Evolution of senescence: Influence of age-dependent death rates on the natural increase of a hypothetical population

A hypothetical population is characterized by functions of age which describe its longevity and its maternity rate. Solution of the renewal equation for the birth rate of the population yields a characteristic equation which, in contradiction to the results of previous studies, may have more than one real root. The largest real root of the characteristic equation is the rate of natural increase, r, of the population and is used as a measure of its selective advantage.The maternity rate is represented by a rising or falling exponential function of age. Longevity is represented by a series each term of which has the form of a gamma distribution function. As the number of terms increases, the mean longevity remains constant, but the function becomes progressively more rectangular in shape; the early death rate declines, while the death rate in old age increases. Unless the reproductive fraction is small, each such decrease in the youthful death rate more than compensates for the corresponding increase in old age and causes an increment in r which is interpreted as a step toward the evolution of senescence. Although the degree of change in r attendant upon a change in the age-dependency of the death rate is related to the initial value of the maternity function, it is not influenced by the age dependency of the maternity function.     

Sociality, age at first reproduction and senescence: comparative analyses of birds

Evolutionary theories of senescence suggest that aging evolves as a consequence of early reproduction imposing later viability costs, or as a consequence of weak selection against mutations that act late in life. In addition, highly social species that live in sites that are protected from extrinsic mortality due to predation should senesce at a slower rate than solitary species. Therefore, species that start reproducing late in life should senesce at a slower rate than species that start reproducing early. In addition, social species should senesce more slowly than solitary species. Here I investigate the rate of senescence using an extensive data set on longevity records under natural field conditions to test predictions about the evolution of senescence among 271 species of birds. Longevity records increased with sampling effort and body mass, but once these confounding variables were controlled statistically, there was a strongly positive relationship between relative longevity and relative adult survival rate. Relative longevity after controlling statistically for sampling effort, body mass and adult survival rate, increased with age at first reproduction, but not with degree of breeding sociality. These findings suggest that the evolution of senescence is related to timing of first reproduction, but that the evolution of breeding sociality has played a negligible role in the evolution of senescence.     

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.     

Evidence for a genetic basis of aging in two wild vertebrate populations

Aging, or senescence, defined as a decline in physiological function with age, has long been a focus of research interest for evolutionary biologists. How has natural selection failed to remove genetic effects responsible for such reduced fitness among older individuals? Current evolutionary theory explains this phenomenon by showing that, as a result of the risk of death from environmental causes that individuals experience, the force of selection inevitably weakens with age. This in turn means that genetic mutations having detrimental effects that are only felt late in life might persist in a population. Although widely accepted, this theory rests on the assumption that there is genetic variation for aging in natural systems, or (equivalently), that genotype-by-age interactions (GxA) occur for fitness. To date, empirical support for this assumption has come almost entirely from laboratory studies on invertebrate systems, most notably Drosophila and C. elegans, whereas tests of genetic variation for aging are largely lacking from natural populations. By using data from two wild mammal populations, we perform quantitative genetic analyses of fitness and provide the first evidence for a genetic basis of senescence to come from a study in the natural environment. We find evidence that genetic differences among individuals cause variation in their rates of aging and that additive genetic variance for fitness increases with age, as predicted by the evolutionary theory of senescence.     

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.     

Reproductive senescence in a long-lived seabird: rates of decline in late-life performance are associated with varying costs of early reproduction

Evolutionary theories of senescence predict that rates of decline in performance parameters should be shaped by early-life trade-offs between reproduction and somatic maintenance. Here we investigate factors influencing the rate of reproductive senescence in a long-lived seabird, the common guillemot Uria aalge, using data collected over a 23-year period. In the last 3 years of life, individual guillemots had significantly reduced breeding success and were less likely to hold a site or attempt to breed. Females senesced at a significantly faster rate than males. At the individual level, high levels of reproductive output earlier in life were associated with increased senescence later in life. This trade-off between early- and late-life reproduction was evident independent of the fact that as birds age, they breed later in the season. The rate of senescence was additionally dependent on environmental conditions experienced earlier in life, with evidence that harsh conditions amplified later declines in breeding success. Overall, individuals with intermediate levels of early-life productivity lived longer. These results provide support for the antagonistic-pleiotropy and disposable-soma theories of senescence and demonstrate for the first time in a wild bird population that increased rates of senescence in reproductive performance are associated with varying costs of reproduction early in life.     

The impact of reproductive investment and early‐life environmental conditions on senescence: support for the disposable soma hypothesis

Several hypotheses have been put forward to explain the evolution of senescence. One of the leading hypotheses, the disposable soma hypothesis, predicts a trade‐off, whereby early‐life investment in reproduction leads to late‐life declines in survival (survival senescence). Testing this hypothesis in natural populations is challenging, but important for understanding the evolution of senescence. We used the long‐term data set from a contained, predator‐free population of individually marked Seychelles warblers (Acrocephalus sechellensis) to investigate how age‐related declines in survival are affected by early‐life investment in reproduction and early‐life environmental conditions. The disposable soma hypothesis predicts that higher investment in reproduction, or experiencing harsh conditions during early life, will lead to an earlier onset, and an increased rate, of senescence. We found that both sexes showed similar age‐related declines in late‐life survival consistent with senescence. Individuals that started breeding at a later age showed a delay in survival senescence, but this later onset of breeding did not result in a less rapid decline in late‐life survival. Although survival senescence was not directly related to early‐life environmental conditions, age of first breeding increased with natal food availability. Therefore, early‐life food availability may affect senescence by influencing age of first breeding. The disposable soma hypothesis of senescence is supported by delayed senescence in individuals that started breeding at a later age and therefore invested less in reproduction.     

The contribution of longevity to population death rates

The magnitude of a population's per capita death rate depends on the maximum age at death and the intensity or schedule of mortality of its members. Knowing the maximum possible lifespan that an animal can achieve when raised under defined conditions makes it possible to calculate the component of per capita death rate due to longevity alone. This component is most important to slow-growing populations of animals with relatively short lifespans. Life-table experiments with two rotifer species and a cladoceran indicate that the short lifespans of these animals account for moderate proportions (up to 37.2%) of their population death rates. Decomposing per capita death rates into two components, one due to maximum length of life and another due to differential mortality of animals of different ages, may therefore be a useful way to examine how deleterious processes, such as predation and starvation, limit growth of zooplankton populations.     

Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women

Evolutionary theory of senescence emphasizes the importance of intense selection on early reproduction owing to the declining force of natural selection with age that constrains lifespan. In humans, recent studies have, however, suggested that late-life mortality might be more closely related to late rather than early reproduction, although the role of late reproduction on fitness remains unclear. We examined the association between early and late reproduction with longevity in historical post-reproductive Sami women. We also estimated the strength of natural selection on early and late reproduction using path analysis, and the effect of reproductive timing on offspring survival to adulthood and maternal risk of dying at childbirth. We found that natural selection favoured both earlier start and later cessation of reproduction, and higher total fecundity. Maternal age at childbirth was not related to offspring or maternal survival. Interestingly, females who produced their last offspring at advanced age also lived longest, while age at first reproduction and total fecundity were unrelated to female longevity. Our results thus suggest that reproductive and somatic senescence may have been coupled in these human populations, and that selection could have favoured late reproduction. We discuss alternative hypotheses for the mechanisms which might have promoted the association between late reproduction and longevity.     

Mortality rates of wild boar Sus scrofa L. in central Europe

In many parts of Europe, wild boar Sus scrofa population increase, and thus, high densities and dispersal into new areas are accompanied by economic problems. Due to many factors like insufficient hunting strategies as well as underestimation of population densities and reproduction rates, harvest rates seem to be insufficient. Thus, we calculated mortality rates of several wild boar populations from 1998 to 2009, to show the efficiency of hunting within several studies distributed over eight European states. For calculating mortality rates, the daily probability of survival of radio telemetrically observed wild boar was analysed according to Mayfield (Wilson Bull 73:255-261, 1961) and with survival analysis in R for three age classes (0, 1, ≥2 years) and both sexes. The mortality rates of wild boar per annum, especially piglets, were comparably low (about 0.5 for piglets and similar for total population). About three third of all observed animals survived at least until the next period of reproduction. Mortality rates differed between some study areas, the sexes and age classes. The sex ratio of the shot piglets equals the sex ratio of captured piglets; there seems to be no sex-biased hunting in this age class, but in an older age. Shooting was the main cause of death; only very few animals died by natural causes, e.g. diseases. The comparative analysis of all studies reflects a low mortality of wild boar in highly productive populations. Our results certified the findings of several studies that predation, natural mortality, and road mortality have only small impact on wild boar populations, whereas especially, nutrition or hunting are mainly decisive. Assuming net reproduction rates of more than 200 % according to literature data, our results indicate that harvest rates are not sufficient at our study sites. In all our studies, mortality rates and, thus, harvest rates are less than the assumed total net reproduction. Especially, the harvest rate of piglets seems to be insufficient. Thus, the population will increase further. High reproduction has to be counteracted by regulating mainly the reproductive animals. For regulating a population, combined and effective hunting methods have to be conducted to harvest at least the net reproduction. Thus, we recommend higher hunting rates of piglets (80 % of the offspring should be harvested) and of adult females. Intensified hunting of piglets by drive hunts and at an early age as well as intensified single hunt on adult females might help regulating wild boar populations.     

Do Insect Populations Die at Constant Rates as They Become Older? Contrasting Demographic Failure Kinetics with Respect to Temperature According to the Weibull Model

Temperature implies contrasting biological causes of demographic aging in poikilotherms. In this work, we used the reliability theory to describe the consistency of mortality with age in moth populations and to show that differentiation in hazard rates is related to extrinsic environmental causes such as temperature. Moreover, experiments that manipulate extrinsic mortality were used to distinguish temperature-related death rates and the pertinence of the Weibull aging model. The Newton-Raphson optimization method was applied to calculate parameters for small samples of ages at death by estimating the maximum likelihoods surfaces using scored gradient vectors and the Hessian matrix. The study reveals for the first time that the Weibull function is able to describe contrasting biological causes of demographic aging for moth populations maintained at different temperature regimes. We demonstrate that at favourable conditions the insect death rate accelerates as age advances, in contrast to the extreme temperatures in which each individual drifts toward death in a linear fashion and has a constant chance of passing away. Moreover, slope of hazard rates shifts towards a constant initial rate which is a pattern demonstrated by systems which are not wearing out (e.g. non-aging) since the failure, or death, is a random event independent of time. This finding may appear surprising, because, traditionally, it was mostly thought as rule that in aging population force of mortality increases exponentially until all individuals have died. Moreover, in relation to other studies, we have not observed any typical decelerating aging patterns at late life (mortality leveling-off), but rather, accelerated hazard rates at optimum temperatures and a stabilized increase at the extremes.In most cases, the increase in aging-related mortality was simulated reasonably well according to the Weibull survivorship model that is applied. Moreover, semi log- probability hazard rate model illustrations and maximum likelihoods may be usefully in defining periods of mortality leveling off and provide clear evidence that environmental variability may affect parameter estimates and insect population failure rate. From a reliability theory standpoint, failure rates vary according to a linear function of age at the extremes indicating that the life system (i.e., population) is able to eliminate earlier failure and/or to keep later failure rates constant. The applied model was able to identify the major correlates of extended longevity and to suggest new ideas for using demographic concepts in both basic and applied population biology and aging.     

THE ZOOLOGICAL SOCIETY OF LONDON STAMFORD RAFFLES LECTURE 1996 From Gaia to Noah: human responsibilities in nature

Life-table data of 56 natural populations of mammals were analysed, modelling mortality rate as a three-phase step function of age (the step model ) instead of using the Gompertz model. In the step model, mortality rale is constant in each phase. The phases correspond to juveniles and young and old adults. The age of transition between young and old adults is referred to as the age of senescence. This approach has the advantages that, for the first time, the age of senescence is identified objectively using a robust statistical procedure, and that young adult mortality rates are estimated without bias since no assumption is made about how adult mortality rate changes with age. A further statistical problem solved here that has previously caused difficulty is that of correctly accounting for the different levels of precision in data from different age classes.
Significant changes ( P < 0.05) in adult mortality rate with age were found in 27 out of 56 populations. In 23 of these 27 cases, adult mortality rate increased with age. Juvenile mortality rate differed significantly from young adult mortality rate in 21 cases; in 18 of these the rate for juveniles was higher. These results are discussed in relation to earlier analyses, in particular that of Promislow (1991).     

Hazard rates and causes of death in a captive group of crab-eating monkeys (Macaca fascicularis)

In an attempt to examine possible associations between stages of agespecific mortality and various causes of death, vital records of 159 male and 192 female crab-eating monkeys (Macaca fascicularis), housed as a single group, were analyzed. Survival and hazard rates associated with each of five distinct categories of causes of death were estimated for males and females, using the nonparametric kernel method. The obtained overall survival and hazard functions were similar to those reported previously for rhesus monkeys. Among two stages identified in age-specific mortality, the first stage, characterized by rapidly decreasing hazard rates up to about 1.5–2 years of age, was discriminated by the occurrence of deaths due to unfitness for postnatal life. The second stage lasted up to the age of 10–15 years and was largely characterized by a high incidence of violent deaths. The respective hazard rates in males and females attained peaks during the early reproductive period of life and markedly decreased thereafter. This pattern was interpreted to indicate that second stage mortality is unlikely related to senescence, but rather, seems to depend on extrinsic environmental factors. Thus, when considering overall hazard rates in Macaca fascicularis, the onset of senescence, as a result of the specific aspects of simian reproduction, may be hidden from view, and mortality due to aging may only be appreciable after 10 to 15 years of age. © 1993 Wiley-Liss, Inc.     

When can a clonal organism escape senescence?

Abstract Some clonal organisms may live for thousands of years and show no signs of senescence, while others consistently die after finite life spans. Using two models, we examined how stage-specific life-history rates of a clone's modules determine whether a genetic individual escapes senescence by replacing old modules with new ones. When the rates of clonal or sexual reproduction and survival of individual modules decline with age, clones are more likely to experience senescence. In addition, the models predict that there is a greater tendency to find senescence in terms of a decline in the rate of sexual reproduction with clone age than in terms of an increase in the probability of clone mortality, unless rates of sexual reproduction increase dramatically with module stage. Using a matrix model modified to represent the clonal lifestyle, we show how a trade-off between sexual and clonal reproduction could result in selection for or against clonal senescence. We also show that, in contrast to unitary organisms, the strength of selection on life-history traits can increase with the age of a clone even in a growing population, countering the evolution of senescence.     

Variation in Male Reproductive Longevity across Traditional Societies

Most accounts of human life history propose that women have short reproductive spans relative to their adult lifespans, while men not only remain fertile but carry on reproducing until late life. Here we argue that studies have overlooked evidence for variation in male reproductive ageing across human populations. We apply a Bayesian approach to census data from Agta hunter-gatherers and Gambian farmers to show that long post-reproductive lifespans characterise not only women but also males in some traditional human populations. We calculate three indices of reproductive ageing in men (oldest age at reproduction, male late-life reproduction, and post-reproductive representation) and identify a continuum of male reproductive longevity across eight traditional societies ranging from !Kung, Hadza and Agta hunter-gatherers exhibiting low levels of polygyny, early age at last reproduction and long post-reproductive lifespans, to male Gambian agriculturalists and Turkana pastoralists showing higher levels of polygyny, late-life reproduction and shorter post-reproductive lifespans. We conclude that the uniquely human detachment between rates of somatic senescence and reproductive decline, and the existence of post-reproductive lifespans, are features of both male and female life histories, and therefore not exclusive consequences of menopause.     

OPTIMALITY THEORY,GOMPERTZ' LAW,AND THE DISPOSABLE SOMA THEORY OF SENESCENCE

The “disposable soma” theory for the evolution of senescence suggests that senescence arises from an optimal balancing of resources between reproduction and somatic repair. Dynamic programming models are constructed and analyzed to determine the optimal relationship between reproduction, diversion of resources from repair, and added senescent mortality. Of particular interest is the relationship between the repair-reproduction trade-off and the form of the mortality-rate-versus-age curve predicted. The models analyzed in the greatest detail assume that the relationship between reproduction and added senescent mortality does not change with age. These suggest that mortality should increase at an increasing rate with age, but may approach a linear rate as mortality becomes very high. General results are derived for the shape of the mortality curves early and late in the senescing part of the life span, and mortality curves for specific trade-off functions are illustrated. An exponential increase in death rate with age (Gompertz' Law) corresponds to only one of many possible relationships between reproduction and aging. The “Law” is unlikely to hold generally if the disposable soma theory accounts for a large fraction of the observed senescent increase in mortality with age. However, support for the generality of Gompertz' Law is weak, and other theories have not produced an evolutionary explanation for the law. The disposable soma theory is consistent with some of the exceptions to Gompertz' Law that have been observed.     

Lifespan is unrelated to investment in reproduction in populations of mammals and birds in captivity

We examined the relationship between number of offspring produced to a certain age and subsequent longevity in captive zoo populations of 18 species of mammal and 12 species of bird. The age cut-offs in each analysis were set to include 50%, 75% and 90% of the offspring produced in each of the population samples. Only one of 68 regressions was significant, and its slope was positive. In addition, we examined the relationship between age at first reproduction up to a certain age and longevity after that age, generally 5 years (3–8), among 17 species of mammal and 12 species of bird. Only one of these regressions had a significantly positive slope, indicating that early reproduction rarely reduces lifespan. Overall, we found no evidence that producing offspring in a zoo environment influences the age at death. Thus, although trade-offs might apply in natural populations under resource limitation, neither pregnancy, growth of the foetus and lactation in mammals, nor egg production in birds, reduces lifespan in the absence of such stress. If genetically based or other intrinsic antagonistic pleiotropy underlies the evolution of senescence, it was not evident in our analyses.     

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.     

On the process of stabilization in the renewal model: approximations for the time to convergence

The transient behaviour of the renewal model leading to the stable age distribution is studied for weakly skewed net maternity functions (found in human as well as in some animal populations). The study, which is partly based on heuristic arguments, first provides approximate expressions for the damping constant and the circular frequency (in terms of the moments of the net maternity function) belonging to the principal oscillatory component of the birth trajectory. The time to stability (defined as the time interval after which the principal oscillatory component has become less than a certain fraction of the stable solution) is then determined in two cases: For the genesis model and for a stable population in which the net reproduction rate is reduced to one. The results are applied to a problem which arises in the mass rearing of pest insects.     

The Evolution of Senescence and Post-Reproductive Lifespan in Guppies (Poecilia reticulata)

The study of post-reproductive lifespan has been of interest primarily with regard to the extended post-menopausal lifespan seen in humans. This unusual feature of human demography has been hypothesized to have evolved because of the “grandmother” effect, or the contributions that post-reproductive females make to the fitness of their children and grandchildren. While some correlative analyses of human populations support this hypothesis, few formal, experimental studies have addressed the evolution of post-reproductive lifespan. As part of an ongoing study of life history evolution in guppies, we compared lifespans of individual guppies derived from populations that differ in their extrinsic mortality rates. Some of these populations co-occur with predators that increase mortality rate, whereas other nearby populations above barrier waterfalls are relatively free from predation. Theory predicts that such differences in extrinsic mortality will select for differences in the age at maturity, allocation of resources to reproduction, and patterns of senescence, including reproductive declines. As part of our evaluation of these predictions, we quantified differences among populations in post-reproductive lifespan. We present here the first formal, comparative study of the evolution of post-reproductive lifespan as a component of the evolution of the entire life history. Guppies that evolved with predators and that experienced high extrinsic mortality mature at an earlier age but also have longer lifespans. We divided the lifespan into three non-overlapping components: birth to age at first reproduction, age at first reproduction to age at last reproduction (reproductive lifespan), and age at last reproduction to age at death (post-reproductive lifespan). Guppies from high-predation environments live longer because they have a longer reproductive lifespan, which is the component of the life history that can make a direct contribution to individual fitness. We found no differences among populations in post-reproductive lifespan, which is as predicted since there can be no contribution of this segment of the life history to an individual's fitness. Prior work on the evolution of post-reproductive lifespan has been dominated by speculation and correlative analyses. We show here that this component of the life history is accessible to formal study as part of experiments that quantify the different segments of an individual's life history. Populations of guppies subject to different mortality pressures from predation evolved differences in total lifespan, but not in post-reproductive lifespan. Rather than showing the direct effects of selection characterizing other life-history traits, post-reproductive lifespan in these fish appears to be a random add-on at the end of the life history. These findings support the hypothesis that differences in lifespan evolving in response to selection are confined to the reproductive lifespan, or those segments of the life history that make a direct contribution to fitness. We also show, for the first time, that fish can have reproductive senescence and extended post-reproductive lifespans despite the general observation that they are capable of producing new primary oocytes throughout their lives.