The song of the old mother: Reproductive senescence in female drosophila

Among animals with multiple reproductive episodes, changes in adult condition over time can have profound effects on lifetime reproductive fitness and offspring performance. The changes in condition associated with senescence can be particularly acute for females who support reproductive processes from oogenesis through fertilization. The pomace fly Drosophila melanogaster is a well-established model system for exploring the physiology of reproduction and senescence. In this review, we describe how increasing maternal age in Drosophila affects reproductive fitness and offspring performance as well as the genetic foundation of these effects. Describing the processes underlying female reproductive senescence helps us understand diverse phenomena including population demographics, condition-dependent selection, sexual conflict, and transgenerational effects of maternal condition on offspring fitness. Understanding the genetic basis of reproductive senescence clarifies the nature of life-history trade-offs as well as potential ways to augment and/or limit female fertility in a variety of organisms.     

The song of the old mother: Reproductive senescence in female drosophila

Among animals with multiple reproductive episodes, changes in adult condition over time can have profound effects on lifetime reproductive fitness and offspring performance. The changes in condition associated with senescence can be particularly acute for females who support reproductive processes from oogenesis through fertilization. The pomace fly Drosophila melanogaster is a well-established model system for exploring the physiology of reproduction and senescence. In this review, we describe how increasing maternal age in Drosophila affects reproductive fitness and offspring performance as well as the genetic foundation of these effects. Describing the processes underlying female reproductive senescence helps us understand diverse phenomena including population demographics, condition-dependent selection, sexual conflict, and transgenerational effects of maternal condition on offspring fitness. Understanding the genetic basis of reproductive senescence clarifies the nature of life-history trade-offs as well as potential ways to augment and/or limit female fertility in a variety of organisms.     

The force of selection on the human life cycle

In this article, I present evidence for a robust and quite general force of selection on the human life cycle. The force of selection acts in remarkably invariant ways on human life histories, despite a great abundance of demographic diversity. Human life histories are highly structured, with mortality and fertility changing substantially through the life cycle. This structure necessitates the use of structured population models to understand human life history evolution. Using such structured models, I find that the vital rates to which fitness is most sensitive are prereproductive survival probabilities, particularly the survival of children ages 0 to 4 years. The fact that the preponderance of selection falls on transitions related to recruitment combined with the late age at first reproduction characteristic of the human life cycle creates a fitness bottleneck out of recruitment. Because of this, antagonistic pleiotropy with any trait that detracts from the constituent transitions to recruitment is expected. I explore the predictors of variation in the force of selection on early survival. High fertility increases the selective premium placed on early survivorship, whereas high life expectancy at birth decreases it.     

Human life histories and the demographic transition: a case study from Finland, 1870-1949

The life histories of humans who were engaged in reproduction during the demographic transition were investigated. It was discovered that these life histories were subject to great changes during the period involving the birth cohorts from the years 1870-1949. Although the number of all and surviving children decreased during this period, the individual fitness values (lambda) of females remained quite even. The lambda values are sensitive not only to reproductive quantity but also to the timing of reproduction. Therefore, the effective change in female fitness during the demographic transition may not be as dramatic as previously thought. When studying the level of selection (or rather the opportunity for selection), it was found that mortality selection steadily decreased to a very low level. However, fertility selection and total selection, which were relatively low for the cohorts 1870-1889, increased before the steep decrease that was detected for the cohorts 1930-1949. The situation reflects the presence of considerable variance in fertility for the cohorts 1890-1929, when the mean fertility was decreasing. A previously found trade-off between female longevity and reproductive success appeared less significant, apparently due to the presence of more plentiful resources and voluntary limitation of reproduction. The deviation from the potential fitness maximization and the presence of subfertility have become prevalent in human populations.     

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

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

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.     

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.     

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.     

Early-life reproduction is associated with increased mortality risk but enhanced lifetime fitness in pre-industrial humans

The physiology of reproductive senescence in women is well understood, but the drivers of variation in senescence rates are less so. Evolutionary theory predicts that early-life investment in reproduction should be favoured by selection at the cost of reduced survival and faster reproductive senescence. We tested this hypothesis using data collected from preindustrial Finnish church records. Reproductive success increased up to age 25 and was relatively stable until a decline from age 41. Women with higher early-life fecundity (ELF; producing more children before age 25) subsequently had higher mortality risk, but high ELF was not associated with accelerated senescence in annual breeding success. However, women with higher ELF experienced faster senescence in offspring survival. Despite these apparent costs, ELF was under positive selection: individuals with higher ELF had higher lifetime reproductive success. These results are consistent with previous observations in both humans and wild vertebrates that more births and earlier onset of reproduction are associated with reduced survival, and with evolutionary theory predicting trade-offs between early reproduction and later-life survival. The results are particularly significant given recent increases in maternal ages in many societies and the potential consequences for offspring health and fitness.     

Age-specific fitness components and their temporal variation in the barn owl

Theory predicts that temporal variability plays an important role in the evolution of life histories, but empirical studies evaluating this prediction are rare. In constant environments, fitness can be measured by the population growth rate lambda, and the sensitivity of lambda to changes in fitness components estimates selection on these traits. In variable environments, fitness is measured by the stochastic growth rate lambda(S), and stochastic sensitivities estimate selection pressure. Here we examine age-specific schedules for reproduction and survival in a barn owl population (Tyto alba). We estimated how temporal variability affected fitness and selection, accounting for sampling variance. Despite large sample sizes of old individuals, we found no strong evidence for senescence. The most variable fitness components were associated with reproduction. Survival was less variable. Stochastic simulations showed that the observed variation decreased fitness by about 30%, but the sensitivities of lambda and lambda(S) to changes in all fitness components were almost equal, suggesting that temporal variation had negligible effects on selection. We obtained these results despite high observed variability in the fitness components and relatively short generation time of the study organism, a situation in which temporal variability should be particularly important for natural selection and early senescence is expected.     

Evolution of indefinite generation lengths

Intrinsic mortality at relatively advanced age results from natural selection favouring early reproduction. When individuals produce many and early offspring, costs are incurred due to the accumulation of pleiotropic mutations with adverse effects late in life, which make senescence an inevitable result of evolution. However, a few organisms exist with seemingly indefinite generation lengths. This paper identifies conditions of life history and ecology under which natural selection favours continually reducing intrinsic mortality. The analysis considers the particular case of populations held at carrying capacity by density dependence suppressing net fertility, acting either on fecundity equally across fecund ages or on juvenile mortality up to the first fecund age. This broad category of density dependence increases the susceptibility of populations to invasion by mutations that extend net fertility into later life. Whether a population then evolves longer generation times depends on the relative timing of period benefit to onset of senescent cost amongst antagonistic pleiotropisms that arise to confront the selection process. Simulations show that if the onset of senescent costs either precedes the benefit, is concurrent with it, or is postponed by a fixed interval, then natural selection will favour those pleiotropisms that increase generation length. The selection on generation-lengthening pleiotropisms continues indefinitely and regardless of current generation length, for as long as the environment remains constant. The wide range of life histories encompassed by these conditions leads to the conclusion that many species may have evolved generation lengths considerably longer than the minimum set by developmental constraints.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 269–280.     

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.     

SELECTION ON MENOPAUSE IN TWO PREMODERN HUMAN POPULATIONS: NO EVIDENCE FOR THE MOTHER HYPOTHESIS

Evolutionary theory suggests that natural selection should synchronize senescence of reproductive and somatic systems. In some species, females show dramatic discordance in senescence rates in these systems, leading to a clear menopause coupled with prolonged postreproductive life span. The Mother Hypothesis proposes that menopause evolved to avoid higher reproductive‐mediated mortality risk in late‐life and ensure the survival of existing offspring. Despite substantial theoretical interest, the critical predictions of this hypothesis have never been fully tested in populations with natural fertility and mortality. Here, we provide an extensive test, investigating both short‐ and long‐term consequences of mother loss for offspring, using multigenerational demographic datasets of premodern Finns and Canadians. We found no support for the Mother Hypothesis. First, although the risk of maternal death from childbirth increased from middle age, the risk only reached 1–2% at age 50 and was predicted to range between 2% and 8% by 70. Second, offspring were adversely affected by maternal loss only in their first two years (i.e., preweaning), having reduced survival probability in early childhood as well as ultimate life span and fitness. Dependent offspring were not affected by maternal death following weaning, either in the short‐ or long‐term. We suggest that although mothers are required to ensure offspring survival preweaning in humans, maternal loss thereafter can be compensated by other family members. Our results indicate that maternal effects on dependent offspring are unlikely to explain the maintenance of menopause or prolonged postreproductive life span in women.     

Sociality, individual fitness and population dynamics of yellow-bellied marmots

Social behaviour was proposed as a density-dependent intrinsic mechanism that could regulate an animal population by affecting reproduction and dispersal. Populations of the polygynous yellow-bellied marmot (Marmota flaviventris) fluctuate widely from year to year primarily driven by the number of weaned young. The temporal variation in projected population growth rate was driven mainly by changes in the age of first reproduction and fertility, which are affected by reproductive suppression. Dispersal is unrelated to population density, or the presence of the father; hence, neither of these limits population growth or acts as an intrinsic mechanism of population regulation; overall, intrinsic regulation seems unlikely. Sociality affects the likelihood of reproduction in that the annual probability of reproducing and the lifetime number of offspring are decreased by the number of older females and by the number of same-aged females present, but are increased by the number of younger adult females present. Recruitment of a yearling female is most likely when her mother is present; recruitment of philopatric females is much more important than immigration for increasing the number of adult female residents. Predation and overwinter mortality are the major factors limiting the number of resident adults. Social behaviour is not directed towards population regulation, but is best interpreted as functioning to maximize direct fitness.     

Biological fitness and action opportunity of natural selection in an urban population of Cuba: Plaza de la Revolución, Havana

This paper describes the biological fitness of an urban population of Havana city, Plaza de la Revolución, which has the lowest fertility and the highest demographic ageing in Cuba. The aim is to assess the biological fitness of this community through the indexes of action opportunity of natural selection, to determine its evolutionary pattern and the influence of its socio-cultural peculiarity. Demographic data were obtained from the reproductive histories of 1200 women between the ages of 55 and 64. Data concerning mortality and surviving offspring from the first embryonic stages until age of reproduction were also collected. In order to measure the level of biological fitness two indexes were used: the Crow index of action opportunity of natural selection and the corrected index proposed by Johnston and Kensinger, which takes into account prenatal mortality. This corrected index was calculated including and excluding induced abortions in order to evaluate the contribution of these to biological fitness. When only postnatal mortality was considered, the results showed an evolutionary pattern similar to that of developed countries, based on low mortality and fertility. However, when prenatal mortality was taken into account, biological fitness decreased and the corrected index of natural selection was 4.5 times higher than when miscarriages and fetal deaths were not considered. Moreover, this corrected index was 2.65 times higher when induced miscarriages were considered, indicating the large decrease in biological fitness as a result of the current reproductive behaviour of frequent induced abortion.     

Mutation Accumulation May Only Be a Minor Force in Shaping Life-History Traits,Even when Reproduction Is Sexual

In a previous theoretical study we investigated whether adaptive or non-adaptive processes are more important in the evolution of senescence. We built a model that combined both processes and found that mutation accumulation is important only at those ages where mortality has a negligible impact on fitness. This model, however, was limited to haploid organisms. Here we extend our model by introducing diploidy and sexual reproduction. We assume that only recessive (mutated) homozygotes experience detrimental effects. Our results corroborate our previous conclusions, confirming that life histories are largely determined by adaptive processes. We also found that the equilibrium frequencies of mutated alleles are at higher values than in haploid model, because mutations in heterozygotes are hidden for directional selection. Nevertheless, the equilibrium frequencies of recessive homozygotes that make mutations visible to selection are very similar to the equilibrium frequencies of these alleles in our haploid model. Diploidy and sexual reproduction with recombination slows down approaching selection-mutation balance.     

An explanation for negligible senescence in animals

Negligible or negative senescence occurs when mortality risk is stable or decreases with age, and has been observed in some wild animals. Age‐independent mortality in animals may lead to an abnormally long maximum individual lifespans and be incompatible with evolutionary theories of senescence. The reason why there is no evidence of senescence in these animals has not been fully understood. Recovery rates are usually very low for wild animals with high dispersal ability and/or small body size (e.g., bats, rodents, and most birds). The only information concerning senescence for most of these species is the reported lifespan when individuals are last seen or caught. We deduced the probability density function of the reported lifespan based on the assumption that the real lifespan corresponding to Weibull or Gompertz distribution. We show that the magnitude of the increase in mortality risk is largely underestimated based on the reported lifespans with low recovery probability. The risk of mortality can aberrantly appear to have a negative correlation with age when it actually increases with increasing lifespan. We demonstrated that the underestimated aging rate for wild animals with low recovery probability can be generalizable to any aging models. Our work provides an explanation for the appearance of negligible senescence in many wild animals. Humans attempt to obtain insights from other creatures to better understand our own biology and its gain insight into how to enhance and extended human health. Our advice is to take a second glance before admiring the negligible senescence in other animals. This ability to escape from senescence is possibly only as beautiful illusion in animals.     

Evolution of senescence: late survival sacrificed for reproduction.

In so far as it is associated with declining fertility and increasing mortality, senescence is directly detrimental to reproductive success. Natural selection should therefore act in the direction of postponing or eliminating senescence from the life history. The widespread occurrence of senescence is explained by observing that (i) the force of natural selection is generally weaker at late ages than at early ages, and (ii) the acquisition of greater longevity usually involves some cost. Two convergent theories are the 'antagonistic pleiotropy' theory, based in population genetics, and the 'disposable soma' theory, based in physiological ecology. The antagonistic pleiotropy theory proposes that certain alleles that are favoured because of beneficial early effects also have deleterious later effects. The disposable soma theory suggests that because of the competing demands of reproduction less effort is invested in the maintenance of somatic tissues than is necessary for indefinite survival.     

Evolution of aging: Theoretical and practical implications from rattlesnakes

Many reptiles live relatively long lives wherein senescence is postponed to an advanced age. Altering nutrition, reproduction, temperature, and other physiological parameters may favorably contribute to increased life spans. But life spans are also evolved characteristics of populations, and the distinctive longevities also result from selective regimes arising within particular environments. Aging is not favored directly by evolution as a way to clear a population of senescent individuals. Instead, aging is probably an indirect byproduct of selection for early physical vitality. Senescence may result from delayed appearance of deleterious genes later in life (mutation accumulation) or from multiple effects of single genes with overriding favorable effects early but coupled deleterious effects later in life (antagonistic pleiotropy). Both physiological and evolutionary causes contribute to species or even population-specific aging characteristics. Separating environmentally imposed mortality from that attributable to senescence has been aided by compiling maximum life spans of captive reptiles. Further understanding the underlying aging biology of reptiles would be aided by following mortalities of age cohorts, identifying differences in aging between populations, documenting the effects, favorable or not, of husbandry practices, and by characterizing senescence not just by mortality, but also by changes in age-related performance. Theoretical issues, inspired by experimental results in rattlesnakes, suggest conditions under which the chance mortalities of young rattlesnakes together with continued growth of adults might favor late appearance of beneficial genes and thereby account for postponed senescence in some reptiles. © 1996 Wiley-Liss, Inc.     

Kin competition,natal dispersal and the moulding of senescence by natural selection

Most theoretical models for the evolution of senescence have assumed a very large, well mixed population. Here, we investigate how limited dispersal and kin competition might influence the evolution of ageing by deriving indicators of the force of selection, similar to Hamilton (Hamilton 1966 J. Theor. Biol. 12, 12–45). Our analytical model describes how the strength of selection on survival and fecundity changes with age in a patchy population, where adults are territorial and a fraction of juveniles disperse between territories. Both parent–offspring competition and sib competition then affect selection on age-specific life-history traits. Kin competition reduces the strength of selection on survival. Mutations increasing mortality in some age classes can even be favoured by selection, but only when fecundity deteriorates rapidly with age. Population structure arising from limited dispersal however selects for a broader distribution of reproduction over the lifetime, potentially slowing down reproductive senescence. The antagonistic effects of limited dispersal on age schedules of fecundity and mortality cast doubts on the generality of conditions allowing the evolution of ‘suicide genes’ that increase mortality rates without other direct pleiotropic effects. More generally, our model illustrates how limited dispersal and social interactions can indirectly produce patterns of antagonistic pleiotropy affecting vital rates at different ages.