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

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

Age‐related variation in reproductive traits in the wandering albatross: evidence for terminal improvement following senescence

The processes driving age‐related variation in demographic rates are central to understanding population and evolutionary ecology. An increasing number of studies in wild vertebrates find evidence for improvements in reproductive performance traits in early adulthood, followed by senescent declines in later life. However, life history theory predicts that reproductive investment should increase with age as future survival prospects diminish, and that raised reproductive investment may have associated survival costs. These non‐mutually exclusive processes both predict an increase in breeding performance at the terminal breeding attempt. Here, we use a 30‐year study of wandering albatrosses (Diomedea exulans) to disentangle the processes underpinning age‐related variation in reproduction. Whilst highlighting the importance of breeding experience, we reveal senescent declines in performance are followed by a striking increase in breeding success and a key parental investment trait at the final breeding attempt.     

Testing the effect of early‐life reproductive effort on age‐related decline in a wild insect

The disposable soma theory of ageing predicts that when organisms invest in reproduction they do so by reducing their investment in body maintenance, inducing a trade‐off between reproduction and survival. Experiments on invertebrates in the lab provide support for the theory by demonstrating the predicted responses to manipulation of reproductive effort or lifespan. However, experimental studies in birds and evidence from observational (nonmanipulative) studies in nature do not consistently reveal trade‐offs. Most species studied previously in the wild are mammals and birds that reproduce over multiple discrete seasons. This contrasts with temperate invertebrates, which typically have annual generations and reproduce over a single season. We expand the taxonomic range of senescence study systems to include life histories typical of most temperate invertebrates. We monitored reproductive effort, ageing, and survival in a natural field cricket population over ten years to test the prediction that individuals investing more in early‐reproduction senesce faster and die younger. We found no evidence of a trade‐off between early‐life reproductive effort and survival, and only weak evidence for a trade‐off with phenotypic senescence. We discuss the possibility that organisms with multiple discrete breeding seasons may have greater opportunities to express trade‐offs between reproduction and senescence.     

Early‐life telomere length predicts lifespan and lifetime reproductive success in a wild bird

Poor conditions during early development can initiate trade‐offs that favour current survival at the expense of somatic maintenance and subsequently, future reproduction. However, the mechanisms that link early and late life‐history are largely unknown. Recently it has been suggested that telomeres, the nucleoprotein structures at the terminal end of chromosomes, could link early‐life conditions to lifespan and fitness. In wild purple‐crowned fairy‐wrens, we combined measurements of nestling telomere length (TL) with detailed life‐history data to investigate whether early‐life TL predicts fitness prospects. Our study differs from previous studies in the completeness of our fitness estimates in a highly philopatric population. The association between TL and survival was age‐dependent with early‐life TL having a positive effect on lifespan only among individuals that survived their first year. Early‐life TL was not associated with the probability or age of gaining a breeding position. Interestingly, early‐life TL was positively related to breeding duration, contribution to population growth and lifetime reproductive success because of their association with lifespan. Thus, early‐life TL, which reflects growth, accumulated early‐life stress and inherited TL, predicted fitness in birds that reached adulthood but not noticeably among fledglings. These findings suggest that a lack of investment in somatic maintenance during development particularly affects late life performance. This study demonstrates that factors in early‐life are related to fitness prospects through lifespan, and suggests that the study of telomeres may provide insight into the underlying physiological mechanisms linking early‐ and late‐life performance and trade‐offs across a lifetime.     

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.     

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.     

Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago

Long-lived iteroparous species often show aging-related changes in reproduction that may be explained by 2 non-mutually exclusive hypotheses. The terminal investment hypothesis predicts increased female reproductive effort toward the end of the life span, as individuals have little to gain by reserving effort for the future. The senescence hypothesis predicts decreased female reproductive output toward the end of the life span due to an age-related decline in body condition. Nonhuman primates are ideal organisms for testing these hypotheses, as they are long lived and produce altricial offspring heavily dependent on maternal investment. In this study, we integrated 50 years of continuous demographic records for the Cayo Santiago rhesus macaque (Macaca mulatta) population with new morphometric and behavioral data to test the senescence and terminal investment hypotheses. We examined relationships between maternal age and activity, mother and infant body condition, interbirth intervals, measures of behavioral investment in offspring, and offspring survival and fitness to test for age-associated declines in reproduction that would indicate senescence, and for age-associated increases in maternal effort that would indicate terminal investment. Compared with younger mothers, older mothers had lower body mass indices and were less active, had longer interbirth intervals, and spent more time in contact with infants, but had infants of lower masses and survival rates. Taken together, our results provide strong evidence for the occurrence of reproductive senescence in free-ranging female rhesus macaques but are also consistent with some of the predictions of the terminal investment hypothesis.     

Early life expenditure in sexual competition is associated with increased reproductive senescence in male red deer

The evolutionary theories of senescence predict that investment in reproduction in early life should come at the cost of reduced somatic maintenance, and thus earlier or more rapid senescence. There is now growing support for such trade-offs in wild vertebrates, but these exclusively come from females. Here, we test this prediction in male red deer (Cervus elaphus) using detailed longitudinal data collected over a 40-year field study. We show that males which had larger harems and thereby allocated more resources to reproduction during early adulthood experienced higher rates of senescence in both harem size and rut duration. Males that carried antlers with more points during early life did not show more pronounced declines in reproductive traits in later life. Overall, we demonstrate that sexual competition shapes male reproductive senescence in wild red deer populations and provide rare empirical support for the disposable soma theory of ageing in males of polygynous vertebrate species.     

Early-late life trade-offs and the evolution of ageing in the wild

Empirical evidence for declines in fitness components (survival and reproductive performance) with age has recently accumulated in wild populations, highlighting that the process of senescence is nearly ubiquitous in the living world. Senescence patterns are highly variable among species and current evolutionary theories of ageing propose that such variation can be accounted for by differences in allocation to growth and reproduction during early life. Here, we compiled 26 studies of free-ranging vertebrate populations that explicitly tested for a trade-off between performance in early and late life. Our review brings overall support for the presence of early-late life trade-offs, suggesting that the limitation of available resources leads individuals to trade somatic maintenance later in life for high allocation to reproduction early in life. We discuss our results in the light of two closely related theories of ageing—the disposable soma and the antagonistic pleiotropy theories—and propose that the principle of energy allocation roots the ageing process in the evolution of life-history strategies. Finally, we outline research topics that should be investigated in future studies, including the importance of natal environmental conditions in the study of trade-offs between early- and late-life performance and the evolution of sex-differences in ageing patterns.     

Allocation of nutrients to somatic tissues in young ovariectomized grasshoppers

The disposable soma hypothesis predicts that when reproduction is reduced, life span is increased because more nutrients are invested in the soma, increasing somatic repair. Rigorously testing the hypothesis requires tracking nutrients from ingestion to allocation to the soma or to reproduction. Fruit flies on life-extending dietary restriction increase allocation to the soma "relative" to reproduction, suggesting that allocation of nutrients can be associated with extension of life span. Here, we use stable isotopes to track ingested nutrients in ovariectomized grasshoppers during the first oviposition cycle. Previous work has shown that ovariectomy extends life span, but investment of protein in reproduction is not reduced until after the first clutch of eggs is laid. Because ovariectomy does not affect investment in reproduction at this age, the disposable soma hypothesis would predict that ovariectomy should also not affect investment in somatic tissues. We developed grasshopper diets with distinct signatures of 13C and 1?N, but that produced equivalent reproductive outputs. These diets are, therefore, appropriate for the reciprocal switches in diet needed for tracking ingested nutrients. Incorporation of stable isotopes into eggs showed that grasshoppers are income breeders, especially for carbon. Allocation to the fat body of nitrogen ingested as adults was slightly increased by ovariectomy; this was our only result that was not consistent with the disposable soma hypothesis. In contrast, ovariectomy did not affect allocation of nitrogen to femoral muscles. Further, allocation of carbon to the fat body or femoral muscles did not appear to be affected by ovariectomy. Total anti-oxidant activities in the hemolymph and femoral muscles were not affected by ovariectomy. These experiments showed that allocation of nutrients was altered little by ovariectomy in young grasshoppers. Additional studies on older individuals are needed to further test the disposable soma hypothesis.     

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.     

The rate of senescence in maternal performance increases with early-life fecundity in red deer

Tradeoffs between reproduction and somatic maintenance are a frequently cited explanation for reproductive senescence in long-lived vertebrates. Between-individual variation in quality makes such tradeoffs difficult to detect and evidence for their presence from wild populations remains scarce. Here, we examine the factors affecting rates of senescence in maternal breeding performance in a natural population of red deer ( Cervus elaphus ), using a mixed model framework to control for between-individual variance. Senescence began at 9 years of age in two maternal performance traits. In both traits, females that produced more offspring in early life had faster rates of senescence. This tradeoff is evident alongside significant effects of individual quality on late life breeding performance. These results present rare evidence in support of the disposable soma and antagonistic pleiotropy theories of senescence from a wild vertebrate population and highlight the utility of mixed models for testing theories of ageing.     

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

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

Food availability as a major driver in the evolution of life‐history strategies of sibling species

Life‐history theory predicts trade‐offs between reproductive and survival traits such that different strategies or environmental constraints may yield comparable lifetime reproductive success among conspecifics. Food availability is one of the most important environmental factors shaping developmental processes. It notably affects key life‐history components such as reproduction and survival prospect. We investigated whether food resource availability could also operate as an ultimate driver of life‐history strategy variation between species. During 13 years, we marked and recaptured young and adult sibling mouse‐eared bats (Myotis myotis and Myotis blythii) at sympatric colonial sites. We tested whether distinct, species‐specific trophic niches and food availability patterns may drive interspecific differences in key life‐history components such as age at first reproduction and survival. We took advantage of a quasi‐experimental setting in which prey availability for the two species varies between years (pulse vs. nonpulse resource years), modeling mark‐recapture data for demographic comparisons. Prey availability dictated both adult survival and age at first reproduction. The bat species facing a more abundant and predictable food supply early in the season started its reproductive life earlier and showed a lower adult survival probability than the species subjected to more limited and less predictable food supply, while lifetime reproductive success was comparable in both species. The observed life‐history trade‐off indicates that temporal patterns in food availability can drive evolutionary divergence in life‐history strategies among sympatric sibling species.     

GENETIC CORRELATION BETWEEN RESISTANCE TO OXIDATIVE STRESS AND REPRODUCTIVE LIFE SPAN IN A BIRD SPECIES

Evolutionary theories propose that aging is the result of a trade‐off between self‐maintenance and reproduction, and oxidative stress may play a crucial role in such a trade‐off. Phenotypic manipulations have revealed that a high investment in reproduction leads to a decline in the organism's resistance to oxidative stress, which could in turn accelerate aging. Here, by using quantitative genetic analyses as a tool to disentangle genetic effects from phenotypic variances, the relationship between resistance to oxidative stress at sexual maturity and two key reproductive life‐history traits (i.e., number of breeding events during life and age at last reproduction) was analyzed in cross‐fostered zebra finches. The age of last reproduction had high narrow‐sense heritability, whereas the number of breeding events and oxidative stress resistance showed medium and low heritabilities, respectively. We detected positive genetic correlations between early resistance to oxidative stress and both life‐history traits, suggesting that the efficiency of the antioxidant machinery at maturity may be related to individual reproductive investment throughout lifetime, possibly by influencing the pattern of cellular senescence. Genes encoding for resistance to oxidative stress would have pleiotropic effects on reproductive capacity and aging. Further work is required to confirm this assert.     

Seasonal patterns in reproductive success of temperate‐breeding birds: Experimental tests of the date and quality hypotheses

For organisms in seasonal environments, individuals that breed earlier in the season regularly attain higher fitness than their late‐breeding counterparts. Two primary hypotheses have been proposed to explain these patterns: The quality hypothesis contends that early breeders are of better phenotypic quality or breed on higher quality territories, whereas the date hypothesis predicts that seasonally declining reproductive success is a response to a seasonal deterioration in environmental quality. In birds, food availability is thought to drive deteriorating environmental conditions, but few experimental studies have demonstrated its importance while also controlling for parental quality. We tested predictions of the date hypothesis in tree swallows (Tachycineta bicolor) over two breeding seasons and in two locations within their breeding range in Canada. Nests were paired by clutch initiation date to control for parental quality, and we delayed the hatching date of one nest within each pair. Subsequently, brood sizes were manipulated to mimic changes in per capita food abundance, and we examined the effects of manipulations, as well as indices of environmental and parental quality, on nestling quality, fledging success, and return rates. Reduced reproductive success of late‐breeding individuals was causally related to a seasonal decline in environmental quality. Declining insect biomass and enlarged brood sizes resulted in nestlings that were lighter, in poorer body condition, structurally smaller, had shorter and slower growing flight feathers and were less likely to survive to fledge. Our results provide evidence for the importance of food resources in mediating seasonal declines in offspring quality and survival.     

Diversity of age‐specific reproductive rates may result from ageing and optimal resource allocation

This paper reports the results of a dynamic programming model which optimizes resource allocation to growth, reproduction and repair of somatic damage, based on the disposable soma theory of ageing. Here it is shown that different age‐dependent patterns of reproductive rates are products of optimal lifetime strategies of resource partitioning. The array of different reproductive patterns generated by the model includes those in which reproduction begins at the maximum rate at maturity and then declines to the end of life, or increases up to a certain age and then drops. The observed patterns reflect optimal resource allocation shaped by the level of extrinsic mortality. A continuous decline in the reproductive rate from the start of reproduction is associated with high extrinsic mortality, and an early increase in the reproductive rate occurs under low extrinsic mortality. A long‐lived organism shows a low reproductive rate early in life, and short‐lived organisms start reproduction at the maximum rate.     

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.     

Experience versus effort: what explains dynamic heterogeneity with respect to age?

Age‐related patterns of survival and reproduction have been explained by accumulated experience (‘experience hypothesis’), increased effort (‘effort hypothesis’), and intrinsic differences in phenotypes (‘selection hypothesis’). We examined the experience and effort hypotheses using a 40‐year data set in a population of Leach's storm‐petrels Oceanodroma leucorhoa, long‐lived seabirds for which the effect of phenotypic variation has been previously demonstrated. Age was quantified by time since recruitment (‘breeding age’). The best model of adult survival included a positive effect of breeding age (1, 2, 3+ years), sex (male > female), and year. Among‐individuals variation (fixed heterogeneity) accounted for 31.6% of the variance in annual reproductive success. We further examined within‐individual patterns in reproductive success (dynamic heterogeneity) in the subset of individuals with at least five breeding attempts. Three distinct phases characterized reproductive success – early increase, long asymptotic peak, late decline. No effect of early reproductive output on longevity was found, however, early success was positively correlated with lifetime reproductive success. Reproductive success was lower earlier than later in life. Among the few natally philopatric individuals in the population, age of first breeding had no effect on longevity, lifetime reproductive success, or early reproductive success. No support for the effort hypothesis was found in this population. Instead, age‐specific patterns of survival and reproduction in these birds are best explained by the experience hypothesis over and above the effect of intrinsic differences among individuals.     

Evaluating the contributions of change in investment and change in efficiency to age‐related declines in male and female reproduction

It is commonly observed that reproduction decreases with age, often at a different rate in males and females. This phenomenon is generally interpreted as senescence. Such reproductive declines may stem from at least two sources: a change in resource allocation and a decline in the ability to convert resources into offspring. This distinction is important because a shift in resource allocation may be favoured by selection, while reduced efficiency is purely deleterious. We propose a way to distinguish whether a decline in reproduction is purely deleterious based on estimating reproductive investment, output, and their ratio, efficiency. We apply this approach to the hermaphroditic snail Physa acuta and demonstrate that both male and female functions decline with age. The male decline largely stems from reduced investment into male activity while female decline is due to increased reproductive inefficiency. This shows that age‐related declines in reproduction can occur for a number of different reasons, a distinction that is usually masked by the general term ‘senescence’. This approach could be applied to any species to evaluate age‐related reproductive decline. We advocate that future studies measure age trajectories of reproductive investment and output to explore the potential processes hidden behind the observation that reproduction declines with age.