Age-specific changes in different components of reproductive output in female reindeer: terminal allocation or senescence?

Two different processes can lead to a change in individual reproductive output with age in long-lived iteroparous vertebrates. The senescence hypothesis predicts a decline of performance in old age, whereas the terminal allocation hypothesis predicts an increase. Using long-term (>30 years) individually based data of female reindeer, we first assessed age-specific variation in body mass and different components of reproductive output. Then we investigated the contribution of senescence and terminal allocation (the increase in components of reproductive output) processes for shaping observed patterns. We found that female reindeer body mass increased up to about 11.5 years of age, and decreased afterwards, supporting the senescence hypothesis. Calf birth mass, both in absolute terms or for a given female mass, first increased and then declined with female age, also supporting the senescence hypothesis. The female mass gain (June–September) decreased with increasing age, and female change in mass between 2 consecutive years decreased with female age, all patterns again supporting the senescence hypothesis. However, the autumn calf mass did not change with age. Calf body mass in autumn tended to be positively related to female mass gain, supporting a quality effect. Raising a calf had a marked negative effect on female mass gain, indicating energetic reproductive costs of raising a calf. Calf body mass in autumn did not influence yearly female mass change. Overall, our results provided consistent evidence for general effects of senescence on most components of reproductive output and highlighted that both individual heterogeneity and reproductive costs shape female reindeer reproductive tactics.     

The cost of growing large: costs of post‐weaning growth on body mass senescence in a wild mammal

Individual body mass often positively correlates with survival and reproductive success, whereas fitness costs of growing large are rarely detected in vertebrates in the wild. Evidence that adult body mass progressively declines with increasing age is accumulating across mammalian populations. Growing fast to a large body can increase the cellular damage accumulated throughout life, leading body growth in early life to be negatively associated with the rate of body mass senescence. Moreover, the onset of mass senescence may strongly depend on both sex‐specific reproductive tactics and environmental conditions. Assessing the timing and the rate of body mass decline with increasing age thus offers an opportunity to look for costs of having grown fast, especially after a poor start during early life, in both sexes and in different environments. Using a unique dataset including 30 years of longitudinal data on age‐specific body mass collected in two roe deer Capreolus capreolus populations subjected to contrasted environmental conditions, we looked for potential costs of high post‐weaning growth rate in terms of steeper rate of body mass senescence. Our analyses of body mass senescence accounted for the potential variation in the onset of senescence and allowed explicit comparisons of this variable between sexes and populations. Higher growth rates late in the growing period (after weaning) were associated with a steeper rate of body mass senescence, regardless of early mass (gained before weaning), but at different extents depending on sex and environmental conditions. Body mass senescence occurred earlier in males than in females, especially in the population facing limiting resources. In the wild, although heavy individuals generally survive better than small ones, the costs of growing large late in the growing period only became apparent late in life through mass senescence.     

Contrasting life histories in neighbouring populations of a large mammal

Background

A fundamental life history question is how individuals should allocate resources to reproduction optimally over time (reproductive allocation). The reproductive restraint hypothesis predicts that reproductive effort (RE; the allocation of resources to current reproduction) should peak at prime-age, whilst the terminal investment hypothesis predicts that individuals should continue to invest more resources in reproduction throughout life, owing to an ever-decreasing residual reproductive value. There is evidence supporting both hypotheses in the scientific literature.

Methodology/Principal Findings

We used an uncommonly large, 38 year dataset on Alpine chamois (Rupicapra rupicapra) shot at various times during the rutting period to test these two hypotheses. We assumed that body mass loss in rutting males was strongly related to RE and, using a process-based approach, modelled how male relative mass loss rates varied with age. For different regions of our study area, we provide evidence consistent with different hypotheses for reproductive allocation. In sites where RE declined in older age, this appears to be strongly linked to declining body condition in old males. In this species, terminal investment may only occur in areas with lower rates of body mass senescence.

Conclusions/Significance

Our results show that patterns of reproductive allocation may be more plastic than previously thought. It appears that there is a continuum from downturns in RE at old age to terminal investment that can be manifest, even across adjacent populations. Our work identifies uncertainty in the relationship between reproductive restraint and a lack of competitive ability in older life (driven by body mass senescence); both could explain a decline in RE in old age and may be hard to disentangle in empirical data. We discuss a number of environmental and anthropogenic factors which could influence reproductive life histories, underlining that life history patterns should not be generalised across different populations.     

Age,state, environment,and season dependence of senescence in body mass

Senescence is a highly variable process that comprises both age‐dependent and state‐dependent components and can be greatly affected by environmental conditions. However, few studies have quantified the magnitude of age‐dependent and state‐dependent senescence in key life‐history traits across individuals inhabiting different spatially structured and seasonal environments. We used longitudinal data from wild female yellow‐bellied marmots (Marmota flaviventer), living in two adjacent environments that differ in elevation and associated phenology, to quantify how age and individual state, measured as “time to death,” affect body mass senescence in different environments. Further, we quantified how patterns of senescence differed between two biologically distinct seasons, spring, and late summer. Body mass senescence had an age‐dependent component, expressed as a decrease in mass in old age. Overall, estimated age‐dependent senescence was greater in females living in the more favorable lower elevation environment, than in the harsher higher elevation environment, and greater in late summer than in spring. Body mass senescence also had a state‐dependent component, captured by effects of time to death, but only in the more favorable lower elevation environment. In spring, body mass gradually decreased from 2 years before death, whereas in late summer, state‐dependent effects were expressed as a terminal decrease in body mass in the last year of life. Contrary to expectations, we found that senescence was more likely to be observed under more favorable environmental conditions, rather than under harsher conditions. By further demonstrating that senescence patterns differ among seasons, our results imply that within‐year temporal environmental variation must be considered alongside spatial environmental variation in order to characterize and understand the pattern and magnitude of senescence in wild populations.     

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

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

Size delays female senescence in a medium sized marsupial: The effects of maternal traits on annual fecundity in the northern brown bandicoot (Isoodon macrourus)

The degree to which females allocate resources between current reproduction, future fecundity and survival is a central theme in life history theory. We investigated two hypotheses proposed to explain patterns of reproductive investment, terminal investment and senescence, by examining the effects of maternal traits (age and maternal mass) on annual fecundity in female northern brown bandicoots, Isoodon macrourus (Marsupialia: Peramelidae). We found that annual fecundity in females declined in their final year of reproduction, indicating reproductive senescence. Maternal mass significantly influenced the rate of senescence and, in turn, a female's lifetime reproductive output. Mass had little effect on fecundity in 1st and 2nd year females, but a positive relationship with fecundity in 3rd year females. This meant that heavy, 3rd year females did not suffer the decline in fecundity shown in light 3rd year females. For 1st year females, mass and leg length increased between their first and second reproductive seasons, indicating a temporary shift, from the allocation of resources to reproduction, to increasing condition or structural size post their first breeding event. There were no net changes to body mass in subsequent years. We suggest that this year of post‐reproductive growth has important consequences for senescent effects on reproduction. Overall, results provided support for the effects of senescence on annual fecundity. Our findings were not consistent with the terminal investment hypothesis; reproductive output did not increase in females' final reproductive season despite a rapid decline in survival. However, this notion cannot be entirely dismissed; other measures of reproductive performance not examined here (e.g. offspring mass) may have provided an indication that females did increase their effort at the end of their lifespan. This study highlights the difficulty of measuring reproductive costs and the importance of understanding the combined effects of specific characteristics of an individual when interpreting reproductive strategies in iteroparous organisms.     

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.     

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.     

Age-dependent terminal declines in reproductive output in a wild bird

In many iteroparous species individual fitness components, such as reproductive output, first increase with age and then decline during late-life. However, individuals differ greatly in reproductive lifespan, but reproductive declines may only occur in the period just before their death as a result of an age-independent decline in physiological condition. To fully understand reproductive senescence it is important to investigate to what extent declines in late-life reproduction can be explained by age, time until death, or both. However, the study of late-life fitness performance in natural populations is challenging as the exact birth and death dates of individuals are often not known, and most individuals succumb to extrinsic mortality before reaching old age. Here, we used an exceptional long-term longitudinal dataset of individuals from a natural, closed, and predator-free population of the Seychelles warbler (Acrocephalus sechellensis) to investigate reproductive output, both in relation to age and to the time until the death of an individual (reverse-age approach). We observed an initial age-dependent increase in reproductive output that was followed by a decline in old age. However, we found no significant decline in reproductive output in the years directly preceding death. Although post-peak reproductive output declined with age, this pattern differed between terminal and non-terminal reproductive attempts, and the age-dependence of the terminal breeding attempt explained much of the variation in age-specific reproductive output. In fact, terminal declines in reproductive output were steeper in very old individuals. These results indicate that not only age-dependent, but also age-independent factors, such as physiological condition, need to be considered to understand reproductive senescence in wild-living animals.     

The oxidative costs of reproduction are group-size dependent in a wild cooperative breeder

Life-history theory assumes that reproduction entails a cost, and research on cooperatively breeding societies suggests that the cooperative sharing of workloads can reduce this cost. However, the physiological mechanisms that underpin both the costs of reproduction and the benefits of cooperation remain poorly understood. It has been hypothesized that reproductive costs may arise in part from oxidative stress, as reproductive investment may elevate exposure to reactive oxygen species, compromising survival and future reproduction and accelerating senescence. However, experimental evidence of oxidative costs of reproduction in the wild remains scarce. Here, we use a clutch-removal experiment to investigate the oxidative costs of reproduction in a wild cooperatively breeding bird, the white-browed sparrow weaver, Plocepasser mahali. Our results reveal costs of reproduction that are dependent on group size: relative to individuals in groups whose eggs were experimentally removed, individuals in groups that raised offspring experienced an associated cost (elevated oxidative damage and reduced body mass), but only if they were in small groups containing fewer or no helpers. Furthermore, during nestling provisioning, individuals that provisioned at higher rates showed greater within-individual declines in body mass and antioxidant protection. Our results provide rare experimental evidence that reproduction can negatively impact both oxidative status and body mass in the wild, and suggest that these costs can be mitigated in cooperative societies by the presence of additional helpers. These findings have implications for our understanding of the energetic and oxidative costs of reproduction, and the benefits of cooperation in animal societies.     

Sex differences in senescence: the role of intra-sexual competition in early adulthood

Males and females frequently differ in their rates of ageing, but the origins of these differences are poorly understood. Sex differences in senescence have been hypothesized to arise, because investment in intra-sexual reproductive competition entails costs to somatic maintenance, leaving the sex that experiences stronger reproductive competition showing higher rates of senescence. However, evidence that sex differences in senescence are attributable to downstream effects of the intensity of intra-sexual reproductive competition experienced during the lifetime remains elusive. Here, we show using a 35 year study of wild European badgers (Meles meles), that (i) males show higher body mass senescence rates than females and (ii) this sex difference is largely attributable to sex-specific downstream effects of the intensity of intra-sexual competition experienced during early adulthood. Our findings provide rare support for the view that somatic maintenance costs arising from intra-sexual competition can cause both individual variation and sex differences in senescence.     

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.     

Short day lengths delay reproductive aging

Caloric restriction and hormone treatment delay reproductive senescence in female mammals, but a natural model of decelerated reproductive aging does not presently exist. In addition to describing such a model, this study shows that an abiotic signal (photoperiod) can induce physiological changes that slow senescence. Relative to animals born in April, rodents born in September delay their first reproductive effort by up to 7 mo, at which age reduced fertility is expected. We tested the hypothesis that the shorter day lengths experienced by late-born Siberian hamsters ameliorate the reproductive decline associated with advancing age. Short-day females (10L:14D) achieved puberty at a much later age than long-day animals (14L:10D) and had twice as many ovarian primordial follicles. At 10 mo of age, 86% of females previously maintained in short day lengths produced litters, compared with 58% of their long day counterparts. Changes in pineal gland production of melatonin appear to mediate the effects of day length on reproductive aging; only 30% of pinealectomized females housed in short days produced litters. Exposure to short days induces substantial decreases in voluntary food intake and body mass, reduced ovarian estradiol secretion, and enhanced production of melatonin. One or more of these changes may account for the protective effect of short day lengths on female reproduction. In delaying reproductive senescence, the decrease in day length after the summer solstice is of presumed adaptive significance for offspring born late in the breeding season that first breed at an advanced chronological age.     

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.     

Can kin selection facilitate the evolution of the genetic program of senescence?

The theory of adaptive senescence, or phenoptosis (“altruistic suicide” of the organism), implies that mutations enhancing mortality growth with age (“senescence genes”) can be favored by selection under some circumstances, although the nature of these circumstances and the frequency of their occurrence are not clear. Here I demonstrate by means of computer simulation that senescence genes can spread in the population’s gene pool via the mechanism of kin selection if two conditions are met. First, the population must have high viscosity (low intermixing), which provides positive correlation between spatial proximity of individuals and their relatedness, an important precondition for kin selection. Second, prior to acquisition of the senescence genes, there must be a sufficiently fast decline in the reproductive potential with age, while viability should decrease slower or remain constant. These conditions are probably met in some territorial and social species with severe competition for social rank and mating partners.     

Decline in mitochondrial bioenergetics and shift to ketogenic profile in brain during reproductive senescence

Background

We have previously demonstrated that mitochondrial bioenergetic deficits precede Alzheimer's pathology in the female triple transgenic Alzheimer's (3xTgAD) mouse model. Herein, we sought to determine the impact of reproductive senescence on mitochondrial function in the normal non-transgenic (nonTg) and 3xTgAD female mouse model of AD.

Methods

Both nonTg and 3xTgAD female mice at 3, 6, 9, and 12 months of age were sacrificed and mitochondrial bioenergetic profile as well as oxidative stress markers were analyzed.

Results

In both nonTg and 3xTgAD mice, reproductive senescence paralleled a significant decline in PDH, and Complex IV cytochrome c oxidase activity and mitochondrial respiration. During the reproductive senescence transition, both nonTg and 3xTgAD mice exhibited greater individual variability in bioenergetic parameters suggestive of divergent bioenergetic phenotypes. Following transition through reproductive senescence, enzymes required for long-chain fatty acid (HADHA) and ketone body (SCOT) metabolism were significantly increased and variability in cytochrome c oxidase (Complex IV) collapsed to cluster at a ∼ 40% decline in both the nonTg and 3xTgAD brain which was indicative of alternative fuel generation with concomitant decline in ATP generation.

Conclusions

These data indicate that reproductive senescence in the normal nonTg female brain parallels the shift to ketogenic/fatty acid substrate phenotype with concomitant decline in mitochondrial function and exacerbation of bioenergetic deficits in the 3xTgAD brain.

General significance

These findings provide a plausible mechanism for increased life-time risk of AD in postmenopausal women and suggest an optimal window of opportunity to prevent or delay decline in bioenergetics during reproductive senescence.     

Senescence of immune defence in Bombus workers

Abstract 1. Senescence in workers of social insects is a particularly intriguing life-history trait as the future fitness of workers relies primarily on age-dependent survival rate. The pattern of senescence of immune defence traits was investigated under laboratory conditions in workers of two bumble bees: Bombus terrestris and B. lucorum .
2. In both species, there was a significant decrease with age in the ability to encapsulate a foreign object (a global measure of the efficiency of immune systems). This pattern of senescence was observed in all colonies in B. terrestris (seven) and B. lucorum (eight) assayed, even though, for the latter, there was some heterogeneity among colonies.
3. In B. terrestris , two other measures of immune defence were taken: the relative percentage of fat body in the abdomen and the concentration of haemocytes (the immune defence cells). The quantity of fat body increased only slightly with age and there was no effect for the concentration of haemocytes. Interestingly, the concentration of haemocytes decreased strongly after an encapsulation response, regardless of the age of workers.
4. The importance of the senescence pattern observed for the immune defence traits is discussed in the context of the social biology of workers.     

The Body Size-Dependent Diet Composition of North American Sea Ducks in Winter

Daily food requirements scale with body mass and activity in animals. While small species of birds have higher mass-specific field metabolic rates than larger species, larger species have higher absolute energy costs. Under energy balance, we thus expect the small species to have a higher energy value diet. Also the weight and time constraints for flighted and diurnal foragers should set a maximum to the amount of prey items taken in one meal and to the daily number of meals, respectively. Further, avoidance of competition causes the species to reduce the amount of shared prey in their diet. Some diet segregation is therefore to be expected between species. We tested these hypotheses and investigated the role of body mass in the diet composition of 12 sea duck species (Somateria mollissima, Somateria spectabilis, Somateria fischeri, Polysticta stelleri, Bucephala clangula, Bucephala islandica, Bucephala albeola, Melanitta nigra, Melanitta perspicillata, Melanitta deglandi, Histrionicus histrionicus and Clangula hyemalis) wintering in North America. This study was based on a literature survey with special emphasis given to the diet data from the former US Bureau of Biological Survey. The data supported our hypothesis that the energy value of winter diet of sea ducks scales negatively with body mass. Diet diversity also scaled negatively with body mass. Our results suggest the existence of a minimum for the energy value of avian diets.     

Changes in intracellular pH in French-bean nodules induced by senescence and nitrate treatment

Intracellular pH of Phaseolus nodules was determined by using radioactive 5,5-dimethyloxazolidine-2,4-dione (DMO) as a probe. A continuous decline in the intracellular pH was observed when nodule age increased. The extracellular volume of nodules, required for the pH calculation, was the lowest in mature nodules and increased in senescing nodules. Low concentrations of nitrate in the culture medium induced a drop in nitrogen fixation associated with a decrease in the intracellular pH. Acidic proteolysis measured by in vitro hydrolysis of leghemoglobin was strongly stimulated under these conditions. In Phaseolus nodules, senescence and nitrate treatment were similarly characterized by a lower intracellular pH and an active proteolysis which both contributed to a decline in nitrogen fixation capacities.     

Effect of juvenile hormone on senescence in males with terminal investment

Senescence, a decline in survival and reproductive prospects with age, is controlled by hormones. In insects, juvenile hormone (JH) is involved in senescence with captive individuals, but its effect under natural conditions is unknown. We have addressed this gap by increasing JH levels in young and old wild males of the damselfly Hetaerina americana. We assessed survival in males that were treated with a JH analogue (methoprene), which is known to promote sexual activity, and an immune challenge, which is known to promote terminal investment in reproduction in the studied species. We replicated the same procedure in captivity (to control for environmental variation), where males were deprived of any activity or food. We expected old males to show the lowest survival after being treated with JH and immune‐challenged, because the effect of terminal investment on senescence would be exacerbated by JH. However, this should be the case for wild animals, but not for captive animals, as the effects of JH and immune challenge should lead to an increase in high energetic‐demanding activities only occurring in the wild. Old animals died sooner compared with young animals in both the wild and captivity, confirming that males are subject to senescence. In wild but not captive animals, JH decreased survival in young males and increased it in old males, confirming that JH is sensitive to the environment when shaping animal senescence. Immune challenge had no effect on survival, suggesting no effect of terminal investment on senescence. Additionally, contrary to the expected effects of terminal investment, with an immune challenge, recapture rates increased in young males and decreased in old males. Our results show that male senescence in the wild is mediated by JH and that terminal investment does not cause senescence. One explanation is that animals undergoing senescence and terminal investment modify their feeding behaviour to compensate for their physiological state.