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.     

Costs of reproduction and terminal investment by females in a semelparous marsupial

Evolutionary explanations for life history diversity are based on the idea of costs of reproduction, particularly on the concept of a trade-off between age-specific reproduction and parental survival, and between expenditure on current and future offspring. Such trade-offs are often difficult to detect in population studies of wild mammals. Terminal investment theory predicts that reproductive effort by older parents should increase, because individual offspring become more valuable to parents as the conflict between current versus potential future offspring declines with age. In order to demonstrate this phenomenon in females, there must be an increase in maternal expenditure on offspring with age, imposing a fitness cost on the mother. Clear evidence of both the expenditure and fitness cost components has rarely been found. In this study, we quantify costs of reproduction throughout the lifespan of female antechinuses. Antechinuses are nocturnal, insectivorous, forest-dwelling small (20-40 g) marsupials, which nest in tree hollows. They have a single synchronized mating season of around three weeks, which occurs on predictable dates each year in a population. Females produce only one litter per year. Unlike almost all other mammals, all males, and in the smaller species, most females are semelparous. We show that increased allocation to current reproduction reduces maternal survival, and that offspring growth and survival in the first breeding season is traded-off with performance of the second litter in iteroparous females. In iteroparous females, increased allocation to second litters is associated with severe weight loss in late lactation and post-lactation death of mothers, but increased offspring growth in late lactation and survival to weaning. These findings are consistent with terminal investment. Iteroparity did not increase lifetime reproductive success, indicating that terminal investment in the first breeding season at the expense of maternal survival (i.e. semelparity) is likely to be advantageous for females.     

NATURAL GENETIC VARIATION OF LIFE SPAN,REPRODUCTION, AND JUVENILE GROWTH IN DAPHNIA

The evolutionary theory of senescence predicts that high extrinsic mortality in natural populations should select for accelerated reproductive investment and shortened life span. Here, we test the theory with natural populations of the Daphnia pulex-pulicaria species complex, a group of freshwater zooplankton that spans an environmental gradient of habitat permanence. We document substantial genetic variation in demographic life-history traits among parent and hybrid populations of this complex. Populations from temporary ponds have shorter life spans, earlier and faster increases of intrinsic mortality risk, and earlier and steeper declines in fecundity than populations from permanent lakes. We also examine the age-specific contribution to fitness, measured by reproductive value, and to expected lifetime reproduction; these traits decline faster in populations from temporary ponds. Despite having more rapid senescence, pond Daphnia exhibit faster juvenile growth and higher early fitness, measured as population growth rate (r). Among populations within this species complex we observed negative genetic correlations between r and indices of life-history timing, suggesting trade-offs between early- and late-life performance. Our results cannot be explained by a trade-off between survival and fecundity or by nonevolutionary theories of senescence. Instead, our data are consistent with the evolutionary theory of senescence because the genetic variation in life histories we observed is roughly congruent with the temporal scale of environmental change in the field.     

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.     

Quantitative evidence for early life fitness defects from 32 longevity-associated alleles in yeast

Reduced fecundity has been associated with some alleles that enhance longevity in invertebrate and mammalian models. This observation has been suggested to support the antagonistic pleiotropy theory of aging, which predicts that alleles of some genes promoting fitness early in life have detrimental effects later in life that limit survival. In only a few cases, however, has the relative fitness of long-lived mutants been quantified through direct competition with the wild type genotype. Here we report the first comprehensive analysis of longevity/fitness trade-offs by measuring the relative fitness of 49 long-lived yeast variants in a direct competition assay with wild type cells. We find that 32 (65%) of these variants show a significant defect in fitness in this competition assay. In 26 (81%) of these cases, this reduction in fitness can be partially accounted for by reduced maximal growth rate during early life, usually resulting from a G0/G1-specific cell cycle defect. A majority of the less fit longevity-enhancing variants are associated with reduced mRNA translation. These findings are therefore consistent with the idea that enhanced longevity often comes with a fitness cost and suggest that this cost is often associated with variation in a subset of longevity factors, such as those regulating mRNA translation, growth, and reproduction.     

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.     

Climate‐dependent costs of reproduction: Survival and fecundity costs decline with length of the growing season and summer temperature

Costs of reproduction are expected to vary with environmental conditions thus influencing selection on life‐history traits. Yet, the effects of habitat conditions and climate on trade‐offs among fitness components remain poorly understood. For 2–5 years, we quantified costs of experimentally increased reproduction in two populations (coastal long‐season vs. inland short‐season) of two long‐lived orchids that differ in natural reproductive effort (RE; 30 vs. 75% fruit set). In both species, survival costs were found only at the short‐season site, whereas growth and fecundity costs were evident at both sites, and both survival and fecundity costs declined with increasing growing season length and/or summer temperature. The results suggest that the expression of costs of reproduction depend on the local climate, and that climate warming could result in selection favouring increased RE in both study species.     

Optimal life histories and the age-specific costs of reproduction

Increases in reproduction at a given age may carry costs measured as reductions in subsequent survival and/or future fertility. Such costs generate constraints within which natural selection may mould life histories to maximize fitness. In this paper, I derive expressions predicting the age-specific costs of reproduction conditional on the maximization of fitness. Survival costs should, on this hypothesis, vary as the inverse of the reproductive value curve; fertility costs should vary as the ratio of successive terms in the stable age distribution. For many organisms, this means that survival costs should increase markedly with age, while fertility costs should be nearly age-invariant. Data on such age-specific costs is scarce, but that which is available (mainly for humans) agrees with these predictions.     

Age and terminal reproductive attempt influence laying date in the thorn‐tailed rayadito

Age‐specific variation in reproductive effort can affect population dynamics, and is a key component of the evolution of reproductive tactics. Late‐life declines are a typical feature of variation in reproduction. However, the cause of these declines, and thus their implications for the evolution of life‐history tactics, may differ. Some prior studies have shown late‐life reproductive declines to be tied to chronological age, whereas other studies have found declines associated with terminal reproduction irrespective of chronological age. We investigated the extent to which declines in late life reproduction are related to chronological age, terminal reproductive attempt or a combination of both in the thorn‐tailed rayadito Aphrastura spinicauda, a small passerine bird that inhabits the temperate forest of South America. To this end we used long‐term data (10 years) obtained on reproductive success (laying date, clutch size and nestling weight) of females in a Chilean population. Neither chronological age nor terminal reproductive attempt explained variation in clutch size or nestling weight, however we observed that during the terminal reproductive attempt older females tended to lay later in the breeding season and younger females laid early in the breeding season, but this was not the case when the reproductive attempt was not the last. These results suggests that both age‐dependent and age‐independent effects influence reproductive output and therefore that the combined effects of age and physiological condition may be more relevant than previously thought.     

Experimental evidence of long‐term reproductive costs in a colonial nesting seabird

Trade‐offs between current and future reproduction are central to the evolution of life histories. Experiments that manipulate brood size provide an effective approach to investigating future costs of current reproduction. Most manipulative studies to date, however, have addressed only the short‐term effects of brood size manipulation. Our goal was to determine whether survival or breeding costs of reproduction in a long‐lived species manifest beyond the subsequent breeding season. To this end, we investigated long‐term survival and breeding effects of a multi‐year reproductive cost experiment conducted on black‐legged kittiwakes Rissa tridactyla, a long‐lived colonial nesting seabird. We used multi‐state capture–recapture modeling to assess hypotheses regarding the role of experimentally reduced breeding effort and other factors, including climate phase and colony size and productivity, on future survival and breeding probabilities during the 16‐yr period following the experiment. We found that forced nest failures had a positive effect on breeding probability over time, but had no effect on long‐term survival. This apparent canalization of survival suggests that adult survival is the most important parameter influencing fitness in this long‐lived species, and that adults should pay reproductive costs in ways that do not compromise this critical life history parameter. When declines in adult survival rate are observed, they may indicate populations of conservation concern.     

The evolution of parental and alloparental effort in cooperatively breeding groups: when should helpers pay to stay?

We used a reproductive skew framework to consider the evolutionof parental and alloparental effort in cooperatively breedinggroups. The model provides the first theoretical treatmentof rent payment (the "pay-to-stay" hypothesis) for the evolutionof helping behavior of subordinates. According to this hypothesis,not all helping behavior is kin selected, but group membershelp in order to be allowed to stay in the group and potentiallygain breeding positions later in life. We show that reproductiveconcessions may be replaced by complete skew and voluntary,costly alloparental effort by subordinates once future prospectsare included in fitness calculations. This suggests that incompleteskew observed in long-lived species is not due to dominantcontrol over reproduction. Rent payment is predicted to occurwhen relatedness between subordinate and dominant is low, survivalis high, ecological constraints are at least moderately tight,and retaining nonhelping subordinates harms the dominant'sfitness. Rent may also be required from related subordinatesif helping is very costly (leading to low voluntary helpingeffort) and ecological constraints are moderately tight. However, related subordinates do not need to have a positive net effecton the dominant's direct fitness to be accepted as group members.We also consider compensatory responses of dominant group membersas a potential threat to the stability of renting behavior.If dominants trade off parental effort against their own survival,they may selfishly reduce their own parental effort as a responseto increased help. As this improves their own survival, theprospects of territorial inheritance diminish for the subordinate,and subordinates should hence be less willing to accept therent agreement. However, we show that compensatory responsesby "lazy" parents prevent group formation only in borderlinecases.     

Quantitative evidence for early life fitness defects from 32 longevity-associated alleles in yeast

Reduced fecundity has been associated with some alleles that enhance longevity in invertebrate and mammalian models. This observation has been suggested to support the antagonistic pleiotropy theory of aging, which predicts that alleles of some genes promoting fitness early in life have detrimental effects later in life that limit survival. In only a few cases, however, has the relative fitness of long-lived mutants been quantified through direct competition with the wild type genotype. Here we report the first comprehensive analysis of longevity/fitness trade-offs by measuring the relative fitness of 49 long-lived yeast variants in a direct competition assay with wild type cells. We find that 32 (65%) of these variants show a significant defect in fitness in this competition assay. In 26 (81%) of these cases, this reduction in fitness can be partially accounted for by reduced maximal growth rate during early life, usually resulting from a G₀/G₁-specific cell cycle defect. A majority of the less fit longevity-enhancing variants are associated with reduced mRNA translation. These findings are therefore consistent with the idea that enhanced longevity often comes with a fitness cost and suggest that this cost is often associated with variation in a subset of longevity factors, such as those regulating mRNA translation, growth and reproduction.Key words: yeast, aging, antagonistic pleiotropy, fitness, translation, longevity, evolution     

SEASONAL DECLINES IN OFFSPRING FITNESS AND SELECTION FOR EARLY REPRODUCTION IN NYMPH-OVERWINTERING GRASSHOPPERS

In this study, I examine the effects of natural and experimentally induced variation in life cycle timing on offspring fitness in Arphia sulphurea and Chortophaga viridifasciata, to understand the selective pressures shaping phenology in these two species of nymph-overwintering grasshoppers. Because these species lack embryonic diapause, hatching varies over a two month range under natural conditions. I used a cold treatment to delay hatching of some egg pods and extend the natural range of hatching dates. Due to the shorter time for growth and poorer growing conditions late in the fall, late-hatching nymphs of both species grew to a smaller size before winter and suffered higher overwinter mortality, compared to early nymphs. In addition, late nymphs that did survive the winter became reproductive later in the following year's breeding season. Size- dependent mortality of offspring during the winter is a strong selective pressure favoring early reproduction in these species. Female adult life history traits appear responsive to the seasonal declines in offspring fitness, in that late-maturing females began reproducing sooner after adult maturation and reproduced at a more rapid rate, even at the expense of having shorter adult longevity and producing fewer total egg pods. Experimental manipulations were crucial in understanding the fitness consequences of intrapopulation variation in the timing of specific life-cycle events for these species.     

Lifetime fitness consequences of early‐life ecological hardship in a wild mammal population

Early‐life ecological conditions have major effects on survival and reproduction. Numerous studies in wild systems show fitness benefits of good quality early‐life ecological conditions (“silver‐spoon” effects). Recently, however, some studies have reported that poor‐quality early‐life ecological conditions are associated with later‐life fitness advantages and that the effect of early‐life conditions can be sex‐specific. Furthermore, few studies have investigated the effect of the variability of early‐life ecological conditions on later‐life fitness. Here, we test how the mean and variability of early‐life ecological conditions affect the longevity and reproduction of males and females using 14 years of data on wild banded mongooses (Mungos mungo). Males that experienced highly variable ecological conditions during development lived longer and had greater lifetime fitness, while those that experienced poor early‐life conditions lived longer but at a cost of reduced fertility. In females, there were no such effects. Our study suggests that exposure to more variable environments in early life can result in lifetime fitness benefits, whereas differences in the mean early‐life conditions experienced mediate a life‐history trade‐off between survival and reproduction. It also demonstrates how early‐life ecological conditions can produce different selection pressures on males and females.     

The forms and fitness cost of senescence: age-specific recapture, survival, reproduction, and reproductive value in a wild bird population

Longitudinal studies of senescence accumulate rapidly from natural populations. However, it is largely unknown whether different fitness components senesce in parallel, how reproductive and survival senescence contribute to declines in reproductive value, and how large the fitness cost of senescence is (the difference between the observed reproductive value and the hypothetical reproductive value, if senescence would not occur). We analyzed age-specific survival in great tits Parus major and combined our results with analyses of reproductive senescence to address these issues. Recapture probability of breeding females declined with age, suggesting age-specific increases in skipped or failed breeding and highlighting an important bias that studies of senescence in wild populations should incorporate. Survival probability also declined with age and in parallel with recruit production. Reproductive value decreased 87% between age 1 and age 9 but at a fitness cost of only 4%; the proportion of the contribution of reproductive senescence versus survival senescence to this cost was 0.7. For 11 other species, we estimated fitness costs of senescence of 6%-63% (average: birds, 9%; mammals, 42%), with relative contributions of reproductive senescence of 0.0-0.7 (average: birds, 0.4; mammals, 0.3). We suggest that understanding when and why reproductive and survival senescence differ will help in the identification of proximate mechanisms underlying variation in rates of senescence and its evolution.     

Cost-free lifespan extension via optimization of gene expression in adulthood aligns with the developmental theory of ageing

Ageing evolves because the force of selection on traits declines with age but the proximate causes of ageing are incompletely understood. The ‘disposable soma’ theory of ageing (DST) upholds that competitive resource allocation between reproduction and somatic maintenance underpins the evolution of ageing and lifespan. In contrast, the developmental theory of ageing (DTA) suggests that organismal senescence is caused by suboptimal gene expression in adulthood. While the DST predicts the trade-off between reproduction and lifespan, the DTA predicts that age-specific optimization of gene expression can increase lifespan without reproduction costs. Here we investigated the consequences for lifespan, reproduction, egg size and individual fitness of early-life, adulthood and post-reproductive onset of RNAi knockdown of five ‘longevity’ genes involved in key biological processes in Caenorhabditis elegans. Downregulation of these genes in adulthood and/or during post-reproductive period increases lifespan, while we found limited evidence for a link between impaired reproduction and extended lifespan. Our findings demonstrate that suboptimal gene expression in adulthood often contributes to reduced lifespan directly rather than through competitive resource allocation between reproduction and somatic maintenance. Therefore, age-specific optimization of gene expression in evolutionarily conserved signalling pathways that regulate organismal life histories can increase lifespan without fitness costs.     

Human-resource subsidies alter the dietary preferences of a mammalian top predator

Seasonal fitness declines are common, but the relative contribution of different reproductive components to the seasonal change in the production of reproductive young, and the component-specific drivers of this change is generally poorly known. We used long-term data (17 years) on breeding time (i.e. date of first egg laid) in northern wheatears (Oenanthe oenanthe) to investigate seasonal reproductive patterns and estimate the relative contributions of reproductive components to the overall decline in reproduction, while accounting for factors potentially linked to seasonal declines, i.e. individual and habitat quality. All reproductive components—nest success (reflecting nest predation rate), clutch size, fledging success and recruitment success—showed a clear decline with breeding time whereas subsequent adult survival did not. A non-linear increase in nest predation rate caused nest success to decline rapidly early in the season and level off at ~80 % success late in the breeding season. The combined seasonal decline in all reproductive components caused the mean production of recruits per nest to drop from around 0.7–0.2; with the relative contribution greatest for recruitment success which accounted for ~50 % of the decline. Our data suggest that changing environmental conditions together with effects of nest predation have strong effects on the seasonal decline in fitness. Our demonstration of the combined effects of all reproductive components and their relative contribution shows that omitting data from later stages of breeding (recruitment) can greatly underestimate seasonal fitness declines.     

Differences in plastic responses to defoliation due to variation in the timing of treatments for two species of Sesbania (Fabaceae)

BACKGROUND AND AIMS: Plastic responses to stress in components of reproduction can have important effects on plant fitness and can vary both within and between species. Responses may also depend on when in the life cycle stress occurs. Here, it is predicted that the timing of initiation of a stress, defoliation, would affect the pattern of plastic responses. These differences should occur because some components of reproduction, such as flower number, are determined earlier in a plant's life than others, such as individual seed mass. METHODS: To test this prediction, 50 % artificial defoliation treatments were initiated at four different times for Sesbania macrocarpa and S. vesicaria. Responses were measured in plant size, number of flowers, number of flowers/plant size, fruit set, number of seeds per fruit, individual seed mass and total seed mass per plant. KEY RESULTS: For S. vesicaria, changes in the timing of stress changed the severity, but not the pattern of response. For S. macrocarpa, plastic responses to defoliation varied strikingly between early and late treatments. Late treatments resulted in over-compensation in this species. Sesbania macrocarpa was generally more plastic than S. vesicaria and the species showed opposite responses for most components of reproduction. CONCLUSIONS: While there were effects of timing of defoliation and differences between species, the nature of these effects did not precisely fit our predictions. Our results suggest that differences in the length and flexibility of the life cycles of the two species allowed for unexpected variation in responses. For example, because flower production continued after the last treatment in S. vesicaria, responses were not constrained to reductions in individual seed mass.     

Exploring the genetics of aging in a wild passerine bird

Senescence is the decline in survival and reproduction as an organism ages and is known to occur in collared flycatchers Ficedula albicollis. We consider annual fitness (the estimated genetic contribution that an individual makes to next year's gene pool) as a measure of age-specific fitness. We apply a restricted maximum likelihood linear mixed-model approach on 25 years of data on 3,844 male and 4,992 female collared flycatchers. Annual fitness had a significant additive genetic component (h2 of about 4%). Annual fitness declined at later ages in both sexes. Using a random regression animal model, we show that the observed age-related phenotypic changes in annual fitness were not present on the additive genetic level, contrary to predictions of genetic hypotheses of senescence. Our study suggests that patterns of aging in the wild need to be interpreted with caution in terms of underlying genetics because they may be largely determined by environmental processes.     

Evolutionary senescence in plants

Senescence is a decline in age-specific survival and reproduction with advancing age. Studies of evolutionary plant senescence are designed to explain this decline in life history components within the context of natural selection. A review of studies of plant demography reveals senescent declines in both annual and perennial plants, but also suggests that there are some plant species which may not be expected to show senescence. Thus, future comparative studies of closely related species, with and without senescence, should be possible. The assumptions of the major evolutionary theories of senescence are evaluated for their validity with respect to plants. Different plant species violate one or more of the assumptions of the theories, yet the consequences of violating these assumptions have never been investigated. Whereas, to date, evolutionary senescence has been studied only indirectly in plants, it is concluded that plants provide good experimental systems for clarifying our understanding of senescence in natural populations.