years of age. However, contrary to our predictions, there were no differences in reproductive senescence along the urban gradient. Similarly, we found that survival rates of adults did not show any strong improvement with age in early life, but decreased with age amongst older birds, providing support for actuarial senescence. However, once again no differences in this pattern were apparent along the urban gradient. This study represents one of the first to examine differences in senescence rates in different habitats. Our results suggest that for this urban adapted species, senescence patterns do not vary according to levels of urbanisation. Whether this pattern holds for species more sensitive to urbanisation remains worthy of exploration.     

Interactive effects of senescence and natural disturbance on the annual survival probabilities of snail kites

Individuals in wild populations face risks associated with both intrinsic (i.e. aging) and external (i.e. environmental) sources of mortality. Condition‐dependent mortality occurs when there is an interaction between such factors; however, few studies have clearly demonstrated condition‐dependent mortality and some have even argued that condition‐dependent mortality does not occur in wild avian populations. Using large sample sizes (2084 individuals, 3746 re‐sights) of individual‐based longitudinal data collected over a 33 year period (1976–2008) on multiple cohorts, we used a capture–mark–recapture framework to model age‐dependent survival in the snail kite Rostrhamus sociabilis plumbeus population in Florida. Adding to the growing amount of evidence for actuarial senescence in wild populations, we found evidence of senescent declines in survival probabilities in adult kites. We also tested the hypothesis that older kites experienced condition‐dependent mortality during a range‐wide drought event (2000–2002). The results provide convincing evidence that the annual survival probability of senescent kites was disproportionately affected by the drought relative to the survival probability of prime‐aged adults. To our knowledge, this is the first evidence of condition‐dependent mortality to be demonstrated in a wild avian population, a finding which challenges recent conclusions drawn in the literature. Our study suggests that senescence and condition‐dependent mortality can affect the demography of wild avian populations. Accounting for these sources of variation may be particularly important to appropriately compute estimates of population growth rate, and probabilities of quasi‐extinctions.     

HAS ACTUARIAL AGING “SLOWED” OVER THE PAST 250 YEARS? A COMPARISON OF SMALL‐SCALE SUBSISTENCE POPULATIONS AND EUROPEAN COHORTS

G.C. Williams's 1957 hypothesis famously argues that higher age-independent, or "extrinsic," mortality should select for faster rates of senescence. Long-lived species should therefore show relatively few deaths from extrinsic causes such as predation and starvation. Theoretical explorations and empirical tests of Williams's hypothesis have flourished in the past decade but it has not yet been tested empirically among humans. We test Williams's hypothesis using mortality data from subsistence populations and from historical cohorts from Sweden and England/Wales, and examine whether rates of actuarial aging declined over the past two centuries. We employ three aging measures: mortality rate doubling time (MRDT), Ricklefs's ω, and the slope of mortality hazard from ages 60–70, m '_60–70, and model mortality using both Weibull and Gompertz–Makeham hazard models. We find that (1) actuarial aging in subsistence societies is similar to that of early Europe, (2) actuarial senescence has slowed in later European cohorts, (3) reductions in extrinsic mortality associate with slower actuarial aging in longitudinal samples, and (4) men senesce more rapidly than women, especially in later cohorts. To interpret these results, we attempt to bridge population-based evolutionary analysis with individual-level proximate mechanisms.     

Parallel lines: nothing has changed?

The exponential increase in mortality rate with age is a universal feature of aging and is described mathematically by the Gompertz equation. When this equation is transformed semilogarithmically, it conforms to a straight line, the slope of which is generally used to reflect the rate of senescence. Historical and contemporary data of human and nonhuman populations show that adverse environmental conditions do not always change the slope of the log mortality rate over age. From these latter observations it is sometimes mistakenly inferred that the rate of senescence is unaffected by environmental conditions. Current biological inference emphasizes that gene action is dependent on the environment in which it is expressed. Here, we propose using the tangent line of the Gompertz equation to assess whether the rate of senescence has altered. Such an approach unmasks different rates of senescence when parameter G has remained constant, an observation that is in line with the notion that a plastic life history trait such as the rate of senescence results from the interplay of both genes and environment.     

Actuarial senescence in laboratory and field populations of Lepidoptera

1. Recent observations of actuarial senescence – an increase in mortality rate with age – have challenged the assertion that the brevity of adult insect life spans precludes ageing. 2. Here the rate of senescence in 22 species of Lepidoptera was quantified by fitting demographic models to adult survivorship data drawn from a range of field and laboratory studies. 3. Senescence was evident in all 22 species investigated, with a model of age‐related mortality consistently fitting the survivorship curves significantly better than an alternative model which assumes constant mortality. 4. The rates of senescence varied significantly among species. The rates of senescence also differed significantly between sexes for all species tested, but not in a consistent way.     

Post‐independence mortality of juveniles is driven by anthropogenic hazards for two passerines in an urban landscape

Urban environments impose novel selection pressures with varying impacts across species and life history stages. The post‐fledging stage for migratory passerines, defined as the period of time from when hatch‐year birds fledge until their first migration, is a poorly understood component of annual productivity that potentially limits population growth. We studied two migratory passerines with positive and negative population responses to urbanization, respectively: gray catbird Dumetella carolinensis and wood thrush Hylocichla mustelina. Our goals were to estimate post‐fledging survival rates for urban bird populations and determine which features of the urban landscape impact mortality risk during the post‐fledging stage. From 2012–2014, we tracked 127 fledglings (60 gray catbirds and 67 wood thrushes). Over 55 d after fledging, cumulative survival of gray catbirds (0.32 [95% CI: 0.22–0.47]) was approximately half that of wood thrushes (0.63 [95% CI: 0.52–0.75]). Thus, survival rates during the post‐fledging stage, taken in isolation, do not explain differential trajectories of gray catbird and wood thrush populations in urban environments. Most mortality (86%) for both species was due to predation. However, after reaching independence from parental care, 6 birds (9.4% of mortalities) died of anthropogenic causes (e.g. building, car strikes). Crossing roads significantly increased mortality risk, but increasing daily movement distance decreased mortality risk. Our results raise the question of whether anthropogenic sources of mortality are compensatory or additive to natural mortality; we emphasize the need to monitor fledgling survival beyond the parental‐dependence stage in order to fully understand the impacts of anthropogenic hazards on juvenile birds.     

Variation of annual apparent survival and detection rates with age,year and individual identity in male Weddell seals (Leptonychotes weddellii) from long-term mark-recapture data

Exploring age- and sex-specific survival rates provides insight regarding population behavior and life-history trait evolution. However, our understanding of how age-specific patterns of survival, including actuarial senescence, compare between the sexes remains inadequate. Using 36 years of mark-recapture data for 7,516 male Weddell seals (Leptonychotes weddellii) born in Erebus Bay, Antarctica, we estimated age-specific annual survival rates using a hierarchical model for mark-recapture data in a Bayesian framework. Our male survival estimates were moderate for pups and yearlings, highest for 2-year-olds, and gradually declined with age thereafter such that the oldest animals observed had the lowest rates of any age. Reports of senescence in other wildlife populations of species with similar longevity occurred at older ages than those presented here. When compared to recently published estimates for reproductive Weddell seal females, we found that peak survival rates were similar (males: 0.94, 95% CI = 0.92–0.96; females: 0.92, 95% CI = 0.93–0.95), but survival rates at older ages were lower in males. Age-specific male Weddell seal survival rates varied across years and individuals, with greater variation occurring across years. Similar studies on a broad range of species are needed to contextualize these results for a better understanding of the variation in senescence patterns between the sexes of the same species, but our study adds information for a marine mammal species to a research topic dominated by avian and ungulate species.     

Life history of breeding partners alters age‐related changes of reproductive traits in a natural population of blue tits

Reproductive senescence, an intra‐individual decline in reproductive function with age, is widespread, but proximate factors determining its rate remain largely unknown. Most studies of reproductive senescence focus on females, leaving senescence in male function and its implications for female function largely understudied. We constructed linear mixed models to explore the interactive effects of paternal and maternal age and a life‐history trait (i.e. age at first reproduction) on four fitness components (i.e. laying date, clutch size, number of fledglings and number of recruits) measured in a wild, breeding population of blue tits Cyanistes caeruleus ogliastrae where individual breeding success has been followed for over 30 years (our dataset spanned 29 years). Previous studies have shown that, across female lifespan, laying date decreases and subsequently increases; earlier laying dates result in higher fitness because hatchlings have greater access to a seasonal food source. Our analyses reveal that females that initiate reproduction early in life show a greater delay in laying date with old age. In addition to delayed laying dates, older females lay smaller clutches. However, the magnitude of female age effects was influenced by the age at first reproduction of their breeding partners. Senescence of laying date and clutch size was reduced when females mated with males that reproduced early in life compared to males that delayed reproduction. We confirmed that both laying date and clutch size were significantly correlated with reproductive fitness suggesting that these dynamics early in the breeding cycle can have long‐term consequences. These complex phenotypic interactions shed light on the proximate mechanisms underlying reproductive senescence in nature and highlight the potential importance of cross‐sex age by life‐history interactions.     

The long shadow of senescence: age impacts survival and territory defense in loons

Senescence, increased mortality that occurs among animals of advanced age, impacts behavior and ecology in many avian species. We investigated actuarial, reproductive, and behavioral senescence using capture, marking, and resighting data from a 26‐year study of common loons Gavia immer. Territorial residents of both sexes exhibited high annual survival (0.94) until their mid 20s, at which point survival fell to 0.76 and 0.77 in males and females, respectively. Sexual symmetry in actuarial senescence is somewhat surprising in this species, because males make a substantially greater investment in territory defense and chick‐rearing and because males engage in lethal contests for territory ownership. Survival of displaced breeders (0.80) was lower than that of territorial residents in both young and old individuals. Old males and females also experienced slightly higher annual probability of eviction (0.16 for males; 0.17 for females) than prime‐aged breeders (0.13 for both sexes), indicating senescence in territory defense. Prime‐aged males reclaimed territories at a high rate (0.49), in contrast to females of the same age (0.33). However, old males resettled with success (0.35) similar to old females (0.31), suggesting that males decline in competitive ability as they age. Nonetheless males, but not females, showed an apparent increase in breeding success over the entire lifetime, a possible indication that very old males make a terminal investment in reproductive output at the cost of survival.     

Within‐species variation in long‐term trajectories of growth,fecundity and mortality in the Collembola Folsomia candida

Senescence – the progressive deterioration of organisms with age – affects many traits of which survival and reproduction are the most commonly studied. Recent comparative studies have revealed a remarkable amount of variation in the patterns of ageing across the tree of life. This between‐species diversity raises many questions about the evolution of senescence and of the shapes of the life‐history age trajectories. Here, we study how the different components of the shapes of these life‐history age trajectories can vary within a single species to shed light on the possible constraints involved in their evolution. To do so, we closely followed in controlled laboratory conditions, and for more than 450 days, the mortality, body length and fecundity of small cohorts of two clonal lineages of the Collembola Folsomia candida. We studied three components of the adult mortality trajectory: the baseline mortality, onset and speed of senescence. We found that they can differ between strains of a single species in such a way that, remarkably, an increased life expectancy is not synonymous with a delayed senescence: the strain that grows bigger has the longest life expectancy but suffers from a precocious senescence. We observed marked differences between the strains in the asymptotic body length and reproductive investment. More generally, our results highlight the importance of finely describing the long‐term trajectories of several life‐history traits in order to better understand how the patterns of senescence have been shaped by natural selection.     

Age-specific demography in Plantago: uncovering age-dependent mortality in a natural population

Accurate measures of age-dependent mortality are critical to life-history analysis and measures of fitness, yet these measures are difficult to obtain in natural populations. Age-dependent mortality patterns can be obscured not only by seasonal variation in environmental conditions and reproduction but also by changes in the heterogeneity among individuals in the population over time due to selection. This study of Plantago lanceolata uses longitudinal data from a field study with a large number of individuals to develop a model to estimate the shape of the baseline hazard function that represents the age-dependent risk of mortality. The model developed here uses both constant (genetics, spatial location) and time-varying (temperature, rainfall, reproduction, size) covariates not only to estimate the underlying mortality pattern but also to demonstrate that the risk of mortality associated with fitness components can change with time/age. Moreover, this analysis suggests that increasing size after reproductive maturity may allow this plant species to escape from demographic senescence.     

Trans‐generational effects on ageing in a wild bird population

Ageing, long thought to be too infrequent to study effectively in natural populations, has recently been shown to be ubiquitous, even in the wild. A major challenge now is to explain variation in the rates of ageing within populations. Here, using 49 years of data from a population of great tits (Parus major), we show that offspring life‐history trajectories vary with maternal age. Offspring hatched from older mothers perform better early in life, but suffer from an earlier onset, and stronger rate, of reproductive senescence later in life. Offspring reproductive lifespan is, however, unaffected by maternal age, and the different life‐history trajectories result in a similar fitness payoff, measured as lifetime reproductive success. This study therefore identifies maternal age as a new factor underlying variation in rates of ageing, and, given the delayed trans‐generational nature of this effect, poses the question as to proximate mechanisms linking age‐effects across generations.