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Telomeres are protective, nucleoprotein structures at the end of chromosomes that have been associated with lifespan across taxa. However, the extent to which these associations can be attributed to absolute length vs. the rate of telomere shortening prior to sampling remains unresolved. In a longitudinal study, we examined the relationship between lifespan, telomere length and the rate of telomere shortening in wild, purple-crowned fairy-wrens (Malurus coronatus coronatus). To this end, we measured telomere length using quantitative polymerase chain reaction in the blood of 59 individuals sampled as nestlings and 4-14 months thereafter, and in 141 known-age individuals sampled on average three times across adulthood. We applied within-subject centring analyses to simultaneously test for associations between lifespan and average telomere length and telomere shortening. We reveal that the rate of telomere shortening and to a lesser extent telomere length in the first year of life independently predicted lifespan, with individuals with faster shortening rates and/or shorter telomeres living less long. In contrast, in adulthood neither telomere shortening nor telomere length predicted lifespan, despite a considerably larger data set. Our results suggest that telomere length measured very early in life (during development) and longitudinal assessments of telomere shortening during the first year of life constitute more useful biomarkers of total life expectancy than either telomere length measured after development, or telomere shortening later in adulthood.

Evidence that telomere length (TL) and dynamics can be interpreted as proxy for ‘life stress’ experienced by individuals stems largely from correlational studies. We tested for effects of an experimental increase of workload on telomere dynamics by equipping male great tits (Parus major) with a 0.9 gram backpack for a full year. In addition, we analysed associations between natural life-history variation, TL and TL dynamics. Carrying 5% extra weight for a year did not significantly accelerate telomere attrition. This agrees with our earlier finding that this experiment did not affect survival or future reproduction. Apparently, great tit males were able to compensate behaviourally or physiologically for the increase in locomotion costs we imposed. We found no cross-sectional association between reproductive success and TL, but individuals with higher reproductive success (number of recruits) lost fewer telomere base pairs in the subsequent year. We used the TRF method to measure TL, which method yields a TL distribution for each sample, and the association between reproductive success and telomere loss was more pronounced in the higher percentiles of the telomere distribution, in agreement with the higher impact of ageing on longer telomeres within individuals. Individuals with longer telomeres and less telomere shortening were more likely to survive to the next breeding season, but these patterns did not reach statistical significance. Whether successful individuals are characterized by losing fewer or more base pairs from their telomeres varies between species, and we discuss aspects of ecology and social organisation that may explain this variation.

Glucocorticoid (GC) variation has long been thought to reflect variation in organismal ‘stress’, but associations between GCs and Darwinian fitness components are diverse in magnitude, direction, and highly context-dependent. This paradox reveals our poor understanding of the causes of GC variation, contrasting with the detailed knowledge of the functional consequences of GC variation. Amongst other things, GCs orchestrate energy availability, to anticipate and recover from predictable and unpredictable environmental fluctuations and challenges. Although this is mechanistically well-known, the extent to which GC levels are quantitatively explained by energy metabolism is unresolved. We investigated this association through meta-analysis, selecting studies of endotherms in which (1) an experiment was performed that affected metabolic rate and (2) metabolic rate and GC-levels were measured simultaneously. We found that an increase in metabolic rate was associated with an increase in GC levels in 20 out of 21 studies (32 out of 35 effect sizes). More importantly, there was a strong positive correlation between the increases in metabolic rate and GCs (p=0.003). This pattern was similar in birds and mammals, and independent of the nature of the experimental treatment. We conclude that metabolic rate is a major driver of GC variation within individuals. Stressors often affect metabolic rate, leading us to question whether GC levels provide information on ‘stress’ beyond the stressor’s effect on metabolic rate.

Food availability modulates survival, reproduction and thereby population size. In addition to direct effects, food availability has indirect effects through density of conspecifics and predators. We tested the prediction that food availability in isolation affects reproductive success by experimentally manipulating food availability continuously for 3 years in zebra finches (Taeniopygia guttata) housed in outdoor aviaries. To this end, we applied a technique that mimics natural variation in food availability: increasing the effort required per food reward without affecting diet. Lower food availability resulted in a slight delay of start of laying and fewer clutches per season, but did not affect clutch size or number of offspring reared per annum. However, increasing foraging costs substantially reduced offspring growth. Thus, food availability in isolation did not impact the quantity of offspring reared, at the expense of offspring quality. Growth declined strongly with brood size, and we interpret the lack of response with respect to offspring number as an adaptation to environments with low predictability, at the time of egg laying, of food availability during the period of peak food demand, typically weeks later. Manipulated natal brood size of the parents did not affect reproductive success. Individuals that were more successful reproducers were more likely to survive to the next breeding season, as frequently found in natural populations. We conclude that the causal mechanisms underlying associations between food availability and reproductive success in natural conditions may be more complex than usually assumed. Experiments in semi-natural meso-populations can contribute to further unravelling these mechanisms.

Quantifying an individual's state as a fitness proxy has proven challenging, but accumulating evidence suggests that telomere length and attrition may indicate individual somatic state and success at self-maintenance, respectively. Sexual ornamentation is also thought to signal phenotypic quality, but links between telomeres and sexual ornamentation have been little explored. To address this issue, we examined whether telomere length and dynamics are predicted by the expression of a sexually selected ornament, the length of the outermost tail feathers (streamers), using longitudinal data from a population of European barn swallows (Hirundo rustica). In 139 adult individuals, each measured twice, we further assessed associations of telomere length with age, sex, breeding status and survival. Telomere length showed high individual repeatability (R = .97) across years while shortening with age in both sexes. Telomere length and dynamics were not significantly associated with survival to the next year, remaining lifespan or reproduction status (comparing breeding and nonbreeding yearlings). Tail streamer length, a sexually selected trait in barn swallows, was negatively associated with telomere length, independent of sex. Thus, telomere length may reflect the costs of carrying an elaborated sexual ornament, although ornament size did not significantly predict telomere shortening. In conclusion, telomere length in adult barn swallows is a highly consistent trait that shows a negative relationship with sexual ornamentation, suggesting a trade-off between sexual ornamentation and telomere length.

An accurate inference of the chronological and biological age of individuals is fundamental to population ecology and our understanding of ageing itself, its evolution and the biological processes that affect or even cause ageing. In humans, epigenetic clocks based on the DNA methylation (DNAm) at selected CpG sites correlate highly with chronological age. Discrepancies between the inferred epigenetic and known chronological age predict morbidity and mortality, and therefore epigenetic clocks are thought to reflect biological age. Recently, a growing number epigenetic clocks in non-model organisms have been developed towards a diverse array of purposes in commercial, conservation and ageing research. Here we review those studies and conduct the first meta-analysis to assess the effects of different aspects of experimental protocol on the accuracy of epigenetic clocks for non-model species. Our analysis reveals higher coefficients of determination (R) of chronological age for epigenetic clocks based on the HorvathMammalMethylChip4, compared to other DNAm quantification approaches. No dependence of (R) was detected for the number of CpG sites in a clock; the sample size; the number or kind of tissue(s) used; the class of animals; or whether captive or wild animals were sampled to infer the epigenetic clocks. We further conclude that epigenetic clocks can predict chronological age with relatively high accuracy, suggesting great potential for the field of ecological epigenetics. We therefore encourage further research on the topic of ecological epigenetics in relation to ageing and, perhaps more importantly, discuss the potential of employing DNAm to assess key traits other than age.

Measuring telomere length (TL) with high precision is challenging. Currently there is insufficient understanding of the causes of variation in measurement precision, particularly for qPCR-based measurement. To better understand how DNA extraction protocols and laboratory-specific analytical factors influence qPCR-based TL measurement precision, we conducted a multi-laboratory study involving four labs and six DNA extraction protocols assaying the same blinded human whole blood samples. DNA extraction protocols differed in underlying principles (magnetic beads, salting out, silica membrane) and commercial kits. A fifth lab performed Telomere Restriction Fragment (TRF) analysis using Southern Blot technique with one DNA extraction protocol. All labs performed TL measurement using their standard procedures on two sets of fifty double blinded samples. Data was sent to a central point for unblinding and statistical analyses. Precision was quantified using the Intraclass Correlation Coefficient (ICC). Correlations with TRF measurements were also calculated. Repeated qPCR-based measurements of the same DNA extraction yielded ICC values ranging from 0.24 to 0.94. ICC values calculated over measurements of repeated DNA extractions were on average 0.23 lower and ranged from 0.02 to 0.83. The latter ICC estimates more strongly predicted the association between qPCR- and Southern blot-based measurements across the protocol / lab combinations (R2=0.56 vs. R2=0.93). We conclude that ICC calculated over measurements on repeated DNA extractions reliably indicates measurement precision, while ICC calculated over multiple measurements of the same DNA extraction overestimates measurement precision. Variation in ICC was driven by variation between laboratories, with few consistent DNA extraction protocol effects. Values of DNA integrity and purity generally characterized as reflecting high sample quality, (e.g. OD 260/280 of 1.8 and OD 260/230 of 2.0) were associated with qPCR-based measurement precision, but did not always predict higher ICCs.

Climate warming is increasingly exposing wildlife to sublethal high temperatures, which may lead to chronic impacts and reduced fitness. Telomere length (TL) may link heat exposure to fitness, particularly at early-life stages, because developing organisms are especially vulnerable to adverse conditions, adversity can shorten telomeres, and TL predicts fitness. Here, we quantify how climatic and environmental conditions during early life are associated with TL in nestlings of wild purple-crowned fairy-wrens ( Malurus coronatus ), endangered songbirds of the monsoonal tropics. We found that higher average maximum air temperature (range 31 to 45 °C) during the nestling period was associated with shorter early-life TL. This effect was mitigated by water availability (i.e., during the wet season, with rainfall), but independent of other pertinent environmental conditions, implicating a direct effect of heat exposure. Models incorporating existing information that shorter early-life TL predicts shorter lifespan and reduced fitness showed that shorter TL under projected warming scenarios could lead to population decline across plausible future water availability scenarios. However, if TL is assumed to be an adaptive trait, population viability could be maintained through evolution. These results are concerning because the capacity to change breeding phenology to coincide with increased water availability appears limited, and the evolutionary potential of TL is unknown. Thus, sublethal climate warming effects early in life may have repercussions beyond individual fitness, extending to population persistence. Incorporating the delayed reproductive costs associated with sublethal heat exposure early in life is necessary for understanding future population dynamics with climate change.

Telomere length and telomere shortening predict survival in many organisms. This raises the question of the contribution of genetic and environmental effects to variation in these traits, which is still poorly known, particularly for telomere shortening. We used experimental (cross-fostering) and statistical (quantitative genetic “animal models”) means to disentangle and estimate genetic and environmental contributions to telomere length variation in pedigreed free-living jackdaws (Corvus monedula). Telomere length was measured twice in nestlings, at ages 4 (n = 715) and 29 days (n = 474), using telomere restriction fragment (TRF) analysis, adapted to exclude interstitial telomeric sequences. Telomere length shortened significantly over the nestling period (10.4 ± 0.3 bp day–1) and was highly phenotypically (rP = 0.95 ± 0.01) and genetically (rG > 0.99 ± 0.01) correlated within individuals. Additive genetic effects explained a major part of telomere length variation among individuals, with its heritability estimated at h2 = 0.74 on average. We note that TRF-based studies reported higher heritabilities than qPCR-based studies, and we discuss possible explanations. Parent–offspring regressions yielded similar heritability estimates for mothers and fathers when accounting for changes in paternal telomere length over life. Year effects explained a small but significant part of telomere length variation. Heritable variation for telomere shortening was low (h2 = 0.09 ± 0.11). The difference in heritability between telomere length (high) and telomere shortening (low) agrees with evolutionary theory, in that telomere shortening has stronger fitness consequences in this population. Despite the high heritability of telomere length, its evolvability, which scales the additive genetic variance by mean telomere length, was on average 0.48%. Hence, evolutionary change of telomere length due to selection is likely to be slow.

Body condition is an important concept in behaviour, evolution and conservation, commonly used as a proxy of an individual's performance, for example in the assessment of environmental impacts. Although body condition potentially encompasses a wide range of health state dimensions (nutritional, immune or hormonal status), in practice most studies operationalize body condition using a single (univariate) measure, such as fat storage. One reason for excluding additional axes of variation may be that multivariate descriptors of body condition impose statistical and analytical challenges. Structural equation modelling (SEM) is used in many fields to study questions relating multidimensional concepts, and we here explain how SEM is a useful analytical tool to describe the multivariate nature of body condition. In this 'Research Methods Guide' paper, we show how SEM can be used to resolve different challenges in analysing the multivariate nature of body condition, such as (a) variable reduction and conceptualization, (b) specifying the relationship of condition to performance metrics, (c) comparing competing causal hypothesis and (d) including many pathways in a single model to avoid stepwise modelling approaches. We illustrated the use of SEM on a real-world case study and provided R-code of worked examples as a learning tool. We compared the predictive power of SEM with conventional statistical approaches that integrate multiple variables into one condition variable: multiple regression and principal component analyses. We show that model performance on our dataset is higher when using SEM and led to more accurate and precise estimates compared to conventional approaches. We encourage researchers to consider SEM as a flexible framework to describe the multivariate nature of body condition and thus understand how it affects biological processes, thereby improving the value of body condition proxies for predicting organismal performance. Finally, we highlight that it can be useful for other multidimensional ecological concepts as well, such as immunocompetence, oxidative stress and environmental conditions.

Collisions between birds and airplanes can damage aircrafts, resulting in delays and cancellation of flights, costing the international civil aviation industry more than 1.4 billion US dollars annually. Driving away birds is therefore crucial, but the effectiveness of current deterrence methods is limited. Live avian predators can be an effective deterrent, because potential prey will not habituate to them, but live predators cannot be controlled entirely. Thus, there is an urgent need for new deterrence methods. We developed the RobotFalcon, a device modelled after the peregrine falcon, and tested its effectiveness to deter flocks of corvids, gulls, starlings and lapwings. We compared its effectiveness with that of a drone, and of conventional methods routinely applied at a military airbase. The RobotFalcon scared away bird flocks from fields immediately, and these fields subsequently remained free of bird flocks for hours. The RobotFalcon outperformed the drone and the best conventional method at the airbase (distress calls). Importantly, there was no evidence that bird flocks habituated to the RobotFalcon over the course of the fieldwork. We conclude that the RobotFalcon is a practical and ethical solution to drive away bird flocks with all advantages of live predators but without their limitations.

Variation in developmental conditions is known to affect fitness in later life, but the mechanisms underlying this relationship remain elusive. We previously found in jackdawsCorvus monedulathat larger eggs resulted in larger nestlings up to fledging. Through a cross-foster experiment of complete clutches we tested whether this association can be attributed to egg size per se, or to more proficient parents producing larger eggs and larger nestlings, with the latter effect being more or less independent of egg size. Due to other manipulations post-hatching, we primarily investigated effects on nestling mass on day 5, which we show to predict survival until fledging. We introduce a new statistical approach to compare the competing hypotheses and conclude that 92% of the association between egg size and nestling mass is attributed to a direct effect of egg size, and that this relationship is not affected by variation in other parental quality. Intriguingly, the effect of egg size on day 5 nestling mass was steeper (1.7 g/cm3) than the effect of egg size on day 1 hatchling mass (0.7 g/cm3). Early growth is exponential, and the difference in effect size may therefore be explained by hatchlings from large eggs being further in their development at hatching. The direct effect of egg size on nestling mass raises the question what causes egg size variation in jackdaws.

Collective behaviour often functions to avoid predation, and is therefore especially conspicuous and complex in flocks of birds under attack by raptors. However, studying collective behaviour experimentally in natural conditions is challenging. Here, we used an artificial predator, the RobotFalcon, developed after a peregrine falcon, a cosmopolitan raptor hunting a wide variety of birds. We hunted with the RobotFalcon flocks of corvids, gulls, starlings and lapwings in an agricultural area in The Netherlands, while recording the collective escape responses of the flocks with a camera. We compared collective escape responses from the RobotFalcon with those from a drone. Flocks of all species responded to the RobotFalcon most often by collectively turning, compacting and splitting in subflocks. The frequency of collective escape was highest in starlings and corvids and lowest in gulls. For starlings only, we also compared their response to a live peregrine falcon using observational data. Similar to hunts by the real falcons, the collective escape response depended on the level of predatory threat. Flocks of all species except starlings responded less often and less intensively to the drone compared to the RobotFalcon. These results give novel insights in the predator-prey dynamics between raptors and bird flocks, and illustrate how artificial predators can be used to study prey-predator interactions experimentally in the field.

Collisions between birds and airplanes, bird strikes, can damage aircrafts, resulting in delays and cancellation of flights, costing the international civil aviation industry more than 1.4 billion U.S. dollars annually. Bird deterrence is therefore crucial, but the effectiveness of all available deterrence methods is limited. For example, live avian predators can be a highly effective deterrent, because potential prey will not habituate to them, but live predators cannot be controlled with sufficient precision. Thus, there is an urgent need for new deterrence methods. To this end we developed the RobotFalcon, a device that we modelled after the peregrine falcon, a cosmopolitan predator that preys on a large range of bird species. Mimicking natural hunting behaviour, we tested the effectiveness of the RobotFalcon to deter flocks of corvids, gulls, starlings and lapwings. We compared its effectiveness with that of a drone, and of conventional methods routinely applied at a military airbase. We show that the RobotFalcon scared away bird flocks from fields immediately, and these fields subsequently remained free of bird flocks for hours. The RobotFalcon outperformed the drone and the best conventional method at the airbase (distress calls). Importantly, there was no evidence that bird flocks habituated to the RobotFalcon. We propose the RobotFalcon to be a practical and ethical solution to drive away bird flocks with all advantages of live predators but without their limitations.HighlightsWe present and test a new method of deterring of deterring birds, the RobotFalcon.The RobotFalcon chased away flocks fast and prevented early returns.The RobotFalcon outperformed both a drone and convential methods.No evidence of habituation to the RobotFalcon was found during the study period.

The innate immune system is essential for survival, yet many immune traits are highly variable between and within individuals. In recent years, attention has shifted to the role of environmental factors in modulating this variation. A key environmental factor is food availability, which plays a major role in shaping life histories, and may affect resource allocation to immune function through its effect on nutritional state. We developed a technique to permanently increase foraging costs in seed-eating birds, and leveraged this technique to study the effects of food availability on the innate immune system over a 3-year period in 230 zebra finches housed in outdoor aviaries. The immune components we studied were haptoglobin, ovotransferrin, nitric oxide, natural antibodies through agglutination, complement-mediated lysis, and killing capacity of Escherichia coli and Candida albicans, covering a broad spectrum of the innate immune system. We explored the effects of food availability in conjunction with other potentially important variables: season, age, sex and manipulated natal brood size. Increased foraging costs affected multiple components of the immune system, albeit in a variable way. Nitric oxide and agglutination levels were lower under harsh foraging conditions, while Escherichia coli killing capacity was increased. Agglutination levels also varied seasonally, but only at low foraging costs. C. albicans killing capacity was lower in winter, and even more so for animals in harsh foraging conditions that were raised in large broods. Effects of food availability on ovotransferrin were also seasonal, and only apparent in males. Haptoglobin levels were independent of foraging costs and season. Males had higher levels of immune function than females for three of the measured immune traits. Innate immune function was independent of age and manipulated natal brood size. Our finding that food availability affects innate immune function suggests that fitness effects of food availability may at least partially be mediated by effects on the immune system. However, food availability effects on innate immunity varied in direction between traits, illustrating the complexity of the immune system and precluding conclusions on the level of disease resistance.

Leukocyte telomere length (LTL) might be causal in cardiovascular disease and major cancers. To elucidate the roles of genetics and geography in LTL variability across humans, we compared LTL measured in 1295 sub-Saharan Africans (SSAs) with 559 African–Americans (AAms) and 2464 European–Americans (EAms). LTL differed significantly across SSAs (P = 0.003), with the San from Botswana (with the oldest genomic ancestry) having the longest LTL and populations from Ethiopia having the shortest LTL. SSAs had significantly longer LTL than AAms [P = 6.5(e-16)] whose LTL was significantly longer than EAms [P = 2.5(e-7)]. Genetic variation in SSAs explained 52% of LTL variance versus 27% in AAms and 34% in EAms. Adjustment for genetic variation removed the LTL differences among SSAs. LTL genetic variation among SSAs, with the longest LTL in the San, supports the hypothesis that longer LTL was ancestral in humans. Identifying factors driving LTL variation in Africa may have important ramifications for LTL-associated diseases.

The assumption that reproductive effort decreases somatic state, accelerating ageing, is central to our understanding of life‐history variation. Maximal reproductive effort early in life is predicted to be maladaptive by accelerating ageing disproportionally, decreasing fitness.Optimality theory predicts that reproductive effort is restrained early in life to balance the fitness contribution of reproduction against the survival cost induced by the reproductive effort. When adaptive, the level of reproductive restraint is predicted to be inversely linked to the remaining life expectancy, potentially resulting in a terminal effort in the last period of reproduction.Experimental tests of the reproductive restraint hypothesis require manipulation of somatic state and subsequent investigation of reproductive effort and residual life span. To our knowledge the available evidence remains inconclusive, and hence reproductive restraint remains to be demonstrated.We modulated somatic state through a lifelong brood size manipulation in wild jackdaws and measured its consequences for age‐dependent mortality and reproductive success.The assumption that lifelong increased brood size reduced somatic state was supported: Birds rearing enlarged broods showed subsequent increased rate of actuarial senescence, resulting in reduced residual life span.The treatment induced a reproductive response in later seasons: Egg volume and nestling survival were higher in subsequent seasons in the increased versus reduced broods' treatment group. We detected these increases in egg volume and nestling survival despite the expectation that in the absence of a change in reproductive effort, the reduced somatic state indicated by the increased mortality rate would result in lower reproductive output. This leads us to conclude that the higher reproductive success we observed was the result of higher reproductive effort.Our findings show that reproductive effort negatively covaries with remaining life expectancy, supporting optimality theory and confirming reproductive restraint as a key factor underpinning life‐history variation., Early life reproductive restraint could be advantageous when it promotes health. This study compares reproductive success of jackdaws among accelerated versus decelerated ageing groups. Reproductive success increased in the accelerated ageing group, demonstrating reproductive restraint. Reproductive restraint provides an explanation for the commonly observed increase in reproductive success with age. Photo credit: Jelle Boonekamp.

Background Short leukocyte telomere length (TL) is associated with atherosclerotic cardiovascular disease. Endothelial repair plays a key role in the development of atherosclerosis. The objective was to examine associations between TL and proliferative dynamics of endothelial colony‐forming cells (ECFCs), which behave as progenitor cells displaying endothelial repair activity. Methods and Results To isolate ECFCs, we performed a clonogenic assay on blood samples from 116 participants (aged 24–94 years) in the TELARTA (Telomere in Arterial Aging) cohort study. We detected no ECFC clones in 29 (group 1), clones with no replating capacity in other 29 (group 2), and clones with replating capacity in the additional 58 (group 3). Leukocyte TL was measured by Southern blotting and ECFCs (ECFC‐TL). Age‐ and sex‐adjusted leukocyte TL (mean±SEM) was the shortest in group 1 (6.51±0.13 kb), longer in group 2 (6.69±0.13 kb), and the longest in group 3 (6.78±0.09 kb) ( P P P r =0.82; P Conclusions Individuals with longer telomeres display a higher number of self‐renewing ECFCs. Our results also indicate that leukocyte TL, as a proxy of TL dynamics in ECFCs, could be used as a surrogate marker of endothelial repair capacity in clinical and laboratory practice because of easy accessibility of leukocytes. Registration URL: https://www.clinicaltrials.gov ; Unique identifier: NCT02176941.

Telomere length (TL) shortens with age but telomere dynamics can relate to fitness components independent of age. Immune function often relates to such fitness components and can also interact with telomeres. Studying the link between TL and immune function may therefore help us understand telomere–fitness associations. We assessed the relationships between erythrocyte TL and four immune indices (haptoglobin, natural antibodies (NAbs), complement activity (CA) and heterophil-lymphocyte (HL) ratio; n = 477–589), from known-aged individuals of a wild passerine ( Malurus coronatus ). As expected, we find that TL significantly declined with age. To verify whether associations between TL and immune function were independent of parallel age-related changes (e.g. immunosenescence), we statistically controlled for sampling age and used within-subject centring of TL to separate relationships within or between individuals. We found that TL positively predicted CA at the between-individual level (individuals with longer average TL had higher CA), but no other immune indices. By contrast, age predicted the levels of NAbs and HL ratio, allowing inference that respective associations between TL and age with immune indices are independent. Any links existing between TL and fitness are therefore unlikely to be strongly mediated by innate immune function, while TL and immune indices appear independent expressions of individual heterogeneity.

Food availability modulates survival, reproduction and thereby population size. In addition to direct effects, food availability has indirect effects through density of conspecifics and predators. We tested the prediction that food availability in isolation affects reproductive success by experimentally manipulating food availability continuously for 3 years in zebra finches (Taeniopygia guttata) housed in outdoor aviaries. To this end, we applied a technique that mimics natural variation in food availability: increasing the effort required per food reward without affecting diet. Lower food availability resulted in a slight delay of start of laying and fewer clutches per season, but did not affect clutch size or number of offspring reared per annum. However, increasing foraging costs substantially reduced offspring growth. Thus, food availability in isolation did not impact the quantity of offspring reared, at the expense of offspring quality. Growth declined strongly with brood size, and we interpret the lack of response with respect to offspring number as an adaptation to environments with low predictability, at the time of egg laying, of food availability during the period of peak food demand, typically weeks later. Manipulated natal brood size of the parents did not affect reproductive success. Individuals that were more successful reproducers were more likely to survive to the next breeding season, as frequently found in natural populations. We conclude that the causal mechanisms underlying associations between food availability and reproductive success in natural conditions may be more complex than usually assumed. Experiments in semi-natural meso-populations can contribute to further unravelling these mechanisms.

Recent technological advancements allow researchers to measure electrophysiological parameters of animals, such as sleep, in remote locations by using miniature dataloggers. Yet, continuous recording of sleep might be constrained by the memory and battery capacity of the recording devices. These limitations can be alleviated by recording intermittently instead of continuously, distributing the limited recording capacity over a longer period. We assessed how reduced sampling of sleep recordings affected measurement precision of NREM sleep, REM sleep, and Wake. We analysed a dataset on sleep in barnacle geese that we resampled following 12 different recording schemes, with data collected for 1 min per 5 min up to 1 min per 60 min in steps of 5 min. Recording 1 min in 5 min still yielded precise estimates of hourly sleep-wake values (correlations of 0.9) while potentially extending the total recording period by a factor of 5. The correlation strength gradually decreased to 0.5 when recording 1 min per 60 min. For hourly values of Wake and NREM sleep, the correlation strength in winter was higher compared with summer, reflecting more fragmented sleep in summer. Interestingly for hourly values of REM sleep, correlations were unaffected by season. Estimates of total 24 h sleep-wake values were similar for all intermittent recording schedules compared to the continuous recording. These data indicate that there is a large safe range in which researchers can periodically record sleep. Increasing the sample size while maintaining precision can substantially increase the statistical power, and is therefore recommended whenever the total recording time is limited.

Birds exposed to food insecurity—defined as temporally variable access to food—respond adaptively by storing more energy. To do this, they may reduce energy allocation to other functions such as somatic maintenance and repair. To investigate this trade-off, we exposed juvenile European starlings ( Sturnus vulgaris , n = 69) to 19 weeks of either uninterrupted food availability or a regime where food was unpredictably unavailable for a 5-h period on 5 days each week. Our measures of energy storage were mass and fat scores. Our measures of somatic maintenance were the growth rate of a plucked feather, and erythrocyte telomere length (TL), measured by analysis of the terminal restriction fragment. The insecure birds were heavier than the controls, by an amount that varied over time. They also had higher fat scores. We found no evidence that they consumed more food overall, though our food consumption data were incomplete. Plucked feathers regrew more slowly in the insecure birds. TL was reduced in the insecure birds, specifically, in the longer percentiles of the within-individual TL distribution. We conclude that increased energy storage in response to food insecurity is achieved at the expense of investment in somatic maintenance and repair.

Mercury is a heavy metal, which is pervasive and persistent in the marine environment. It bioaccumulates within organisms and biomagnifies in the marine food chain. Due to its high toxicity, mercury contamination is a major concern for wildlife and human health. Telomere length is a biomarker of aging and health, because it predicts survival, making it a potential tool to investigate sublethal effects of mercury contamination. However, the relationship between telomeres and mercury contamination is unclear. We measured feather mercury concentration in Cory's Shearwaters Calonectris borealis, long-lived seabirds and top predators, between 9 and 35 years of age and related it to telomere length in erythrocytes. Cory's Shearwaters with higher mercury concentrations had shorter telomeres and the effect was sex-dependent, reaching significance in males only. This may be explained by the fact that males have longer telomeres and higher and more variable mercury concentrations than females in this population. The mercury effect on telomere length was stronger on longer telomeres in the genome within individuals. We discuss the hypotheses that the negative correlation could either be a direct effect of mercury on telomere shortening and/or a consequence of variation in phenotypic quality among individuals that results in a covariation between mercury contamination and telomere length. Fundação para a Ciência e Tecnologia - FCT info:eu-repo/semantics/publishedVersion

Early life conditions can affect individuals for life, with harsh developmental conditions resulting in lower fitness, but the underlying mechanisms are not well understood. We hypothesized that immune function may be part of the underlying mechanism, when harsh developmental conditions result in less effective immune function. We tested this hypothesis by comparing innate immune function between zebra finches (Taeniopygia guttata) in adulthood (n=230; age 108–749 days) that were reared in either small or large broods. We used this experimental background to follow up our earlier finding that finches reared in large broods have a shorter lifespan. To render a broad overview of innate immune function, we used an array of six measures: bacterial killing capacity, hemagglutination, hemolysis, haptoglobin, nitric oxide and ovotransferrin. We found no convincing evidence for effects of natal brood size on any of the six measures of innate immune function. This raised the question whether the origin of variation in immune function was genetic, and we therefore estimated heritabilities using animal models. However, we found heritability estimates to be low (range 0.04–0.11) for all measured immune variables, suggesting variation in innate immune function can largely be attributed to environmental effects independent of early-life conditions as modified by natal brood size., Summary: Developmental hardship has many long-term implications, but its effects on adult immune function are unknown. We found no effects of a developmental manipulation on innate immune function during adulthood in zebra finches.

Immunosenescence, the decline in immune defense with age, is an important mortality source in elderly humans but little is known of immunosenescence in wild animals. We systematically reviewed and meta-analysed evidence for age-related changes in immunity in captive and free-living populations of wild species (321 effect sizes in 62 studies across 44 species of mammals, birds and reptiles). As in humans, senescence was more evident in adaptive (acquired) than innate immune functions. Declines were evident for cell function (antibody response), the relative abundance of naïve immune cells and an in vivo measure of overall immune responsiveness (local response to phytohaemagglutinin injection). Inflammatory markers increased with age, similar to chronic inflammation associated with human immunosenescence. Comparisons across taxa and captive vs free-living animals were difficult due to lack of overlap in parameters and species measured. Most studies are cross-sectional, which yields biased estimates of age-effects when immune function co-varies with survival. We therefore suggest longitudinal sampling approaches, and highlight techniques from human cohort studies that can be incorporated into ecological research. We also identify avenues to address predictions from evolutionary theory and the contribution of immunosenescence to age-related increases in disease susceptibility and mortality.

Telomere length (TL) is increasingly used as a biomarker of senescence, but measuring telomeres remains a challenge. Within tissue samples, TL varies between cells and chromosomes. Class I telomeres are (presumably static) interstitial telomeric sequences, and terminal telomeres have been divided in shorter (Class II) telomeres and ultra-long (Class III) telomeres, and the presence of the latter varies strongly between species. Class II telomeres typically shorten with age, but little is known of Class III telomere dynamics. Using multiple experimental approaches, we show great tits to have ultra-long telomeres, and we investigated age effects on Class II and III telomeres using a longitudinal approach (our method excludes Class I telomeres). In adults, TL averaged over the whole distribution did not significantly change with age. However, more detailed analyses showed that Class II TL did shorten with age, and, as in other species, the longest Class II telomeres within individuals shortened faster with age. In contrast, Class III TL did not shorten with age within individual adults. Surprisingly, we found the opposite pattern in nestlings: Class III TL shortened significantly with age, while the age effect on Class II TL was close to zero. Thus, Class III telomere length may provide information on developmental history, while Class II telomere length provides information on telomere dynamics in adulthood. These findings have practical implications for telomere studies and raise the interesting question what causes variation in TL dynamics between chromosomes within individuals and how this is related to development. This article is protected by copyright. All rights reserved.

Whether lifespan scales to age-associated changes in health and disease is an urgent question in societies with increasing lifespan. Body mass is associated with organismal functioning in many species, and often changes with age. We here tested in zebra finches whether two factors that decreased lifespan, sex and poor environmental quality, accelerated the onset of body mass declines. We subjected 597 birds for nine years to experimentally manipulated foraging costs (harsh = H, benign = B) during development (small vs large brood size) and in adulthood (easy vs hard foraging conditions) in a 2 × 2 design. This yielded four treatment combinations (HH, HB, BH, BB) for each sex. Harsh environments during development and in adulthood decreased average body mass additively. The body mass aging trajectory showed a short steep increase in early adulthood, followed by a plateau and then a decline after 5 years. This decline occurred in all groups except for HB females, which gained mass until death. Surprisingly, the onset of body mass decline was earlier in experimental groups with a longer lifespan. In contrast, the onset of body mass decline was one year earlier in females, which lived two months (4%) shorter than males. Thus, the onset of body mass aging associated positively with the sex-specific differences in lifespan, but negatively with the environmental modulation of lifespan. Thus, body mass aging trajectories did not generally scale to lifespan, and we discuss the possible causes and implications of this finding.

Quantifying an individual’s state as fitness proxy has proven challenging, but accumulating evidence suggests that telomere length and attrition may indicate individual somatic state and success at self-maintenance, respectively. Sexual ornamentation is also thought to signal phenotypic quality, but links between telomeres and sexual ornamentation have been little explored. To address this issue, we examined whether telomere length and dynamics are predicted by the expression of a sexually selected ornament, the length of outermost tail feathers (streamers), using longitudinal data from a population of European barn swallows (Hirundo rustica). We further assessed associations of telomere length with age, sex, breeding status and survival. Telomere length showed high individual repeatability (R = 0.97) across years while shortening with age in both sexes. Telomere length and dynamics were not significantly associated with survival to the next year, remaining lifespan or reproduction status (comparing breeding and non-breeding yearlings). Tail streamer length was negatively associated with telomere length, independent of sex. Thus, telomere length may reflect the costs of carrying an elaborated sexual ornament, although ornament size did not significantly predict telomere shortening. In conclusion, telomere length in adult barn swallows is a highly consistent trait and shows a negative relationship with sexual ornamentation, suggesting a trade-off between sexual ornamentation and telomere length.

Telomeres are protective, nucleoprotein structures at the end of chromosomes that have been associated with lifespan across taxa. However, the extent to which these associations can be attributed to absolute length versus the rate of telomere shortening prior to sampling remains unresolved. In a longitudinal study, we examined the relationship between lifespan, telomere length and the rate of telomere shortening in wild, purple-crowned fairy-wrens (Malurus coronatus coronatus). To this end, we measured telomere length using qPCR in the blood of 59 individuals sampled as nestling and 4-14 months thereafter, and in 150 individuals sampled on average three times across adulthood. We applied within-subject centering analyses to simultaneously test for associations between lifespan and average telomere length and telomere shortening. We reveal that the rate of telomere shortening in the first year of life predicted lifespan, with individuals with faster shortening rates living less long. We also report a trend for an effect of telomere length in the first year of life on lifespan, independent of telomere shortening. In contrast, in adulthood neither telomere shortening, nor telomere length predicted lifespan, despite a considerably larger data set. Our results suggest that telomere length measured very early in life (during development) and longitudinal assessments of telomere shortening during the first year of life constitute more useful biomarkers of total life expectancy than either telomere length measured after development, or telomere shortening later in adulthood.

The slow pace of global vaccination and the rapid emergence of SARS-CoV-2 variants suggest recurrent waves of COVID-19 in coming years. Therefore, understanding why deaths from COVID-19 are highly concentrated among older adults is essential for global health. Severe COVID-19 T-cell lymphopenia is more common among older adults, and it entails poor prognosis. Much about the primary etiology of this form of lymphopenia remains unknown, but regardless of its causes, offsetting the decline in T-cell count during SARS-CoV-2 infection demands fast and massive T-cell clonal expansion, which is telomere length (TL)-dependent. We have built a model that captures the effect of age-dependent TL shortening in hematopoietic cells and its effect on T-cell clonal expansion capacity. The model shows that an individual with average hematopoietic cell TL (HCTL) at age twenty years maintains maximal T-cell clonal expansion capacity until the 6th decade of life when this capacity plummets by more than 90% over the next ten years. The collapse coincides with the steep increase in COVID-19 mortality with age. HCTL metrics may thus explain the vulnerability of older adults to COVID-19. That said, the wide inter-individual variation in HCTL across the general population means that some younger adults with inherently short HCTL might be at risk of severe COVID-19 lymphopenia and mortality from the disease.Significance StatementDeclining immunity with advancing age is a general explanation for the increased mortality from COVID-19 among older adults. This mortality far exceeds that from viral illnesses such as the seasonal influenza, and it thus requires specific explanations. One of these might be diminished ability with age to offset the development of severe T-cell lymphopenia (a low T-cell count in the blood) that often complicates COVID-19. We constructed a model showing that age-dependent shortening of telomeres might constrain the ability of T-cells of some older COVID-19 patients to undertake the massive proliferation required to clear the virus that causes the infection. The model predicts that individuals with short telomeres, principally seniors, might be at a higher risk of death from COVID-19.

1. Crucial to our understanding of the ageing process is identifying how traits change with age, which variables alter their ageing process and how these traits associate with fitness.2. Here we investigated metabolic ageing in outdoor-living captive zebra finches experiencing foraging costs. We longitudinally monitored 407 individuals over 6 years and collected 3,213 measurements of two independent mass-adjusted metabolic traits: basal metabolic rate (BMRm) at thermoneutral temperatures and standard metabolic rate (SMRm), measured as BMRm but at ambient temperatures below thermoneutrality.3. We define mosaic or asynchronous ageing as the difference in standardized absolute ageing rates between traits, and we estimate the degree of asynchrony using the within-individual correlation of change in trait values with age.4. BMRm decreased linearly with age, consistent with earlier reports. In contrast, SMRm increased linearly with age. The absolute standardized change with age was significantly faster for BMRm compared to SMRm, and the within-individual correlation of age related change was negligible. To the best of our knowledge, this is the first quantification of SMRm ageing, and the finding that SMRm and BMRm age in opposite directions.5. Neither metabolic rate nor metabolic ageing rate were associated with variation in life span between individuals. Moreover, experimental manipulations of environmental quality that decreased BMRm and SMRm and shortened life span by 6 months (12%) did not affect the ageing of either metabolic trait. Females lived 2 months (4%) shorter than males, but none of the metabolic traits showed sex-specific differences at any age.6. Our findings indicate, in contrast to the current view, that baseline energy requirements increase with age, because animals do not generally live in thermoneutral conditions, and illustrate the importance of studying the ageing phenotype in an ecologically realistic setting.