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.     

The dissimilar costs of love and war: age-specific mortality as a function of the operational sex ratio

Lifespan and ageing are strongly affected by many environmental factors, but the effects of social environment on these life-history traits are not well understood. We examined effects of social interaction on age-specific mortality rate in the sexually dimorphic neriid fly Telostylinus angusticollis. We found that although interaction with other individuals reduced longevity of both sexes, the costs associated with variation in operational sex ratio were sex specific: males' early-life mortality rate increased, and lifespan decreased, with increasing male bias in the sex ratio, whereas surprisingly, the presence of males had no effect on early-life mortality or lifespan of females. Intriguingly, early-life (immediate) mortality costs did not covary with late-life (latent) costs. Rather, both sexes aged most rapidly in a social environment dominated by the opposite sex. Our findings suggest that distinct reproductive activities, such as mating and fighting, impose different age-specific patterns of mortality, and that such costs are strongly sex specific.     

Adaptive male effects on female ageing in seed beetles

Selection can favour the evolution of a high reproductive rate early in life even when this results in a subsequent increase in the rate of mortality, because selection is relatively weak late in life. However, the optimal reproductive schedule of a female may be suboptimal to any one of her mates, and males may thus be selected to modulate female reproductive rate. Owing to such sexual conflict, coevolution between males and females may contribute to the evolution of senescence. By using replicated beetle populations selected for reproduction at an early or late age, we show that males evolve to affect senescence in females in a manner consistent with the genetic interests of males. 'Late' males evolved to decelerate senescence and increase the lifespan of control females, relative to 'early' males. Our findings demonstrate that adaptive evolution in one sex may involve its effects on senescence in the other, showing that the evolution of optimal life histories in one sex may be either facilitated or constrained by genes expressed in the other.     

Adaptation of <Emphasis Type="Italic">Drosophila melanogaster</Emphasis> to unfavorable growth medium affects lifespan and age-related fecundity

Experimental adaptation of Drosophila melanogaster to nutrient-deficient starch-based (S) medium resulted in lifespan shortening, increased early-life fecundity, accelerated reproductive aging, and sexually dimorphic survival curves. The direction of all these evolutionary changes coincides with the direction of phenotypic plasticity observed in non-adapted flies cultured on S medium. High adult mortality rate caused by unfavorable growth medium apparently was the main factor of selection during the evolutionary experiment. The results are partially compatible with Williams’ hypothesis, which states that increased mortality rate should result in relaxed selection against mutations that decrease fitness late in life, and thus promote the evolution of shorter lifespan and earlier reproduction. However, our results do not confirm Williams’ prediction that the sex with higher mortality rate should undergo more rapid aging: lifespan shortening by S medium is more pronounced in naive males than females, but it was female lifespan that decreased more in the course of adaptation. These data, as well as the results of testing of F₁ hybrids between adapted and control lineages, are compatible with the idea that the genetic basis of longevity is different in the two sexes, and that evolutionary response to increased mortality rate depends on the degree to which the mortality is selective. Selective mortality can result in the development of longer (rather than shorter) lifespan in the course of evolution. The results also imply that antagonistic pleiotropy of alleles, which increase early-life fecundity at the cost of accelerated aging, played an important role in the evolutionary changes of females in the experimental lineage, while accumulation of deleterious mutations with late-life effects due to drift was more important in the evolution of male traits.     

Effects of recruiting age on senescence, lifespan and lifetime reproductive success in a long-lived seabird

Theories of ageing predict that early reproduction should be associated with accelerated reproductive senescence and reduced longevity. Here, the influence of age of first reproduction on reproductive senescence and lifespan, and consequences for lifetime reproductive success (LRS), were examined using longitudinal reproductive records of male and female blue-footed boobies (Sula nebouxii) from two cohorts (1989 and 1991). The two sexes showed different relationships between age of first reproduction and rate of senescent decline: the earlier males recruited, the faster they experienced senescence in brood size and breeding success, whereas in females, recruiting age was unrelated to age-specific patterns of reproductive performance. Effects of recruiting age on lifespan, number of reproductive events and LRS were cohort- and/or sex-specific. Late-recruiting males of the 1989 cohort lived longer but performed as well over the lifetime as early recruits, suggesting the existence of a trade-off between early recruitment and long lifespan. In males of the 1991 cohort and females of both cohorts, recruiting age was apparently unrelated to lifespan, but early recruits reproduced more frequently and fledged more chicks over their lifetime than late recruits. Male boobies may be more likely than females to incur long-term costs of early reproduction, such as early reproductive senescence and diminished lifespan, because they probably invest more heavily than females. In the 1991 cohort, which faced the severe environmental challenge of an El Ni?o event in the first year of life, life-history trade-offs of males may have been masked by effects of individual quality.     

Helper effects on pup lifetime fitness in the cooperatively breeding red wolf (Canis rufus)

The evolutionary maintenance of cooperative breeding systems is thought to be a function of relative costs and benefits to breeders, helpers and juveniles. Beneficial effects of helpers on early-life survivorship and performance have been established in several species, but lifetime fitness benefits and/or costs of being helped remain unclear, particularly for long-lived species. We tested for effects of helpers on early- and late-life traits in a population of reintroduced red wolves (Canis rufus), while controlling for ecological variables such as home-range size and population density. We found that the presence of helpers in family groups was positively correlated with pup mass and survival at low population density, but negatively correlated with mass/size at high density, with no relation to survival. Interestingly, mass/size differences persisted into adulthood for both sexes. While the presence of helpers did not advance age at first reproduction for pups of either sex, females appeared to garner long-term fitness benefits from helpers through later age at last reproduction, longer reproductive lifespan and a greater number of lifetime reproductive events, which translated to higher lifetime reproductive success. In contrast, males with helpers exhibited diminished lifetime reproductive performance. Our findings suggest that while helper presence may have beneficial short-term effects in some ecological contexts, it may also incur long-term sex-dependent costs with critical ramifications for lifetime fitness.     

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.     

Direct and indirect genetic effects of sex-specific mitonuclear epistasis on reproductive ageing

Mitochondria are involved in ageing and their function requires coordinated action of both mitochondrial and nuclear genes. Epistasis between the two genomes can influence lifespan but whether this also holds for reproductive senescence is unclear. Maternal inheritance of mitochondria predicts sex differences in the efficacy of selection on mitonuclear genotypes that should result in differences between females and males in mitochondrial genetic effects. Mitonuclear genotype of a focal individual may also indirectly affect trait expression in the mating partner. We tested these predictions in the seed beetle Callosobruchus maculatus, using introgression lines harbouring distinct mitonuclear genotypes. Our results reveal both direct and indirect sex-specific effects of mitonuclear epistasis on reproductive ageing. Females harbouring coadapted mitonuclear genotypes showed higher lifetime fecundity due to slower senescence relative to novel mitonuclear combinations. We found no evidence for mitonuclear coadaptation in males. Mitonuclear epistasis not only affected age-specific ejaculate weight, but also influenced male age-dependent indirect effects on traits expressed by their female partners (fecundity, egg size, longevity). These results demonstrate important consequences of sex-specific mitonuclear epistasis for both mating partners, consistent with a role for mitonuclear genetic constraints upon sex-specific adaptive evolution.     

Do age‐specific survival patterns of wild boar fit current evolutionary theories of senescence?

Actuarial senescence is widespread in age‐structured populations. In growing populations, the progressive decline of Hamiltonian forces of selection with age leads to decreasing survival. As actuarial senescence is overcompensated by a high fertility, actuarial senescence should be more intense in species with high reproductive effort, a theoretical prediction that has not been yet explicitly tested across species. Wild boar (Sus scrofa) females have an unusual life‐history strategy among large mammals by associating both early and high reproductive effort with potentially long lifespan. Therefore, wild boar females should show stronger actuarial senescence than similar‐sized related mammals. Moreover, being polygynous and much larger than females, males should display higher senescence rates than females. Using a long‐term monitoring (18 years) of a wild boar population, we tested these predictions. We provided clear evidence of actuarial senescence in both sexes. Wild boar females had earlier but not stronger actuarial senescence than similar‐sized ungulates. Both sexes displayed similar senescence rates. Our study indicates that the timing of senescence, not the rate, is associated with the magnitude of fertility in ungulates. This demonstrates the importance of including the timing of senescence in addition to its rate to understand variation in senescence patterns in wild populations.     

Divergent patterns of age-dependence in ornamental and reproductive traits in the collared flycatcher

Sexual ornaments are predicted to honestly signal individual condition. We might therefore expect ornament expression to show a senescent decline, in parallel with late-life deterioration of other characters. Conversely, life-history theory predicts the reduced residual reproductive value of older individuals will favor increased investment in sexually attractive traits. Using a 25-year dataset of more than 5000 records of breeding collared flycatchers (Ficedula albicollis) of known age, we quantify cross-sectional patterns of age-dependence in ornamental plumage traits and report long-term declines in expression that mask highly significant positive age-dependency. We partition this population-level age-dependency into its between- and within-individual components and show expression of ornamental white plumage patches exhibits within-individual increases with age in both sexes, consistent with life-history theory. For males, ornament expression also covaries with life span, such that, within a cohort, ornamentation indicates survival. Finally, we compared longitudinal age-dependency of reproductive traits and ornamental traits in both sexes, to assess whether these two trait types exhibit similar age-dependency. These analyses revealed contrasting patterns: reproductive traits showed within-individual declines in late-life females consistent with senescence; ornamental traits showed the opposite pattern in both males and females. Hence, our results for both sexes suggest that age-dependent ornament expression is consistent with life-history models of optimal signaling and, unlike reproductive traits, proof against senescence.     

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.     

Age-specific variation in survival, reproductive success and offspring quality in red squirrels: evidence of senescence

Individual performance is expected to decrease with age because of senescence. We analyzed long-term data collected on a North American red squirrel population to assess the influence of age on body mass, survival and reproductive performance, and to study the effects of sex and of environmental conditions during early life on senescence patterns. Mass of males and females did not decrease at the end of life, possibly because body mass mostly reflects overall size in income breeders such as red squirrels. On the other hand, we found evidence of senescence in survival of both sexes and, to a lesser extent, in female reproductive traits. When compared to females, males had both higher survival and delayed decrease in survival, suggesting a weaker senescence in males. The offspring survival from weaning to one year of age also decreased with increasing mother age. This suggests that older females produce juveniles of lower quality, providing evidence of an intergenerational effect of mother's age on juveniles' fitness. Finally, our results indicate that variations in food conditions during early life influenced the reproductive tactics of females in the first years of their life, but not senescence patterns.     

Best squirrels trade a long life for an early reproduction

Age at primiparity plays a crucial role in population dynamics and life-history evolution. Long-term data on female North American red squirrels were analysed to study the fitness consequences of delaying first reproduction. Early breeders were born earlier, had a higher breeding success and achieved a higher lifetime reproductive success than females who delayed their first reproduction, which suggests a higher quality of early breeders. However, early breeders had similar mass when tagged, and similar number of food caches available at one year of age as late breeders. Nevertheless, we found evidence of survival costs of early primiparity. Early breeders had a lower survival between one and two years of age than late breeders and a lower lifespan. Our study points out that two reproductive tactics co-occurred in this population: a tactic based on early maturity at the cost of a lower survival versus a tactic based on delayed maturity and long lifespan. High quality individuals express the most profitable tactic by breeding early whereas low quality individuals do the best of a bad job by delaying their first reproduction.     

What shall I do now? State-dependent variations of life-history traits with aging in Wandering Albatrosses

Allocation decisions depend on an organism's condition which can change with age. Two opposite changes in life‐history traits are predicted in the presence of senescence: either an increase in breeding performance in late age associated with terminal investment or a decrease due to either life‐history trade‐offs between current breeding and future survival or decreased efficiency at old age. Age variation in several life‐history traits has been detected in a number of species, and demographic performances of individuals in a given year are influenced by their reproductive state the previous year. Few studies have, however, examined state‐dependent variation in life‐history traits with aging, and they focused mainly on a dichotomy of successful versus failed breeding and non‐breeding birds. Using a 50‐year dataset on the long‐lived quasi‐biennial breeding wandering albatross, we investigated variations in life‐history traits with aging according to a gradient of states corresponding to potential costs of reproduction the previous year (in ascending order): non‐breeding birds staying at sea or present at breeding grounds, breeding birds that failed early, late or were successful. We used multistate models to study survival and decompose reproduction into four components (probabilities of return, breeding, hatching, and fledging), while accounting for imperfect detection. Our results suggest the possible existence of two strategies in the population: strict biennial breeders that exhibited almost no reproductive senescence and quasi‐biennial breeders that showed an increased breeding frequency with a strong and moderate senescence on hatching and fledging probabilities, respectively. The patterns observed on survival were contrary to our predictions, suggesting an influence of individual quality rather than trade‐offs between reproduction and survival at late ages. This work represents a step further into understanding the evolutionary ecology of senescence and its relationship with costs of reproduction at the population level. It paves the way for individual‐based studies that could show the importance of intra‐population heterogeneity in those processes.     

SEXUAL SELECTION AFFECTS THE EVOLUTION OF LIFESPAN AND AGEING IN THE DECORATED CRICKET GRYLLODES SIGILLATUS

Recent work suggests that sexual selection can influence the evolution of ageing and lifespan by shaping the optimal timing and relative costliness of reproductive effort in the sexes. We used inbred lines of the decorated cricket, Gryllodes sigillatus, to estimate the genetic (co)variance between age‐dependent reproductive effort, lifespan, and ageing within and between the sexes. Sexual selection theory predicts that males should die sooner and age more rapidly than females. However, a reversal of this pattern may be favored if reproductive effort increases with age in males but not in females. We found that male calling effort increased with age, whereas female fecundity decreased, and that males lived longer and aged more slowly than females. These divergent life‐history strategies were underpinned by a positive genetic correlation between early‐life reproductive effort and ageing rate in both sexes, although this relationship was stronger in females. Despite these sex differences in life‐history schedules, age‐dependent reproductive effort, lifespan, and ageing exhibited strong positive intersexual genetic correlations. This should, in theory, constrain the independent evolution of these traits in the sexes and may promote intralocus sexual conflict. Our study highlights the importance of sexual selection to the evolution of sex differences in ageing and lifespan in G. sigillatus.     

Complex genetic architecture of population differences in adult lifespan of a beetle: nonadditive inheritance, gender differences, body size and a large maternal effect

Evolutionary responses to selection can be complicated when there is substantial nonadditivity, which limits our ability to extrapolate from simple models of selection to population differentiation and speciation. Studies of Drosophila melanogaster indicate that lifespan and the rate of senescence are influenced by many genes that have environment- and sex-specific effects. These studies also demonstrate that interactions among alleles (dominance) and loci (epistasis) are common, with the degree of interaction differing between the sexes and among environments. However, little is known about the genetic architecture of lifespan or mortality rates for organisms other than D. melanogaster. We studied genetic architecture of differences in lifespan and shapes of mortality curves between two populations of the seed beetle, Callosobruchus maculatus (South India and Burkina Faso populations). These two populations differ in various traits (such as body size and adult lifespan) that have likely evolved via host-specific selection. We found that the genetic architecture of lifespan differences between populations differs substantially between males and females; there was a large maternal effect on male lifespan (but not on female lifespan), and substantial dominance of long-life alleles in females (but not males). The large maternal effect in males was genetically based (there was no significant cytoplasmic effect) likely due to population differences in maternal effects genes that influence lifespan of progeny. Rearing host did not affect the genetic architecture of lifespan, and there was no evidence that genes on the Y-chromosome influence the population differences in lifespan. Epistatic interactions among loci were detectable for the mortality rate of both males and females, but were detectable for lifespan only after controlling for body size variation among lines. The detection of epistasis, dominance, and sex-specific genetic effects on C. maculatus lifespan is consistent with results from line cross and quantitative trait locus studies of D. melanogaster.     

The interaction between reproductive lifespan and protandry in seasonal breeders

The timing and duration of reproductive activities are highly variable both at the individual and population level. Understanding how this variation evolved by natural selection is fundamental to understanding many important aspects of an organism's life history, ecology and behaviour. Here, we combine game theoretic principles governing reproductive timing and the evolutionary theory of senescence to study the interaction between protandry (the earlier arrival or emergence of males to breeding areas than females) and senescence in seasonal breeders. Our general model applies to males who are seeking to mate as frequently as possible over a relatively short period, and so is relevant to many organisms including annual insects and semelparous vertebrates. The model predicts that protandry and maximum reproductive lifespans should increase in environments characterized by high survival and by a low competitive cost of maintaining the somatic machinery necessary for survival. In relatively short seasons under these same conditions, seasonal declines in the reproductive lifespans of males of equivalent quality will be evolutionarily stable. However, over a broad range of potential values for daily survival and maintenance cost, reproductive lifespan is expected to be relatively short and constant throughout a large fraction of the season. We applied the model to sockeye (or kokanee) salmon Oncorhynchus nerka and show that pronounced seasonal declines in reproductive lifespan, a distinctive feature of semelparous Oncorhynchus spp., is likely part of a male mating strategy to maximize mating opportunities.     

Age-independent and age-dependent decreases in reproduction of females

The terminal allocation and senescence hypotheses make opposite predictions about how age-specific reproductive effort should vary during old age. There is empirical support for both hypotheses, although reports on senescence are more numerous. Individual heterogeneity and selective mortality, however, decrease our ability to measure how reproductive effort varies during late life. The damage accumulation model proposes that terminal allocation and senescence could be partly age-independent. Using a reverse-age approach, we analysed an unusually complete record of annual reproductive success for 90 bighorn ewes that died between 7 and 18years of age. We estimated age-specific and age-independent variation of reproductive effort in late-life. Reproductive effort decreased in the two last reproductions, independently of age at death. Fecundity also decreased in the last 2years of life, with a steeper decline for older individuals. Our study reveals that reproductive senescence includes both age-dependent and age-independent components.     

Great tits growing old: selective disappearance and the partitioning of senescence to stages within the breeding cycle

Deterioration of reproductive traits with age is observed in an increasing number of species. Although such deterioration is often attributed to reproductive senescence, a within-individual decline in reproductive success with age, few studies on wild animals have focused on direct fitness measures while accounting for selective disappearance and terminal effects, and to our knowledge none have determined how senescence effects arise from underlying reproductive traits. We show for female great tits that such an approach helps understanding of the onset, impact and architecture of senescence. Cross-sectional analysis of 49 years of breeding data shows annual recruit production to decline from 3.5 years of age, this decline affecting 9 per cent of females each year. Longitudinal analyses, however, show that selective disappearance of poor-quality breeders partly masks senescence, which in fact starts at 2.8 years and affects 21 per cent of females each year. There is no evidence for abrupt terminal effects. Analyses of underlying traits show no deterioration in clutch size, but significant declines in brood size and fledgling number. Furthermore, these traits contribute −9, 12 and 39 per cent to the senescent decline in recruit production, respectively. Besides providing detailed knowledge of the patterns and architecture of senescence in a natural population, these results illustrate the importance of modelling individual variation, and facilitate study of the underlying mechanisms of senescence.     

Early growth,dominance acquisition and lifetime reproductive success in male and female cooperative meerkats

In polygynous species, variance in reproductive success is higher in males than females. There is consequently stronger selection for competitive traits in males and early growth can have a greater influence on later fitness in males than in females. As yet, little is known about sex differences in the effect of early growth on subsequent breeding success in species where variance in reproductive success is higher in females than males, and competitive traits are under stronger selection in females. Greater variance in reproductive success has been documented in several singular cooperative breeders. Here, we investigated consequences of early growth for later reproductive success in wild meerkats. We found that, despite the absence of dimorphism, females who exhibited faster growth until nutritional independence were more likely to become dominant, whereas early growth did not affect dominance acquisition in males. Among those individuals who attained dominance, there was no further influence of early growth on dominance tenure or lifetime reproductive success in males or females. These findings suggest that early growth effects on competitive abilities and fitness may reflect the intensity of intrasexual competition even in sexually monomorphic species.