Repeated intraspecific divergence in life span and aging of African annual fishes along an aridity gradient

Life span and aging are substantially modified by natural selection. Across species, higher extrinsic (environmentally related) mortality (and hence shorter life expectancy) selects for the evolution of more rapid aging. However, among populations within species, high extrinsic mortality can lead to extended life span and slower aging as a consequence of condition‐dependent survival. Using within‐species contrasts of eight natural populations of Nothobranchius fishes in common garden experiments, we demonstrate that populations originating from dry regions (with short life expectancy) had shorter intrinsic life spans and a greater increase in mortality with age, more pronounced cellular and physiological deterioration (oxidative damage, tumor load), and a faster decline in fertility than populations from wetter regions. This parallel intraspecific divergence in life span and aging was not associated with divergence in early life history (rapid growth, maturation) or pace‐of‐life syndrome (high metabolic rates, active behavior). Variability across four study species suggests that a combination of different aging and life‐history traits conformed with or contradicted the predictions for each species. These findings demonstrate that variation in life span and functional decline among natural populations are linked, genetically underpinned, and can evolve relatively rapidly.     

Experimental evolution of slowed cognitive aging in Drosophila melanogaster

Reproductive output and cognitive performance decline in parallel during aging, but it is unknown whether this reflects a shared genetic architecture or merely the declining force of natural selection acting independently on both traits. We used experimental evolution in Drosophila melanogaster to test for the presence of genetic variation for slowed cognitive aging, and assess its independence from that responsible for other traits’ decline with age. Replicate experimental populations experienced either joint selection on learning and reproduction at old age (Old + Learning), selection on late‐life reproduction alone (Old), or a standard two‐week culture regime (Young). Within 20 generations, the Old + Learning populations evolved a slower decline in learning with age than both the Old and Young populations, revealing genetic variation for cognitive aging. We found little evidence for a genetic correlation between cognitive and demographic aging: although the Old + Learning populations tended to show higher late‐life fecundity than Old populations, they did not live longer. Likewise, selection for late reproduction alone did not result in improved late‐life learning. Our results demonstrate that Drosophila harbor genetic variation for cognitive aging that is largely independent from genetic variation for demographic aging and suggest that these two aspects of aging may not necessarily follow the same trajectories.     

Comparative idiosyncrasies in life extension by reduced mTOR signalling and its distinctiveness from dietary restriction

Reduced mechanistic target of rapamycin (mTOR) signalling extends lifespan in yeast, nematodes, fruit flies and mice, highlighting a physiological pathway that could modulate aging in evolutionarily divergent organisms. This signalling system is also hypothesized to play a central role in lifespan extension via dietary restriction. By collating data from 48 available published studies examining lifespan with reduced mTOR signalling, we show that reduced mTOR signalling provides similar increases in median lifespan across species, with genetic mTOR manipulations consistently providing greater life extension than pharmacological treatment with rapamycin. In contrast to the consistency in changes in median lifespan, however, the demographic causes for life extension are highly species specific. Reduced mTOR signalling extends lifespan in nematodes by strongly reducing the degree to which mortality rates increase with age (aging rate). By contrast, life extension in mice and yeast occurs largely by pushing back the onset of aging, but not altering the shape of the mortality curve once aging starts. Importantly, in mice, the altered pattern of mortality induced by reduced mTOR signalling is different to that induced by dietary restriction, which reduces the rate of aging. Effects of mTOR signalling were also sex dependent, but only within mice, and not within flies, thus again species specific. An alleviation of age‐associated mortality is not a shared feature of reduced mTOR signalling across model organisms and does not replicate the established age‐related survival benefits of dietary restriction.     

A dynamic framework for the study of optimal birth intervals reveals the importance of sibling competition and mortality risks

Human reproductive patterns have been well studied, but the mechanisms by which physiology, ecology and existing kin interact to affect the life history need quantification. Here, we create a model to investigate how age‐specific interbirth intervals adapt to environmental and intrinsic mortality, and how birth patterns can be shaped by competition and help between siblings. The model provides a flexible framework for studying the processes underlying human reproductive scheduling. We developed a state‐based optimality model to determine age‐dependent and family‐dependent sets of reproductive strategies, including the state of the mother and her offspring. We parameterized the model with realistic mortality curves derived from five human populations. Overall, optimal birth intervals increase until the age of 30 after which they remain relatively constant until the end of the reproductive lifespan. Offspring helping each other does not have much effect on birth intervals. Increasing infant and senescent mortality in different populations decreases interbirth intervals. We show that sibling competition and infant mortality interact to lengthen interbirth intervals. In lower‐mortality populations, intense sibling competition pushes births further apart. Varying the adult risk of mortality alone has no effect on birth intervals between populations; competition between offspring drives the differences in birth intervals only when infant mortality is low. These results are relevant to understanding the demographic transition, because our model predicts that sibling competition becomes an important determinant of optimal interbirth intervals only when mortality is low, as in post‐transition societies. We do not predict that these effects alone can select for menopause.     

A DEMOGRAPHIC TRANSITION ALTERED THE STRENGTH OF SELECTION FOR FITNESS AND AGE‐SPECIFIC SURVIVAL AND FERTILITY IN A 19TH CENTURY AMERICAN POPULATION

Modernization has increased longevity and decreased fertility in many human populations, but it is not well understood how or to what extent these demographic transitions have altered patterns of natural selection. I integrate individual‐based multivariate phenotypic selection approaches with evolutionary demographic methods to demonstrate how a demographic transition in 19th century female populations of Utah altered relationships between fitness and age‐specific survival and fertility. Coincident with this demographic transition, natural selection for fitness, as measured by the opportunity for selection, increased by 13% to 20% over 65 years. Proportional contributions of age‐specific survival to total selection (the complement to age‐specific fertility) diminished from approximately one third to one seventh following a marked increase in infant survival. Despite dramatic reductions in age‐specific fertility variance at all ages, the absolute magnitude of selection for fitness explained by age‐specific fertility increased by approximately 45%. I show that increases in the adaptive potential of fertility traits followed directly from decreased population growth rates. These results suggest that this demographic transition has increased the adaptive potential of the Utah population, intensified selection for reproductive traits, and de‐emphasized selection for survival‐related traits.     

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.     

Evolutionary ecology of aging: time to reconcile field and laboratory research

Aging is an increase in mortality risk with age due to a decline in vital functions. Research on aging has entered an exciting phase. Advances in biogerontology have demonstrated that proximate mechanisms of aging and interventions to modify lifespan are shared among species. In nature, aging patterns have proven more diverse than previously assumed. The paradigm that extrinsic mortality ultimately determines evolution of aging rates has been questioned and there appears to be a mismatch between intra‐ and inter‐specific patterns. The major challenges emerging in evolutionary ecology of aging are a lack of understanding of the complexity in functional senescence under natural conditions and unavailability of estimates of aging rates for matched populations exposed to natural and laboratory conditions. I argue that we need to reconcile laboratory and field‐based approaches to better understand (1) how aging rates (baseline mortality and the rate of increase in mortality with age) vary across populations within a species, (2) how genetic and environmental variation interact to modulate individual expression of aging rates, and (3) how much intraspecific variation in lifespan is attributable to an intrinsic (i.e., nonenvironmental) component. I suggest integration of laboratory and field assays using multiple matched populations of the same species, along with measures of functional declines.     

Age-at-death estimation in an Italian historical sample: A test of the Suchey-Brooks and transition analysis methods

A growing body of research is demonstrating increased accuracy in aging from a relatively new method, transition analysis. Although transition analysis was developed for paleodemographic research, a majority of subsequent studies have been in the forensic arena, with very little work in bioarchaeological contexts. Using the Suchey‐Brooks pubic symphysis phases, scored on a target sample of historic Italians from the island of Sardinia, we compare accuracy of aging between transition analysis combined with a Bayesian approach and the standard Suchey‐Brooks age ranges. Because of the difficulty in identifying a reasonable informative prior for bioarchaeological samples, we also compared results of both an informative prior and a uniform prior for age estimation. Published ages‐of‐transition for the Terry Collection and Balkan genocide victims were used in conjunction with parameters generated from Gompertz hazard models derived from the priors. The ages‐of‐transition and hazard parameters were utilized to calculate the highest posterior density regions, otherwise known as “coverages” or age ranges, for each Suchey‐Brooks phase. Each prior, along with the parameters, were input into cumulative binomial tests. The results indicate that the Bayesian approach outperformed the Suchey‐Brooks technique alone. The Terry Collection surpassed the Balkans as a reasonable sample from which to derive transition analysis parameters. This discrepancy between populations is due to different within phase age‐at‐death distributions that reflect differences in aging between the populations. These results indicate bioarchaeologists should strive to apply a Bayesian analysis when aging historic and archaeological populations by employing an informative prior. Am J Phys Anthropol 149:259–265, 2012. © 2012 Wiley Periodicals, Inc.     

Decline of tuberculosis mortality in an urban Mexican‐origin population, 1935–1984

Abstract

Through a series of life table analyses, this paper describes the natural history of tuberculosis mortality in a Mexican‐origin community over five decades (1935–84) during which the disease underwent a transition from a major underlying cause of death to a disease conditioned mentioned more often on death certificates as contributing to death than causing death. The decline in death rates from 1940 to 1950 was especially remarkable. Successive birth cohorts of Mexican Americans, separated by as little as five years of age, experienced distinctly lower risk of death from tuberculosis as they entered young adulthood. There was a rapid convergence in age‐specific patterns of tuberculosis death rates in Mexican Americans toward those of non‐Hispanic whites, so that by 1960 tuberculosis was primarily a cause of death in old age rather than young adulthood. The impact of changing environment, both through improvements of conditions within neighborhoods and through residential mobility, on birth cohorts at risk of tuberculosis needs to be examined in further research.     

Late life: a new frontier for physiology

Late life is a distinct phase of life that occurs after the aging period and is now known to be general among aging organisms. While aging is characterized by a deterioration in survivorship and fertility, late life is characterized by the cessation of such age-related deterioration. Thus, late life presents a new and interesting area of research not only for evolutionary biology but also for physiology. In this article, we present the theoretical and experimental background to late life, as developed by evolutionary biologists and demographers. We discuss the discovery of late life and the two main theories developed to explain this phase of life: lifelong demographic heterogeneity theory and evolutionary theory based on the force of natural selection. Finally, we suggest topics for future physiological research on late life.     

GENOMIC BASIS OF AGING AND LIFE‐HISTORY EVOLUTION IN DROSOPHILA MELANOGASTER

Natural diversity in aging and other life‐history patterns is a hallmark of organismal variation. Related species, populations, and individuals within populations show genetically based variation in life span and other aspects of age‐related performance. Population differences are especially informative because these differences can be large relative to within‐population variation and because they occur in organisms with otherwise similar genomes. We used experimental evolution to produce populations divergent for life span and late‐age fertility and then used deep genome sequencing to detect sequence variants with nucleotide‐level resolution. Several genes and genome regions showed strong signatures of selection, and the same regions were implicated in independent comparisons, suggesting that the same alleles were selected in replicate lines. Genes related to oogenesis, immunity, and protein degradation were implicated as important modifiers of late‐life performance. Expression profiling and functional annotation narrowed the list of strong candidate genes to 38, most of which are novel candidates for regulating aging. Life span and early age fecundity were negatively correlated among populations; therefore, the alleles we identified also are candidate regulators of a major life‐history trade‐off. More generally, we argue that hitchhiking mapping can be a powerful tool for uncovering the molecular bases of quantitative genetic variation.     

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.     

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.     

Age‐dependent mutational effects curtail the evolution of senescence by antagonistic pleiotropy

One of the two main hypotheses to account for ageing is antagonistic pleiotropy (AP). This model requires alleles that increase vital rates (reproduction or survival) at early age at the expense of vital rates at late age. An important focus of evolutionary studies has been to assess the relative abundance of AP‐type aging alleles that arise through mutation. Here, we develop theory that predicts that senescence per se reduces the probability that these alleles arise by mutation. A direct result is that these mutations should arise with extremely low frequencies in already senescing populations. This has profound implications for the evolution of life histories because it implies that the adaptive evolution of aging via AP will experience negative feedback. This theory also clarifies the previously inexplicable epistatic patterns of genetic covariance across age‐specific vital rates that are observed in mutation accumulation experiments. We show that this epistasis is an emergent property of aging.     

A trait‐based trade‐off between growth and mortality: evidence from 15 tropical tree species using size‐specific relative growth rates

A life‐history trade‐off between low mortality in the dark and rapid growth in the light is one of the most widely accepted mechanisms underlying plant ecological strategies in tropical forests. Differences in plant functional traits are thought to underlie these distinct ecological strategies; however, very few studies have shown relationships between functional traits and demographic rates within a functional group. We present 8 years of growth and mortality data from saplings of 15 species of Dipterocarpaceae planted into logged‐over forest in Malaysian Borneo, and the relationships between these demographic rates and four key functional traits: wood density, specific leaf area (SLA), seed mass, and leaf C:N ratio. Species‐specific differences in growth rates were separated from seedling size effects by fitting nonlinear mixed‐effects models, to repeated measurements taken on individuals at multiple time points. Mortality data were analyzed using binary logistic regressions in a mixed‐effects models framework. Growth increased and mortality decreased with increasing light availability. Species differed in both their growth and mortality rates, yet there was little evidence for a statistical interaction between species and light for either response. There was a positive relationship between growth rate and the predicted probability of mortality regardless of light environment, suggesting that this relationship may be driven by a general trade‐off between traits that maximize growth and traits that minimize mortality, rather than through differential species responses to light. Our results indicate that wood density is an important trait that indicates both the ability of species to grow and resistance to mortality, but no other trait was correlated with either growth or mortality. Therefore, the growth mortality trade‐off among species of dipterocarp appears to be general in being independent of species crossovers in performance in different light environments.     

Early reproductive investment,senescence and lifetime reproductive success in female Asian elephants

The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early‐life over late‐life reproduction. Studies on natural vertebrate populations show early reproduction may impair later‐life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants (Elephas maximus) to investigate associations between early‐life reproduction and female age‐specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age‐specific fecundity and offspring survival, but significantly impaired a female's own later‐life survival. Despite the negative effects of early reproduction on late‐life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade‐off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later‐life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi‐)captive breeding programmes of this endangered species.     

The diversity of population responses to environmental change

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

Age-specific metabolic rates and mortality rates in the genus Drosophila

Early theories of aging suggested that organisms with relatively high metabolic rates would live shorter lives. Despite widespread tests of this 'rate of living' theory of aging, there is little empirical evidence to support the idea. A more fine-grained approach that examined age-related changes in metabolic rate over the life span could provide valuable insight into the relationship between metabolic rate and aging. Here we compare age-related metabolic rate (measured as CO2 production per hour) and age-related mortality rate among five species in the genus Drosophila. We find no evidence that longer-lived species have lower metabolic rates. In all five species, there is no clear evidence of an age-related metabolic decline. Metabolic rates are strikingly constant throughout the life course, with the exception of females of D. hydei, in which metabolic rates show an increase over the first third of the life span and then decline. We argue that some physiological traits may have been shaped by such strong selection over evolutionary time that they are relatively resistant to the decline in the force of selection that occurs within the life time of a single individual. We suggest that comparisons of specific traits that do not show signs of aging with those traits that do decline with age could provide insight into the aging process.     

Evolution of male age‐specific reproduction under differential risks and causes of death: males pay the cost of high female fitness

Classic theories of ageing evolution predict that increased extrinsic mortality due to an environmental hazard selects for increased early reproduction, rapid ageing and short intrinsic lifespan. Conversely, emerging theory maintains that when ageing increases susceptibility to an environmental hazard, increased mortality due to this hazard can select against ageing in physiological condition and prolong intrinsic lifespan. However, evolution of slow ageing under high‐condition‐dependent mortality is expected to result from reallocation of resources to different traits and such reallocation may be hampered by sex‐specific trade‐offs. Because same life‐history trait values often have different fitness consequences in males and females, sexually antagonistic selection can preserve genetic variance for lifespan and ageing. We previously showed that increased condition‐dependent mortality caused by heat shock leads to evolution of long‐life, decelerated late‐life mortality in both sexes and increased female fecundity in the nematode, Caenorhabditis remanei. Here, we used these cryopreserved lines to show that males evolving under heat shock suffered from reduced early‐life and net reproduction, while mortality rate had no effect. Our results suggest that heat‐shock resistance and associated long‐life trade‐off with male, but not female, reproduction and therefore sexually antagonistic selection contributes to maintenance of genetic variation for lifespan and fitness in this population.     

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.