Demographic balancing of migrant and resident elk in a partially migratory population through forage–predation tradeoffs

Partial migration is widespread in ungulates, yet few studies have assessed demographic mechanisms for how these alternative strategies are maintained in populations. Over the past two decades the number of resident individuals of the Ya Ha Tinda elk herd near Banff National Park has been increasing proportionally despite an overall population decline. We compared demographic rates of migrant and resident elk to test for demographic mechanisms partial migration. We determined adult female survival for 132 elk, pregnancy rates for 150 female elk, and elk calf survival for 79 calves. Population vital rates were combined in Leslie‐matrix models to estimate demographic fitness, which we defined as the migration strategy‐specific population growth rate. We also tested for differences in factors influencing risk of mortality between migratory strategies for adult females using Cox‐proportional hazards regression and time‐varying covariates of exposure to forage biomass, wolf predation risk, and group size. Despite higher pregnancy rates and winter calf weights associated with higher forage quality, survival of migrant adult females and calves were lower than resident elk. Resident elk traded high quality food to reduce predation risk by selecting areas close to human activity, and by living in group sizes 20% larger than migrants. Thus, residents experienced higher adult female survival and calf survival, but lower pregnancy and calf weights. Cause‐specific mortality of migrants was dominated by wolf and grizzly bear mortality, whereas resident mortality was dominated by human hunting. Demographic differences translated into slightly higher (2–3%), but non‐significant, resident population growth rate compared to migrant elk, suggesting demographic balancing between resident strategies during our study. Despite statistical equivalence, our results are also consistent with slow long‐term declines in migrants because of high predation because of higher wolf‐caused mortality in migrants. These results emphasize that migrants and residents will make different tradeoffs between forage and risk may affect the demographic balance of partially migratory populations, which may explain recent declines in migratory behavior in many ungulate populations around the world.     

Evidence for senescence in survival but not in reproduction in a short‐lived passerine

Senescence has been studied since a long time by theoreticians in ecology and evolution, but empirical support in natural population has only recently been accumulating. One of the current challenges is the investigation of senescence of multiple fitness components and the study of differences between sexes. Until now, studies have been more frequently conducted on females than on males and rather in long‐lived than in short‐lived species. To reach a more fundamental understanding of the evolution of senescence, it is critical to investigate age‐specific survival and reproduction performance in both sexes and in a large range of species with contrasting life histories. In this study, we present results on patterns of age‐specific and sex‐specific variation in survival and reproduction in the whinchat Saxicola rubetra, a short‐lived passerine. We compiled individual‐based long‐term datasets from seven populations that were jointly analyzed within a Bayesian modeling framework. We found evidence for senescence in survival with a continuous decline after the age of 1 year, but no evidence of reproductive senescence. Furthermore, we found no clear evidence for sex effects on these patterns. We discuss these results in light of previous studies documenting senescence in short‐lived birds. We note that most of them have been conducted in populations breeding in nest boxes, and we question the potential effect of the nest boxes on the shape of age‐reproductive trajectories.     

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.     

Individual variation in early‐life telomere length and survival in a wild mammal

Individual variation in survival probability due to differential responses to early‐life environmental conditions is important in the evolution of life histories and senescence. A biomarker allowing quantification of such individual variation, and which links early‐life environmental conditions with survival by providing a measure of conditions experienced, is telomere length. Here, we examined telomere dynamics among 24 cohorts of European badgers (Meles meles). We found a complex cross‐sectional relationship between telomere length and age, with no apparent loss over the first 29 months, but with both decreases and increases in telomere length at older ages. Overall, we found low within‐individual consistency in telomere length across individual lifetimes. Importantly, we also observed increases in telomere length within individuals, which could not be explained by measurement error alone. We found no significant sex differences in telomere length, and provide evidence that early‐life telomere length predicts lifespan. However, while early‐life telomere length predicted survival to adulthood (≥1 year old), early‐life telomere length did not predict adult survival probability. Furthermore, adult telomere length did not predict survival to the subsequent year. These results show that the relationship between early‐life telomere length and lifespan was driven by conditions in early‐life, where early‐life telomere length varied strongly among cohorts. Our data provide evidence for associations between early‐life telomere length and individual life history, and highlight the dynamics of telomere length across individual lifetimes due to individuals experiencing different early‐life environments.     

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.     

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.     

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.     

Insights from comparative analyses of aging in birds and mammals

Many laboratory models used in aging research are inappropriate for understanding senescence in mammals, including humans, because of fundamental differences in life history, maintenance in artificial environments, and selection for early aging and high reproductive rate. Comparative studies of senescence in birds and mammals reveal a broad range in rates of aging among a variety of taxa with similar physiology and patterns of development. These comparisons suggest that senescence is a shared property of all vertebrates with determinate growth, that the rate of senescence has been modified by evolution in response to the potential life span allowed by extrinsic mortality factors, and that most variation among species in the rate of senescence is independent of commonly ascribed causes of aging, such as oxidative damage. Individuals of potentially long‐lived species, particularly birds, appear to maintain high condition to near the end of life. Because most individuals in natural populations of such species die of aging‐related causes, these populations likely harbor little genetic variation for mechanisms that could extend life further, or these mechanisms are very costly. This, and the apparent evolutionary conservatism in the rate of increase in mortality with age, suggests that variation in the rate of senescence reflects fundamental changes in organism structure, likely associated with the rate of development, rather than physiological or biochemical processes influenced by a few genes. Understanding these evolved differences between long‐lived and short‐lived organisms would seem to be an essential foundation for designing therapeutic interventions with respect to human aging and longevity.     

To breed or not to breed: a model of partial migration

Migration is used by a number of species as a strategy for dealing with a seasonally variable environment. In many migratory species, only some individuals migrate within a given season (migrants) while the rest remain in the same location (residents), a phenomenon called ‘partial migration’. Most examples of partial migration considered in the literature (both empirically and theoretically) fall into one of two categories: either species where residents and migrants share a breeding ground and winter apart, or species where residents and migrants share an overwintering ground and breed apart. However, a third form of partial migration can occur when non‐migrating individuals actually forgo reproduction, essentially a special form of low‐frequency reproduction. While this type of partial migration is well documented in many taxa, it is not often included in the partial migration literature, and has not been considered theoretically to date. In this paper we present a model for this partial migration scenario and determine under what conditions an individual should skip a breeding opportunity (resulting in partial migration), and under what conditions individuals should breed every chance they get (resulting in complete migration). In a constant environment, we find that partial migration is expected to occur when the mortality cost of migration is high, and when individuals can greatly increase their fecundity by skipping a year before breeding. In a stochastic environment, we find that an individual should skip migration more frequently with increased risk of a bad year (higher probability and severity), with higher mortality cost of migration, and with lower mortality cost of skipping. We discuss these results in the context of empirical data and existing life history theory.     

Hematocrit,age, and survival in a wild vertebrate population

Understanding trade‐offs in wild populations is difficult, but important if we are to understand the evolution of life histories and the impact of ecological variables upon them. Markers that reflect physiological state and predict future survival would be of considerable benefit to unraveling such trade‐offs and could provide insight into individual variation in senescence. However, currently used markers often yield inconsistent results. One underutilized measure is hematocrit, the proportion of blood comprising erythrocytes, which relates to the blood's oxygen‐carrying capacity and viscosity, and to individual endurance. Hematocrit has been shown to decline with age in cross‐sectional studies (which may be confounded by selective appearance/disappearance). However, few studies have tested whether hematocrit declines within individuals or whether low hematocrit impacts survival in wild taxa. Using longitudinal data from the Seychelles warbler (Acrocephalus sechellensis), we demonstrated that hematocrit increases with age in young individuals (<1.5 years) but decreases with age in older individuals (1.5–13 years). In breeders, hematocrit was higher in males than females and varied relative to breeding stage. High hematocrit was associated with lower survival in young individuals, but not older individuals. Thus, while we did not find support for hematocrit as a marker of senescence, high hematocrit is indicative of poor condition in younger individuals. Possible explanations are that these individuals were experiencing dehydration and/or high endurance demands prior to capture, which warrants further investigation. Our study demonstrates that hematocrit can be an informative metric for life‐history studies investigating trade‐offs between survival, longevity, and reproduction.     

Comparing individual and population measures of senescence across 10 years in a wild insect population

Declines in survival and performance with advancing age (senescence) have been widely documented in natural populations, but whether patterns of senescence across traits reflect a common underlying process of biological ageing remains unclear. Senescence is typically characterized via assessments of the rate of change in mortality with age (actuarial senescence) or the rate of change in phenotypic performance with age (phenotypic senescence). Although both phenomena are considered indicative of underlying declines in somatic integrity, whether actuarial and phenotypic senescence rates are actually correlated has yet to be established. Here we present evidence of both actuarial and phenotypic senescence from a decade‐long longitudinal field study of wild insects. By tagging every individual and using continuous video monitoring with a network of up to 140 video cameras, we were able to record survival and behavioral data on an entire adult population of field crickets. This reveals that both actuarial and phenotypic senescence vary substantially across 10 annual generations. This variation allows us to identify a strong correlation between actuarial and phenotypic measures of senescence. Our study demonstrates age‐related phenotypic declines reflected in population level mortality rates and reveals that observations of senescence in a single year may not be representative of a general pattern.     

Fat tissue,aging, and cellular senescence

Fat tissue, frequently the largest organ in humans, is at the nexus of mechanisms involved in longevity and age‐related metabolic dysfunction. Fat distribution and function change dramatically throughout life. Obesity is associated with accelerated onset of diseases common in old age, while fat ablation and certain mutations affecting fat increase life span. Fat cells turn over throughout the life span. Fat cell progenitors, preadipocytes, are abundant, closely related to macrophages, and dysdifferentiate in old age, switching into a pro‐inflammatory, tissue‐remodeling, senescent‐like state. Other mesenchymal progenitors also can acquire a pro‐inflammatory, adipocyte‐like phenotype with aging. We propose a hypothetical model in which cellular stress and preadipocyte overutilization with aging induce cellular senescence, leading to impaired adipogenesis, failure to sequester lipotoxic fatty acids, inflammatory cytokine and chemokine generation, and innate and adaptive immune response activation. These pro‐inflammatory processes may amplify each other and have systemic consequences. This model is consistent with recent concepts about cellular senescence as a stress‐responsive, adaptive phenotype that develops through multiple stages, including major metabolic and secretory readjustments, which can spread from cell to cell and can occur at any point during life. Senescence could be an alternative cell fate that develops in response to injury or metabolic dysfunction and might occur in nondividing as well as dividing cells. Consistent with this, a senescent‐like state can develop in preadipocytes and fat cells from young obese individuals. Senescent, pro‐inflammatory cells in fat could have profound clinical consequences because of the large size of the fat organ and its central metabolic role.     

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.     

Senescence rates are determined by ranking on the fast-slow life-history continuum

Comparative analyses of survival senescence by using life tables have identified generalizations including the observation that mammals senesce faster than similar-sized birds. These generalizations have been challenged because of limitations of life-table approaches and the growing appreciation that senescence is more than an increasing probability of death. Without using life tables, we examine senescence rates in annual individual fitness using 20 individual-based data sets of terrestrial vertebrates with contrasting life histories and body size. We find that senescence is widespread in the wild and equally likely to occur in survival and reproduction. Additionally, mammals senesce faster than birds because they have a faster life history for a given body size. By allowing us to disentangle the effects of two major fitness components our methods allow an assessment of the robustness of the prevalent life-table approach. Focusing on one aspect of life history – survival or recruitment – can provide reliable information on overall senescence.     

Stabilizing survival selection on presenescent expression of a sexual ornament followed by a terminal decline

Senescence is a decrease in functional capacity, increasing mortality rate with age. Sexual signals indicate functional capacity, because costs of ornamentation ensure signal honesty, and are therefore expected to senesce, tracking physiological deterioration and mortality. For sexual traits, mixed associations with age and positive associations with life expectancy have been reported. However, whether these associations are caused by selective disappearance and/or within‐individual senescence of sexual signals, respectively, is not known. We previously reported that zebra finches with redder bills had greater life expectancy, based on a single bill colour measurement per individual. We here extend this analysis using longitudinal data and show that this finding is attributable to terminal declines in bill redness in the year before death, with no detectable change in presenescent redness. Additionally, there was a quadratic relationship between presenescent bill colouration and survival: individuals with intermediate bill redness have maximum survival prospects. This may reflect that redder individuals overinvest in colouration and/or associated physiological changes, while below‐average bill redness probably reflects poorer phenotypic quality. Together, this pattern suggests that bill colouration is defended against physiological deterioration, because of mate attraction benefits, or that physiological deterioration is not a gradual process, but accelerates sharply prior to death. We discuss these possibilities in the context of the reliability theory of ageing and sexual selection.     

Age at the onset of senescence in birds and mammals is predicted by early-life performance

Life-history theory predicts that traits involved in maturity, reproduction and survival correlate along a fast–slow continuum of life histories. Evolutionary theories and empirical results indicate that senescence-related traits vary along this continuum, with slow species senescing later and at a slower pace than fast species. Because senescence patterns are typically difficult to estimate from studies in the wild, here we propose to predict the associated trait values in the frame of life-history theory. From a comparative analysis based on 81 free-ranging populations of 72 species of birds and mammals, we find that a nonlinear combination of fecundity, age at first reproduction and survival over the immature stage can account for ca two-thirds of the variance in the age at the onset of actuarial senescence. Our life-history model performs better than a model predicting the onset based on generation time, and it only includes life-history traits during early life as explanatory variables, i.e. parameters that are both theoretically expected to shape senescence and are measurable within relatively short studies. We discuss the good-fit of our life-history model to the available data in the light of current evolutionary theories of senescence. We further use it to evaluate whether studies that provided no evidence for senescence lasted long enough to include the onset of senescence.     

Equal nonbreeding period survival in adults and juveniles of a long‐distant migrant bird

In migrant birds, survival estimates for the different life‐history stages between fledging and first breeding are scarce. First‐year survival is shown to be strongly reduced compared with annual survival of adult birds. However, it remains unclear whether the main bottleneck in juvenile long‐distant migrants occurs in the postfledging period within the breeding ranges or en route. Quantifying survival rates during different life‐history stages and during different periods of the migration cycle is crucial to understand forces driving the evolution of optimal life histories in migrant birds. Here, we estimate survival rates of adult and juvenile barn swallows (Hirundo rustica L.) in the breeding and nonbreeding areas using a population model integrating survival estimates in the breeding ranges based on a large radio‐telemetry data set and published estimates of demographic parameters from large‐scale population‐monitoring projects across Switzerland. Input parameters included the country‐wide population trend, annual productivity estimates of the double‐brooded species, and year‐to‐year survival corrected for breeding dispersal. Juvenile survival in the 3‐week postfledging period was low (S = 0.32; SE = 0.05), whereas in the rest of the annual cycle survival estimates of adults and juveniles were similarly high (S > 0.957). Thus, the postfledging period was the main survival bottleneck, revealing the striking result that nonbreeding period mortality (including migration) is not higher for juveniles than for adult birds. Therefore, focusing future research on sources of variation in postfledging mortality can provide new insights into determinants of population dynamics and life‐history evolution of migrant birds.     

Age‐specific reproduction and disposable soma in an urban population of Common Blackbirds Turdus merula

The mechanism of senescence is an important subject of current research, but our knowledge of the factors influencing the rate of ageing in naturally occurring populations remains rudimentary. Evolutionary theories of senescence predict that investment in reproduction in early life should come at the cost of reduced somatic maintenance and thus result in earlier or more rapid senescence. We use data on the complete reproductive histories of 431 Common Blackbirds (222 males and 209 females) collected during a 19‐year study of the ecology of an urban population of this species to test the main hypotheses addressing the issue of senescence. On average, the birds in this population survived for 3.7 (± 1.9 sd) years. Reproductive success in females peaked at the age of 4, but in males remained stable until the 5th year of life. We observed declines in reproductive success, indicative of senescence, after the peak years in both sexes. The mechanism of age‐related changes in the reproduction of females confirms the individual improvement and selective disappearance hypotheses. In the case of males, the increase in reproductive performance comes as a consequence of the disappearance of poor reproducers. The parental investment associated with early life fecundity (the first two breeding seasons in males and females) impairs the breeding success of females later on. Contrary to expectations, there was no negative impact of high early life fecundity on either mortality or lifespan. Individuals of both sexes with a high early life fecundity had a higher lifetime reproductive success than those in which early life fecundity was low. Hence, the most profitable strategy is to maximize reproductive effort in the early stages of life. This yields the highest lifetime reproductive success, despite the increased impact of senescence, especially in females. These results are consistent with the disposable soma hypothesis.     

Retired flies,hidden plateaus,and the evolution of senescence in Drosophila melanogaster

Late‐life plateaus in age‐specific mortality have been an evolutionary and biodemographic puzzle for decades. Although classic theory on the evolution of senescence predicts late‐life walls of death, observations in experimental organisms document the opposite trend: a slowing in the rate of increase of mortality at advanced ages. Here, I analyze published life‐history data on individual Drosophila melanogaster females and argue for a fundamental change in our understanding of mortality in this important model system. Mortality plateaus are not, as widely assumed, exclusive to late life, and are not explained by population heterogeneity—they are intimately connected to individual fecundity. Female flies begin adult life in the working stage, a period of active oviposition and low but accelerating mortality. Later they transition to the retired stage, a terminal period characterized by limited fecundity and relatively constant mortality. Because ages of transition differ between flies, age‐synchronized cohorts contain a mix of working and retired flies. Early‐ and mid‐life plateaus are obscured by the presence of working flies, but can be detected when cohorts are stratified by retirement status. Stage‐specificity may be an important component of Drosophila life‐history evolution.     

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.