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.     

Age-specific survival and reproductive performances in fur seals: evidence of senescence and individual quality

Life history theory hypothesises that breeding events induce reproductive costs that may vary among individuals. However, the growing number of studies addressing this question are taxonomically biased, therefore impeding the generalisation of this hypothesis, especially with regard to marine top predators. This study investigated age‐related survival and breeding performances in subantarctic fur seal (Arctocephalus tropicalis) females from Amsterdam Island, southern Indian Ocean. Using multistate capture–recapture models on data obtained from known‐age tagged females over eight consecutive years, we tested for evidence of senescence, individual quality, and reproductive costs in terms of future survival and fecundity. Adult female yearly survival appeared high and constant throughout time. While a two age‐class model was preferred in non‐breeders, breeding females exhibited three age classes with a maximum survival for the prime‐age class (7–12 years). Survival and reproductive probabilities decreased from 13 years onward, suggesting senescence in this population. Survival was lower for non‐breeders than for breeders, among both prime‐aged (0.938 vs 0.982) and older (0.676 vs 0.855) females. Furthermore, non‐breeders exhibited higher probabilities of being non‐breeders the following year than did breeders (0.555 vs 0.414). Such results suggest consistency in female breeding performance over years, supporting the hypothesis that non‐breeding tend to occur among lower quality individuals rather than representing an alternative strategy to enhance residual reproductive value. However, the high proportion of females that did not breed during two consecutive years, and the lower probability of being a successful breeder after a greater reproductive effort confirmed the existence of reproductive costs, especially during the second half of the lactation. These results also suggest that younger age‐classes included a higher proportion of lower quality individuals, which are likely to face higher costs of reproduction. Such hypotheses lead to consider the first breeding event as a filter generating a within‐cohort selection process in females.     

Heterogeneity in individual quality overrides costs of reproduction in female reindeer

Reproductive allocation at one age is predicted to reduce the probability of surviving to the next year or to lead to a decrease in future reproduction. This prediction assumes that reproduction involves fitness costs. However, few empirical studies have assessed whether such costs may vary with the age at primiparity or might be overridden by heterogeneities in individual quality. We used data from 35 years’ monitoring of individually marked semi-domestic reindeer females to investigate fitness costs of reproduction. Using multi-state statistical models, we compared age-specific survival and reproduction among four reproductive states (never reproduced, experienced non-breeders, reproduced but did not wean offspring, and reproduced and weaned offspring) and among contrasted age at primiparity. We assessed whether reproductive costs occurred, resulting in a trade-off between current reproduction and future reproduction or survival, and whether early maturation was costly or rather reflected differences in individual quality of survival and reproduction capabilities. We did not find any evidence for fitness costs of reproduction in female reindeer. We found no cost of gestation and lactation in terms of future reproduction and survival. Conversely, successful breeders had higher survival and subsequent reproductive success than experienced non-breeders and unsuccessful breeders, independently of the age at primiparity. Moreover, it was beneficial to mature earlier, especially for females that successfully weaned their first offspring. Successful females at early primiparity remained successful throughout their life, clearly supporting the existence of marked among-female differences in quality. The weaning success peaked for multiparous females and was lower for first-time breeders, indicating a positive effect of experience on reproductive performance. Our findings emphasize an overwhelming importance of individual quality and experience to account for observed variation in survival and reproductive patterns of female reindeer that override trade-offs between current reproduction and future performance, at least in the absence of harsh winters.     

Determinants of age at first reproduction and lifetime breeding success revealed by full paternity assignment in a male ungulate

Age at first reproduction is an important determinant of individual variation in reproductive success in ungulates, but few studies have examined its relationship with later fitness‐related traits in males. We used a long‐term individual based study of a harvested moose population to quantify the individual reproductive performance and survival of males, as well as to examine the determinants of age at first reproduction and consequences of age at first reproduction on lifetime breeding success. The probability that a male successfully reproduced at the age of two was negatively related to the mean age of adult males in the population, but the relationship weakened with increasing population size. Large antlers and large body mass relative to other males in the population increased the number of calves sired at their first successful mating season. In addition, those that successfully reproduced as two year‐olds were more likely to sire calves the next year, making them more productive at a given age compared to those that first reproduced at the age of three or older. We emphasize the importance for males to start reproducing as soon as possible in a harvested population to gain lifetime fitness benefits, as surviving the hunt is a major determinant of reproductive success in this population. We found no costs of early reproduction in males, hence leading to high individual heterogeneity in male reproductive performance. The apparent lack of reproductive costs could partly be explained by the age distribution in the population, individual variation in early‐life body mass and antler size, and differences in probabilities of being hunted of successful and unsuccessful males.     

Is bigger better? The relationship between size and reproduction in female Asian elephants

The limited availability of resources is predicted to impose trade‐offs between growth, reproduction and self‐maintenance in animals. However, although some studies have shown that early reproduction suppresses growth, reproduction positively correlates with size in others. We use detailed records from a large population of semi‐captive elephants in Myanmar to assess the relationships between size (height and weight), reproduction and survival in female Asian elephants, a species characterized by slow, costly life history. Although female height gain during the growth period overlapped little with reproductive onset in the population, there was large variation in age at first reproduction and only 81% of final weight had been reached by peak age of reproduction at the population level (19 years). Those females beginning reproduction early tended to be taller and lighter later in life, although these trends were not significant. We found that taller females were more likely to have reproduced by a given age, but such effects diminished with age, suggesting there may be a size threshold to reproduction which is especially important in young females. Because size was not linked with female survival during reproductive ages, the diminishing effect of height on reproduction with age is unlikely to be due to biased survival of larger females. We conclude that although reproduction may not always impose significant costs on growth, height may be a limiting factor to reproduction in young female Asian elephants, which could have important implications considering their birth rates are low and peak reproduction is young – 19 years in this population.     

Individual variation in reproductive costs of reproduction: high-quality females always do better

1. Although life-history theory predicts substantial costs of reproduction, individuals often show positive correlations among life-history traits, rather than trade-offs. The apparent absence of reproductive costs may result from heterogeneity in individual quality. 2. Using detailed longitudinal data from three contrasted ungulate populations (mountain goats, Oreamnos americanus; bighorn sheep, Ovis canadensis; and roe deer, Capreolus capreolus), we assessed how individual quality affects the probability of detecting a cost of current reproduction on future reproduction for females. We used a composite measure of individual quality based on variations in longevity (all species), success in the last breeding opportunity before death (goats and sheep), adult mass (all species), and social rank (goats only). 3. In all species, high-quality females consistently had a higher probability of reproduction, irrespective of previous reproductive status. In mountain goats, we detected a cost of reproduction only after accounting for differences in individual quality. Only low-quality female goats were less likely to reproduce following years of breeding than of nonbreeding. Offspring survival was lower in bighorn ewes following years of successful breeding than after years when no lamb was produced, but only for low-quality females, suggesting that a cost of reproduction only occurred for low-quality females. 4. Because costs of reproduction differ among females, studies of life-history evolution must account for heterogeneity in individual quality.     

Mechanisms and reproductive consequences of breeding dispersal in a specialist predator under temporally varying food conditions

Individual variation in breeding dispersal has extensive ecological and evolutionary consequences, but the factors driving individual dispersal behaviour and their fitness consequences remain poorly understood. Our data on dispersal events of a rodent‐specialist predator, the Eurasian kestrel Falco tinnunculus, over 20 years in western Finland offers a unique opportunity to explore the mechanisms underlying breeding dispersal behaviour and its reproductive consequences in a wild bird population. Sex, age, body condition and previous breeding success affected breeding dispersal. Dispersal distances were longer in females than in males as well as longer in yearlings than in older individuals. Body condition was positively correlated to breeding dispersal distances, particularly for females. The lowest dispersal distances were recorded for intermediate brood sizes in the year preceding dispersal. Our results highlight sex‐ and environment‐specific consequences of breeding dispersal on reproductive performance. During increase phases of the three‐year vole cycles, males dispersing further had lower reproductive performance after dispersal, whereas in females, long breeding dispersal distances were associated with increased breeding success under all environmental conditions. These results suggest benefits associated to breeding dispersal in females, potentially related to large spatio‐temporal variation in main food abundance and intensity of intra‐specific competition. Breeding dispersal of males was costly during increasing food abundance, indicating the potential fitness benefits of environmental familiarity in this migratory species. Overall, our results indicate that both individual traits and environmental factors interact to shape breeding dispersal strategies in wide‐ranging predator populations under fluctuating food conditions.     

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

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

Reproductive trade‐offs in a long‐lived bird species: condition‐dependent reproductive allocation maintains female survival and offspring quality

Life history theory is an essential framework to understand the evolution of reproductive allocation. It predicts that individuals of long‐lived species favour their own survival over current reproduction, leading individuals to refrain from reproducing under harsh conditions. Here we test this prediction in a long‐lived bird species, the Siberian jay Perisoreus infaustus. Long‐term data revealed that females rarely refrain from breeding, but lay smaller clutches in unfavourable years. Neither offspring body size, female survival nor offspring survival until the next year was influenced by annual condition, habitat quality, clutch size, female age or female phenotype. Given that many nests failed due to nest predation, the variance in the number of fledglings was higher than the variance in the number of eggs and female survival. An experimental challenge with a novel pathogen before egg laying largely replicated these patterns in two consecutive years with contrasting conditions. Challenged females refrained from breeding only in the unfavourable year, but no downstream effects were found in either year. Taken together, these findings demonstrate that condition‐dependent reproductive allocation may serve to maintain female survival and offspring quality, supporting patterns found in long‐lived mammals. We discuss avenues to develop life history theory concerning strategies to offset reproductive costs.     

Brood rearing costs affect future reproduction in the precocial common goldeneye Bucephala clangula

Life-history theory assumes a trade-off between current reproductive effort and future reproductive success. There are a large number of studies demonstrating reproductive trade-offs in different animal taxa, particularly in birds. Most bird studies have focused on the costs of chick rearing in altricial species. These costs have been assumed to be low in precocial species, but this aspect has been little studied. We used long-term individual reproductive data from the common goldeneye Bucephala clangula , an iteroparous precocial duck with uniparental female care, to examine whether brood rearing carries costs that affect future reproductive performance. All females were experienced breeders, and possible differences in female quality were ruled out. We compared within-individual (between-year) changes in clutch size, hatching date and body mass between females that had reared a brood in the previous year and females that had not. It turned out that brood rearing involved a cost in terms of clutch size and hatching date the next year, but not in terms of body mass: females that had reared a brood in the previous year laid relatively smaller clutches and laid relatively later than females that had not reared a brood. Our results show that normal brood rearing in a precocial species involves costs that affect future reproduction.     

Long‐lived and heavier females give birth earlier in roe deer

In seasonal environments, parturition of most vertebrates generally occurs within a short time‐window each year. This synchrony is generally interpreted as being adaptive, as early born young survive better over the critical season than late born young. Among large herbivores, the factors involved in driving among‐ and within‐individual variation in parturition date are poorly understood. We explored this question by analyzing the relative importance of attributes linked to female quality (longevity, median adult body mass and cohort), time‐dependent attributes linked to female condition (reproductive success the previous year, relative annual body mass and offspring cohort (year)), and age in shaping observed variation in parturition date of roe deer. A measure of quality combining the effects of female longevity and median adult body mass accounted for 11% of the observed among‐individual variation in parturition date. Females of 2 yr old give birth 5 d later than older females. Our study demonstrates that high quality (heavy and long‐lived) females give birth earlier than low quality females. Temporally variable attributes linked to female condition, such as reproductive success in the previous year and relative annual body mass, had no detectable influence on parturition date. We conclude that parturition date, a crucial determinant of reproductive success, is shaped by attributes linked to female quality rather than by time‐dependent attributes linked to female condition in income breeders (individuals that rely on current resource intake rather than on accumulated body reserves to offset the increased energy requirements due to reproduction) such as roe deer.     

Age‐dependent changes in infidelity in Seychelles warblers

Extra‐pair paternity (EPP) is often linked to male age in socially monogamous vertebrates; that is, older males are more likely to gain EPP and less likely to be cuckolded. However, whether this occurs because males improve at gaining paternity as they grow older, or because “higher quality” males that live longer are preferred by females, has rarely been tested, despite being central to our understanding of the evolutionary drivers of female infidelity. Moreover, how extra‐pair reproduction changes with age within females has received even less attention. Using 18 years of longitudinal data from an individually marked population of Seychelles warblers (Acrocephalus sechellensis), we found considerable within‐individual changes in extra‐pair reproduction in both sexes: an early‐life increase and a late‐life decline. Furthermore, males were cuckolded less as they aged. Our results indicate that in this species age‐related patterns of extra‐pair reproduction are determined by within‐individual changes with age, rather than differences among individuals in longevity. These results challenge the hypothesis—based on longevity reflecting intrinsic quality—that the association between male age and EPP is due to females seeking high‐quality paternal genes for offspring. Importantly, EPP accounted for up to half of male reproductive success, emphasizing the male fitness benefits of this reproductive strategy. Finally, the occurrence of post‐peak declines in extra‐pair reproduction provides explicit evidence of senescence in infidelity in both males and females.     

Diet‐dependent female evolution influences male lifespan in a nuptial feeding insect

Theory predicts that lifespan will depend on the dietary intake of an individual, the allocation of resources towards reproduction and the costs imposed by the opposite sex. Although females typically bear the majority of the cost of offspring production, nuptial feeding invertebrates provide an ideal opportunity to examine the extent to which reproductive interactions through gift provisioning impose a cost on males. Here we use experimental evolution in an Australian ground cricket to assess how diet influences male lifespan and how the costs of mating evolve for males. Our findings show that males had significantly shorter lifespans in populations that adapted to a low‐quality diet and that this divergence is driven by evolutionary change in how females interact with males over reproduction. This suggests that the extent of sexual conflict over nuptial feeding may be under‐realized by focusing solely on the consequences of reproductive interactions from the female’s perspective.     

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.     

Assessment of costs of reproduction in a pelagic seabird using multistate mark-recapture models

We used a long‐term population band‐resight survey database, a parallel reproduction database, and multistate mark–recapture analysis to assess the costs of reproduction, a keystone concept of life‐history evolution, in Nazca boobies (Sula granti) from Punta Cevallos, Isla Española, Galápagos, Ecuador. We used eight years of resight and breeding data to compare models that included sex‐ and state‐specific survival probabilities and probabilities of transition between reproductive states using multistate mark–recapture models. Models that included state‐specific effects were compared with models lacking such effects to evaluate costs of reproduction. The top model, optimizing the trade‐off of model simplicity and fit to the data using the Akaike Information Criterion (AIC), showed evidence of a temporally varying survival cost of reproduction: nonbreeders showed higher annual survival than breeders did in some years. Because increasing investment among breeders showed no negative association with survival and subsequent breeding success, this evidence indicates a cost to both males and females of initiating, but not of continuing, a reproductive attempt. In some cases, breeders reaching the highest reproductive state (fledging an offspring) showed higher survival or subsequent breeding success than did failed breeders, consistent with differences in overall quality that promote both survival and reproduction. Although a male‐biased adult sex ratio was observed in this population of Nazca boobies, models of state‐ and sex‐specific survival and transition probabilities were not supported, indicating that males and females do not incur different costs of reproduction, and that the observed sex ratio bias is not due to sex‐specific adult mortality.     

Density-dependence vs. density-independence - linking reproductive allocation to population abundance and vegetation greenness

1. Recent studies have shown that optimal reproductive allocation depends on both climatic conditions and population density. We tested this hypothesis using six years of demographic data from eight reindeer (Rangifer tarandus) populations coupled with data on population abundance and vegetation greenness [measured using the Enhanced Vegetation Index (EVI)]. 2. Female spring body mass positively affected summer body mass gain, and lactating females were unable to compensate for harsh winters as efficiently as barren ones. Female spring body mass was highly sensitive to changes in population abundance and vegetation greenness and less dependent on previous autumn body mass and reproductive status. Lactating females were larger than barren females in the spring. Moreover, female autumn body mass was positively related to female autumn body mass and reproductive success and was not very sensitive to changes in vegetation greenness and population abundance. 3. Offspring autumn body mass was positively related to both maternal spring and autumn body mass, and as predicted from theory, offspring were more sensitive to changes in vegetation greenness and population abundance than adult females. A lagged cost of reproduction was present as larger females who were barren, the previous year produced larger offspring than equally sized females that successfully reproduced the previous year. 4. Reproductive success was negatively related to female autumn body mass and positively related to female spring body mass. Moreover, females who successfully reproduced the previous year experienced the highest reproductive success. The fact that negative density-dependence was only present for females that had successfully reproduced the previous year further support the hypothesis that reproduction is costly. 5. This study shows that female reindeer buffer their reproductive allocation according to expected winter conditions and that their buffering abilities were limited by population abundance and a lagged cost of reproduction and enhanced by vegetation greenness.     

Modelling time to population extinction when individual reproduction is autocorrelated

In nature, individual reproductive success is seldom independent from year to year, due to factors such as reproductive costs and individual heterogeneity. However, population projection models that incorporate temporal autocorrelations in individual reproduction can be difficult to parameterise, particularly when data are sparse. We therefore examine whether such models are necessary to avoid biased estimates of stochastic population growth and extinction risk, by comparing output from a matrix population model that incorporates reproductive autocorrelations to output from a standard age‐structured matrix model that does not. We use a range of parameterisations, including a case study using moose data, treating probabilities of switching reproductive class as either fixed or fluctuating. Expected time to extinction from the two models is found to differ by only small amounts (under 10%) for most parameterisations, indicating that explicitly accounting for individual reproductive autocorrelations is in most cases not necessary to avoid bias in extinction estimates.     

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.     

Variation in probability of first reproduction of Weddell seals

1. For many species, when to begin reproduction is an important life-history decision that varies by individual and can have substantial implications for lifetime reproductive success and fitness. 2. We estimated age-specific probabilities of first-time breeding and modelled variation in these rates to determine age at first reproduction and understand why it varies in a population of Weddell seals in Erebus Bay, Antarctica. We used multistate mark-recapture modelling methods and encounter histories of 4965 known-age female seals to test predictions about age-related variation in probability of first reproduction and the effects of annual variation, cohort and population density. 3. Mean age at first reproduction in this southerly located study population (7.62 years of age, SD=1.71) was greater than age at first reproduction for a Weddell seal population at a more northerly and typical latitude for breeding Weddell seals (mean=4-5 years of age). This difference suggests that age at first reproduction may be influenced by whether a population inhabits the core or periphery of its range. 4. Age at first reproduction varied from 4 to 14 years, but there was no age by which all seals recruited to the breeding population, suggesting that individual heterogeneity exists among females in this population. 5. In the best model, the probability of breeding for the first time varied by age and year, and the amount of annual variation varied with age (average variance ratio for age-specific rates=4.3%). 6. Our results affirmed the predictions of life-history theory that age at first reproduction in long-lived mammals will be sensitive to environmental variation. In terms of life-history evolution, this variability suggests that Weddell seals display flexibility in age at first reproduction in order to maximize reproductive output under varying environmental conditions. Future analyses will attempt to test predictions regarding relationships between environmental covariates and annual variation in age at first reproduction and evaluate the relationship between age at first reproduction and lifetime reproductive success.