Breeding Lifespan Research Articles

Timing of reproduction modifies transgenerational effects of chronic exposure to stressors in an annual vertebrate.

Stressful environmental conditions can shape both an individual's phenotype and that of its offspring. However, little is known about transgenerational effects of chronic (as opposed to acute) stressors, nor whether these vary across the breeding lifespan of the parent. We exposed adult female (F0 generation) three-spined sticklebacks (Gasterosteus aculeatus) to chronic environmental stressors and compared their reproductive allocation with that of non-exposed controls across early, middle and late clutches produced within the single breeding season of this annual population. There was a seasonal trend (but no treatment difference) in F0 reproductive allocation, with increases in egg mass and fry size in late clutches. We then tested for transgenerational effects in the non-exposed F1 and F2 generations. Exposure of F0 females to stressors resulted in phenotypic change in their offspring and grandoffspring that were produced late in their breeding lifespan: F1 offspring produced from the late-season clutches of stressor-exposed F0 females had higher early life survival, and subsequently produced heavier eggs and F2 fry that were larger at hatching. Changed maternal allocation due to a combination of seasonal factors and environmental stressors can thus have a transgenerational effect by influencing the reproductive allocation of daughters, especially those born late in life.

Environmental conditions experienced upon first breeding modulate costs of early breeding but not age-specific reproductive output in peregrine falcons.

Although once considered uncommon, there is growing evidence of widespread senescence in wildlife populations. However, few studies have examined the traits involved, inter-sexual differences, and environmental correlates of age-specific performance in raptors. We studied age-specific reproductive performance and actuarial senescence (decrease in survival probability with age) in a peregrine falcon population monitored for 21 years. We analysed changes with age in the number of offspring produced and incubation start date. We also inspected variation in lifespan and breeding lifespan (number of breeding occasions in a lifetime). In every case, we assessed associations between variations in traits and age, sex, recruitment age, and environmental conditions (cumulative rainfall during breeding season) experienced upon the first breeding attempt. We found scarce evidence for reproductive senescence. Only the incubation start date in females, which was delayed after approximately 8 cy (calendar years), suggested reproductive senescence in our study population. Regarding actuarial senescence, our data did not support it as we only found evidence of higher juvenile mortality. Furthermore, expected lifespan in peregrines recruited at 2 cy was associated with conditions experienced upon the first breeding attempt. The lifespan and breeding career of individuals recruited as yearlings and experiencing low rainfall upon first breeding did not significantly differ from those recruited as adults. However, those recruited as yearlings and experiencing poor environmental conditions upon the first breeding attempt showed reduced lifespan and breeding lifespan.

Silver spoon effects of hatching order in an asynchronous hatching bird

The silver spoon hypothesis proposes that individuals which develop under favorable conditions will gain fitness benefits throughout their lifetime. Hatching order may create a considerable size hierarchy within a brood and lead to earlier-hatched nestlings having a competitive advantage over their siblings, which has been illustrated in some studies. However, there have been few explorations into the effect on subsequent generations. Here, using a 15-year-long study, we investigated the long-term fitness consequences of hatching order in the endangered crested ibis, Nipponia nippon, a species with complete hatching asynchrony. In this study, we found strong support for silver spoon effects acting on hatching order. Compared with later-hatched nestlings, first-hatched nestlings begin reproduction at an earlier age, have higher adult survival rates, possess a longer breeding life span, and achieve higher lifetime reproductive success. Interestingly, we found carry-over effects of hatching order into the next generation. Nestlings which hatched earlier and became breeders in turn also produced nestlings with larger tarsus and better body condition. Additionally, we found a positive correlation among life-history traits in crested ibis. Individuals which started reproduction at a younger age were shown to possess a longer breeding life span, and the annual brood size increased with an individual's breeding life span. This suggests that the earlier-hatched nestlings are of better quality and the silver spoon effects of hatching order cover all life-history stages and next generation effects.

Intrinsic factors are relatively more important than habitat features in modulating risk perception in a tropical lizard

Anti-predator responses in animals are dynamic and depend on multiple factors. However, most of our understanding about animal escape responses comes from studies which examine only a small set of factors at a time and are done over a short period of animal life spans. This limits our understanding of the dynamic nature of animal escape behaviour and the relative importance of individual factors in determining their escape behaviour. We used a repeated-measures study design to assess the anti-predator response of a wild population of a sexually dimorphic tropical lizard, Psammophilus dorsalis. We followed marked individuals throughout their breeding lifespan, repeatedly assayed their escape response and measured representative intrinsic and extrinsic factors that could modulate their escape response. Our findings suggest that intrinsic factors, such as sex and body size, influenced escape response relatively more than extrinsic factors did, such as distance to refuge and perch height. Although individual variables influenced escape behaviour, in a direction mostly consistent with predictions from optimal escape theory, the interaction between factors led to novel insights into how animals dynamically evaluate multiple and changing costs throughout their lifetime to evade predation. Fleeing from a potential predator is crucial to animals and depends on different factors, as there are various costs to escaping. Although several studies in the past have evaluated the role of various factors in determining escape response, the relative importance of factors and how it changes across the lifetime of individuals are not clear. By assessing individuals repeatedly over a substantial part of their lifespan, we could gain insight into how escape response changes as associated factors, intrinsic or extrinsic, change for an individual over time. This approach provided us a more robust and accurate representation of the dynamic nature of escape decisions. We also demonstrate that when multiple factors are considered simultaneously, their relative importance in determining timing of escape can considerably differ from theoretical predictions.

Pale and dark morphs of tawny owls show different patterns of telomere dynamics in relation to disease status.

Parasites are expected to exert long-term costs on host fecundity and longevity. Understanding the consequences of heritable polymorphic variation in disease defence in wild populations is essential in order to predict evolutionary responses to changes in disease risk. Telomeres have been found to shorten faster in malaria-diseased individuals compared with healthy ones with negative effects on longevity and thereby fitness. Here, we study the impact of haemosporidian blood parasites on telomere dynamics in tawny owls, which display a highly heritable plumage colour polymorphism. Previously, it has been shown that blood parasites have morph-specific impact on body mass maintenance. Here, we show that telomeres shortened faster in individuals with shorter breeding lifespan. Telomere length was negatively associated with the degree of pheomelanic brown coloration and shorter in infected than uninfected individuals. The rate of telomere shortening between breeding seasons was faster in darker pheomelanic individuals and suppression of parasite intensity between seasons was associated with faster telomere shortening in the paler individuals but not in darker ones. We propose that morph-specific physiological profiles cause differential telomere shortening and that this is likely to be a mechanism involved in previously documented environment-driven survival selection against the pheomelanic morph in this population.

TNFα depleting therapy improves fertility and animal welfare in TNFα-driven transgenic models of polyarthritis when administered in their routine breeding.

Transgenic tumour necrosis factor alpha (TNFα)-driven models of polyarthritis such as the TNFΔARE mouse have proven to be invaluable in delineating aspects of inflammatory disease pathophysiology in humans. Unfortunately, the onset of joint destruction and inflammation in these models represents a significant detriment to breeding management. We examined whether TNFα depleting therapy ‘infliximab’ might represent a significant refinement in routine breeding. Clinical scores of joint inflammation were assessed in TNFΔARE males receiving either infliximab (10 mg/kg) or saline by twice-weekly intraperitoneal injection. Joint histology and bone morphology were assessed by histological analysis and micro-computed tomography (CT), respectively. Analysis of breeding was examined retrospectively in TNFΔARE males prior to, and following, regular introduction of infliximab. Clinical scores of inflammation were significantly reduced in TNFΔARE males receiving infliximab (control 6.6 arbitrary units [AU] ± 0.88 versus infliximab 4.4 AU ± 1.4; P < 0.05), while measures of pannus invasion and bone erosion by histology and micro-CT were markedly reduced. In the breeding groups, TNFΔARE males receiving infliximab injections sired more litters over their breeding lifespan (control 1.69 ± 0.22 versus infliximab 3.00 ± 0.19; P < 0.005). Furthermore, prior to infliximab, TNFΔARE males had a 26% risk of failing to sire any litters. This was reduced to 7% after the introduction of infliximab. This study is the first to report that regular administration of infliximab is effective at suppressing disease activity and improving animal welfare in TNFΔARE animals. In addition, we have shown that infliximab is highly efficacious in improving breeding behaviour and increasing the number of litters sired by TNFΔARE males.

Rearing conditions have long-term sex-specific fitness consequences in the collared flycatcher

Lay Summary Early-life conditions have stronger effects on the fitness of male than female collared flycatchers. Male nestlings from experimentally enlarged broods had fewer eggs from their mates during their life than male nestlings from reduced broods, which was a consequence of their shorter breeding lifespan. In females, rearing conditions had no effect on fitness. Together with earlier results, we show that although sex differences in growth disappear by fledging, the greater sensitivity of males had lifelong consequences.

Life expectancy, maximum longevity and lifetime reproductive success in female Thornicroft's giraffe in Zambia

AbstractGestation and longevity scale with body mass across taxa, yet within size dimorphic taxa, males tend to have reduced lifespans compared with females. Testing life history models, and accounting for sex differences in longevity, requires obtaining accurate longitudinal data from wild populations. We provide the first report describing key life history parameters from a long‐term study of giraffes in Africa. We followed a population of Thornicroft's giraffe (Giraffa camelopardalis thornicrofti) in Zambia for over 40 years. Maximum longevity among females was approximately 28 years, with lifespan accounting for 81% of the variance in lifetime reproductive success. Average adult female life expectancy was no different than average adult male life expectancy. However, the breeding lifespan of males was about half that of females, while maximum lifespan of males was 75% that of females. Our findings support the suggestion that sex differences in maximum lifespan arise from stronger selection for lengthy lives in females than in males. Among females, longer lives are associated with greater reproductive output.

Length polymorphism at the avpr1a locus is correlated with male reproductive behavior in a natural population of prairie voles (Microtus ochrogaster)

Laboratory studies have shown that vasopressin can influence sociosexual behavior through its action on the vasopressin 1a receptor (V1aR). There is substantial evidence that the length of a microsatellite in the gene (avpr1a) encoding for the V1aR can affect social attachment to females and paternal behavior in male prairie voles under laboratory conditions. However, previous field studies of prairie voles have failed to detect a strong effect of the length of a male’s avpr1a allele on their sociosexual behavior, but these studies are typically much shorter than the average prairie vole breeding lifespan. We examined the relationship between male avpr1a microsatellite allele length and sociosexual behavior in a natural population of prairie voles for 15 weeks, closer to the lifespan of prairie voles in nature. Contrary to predictions, we found that males with the longest avpr1a microsatellite alleles were significantly more likely to sire offspring with more than one female and to sire offspring that survived until trappable age than males with the shortest avpr1a microsatellite allele lengths. This relationship was the strongest for males with the longest tenure on the study site. As in previous field studies, we did not find evidence of a relationship between a male’s avpr1a genotype and any index of social behavior including male residency status or the number of females with which males associate. This is the first study to support the hypothesis that a male’s avpr1a genotype is a factor underlying variation in the genetic mating system of prairie voles under natural conditions.

Costs of mating competition limit male lifetime breeding success in polygynous mammals.

Although differences in breeding lifespan are an important source of variation in male fitness, the factors affecting the breeding tenure of males have seldom been explored. Here, we use cross-species comparisons to investigate the correlates of breeding lifespan in male mammals. Our results show that male breeding lifespan depends on the extent of polygyny, which reflects the relative intensity of competition for access to females. Males have relatively short breeding tenure in species where individuals have the potential to monopolize mating with multiple females, and longer ones where individuals defend one female at a time. Male breeding tenure is also shorter in species in which females breed frequently than in those where females breed less frequently, suggesting that the costs of guarding females may contribute to limiting tenure length. As a consequence of these relationships, estimates of skew in male breeding success within seasons overestimate skew calculated across the lifetime and, in several polygynous species, variance in lifetime breeding success is not substantially higher in males than in females.

Lifetime offspring production in relation to breeding lifespan, attractiveness, and mating status in male collared flycatchers

As a comprehensive fitness parameter, lifetime reproductive success (LRS) is influenced by many different environmental and genetic factors, among which longevity is one of the most important. These factors can be reflected in secondary sexual characters, which may affect the life histories of individuals via social relations with conspecifics. Facultative polygyny in birds is another conspicuous reproductive trait that potentially increases male reproductive success, but lifetime success data in relation to polygyny are scarce. Here, we used 17 years of breeding data to quantify the LRS of male collared flycatchers (Ficedula albicollis) on the basis of lifetime recruitment of offspring. Breeding lifespan showed a positive relationship with LRS, and it was also significantly associated with mean recruitment of offspring per breeding year. Body size and sexually selected forehead patch size did not predict the number of recruits. Polygyny was positively associated with LRS, but when we corrected for lifespan, this relationship disappeared. Our results demonstrate that the relationship between longevity and LRS is not explained by the higher number of reproductive attempts when living longer, and question the adaptive value of polygyny in this population. The lack of association between forehead patch size and recruitment suggests that forehead patch is a poor indicator of phenotypic quality in our birds.

Maternal effects on offspring Igs and egg size in relation to natural and experimentally improved food supply

1. Maternal effects have been suggested to function as a mechanism for transgenerational plasticity, in which the environment experienced by the mother is translated into the phenotype of the offspring. In birds and other oviparous vertebrates where early development is within the egg, mothers may be able to improve the viability prospects of their offspring at hatching by priming eggs with immunological and nutritional components. 2. We studied how resource availability affects maternal investment in offspring by feeding Ural owl (Strix uralensis, Pall.) females prior to egg-laying in 3 years of dramatically different natural food conditions. 3. Supplementary feeding prior to laying increased body mass and the level of Igs of females measured at clutch completion. Supplementary fed Ural owl females laid larger eggs than control females, and had offspring with higher levels of Igs at hatching compared to offspring of control females. 4. We found variation in maternal allocation of resources to the eggs in response to environmental conditions: during a year of rapidly declining food abundance, maternal Igs in hatchlings were higher, whereas egg size was smaller compared to years with a more stable food supply. 5. Egg size had a positive effect on offspring body mass at fledging, whereas Igs at hatching did not affect Igs at fledging. 6. We conclude that maternal body condition and maternal Igs, as well as hatchling Igs and egg size are limited by food resources during egg production. Hatchlings rely on maternally derived Igs and, hence, our results suggest that mothers with high levels of Igs passively transfer higher Igs levels to their eggs instead of active manipulation of Igs levels in eggs. Ural owl egg size appears to be highly sensitive to short-term changes in food abundance, with important consequences for nestling growth.

Lifetime Reproduction of Flammulated Owls in Colorado

ABSTRACT We investigated lifetime reproductive success (LRS) of 22 male and 46 female adult Flammulated Owls (Otus flammeolus) in Colorado from 1981–2003. Sexual differences in LRS were at least partially attributable to incomplete breeding histories of females, due to females having a higher estimated emigration rate from the study area than males. The mean number of lifetime breeding attempts for males was 3.4 ± 0.6 (SE; range = 1–12), and for females it was 1.9 ± 0.3 (range = 1–8). Adjusted for emigration beyond the study area, the estimated mean number of lifetime breeding attempts was 3.6 for males and 2.5 for females. The mean number of lifetime successful breeding attempts (fledging at least one owlet) was similar to lifetime breeding attempts for each sex, reflecting the fact that 84% (85 of 101) of all breeding attempts were successful. Breeding lifespan was correlated with lifetime reproduction for both sexes. Males tended nests that produced 6.9 ± 1.2 fledglings over 4.3 ± 0.8 yr, while fem...

The effect of climate on adult survival in five species of North Atlantic seabirds

Summary 1 In long-lived species, adult survival is an important life-history trait. Better knowledge of the effects of non-catastrophic climate variation on the adult survival of long-lived seabirds is therefore needed. However, documentation of such effects is still rare. 2 Using capture–mark–resighting data, we modelled the annual survival rates of five species of seabirds, the common guillemot (Uria aalge), Brunnich's guillemot (Uria lomvia), razorbill (Alca torda), Atlantic puffin (Fratercula arctica) and black-legged kittiwake (Rissa tridactyla). The data spanned 14 years of observation at a colony on Hornoya, off Northern Norway in the western Barents Sea. 3 A method of taking into account ring-loss of marked individuals is proposed. This approach made it possible to keep many observations which otherwise would have to be discarded. 4 The estimated survival rates were higher and less variable than most estimates for the same species from other colonies. There was extensive resighting heterogeneity. Ignoring this effect would have underestimated breeding life span by more than 50% in some species. 5 The analysis presented is the first study to document a correlation between the North Atlantic Oscillation (NAO) index and adult survival in North Atlantic seabirds. Other environmental variables considered were sea surface temperatures (SST) and prey stocks. In most of the species, models incorporating climatological variables were considerably better supported than models with constant survival, time-dependent survival or prey effects. SSTs tended to explain more of the variability in seabird survival than did the NAO. 6 The importance of prey availability was evident in some of the species, but climate was generally a better predictor of survival. Nevertheless, the evidence suggests that meteorological parameters affect seabird mortality only indirectly, possibly through the food chain. This conclusion rests on the observations that most NAO effects are lagged, and that survival rates decreased with increasing SSTs.

Determinants of lifetime fitness in a cooperative breeder, the long‐tailed tit Aegithalos caudatus

Summary 1 Long-tailed tits (Aegithalos caudatus) are a cooperatively breeding species in which helpers often invest effort in the provisioning of young that are not their own. 2 We quantified the lifetime reproductive success (LRS) and the individual fitness, lambda, of 228 long-tailed tits using 8 years of field data. Calculation of lambda took account of the effect of helpers on reproductive success, and thus lambda estimates the inclusive fitness of individuals. We examined the relationships between the fitness estimators and the provisioning effort, cohort, body size and dispersal status of individuals. 3 LRS of individuals which bred successfully varied between 0 and 13 local recruits (mean 0·71 ± 0·11 SE); lambda varied between 0 and 2·54 (mean 0·28 ± 0·04). The measures were highly correlated, and their distributions were strongly skewed. Helping by individuals contributed little to their fitness, but one-fifth of birds that accrued fitness did so only through helping. In general, individuals that gained fitness from helping did not gain fitness directly. 4 Both LRS and individual fitness were significant predictors of the number of grand-offspring that an individual had, but they accounted for only about one-third of the variation. 5 When variance in LRS was partitioned between length of breeding life span, average fecundity and offspring survival, the latter component was the most important in accounting for variance in LRS. 6 Offspring local survival was positively related to the provisioning effort of mothers, but was unrelated to that of fathers. As a result, the fitness of females was positively related to their provisioning effort. 7 Immigrant birds tended to be more reproductively successful than philopatric ones. Among females, only immigrant birds accrued any LRS or individual fitness. 8 The probability that an individual had at least one offspring recruit to the local breeding population varied among cohorts, probably as a result of variation among years in offspring local survival. This resulted in variation among cohorts in the individual fitness of females, but not in their LRS, nor in the LRS or individual fitness of males.

State‐dependent parental care in the Antarctic petrel: responses to manipulated chick age during early chick rearing

Life histories are state‐dependent, and an individual's reproductive decisions are determined by its available resources and the needs of its offspring. Here we test how a chick's needs for food and protection influence parental decisions in the Antarctic petrel, Thalassoica antarctica, where the parents, due to their long breeding lifespan, are expected to give priority to their own needs before those of the young. We exchanged one‐day‐old chicks with four‐day‐old chicks and studied how the parents subsequently provided care to the chick. The duration of the guarding period was adjusted, and parents left older chicks earlier and younger chicks later compared to controls. Three mechanisms were responsible for the adjustments. 1) Parents with an older chick co‐ordinated fewer guarding spells whereas parents with a younger chick co‐ordinated more guarding spells. 2) At the last guarding spell, i.e. where a parent left the chick alone before the partner returned, less time was spent with older chicks, and more time with younger chicks. 3) Foraging trip duration was shortened by parents given older chicks and prolonged by parents given younger chicks, probably in response to the chick's food demand. Hence, the parents responded quickly to the altered needs of the chick. Parents with high body mass guarded longer and were better able to co‐ordinate the guarding spells compared to lighter parents. In conclusion, Antarctic petrels adjust reproductive decisions to their own, their mate's, and their chick's state, and they seem to respond to the chick's needs for both food and protection.

Qualitative population divergence in proximate determination of a sexually selected trait in the collared flycatcher

Abstract We examined proximate determination of sexually selected forehead patch size in a Central-European population of Ficedula albicollis, the collared flycatcher, using a 9-year database, and compared our results with those obtained in other populations of the same and the sister species. Between-individual variation of forehead patch size was large, its repeatability larger than, and heritability similar to the Swedish population. Unlike in the other populations, the trait proved unaffected by body condition, and only very slightly influenced by age. There was no relationship between forehead patch size and breeding lifespan, and a marginal negative association with survivorship in adult males. Our results suggest that additive genetic variance of the trait in this population is large, but genes act independently of body condition, and there is no viability indicator value of the trait. This is the first report of a qualitative intraspecific difference in proximate determination of a sexually selected trait.

Lifetime reproductive success in common buzzard, Buteo buteo: from individual variation to population demography

We studied annual and lifetime reproductive success (LRS) of both sexes of common buzzard Buteo buteo in eastern Westphalia, Germany. We followed a bottom‐up approach starting from individual breeding attempts, over lifetime reproductive success to derive population demography. Annual breeding performance and survival followed a quadratic relationship with breeding experience; individuals starting their breeding career were less likely to survive and breed successfully than birds of intermediate breeding experience. According to an analysis of selection gradients, both the opportunity and intensity of selection peaked in the early stages of the breeding career. The distribution of both LRS and another fitness measure, λ, was highly skewed, with ca 17% of adult birds producing 50% of fledglings in both sexes. Besides breeding life span and number of breeding attempts, habitat quality and plumage morph were significant predictors of LRS. There were strong differences in LRS and λ between the plumage morphs in both sexes: intermediate pigmented buzzards were much more successful than either dark or light ones. There was no significant difference between buzzard cohorts either in LRS or λ, nor did these fitness measures differ between individuals starting their breeding career at different conditions of food availability. Based on individual life histories, we formed a transition matrix and analysed its properties to study the population as a whole. This analysis showed that the population growth rate was close to unity (0.906, bootstrapped 95% confidence limits: 0.834 and 0.962). Analysis of reproductive values and elasticities further emphasised colour morph differences: the contribution of intermediate individuals to population growth greatly exceeded that of dark or light individuals. Thus most phenomena on all levels from individual breeding attempts over lifetime reproductive success to population demography can be explained by the fitness differences between the colour morphs with the intermediate morph maintaining the current population renewal potential.

Intermittent breeding in the short‐tailed shearwater Puffinus tenuirostris

1. At one colony of short‐tailed shearwaters in Bass Strait, Australia, all birds breeding have been recorded individually each year for over 50 years. Among individuals known to be alive and to have bred before, 14% of each sex were not present at their breeding colony, on average, in any one year. 2. A further 15% of males and 13% of females (a significant difference), known to have bred before, were present but not associated with an egg in any one year. 3. Intermittent breeding was associated with pair bond breakdown and with a reduced ability to raise offspring, even when years of absence were allowed for. 4. The frequency of attendance, laying and successful rearing of progeny to fledging increased with age in the early years of breeding. However, this was followed by a decrease, except in the case of laying frequency, which continued to increase throughout life. 5. Our analysis indicated that intermittent breeding in short‐tailed shearwaters did not result from individuals implementing trade‐offs between the effort required for breeding success and their breeding life span. Rather, we suggest that individuals of higher quality are able to breed more frequently than others without any compensatory reduction in either their annual breeding success or their overall breeding life span.

Breeding lifespan and nest predation determine lifetime production of fledglings by male merlinsFalco columbarius

Components of variance in lifetime production of fledglings were determined for 92 male merlins Falco columbarius that bred in north Sweden up until 1994. Nest predation and breeding lifespan were the most important components of variance in lifetime production of fledglings. Owing to nest predation, 20% of the males failed to produce any fledglings at all. The nest predation frequency was higher before than after the eggs had hatched, and higher among pairs that commenced laying late than among other pairs. Breeding experience did not reduce the nest predation risk but inexperienced as well as experienced breeders could fail due to predation on nest contents. Males with a long breeding lifespan produced more fledglings because a long lifespan increased the number of successful breedings. These results agree with previous observations that nest defence by the parents improves annual offspring production in merlins.