A unified framework for evolutionary genetic and physiological theories of aging.

Why and how we age are 2 intertwined questions that have fascinated scientists for many decades. However, attempts to answer these questions remain compartmentalized, preventing a comprehensive understanding of the aging process. We argue that the current lack of knowledge about the evolution of aging mechanisms is due to a lack of clarity regarding evolutionary theories of aging that explicitly involve physiological processes: the disposable soma theory (DST) and the developmental theory of aging (DTA). In this Essay, we propose a new hierarchical model linking genes to vital rates, enabling us to critically reevaluate the DST and DTA in terms of their relationship to evolutionary genetic theories of aging (mutation accumulation (MA) and antagonistic pleiotropy (AP)). We also demonstrate how these 2 theories can be incorporated in a unified hierarchical framework. The new framework will help to generate testable hypotheses of how the hallmarks of aging are shaped by natural selection.

Thermal conditions predict intraspecific variation in senescence rate in frogs and toads.

Variation in temperature is known to influence mortality patterns in ectotherms. Even though a few experimental studies on model organisms have reported a positive relationship between temperature and actuarial senescence (i.e., the increase in mortality risk with age), how variation in climate influences the senescence rate across the range of a species is still poorly understood in free-ranging animals. We filled this knowledge gap by investigating the relationships linking senescence rate, adult lifespan, and climatic conditions using long-term capture-recapture data from multiple amphibian populations. We considered two pairs of related anuran species from the Ranidae (Rana luteiventris and Rana temporaria) and Bufonidae (Anaxyrus boreas and Bufo bufo) families, which diverged more than 100 Mya and are broadly distributed in North America and Europe. Senescence rates were positively associated with mean annual temperature in all species. In addition, lifespan was negatively correlated with mean annual temperature in all species except A. boreas In both R. luteiventris and A. boreas, mean annual precipitation and human environmental footprint both had negligible effects on senescence rates or lifespans. Overall, our findings demonstrate the critical influence of thermal conditions on mortality patterns across anuran species from temperate regions. In the current context of further global temperature increases predicted by Intergovernmental Panel on Climate Change scenarios, a widespread acceleration of aging in amphibians is expected to occur in the decades to come, which might threaten even more seriously the viability of populations and exacerbate global decline.

Amplified Cyclicality in Mast Seeding Dynamics Positively Influences the Dynamics of a Seed Consumer Species.

AbstractTemporal autocorrelation in environmental conditions influences population dynamics through its effects on vital rates. However, a comprehensive understanding of how and to what extent temporal autocorrelation shapes population dynamics is still lacking because most empirical studies have unrealistically assumed that environmental conditions are temporally independent. Mast seeding is a biological event characterized by highly fluctuating and synchronized seed production at the tree population scale as well as a marked negative temporal autocorrelation. In the current context of global change, mast seeding events are expected to become more frequent, leading to strengthened negative temporal autocorrelations and thereby amplified cyclicality in mast seeding dynamics. Theory predicts that population growth rates are maximized when the environmental cyclicality of consumer resources and their generation times are closely matched. To test this prediction, we took advantage of the long-term monitoring of a wild boar population, a widespread seed consumer species characterized by a short generation time (∼2 years). As expected, simulations indicated that its stochastic population growth rate increased as mast seeding dynamics became more negatively autocorrelated. Our findings demonstrate that accounting for temporal autocorrelations in environmental conditions relative to the generation time of the focal population is required, especially under conditions of global warming, where the cyclicality in resource dynamics is likely to change.

Reproductive tactics, birth timing and the risk-resource trade-off in an income breeder.

In variable environments, habitats that are rich in resources often carry a higher risk of predation. As a result, natural selection should favour individuals that balance allocation of time to foraging versus avoiding predation through an optimal decision-making process that maximizes fitness. The behavioural trade-off between resource acquisition and risk avoidance is expected to be particularly acute during gestation and lactation, when the energetic demands of reproduction peak. Here, we investigated how reproductive female roe deer adjust their foraging activity and habitat use during the birth period to manage this trade-off compared with non-reproductive juveniles, and how parturition date constrains individual tactics of risk-resource management. Activity of reproductive females more than doubled immediately following parturition, when energy demand is highest. Furthermore, compared with non-reproductive juveniles, they increased their exposure to risk by using open habitat more during daytime and ranging closer to roads. However, these post-partum modifications in behaviour were particularly pronounced in late-parturient females who adopted a more risk-prone tactic, presumably to compensate for the growth handicap of their late-born offspring. In income breeders, individuals that give birth late may be constrained to trade risk avoidance for foraging during peak allocation to reproduction, with probable consequences for individual fitness.

Individual life histories: neither slow nor fast, just diverse.

The slow-fast continuum is a commonly used framework to describe variation in life-history strategies across species. Individual life histories have also been assumed to follow a similar pattern, especially in the pace-of-life syndrome literature. However, whether a slow-fast continuum commonly explains life-history variation among individuals within a population remains unclear. Here, we formally tested for the presence of a slow-fast continuum of life histories both within populations and across species using detailed long-term individual-based demographic data for 17 bird and mammal species with markedly different life histories. We estimated adult lifespan, age at first reproduction, annual breeding frequency, and annual fecundity, and identified the main axes of life-history variation using principal component analyses. Across species, we retrieved the slow-fast continuum as the main axis of life-history variation. However, within populations, the patterns of individual life-history variation did not align with a slow-fast continuum in any species. Thus, a continuum ranking individuals from slow to fast living is unlikely to shape individual differences in life histories within populations. Rather, individual life-history variation is likely idiosyncratic across species, potentially because of processes such as stochasticity, density dependence, and individual differences in resource acquisition that affect species differently and generate non-generalizable patterns across species.

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

In human populations, women consistently outlive men, which suggests profound biological foundations for sex differences in survival. Quantifying whether such sex differences are also pervasive in wild mammals is a crucial challenge in both evolutionary biology and biogerontology. Here, we compile demographic data from 134 mammal populations, encompassing 101 species, to show that the female's median lifespan is on average 18.6% longer than that of conspecific males, whereas in humans the female advantage is on average 7.8%. On the contrary, we do not find any consistent sex differences in aging rates. In addition, sex differences in median adult lifespan and aging rates are both highly variable across species. Our analyses suggest that the magnitude of sex differences in mammalian mortality patterns is likely shaped by local environmental conditions in interaction with the sex-specific costs of sexual selection.

Reproductive dispersion and damping time scale with life-history speed.

Iteroparous species may reproduce at many different ages, resulting in a reproductive dispersion that affects the damping of population perturbations, and varies among life histories. Since generation time ( T c ) is known to capture aspects of life-history variation, such as life-history speed, does T c also determine reproductive dispersion ( S ) or damping time ( τ )? Using phylogenetically corrected analyses on 633 species of animals and plants, we find, firstly, that reproductive dispersion S scales isometrically with T c . Secondly, and unexpectedly, we find that the damping time ( τ ) does not scale isometrically with generation time, but instead changes only as T c b with b < 1 (also, there is a similar scaling with S ). This non-isometric scaling implies a novel demographic contrast: increasing generation times correspond to a proportional increase in reproductive dispersion, but only to a slower increase in the damping time. Thus, damping times are partly decoupled from the slow-fast continuum, and are determined by factors other than allometric constraints.

Temporal correlations among demographic parameters are ubiquitous but highly variable across species.

Temporal correlations among demographic parameters can strongly influence population dynamics. Our empirical knowledge, however, is very limited regarding the direction and the magnitude of these correlations and how they vary among demographic parameters and species' life histories. Here, we use long-term demographic data from 15 bird and mammal species with contrasting pace of life to quantify correlation patterns among five key demographic parameters: juvenile and adult survival, reproductive probability, reproductive success and productivity. Correlations among demographic parameters were ubiquitous, more frequently positive than negative, but strongly differed across species. Correlations did not markedly change along the slow-fast continuum of life histories, suggesting that they were more strongly driven by ecological than evolutionary factors. As positive temporal demographic correlations decrease the mean of the long-run population growth rate, the common practice of ignoring temporal correlations in population models could lead to the underestimation of extinction risks in most species.

Decline in telomere length with increasing age across nonhuman vertebrates: A meta-analysis.

The prediction that telomere length (TL) shortens with increasing age is a major element in considering the role of telomeres as a key player in evolution. While telomere attrition is found in humans both in vitro and in vivo, the increasing number of studies reporting diverse age-specific patterns of TL challenges the hypothesis of a universal decline of TL with increasing age. Here, we performed a meta-analysis to estimate the relationship between TL and age across 175 estimates encompassing 98 species of vertebrates. We found that, on average, TL does decline with increasing age during adulthood. However, this decline was weak and variable across vertebrate classes, and we also found evidence for a publication bias that might weaken our current evidence of decreasing TL with increasing age. We found no evidence for a faster decline in TL with increasing age when considering the juvenile stage (from birth to age at first reproduction) compared to the adult stage. Heterogeneity in TL ageing rates was explained by the method used to measure telomeres: detectable TL declines with increasing age were found only among studies using TRF with in-gel hybridisation and qFISH methods, but not in studies using qPCR and Southern blot-based TRF methods. While we confirmed that TL declines with increasing age in most adult vertebrates, our results identify an influence of telomere measurement methodology, which highlights the need to examine more thoroughly the effect of the method of measurement on TL estimates.

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

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.

On this side of the fence: Functional responses to linear landscape features shape the home range of large herbivores.

Understanding the consequences of global change for animal movement is a major issue for conservation and management. In particular, habitat fragmentation generates increased densities of linear landscape features that can impede movements. While the influence of these features on animal movements has been intensively investigated, they may also play a key role at broader spatial scales (e.g. the home range scale) as resources, cover from predators/humans, corridors/barriers or landmarks. How space use respond to varying densities of linear features has been mostly overlooked in large herbivores, in contrast to studies done on predators. Focusing on large herbivores should provide additional insights to understand how animals solve the trade-off between energy acquisition and mortality risk. Here, we investigated the role of anthropogenic (roads and tracks) and natural (ridges, valley bottoms and forest edges) linear features on home range features in five large herbivores. We analysed an extensive GPS monitoring database of 710 individuals across nine populations, ranging from mountain areas mostly divided by natural features to lowlands that were highly fragmented by anthropogenic features. Nearly all of the linear features studied were found at the home range periphery, suggesting that large herbivores primarily use them as landmarks to delimit their home range. In contrast, for mountain species, ridges often occurred in the core range, probably related to their functional role in terms of resources and refuge. When the density of linear features was high, they no longer occurred predominantly at the home range periphery, but instead were found across much of the home range. We suggest that, in highly fragmented landscapes, large herbivores are constrained by the costs of memorising the spatial location of key features, and by the requirement for a minimum area to satisfy their vital needs. These patterns were mostly consistent in both males and females and across species, suggesting that linear features have a preponderant influence on how large herbivores perceive and use the landscape.

Does mast seeding shape mating time in wild boar? A comparative study.

In seasonal environments, the timing of reproduction often matches with the peak of food resources. One well-known effect of global warming is an earlier phenology of resources, leading to a possible mismatch between the timing of reproduction for consumers and food peak. However, global warming may also change the dynamics of food resources, such as the intensity and frequency of pulsed mast seeding. How quantitative changes in mast seeding influence the timing of reproduction of seed consumers remains unexplored. Here, we assess how yearly variation in mast seeding influences mating time in wild boar (Sus scrofa), a widespread seed consumer species. We took advantage of the intensive monitoring of both female reproduction (1636 females) and acorn production over 6 consecutive years across 15 populations of wild boar in the wild. We found that mating time occurs earlier when acorn production increases in most but not all populations. In two out of 15 populations, heavy females mated earlier than light ones. Our findings demonstrate that mast seeding advances the mating time in some populations, which could perhaps impact how boars respond to climate change.

Data gaps and opportunities for comparative and conservation biology.

Biodiversity loss is a major challenge. Over the past century, the average rate of vertebrate extinction has been about 100-fold higher than the estimated background rate and population declines continue to increase globally. Birth and death rates determine the pace of population increase or decline, thus driving the expansion or extinction of a species. Design of species conservation policies hence depends on demographic data (e.g., for extinction risk assessments or estimation of harvesting quotas). However, an overview of the accessible data, even for better known taxa, is lacking. Here, we present the Demographic Species Knowledge Index, which classifies the available information for 32,144 (97%) of extant described mammals, birds, reptiles, and amphibians. We show that only 1.3% of the tetrapod species have comprehensive information on birth and death rates. We found no demographic measures, not even crude ones such as maximum life span or typical litter/clutch size, for 65% of threatened tetrapods. More field studies are needed; however, some progress can be made by digitalizing existing knowledge, by imputing data from related species with similar life histories, and by using information from captive populations. We show that data from zoos and aquariums in the Species360 network can significantly improve knowledge for an almost eightfold gain. Assessing the landscape of limited demographic knowledge is essential to prioritize ways to fill data gaps. Such information is urgently needed to implement management strategies to conserve at-risk taxa and to discover new unifying concepts and evolutionary relationships across thousands of tetrapod species.

Distributions of LRS in varying environments.

The lifetime reproductive success (LRS) of individuals is affected by random events such as death, realized growth or realized reproduction, and the outcomes of these events can differ even when individuals have identical probabilities. Another source of randomness arises when these probabilities also change over time in variable environments. For structured populations in stochastic environments, we extend our recent method to determine how birth environment and birth stage determine the random distribution of the LRS. Our results provide a null model that quantifies effects on LRS of just the birth size or stage. Using Roe deer Capreolus capreolus as a case study, we show that the effect of an individual's birth environment on LRS varies with the frequency of environments and their temporal autocorrelation, and that lifetime performance is affected by changes in the pattern of environmental states expected as a result of climate change.

Maternal effects shape offspring physiological condition but do not senesce in a wild mammal.

In vertebrates, offspring survival often decreases with increasing maternal age. While many studies have reported a decline in fitness-related traits of offspring with increasing maternal age, the study of senescence in maternal effect through age-specific changes in offspring physiological condition is still at its infancy. We assessed the influence of maternal age and body mass on offspring physiological condition in two populations of roe deer (Capreolus capreolus) subjected to markedly different environmental conditions. We measured seven markers to index body condition and characterize the immune profile in 86 fawns which became recently independent of their known-aged mothers. We did not find striking effects of maternal age on offspring physiological condition measured at 8 months of age. This absence of evidence for senescence in maternal effects is likely due to the strong viability selection observed in the very first months of life in this species. Offspring physiological condition was, on the other hand, positively influenced by maternal body mass. Between-population differences in environmental conditions experienced by fawns also influenced their average body condition and immune phenotype. Fawns facing food limitation displayed lower values in some markers of body condition (body mass and haemoglobin levels) than those living in good quality habitat. They also allocated preferentially to humoral immunity, contrary to those living in good conditions, which allocated more to cellular response. These results shed a new light on the eco-physiological pathways mediating the relationship between mother's mass and offspring condition.

Sex-specific demography and generalization of the Trivers-Willard theory.

The Trivers-Willard theory proposes that the sex ratio of offspring should vary with maternal condition when it has sex-specific influences on offspring fitness. In particular, mothers in good condition in polygynous and dimorphic species are predicted to produce an excess of sons, whereas mothers in poor condition should do the opposite. Despite the elegance of the theory, support for it has been limited. Here we extend and generalize the Trivers-Willard theory to explain the disparity between predictions and observations of offspring sex ratio. In polygynous species, males typically have higher mortality rates, different age-specific reproductive schedules and more risk-prone life history tactics than females; however, these differences are not currently incorporated into the Trivers-Willard theory. Using two-sex models parameterized with data from free-living mammal populations with contrasting levels of sex differences in demography, we demonstrate how sex differences in life history traits over the entire lifespan can lead to a wide range of sex allocation tactics, and show that correlations between maternal condition and offspring sex ratio alone are insufficient to conclude that mothers adaptively adjust offspring sex ratio.

Short-term telomere dynamics is associated with glucocorticoid levels in wild populations of roe deer.

While evidence that telomere length is associated with health and mortality in humans and birds is accumulating, a large body of research is currently seeking to identify factors that modulate telomere dynamics. We tested the hypothesis that high levels of glucocorticoids in individuals under environmental stress should accelerate telomere shortening in two wild populations of roe deer (Capreolus capreolus) living in different ecological contexts. From two consecutive annual sampling sessions, we found that individuals with faster rates of telomere shortening had higher concentrations of fecal glucocorticoid metabolites, suggesting a functional link between glucocorticoid levels and telomere attrition rate. This relationship was consistent for both sexes and populations. This finding paves the way for further studies of the fitness consequences of exposure to environmental stressors in wild vertebrates.

The hidden ageing costs of sperm competition.

Ageing and sexual selection are intimately linked. There is by now compelling evidence from studies performed across diverse organisms that males allocating resources to mating competition incur substantial physiological costs, ultimately increasing ageing. However, although insightful, we argue here that to date these studies cover only part of the relationship linking sexual selection and ageing. Crucially, allocation to traits important in post-copulatory sexual selection, that is sperm competition, has been largely ignored. As we demonstrate, such allocation could potentially explain much diversity in male and female ageing patterns observed both within and among species. We first review how allocation to sperm competition traits such as sperm and seminal fluid production depends on the quality of resources available to males and can be associated with a wide range of deleterious effects affecting both somatic tissues and the germline, and thus modulate ageing in both survival and reproductive terms. We further hypothesise that common biological features such as plasticity, prudent sperm allocation and seasonality of ejaculate traits might have evolved as counter-adaptations to limit the ageing costs of sperm competition. Finally, we discuss the implications of these emerging ageing costs of sperm competition for current research on the evolutionary ecology of ageing.

Life-history strategy varies with the strength of competition in a food-limited ungulate population.

Fluctuating population density in stochastic environments can contribute to maintain life-history variation within populations via density-dependent selection. We used individual-based data from a population of Soay sheep to examine variation in life-history strategies at high and low population density. We incorporated life-history trade-offs among survival, reproduction and body mass growth into structured population models and found support for the prediction that different life-history strategies are optimal at low and high population densities. Shorter generation times and lower asymptotic body mass were selected for in high-density environments even though heavier individuals had higher probabilities to survive and reproduce. In contrast, greater asymptotic body mass and longer generation times were optimal at low population density. If populations fluctuate between high density when resources are scarce, and low densities when they are abundant, the variation in density will generate fluctuating selection for different life-history strategies, that could act to maintain life-history variation.

Skewed distributions of lifetime reproductive success: beyond mean and variance.

Lifetime reproductive performance is quantified here by the LRS (lifetime reproductive success), the random number of offspring an individual produces over its lifetime. Many field studies find that distributions of LRS among individuals are non-normal, zero-inflated and highly skewed. These results beg the question, what is the distribution of LRS predicted by demographic models when the only source of randomness is demographic stochasticity? Here we present the first exact analysis of the probability distribution of LRS for species described by age + stage models; our analysis starts with estimated vital rates. We illustrate with three examples: the Hadza, human hunter-foragers (age-only), the evergreen tree Tsuga canadensis (stage-only) and Roe deer, Capreolus capreolus (age + stage). For each we obtain the exact distribution of LRS, but also calculate and discuss the first three moments. Our results point to important questions about how such LRS distributions affect natural selection, and life history evolution.