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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.

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.

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.

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.

Many organisms are capable of growing faster than they do. Restrained growth rate has functionally been explained by negative effects on lifespan of accelerated growth. However, the underlying mechanisms remain elusive. Telomere attrition has been proposed as a causal agent and has been studied in endothermic vertebrates. We established that telomeres exist as chromosomal-ends in a model insect, the field cricket, using terminal restriction fragment andBal 31methods. Telomeres comprised TTAGGn repeats of 38kb on average, more than four times longer than the telomeres of human infants.Bal 31assays confirmed that telomeric repeats were located at the chromosome-ends. We tested whether rapid growth is achieved at the expense of telomere length by comparing crickets reared at 23°C with their siblings reared at 28°C, which grew three times faster. Surprisingly, neither temperature treatment nor age affected average telomere length. Concomitantly, the broad sense heritability of telomere length was remarkably high at ~100%. Despite high heritability, the evolvability (a mean standardized measure of genetic variance) was low relative to that of body mass. We discuss the different interpretations of these scaling methods in the context of telomere evolution. It is clear that some important features of vertebrate telomere biology are evident in an insect species dating back to the Triassic, but also that there are some striking differences. The apparent lack of an effect of growth rate and the total number of cell divisions on telomere length is puzzling, suggesting that telomere length could be actively maintained during the growth phase. Whether such maintenance of telomere length is adaptive remains elusive and requires further study investigating the links with fitness in the wild.

Telomere length (TL) and shortening is increasingly shown to predict variation in survival and lifespan, raising the question of what causes variation in these traits. Oxidative stress is well known to accelerate telomere attrition in vitro, but its importance in vivo is largely hypothetical. We tested this hypothesis experimentally by supplementing white stork (Ciconia ciconia) chicks with antioxidants. Individuals received either a control treatment, or a supply of tocopherol (vitamin E) and selenium, which both have antioxidant properties. The antioxidant treatment increased the concentration of tocopherol for up to two weeks after treatment but did not affect growth. Using the telomere restriction fragment technique, we evaluated erythrocyte TL and its dynamics. Telomeres shortened significantly over the 21 days between the baseline and final sample, independent of sex, mass, size and hatching order. The antioxidant treatment significantly mitigated shortening rate of average TL (−31% in shorter telomeres; percentiles 10th, 20th and 30th). Thus, our results support the hypothesis that oxidative stress shortens telomeres in vivo., Diego San Mauro for his financial support for the telomere assays (Project CGL2017-85637-P financed by the Spanish Ministry of Economy and Competitiveness). Fieldwork for this study and oxidative stress assays were partly supported by project RTA2011-00111-C03-02 financed by the Spanish National Institute for Agricultural Research INIA. J.P.-P. was funded by a grant from the Complutense University of Madrid (CT45/15-CT46/15).

Telomere length (TL) and shortening rate predict survival in many organisms. Evolutionary dynamics of TL in response to survival selection depend on the presence of genetic variation that selection can act upon. However, the amount of standing genetic variation is poorly known for both TL and TL shortening rate, and has not been studied for both traits in combination in a wild vertebrate. We used experimental (cross-fostering) and statistical (animal models) means to disentangle and estimate genetic and environmental contributions to TL variation in pedigreed free-living jackdaws (Corvus monedula). TL was measured twice early in life (age- and interval-standardized), when shortening is highest, using the high-precision TRF technique, adapted to exclude interstitial telomeric sequences. TL shortened significantly during the nestling phase (10.4 bp/day), was highly repeatable within individuals (R=0.97) and genetically correlated between the two ages (rG>0.99). Additive genetic effects explained the major part of TL variation between individuals, with heritability on average estimated ath2=0.74. Parent- offspring regressions yielded similar estimates for the sexes when accounting for changes in paternal TL over life. Cohort effects explained a small but significant part of TL variation. Heritable variation for telomere shortening was negligible. Despite the high heritability of TL, its evolvability, which scales the additive genetic variance by mean TL, was close to zero. Hence evolutionary change of TL is likely to be slow despite significant selection.

Ecological conditions affect fitness, but mechanisms causing such effects are not well known, while evolved responses to environmental variation may depend on the underlying mechanisms. Consequences of environmental conditions vary strongly between traits, but a framework to interpret such variation is lacking. We propose that variation in trait response may be explained by differential canalisation, with traits with larger fitness effects showing weaker responses to environmental perturbations due to preferential resource allocation to such traits. We tested the canalisation hypothesis using brood size manipulation in wild jackdaw nestlings in which we measured eight physiological traits (mainly oxidative stress markers), and two feather traits. For each trait, we estimated manipulation response and association with fitness (over-winter survival). As predicted, a strong negative correlation emerged between manipulation response and association with fitness (r = -0.76). We discuss the consequences of differential trait canalisation for the study of mechanisms mediating environmental effects on fitness.

As attrition of telomeres, DNA caps that protect chromosome integrity, is accelerated by various forms of stress, telomere length (TL) has been proposed as an indicator of lifetime accumulated stress. In ecological studies, it has been used to provide insights into ageing, life history trade-offs, the costs of reproduction and disease. qPCR is a high-throughput and cost-effective tool to measure relative TL (rTL) that can be applied to newly collected and archived ecological samples. However, qPCR is susceptible to error both from the method itself and pre-analytical steps. Here, repeatability was assessed overall and separately across multiple levels (intra-assay, inter-assay and inter-extraction) to elucidate the causes of measurement error, as a step towards improving precision. We also tested how accuracy, defined as the correlation between the "gold standard" for TL estimation (telomere restriction fragment length analysis with in-gel hybridization), could be improved. We find qPCR repeatability (intra- and inter-assay levels) to be at similar levels across three common storage media (ethanol, Longmire's and Queen's). However, inter-extraction repeatability was 50% lower for samples stored in Queen's lysis buffer, indicating storage medium can influence precision. Precision as well as accuracy could be increased by estimating rTL from multiple qPCR reactions and from multiple extractions. Repetition increased statistical power equivalent to a 25% (single extraction analysed twice) and 17% (two extractions) increase in sample size. Overall, this study identifies novel sources of variability in high-throughput telomere quantification and provides guidance on sampling strategy design and how to increase rTL precision and accuracy.

Oxidative stress shortens telomeres in cell culture, but whether oxidative stress explains variation in telomere shortening in vivo at physiological oxidative stress levels is not well known. We therefore tested for correlations between six oxidative stress markers and telomere attrition in nestling birds (jackdaws Corvus monedula ) that show a high rate of telomere attrition in early life. Telomere attrition was measured between ages 5 and 30 days, and was highly variable (average telomere loss: 323 bp, CV = 45%). Oxidative stress markers were measured in blood at age 20 days and included markers of oxidative damage (TBARS, dROMs and GSSG) and markers of antioxidant protection (GSH, redox state, uric acid). Variation in telomere attrition was not significantly related to these oxidative stress markers (| r | ≤ 0.08, n = 87). This finding raises the question whether oxidative stress accelerates telomere attrition in vivo . The accumulation of telomere attrition over time depends both on the number of cell divisions and on the number of base pairs lost per DNA replication and, based on our findings, we suggest that in a growing animal cell proliferation, dynamics may be more important for explaining variation in telomere attrition than oxidative stress.

Telomere length (TL) predicts health and survival across taxa. Variation in TL between individuals is thought to be largely of genetic origin, but telomere inheritance is unusual, because zygotes already express a TL phenotype, the TL of the parental gametes. Offspring TL changes with paternal age in many species including humans, presumably through age-related TL changes in sperm, suggesting an epigenetic inheritance mechanism. However, present evidence is based on cross-sectional analyses, and age at reproduction is confounded with between-father variation in TL. Furthermore, the quantitative importance of epigenetic TL inheritance is unknown. Using longitudinal data of free-living jackdaws Corvus monedula, we show that erythrocyte TL of subsequent offspring decreases with parental age within individual fathers, but not mothers. By cross-fostering eggs, we confirmed the paternal age effect to be independent of paternal age dependent care. Epigenetic inheritance accounted for a minimum of 34% of the variance in offspring TL that was explained by paternal TL. This is a minimum estimate, because it ignores the epigenetic component in paternal TL variation and sperm TL heterogeneity within ejaculates. Our results indicate an important epigenetic component in the heritability of TL with potential consequences for offspring fitness prospects., Author summary Telomeres are DNA-protein structures at chromosome ends and a short telomere length predicts reduced survival in humans, birds and other organisms. Variation in telomere length between individuals is thought to be largely of genetic origin, but telomere inheritance may be unusual because not only genes regulating telomere length are inherited, but a fertilised cell already has a telomere length (from the parental gametes). Using long-term individual-based data of jackdaw families (a small corvid species), we found that as fathers aged, they produced chicks with shorter telomeres. This suggests that telomere length inheritance has an epigenetic component. To investigate to what extent telomere length in the fertilised cell affects telomere length after birth, we compared telomere length over years within fathers with the telomere length of their consecutive offspring. This epigenetic component explained a substantial part (≥ one third) of the telomere length inheritance; whereas there was no such effect of maternal telomere length. The sex difference fits the idea that lifelong sperm formation leads to change in telomere length of the sperm cells, whereas female gametes are all formed before birth and their telomere length does not change over time.

Bird populations provide excellent systems to investigate variation in longevity in the wild since individuals can often be monitored over their lifetime. A number of recent studies suggest that the dynamics of protective telomere chromosome caps (telomere length and rate of loss) are indicative of biological state and potentially useful as indicators of future longevity. Currently, Terminal Restriction Fragment (TRF) analysis and relative quantitative PCR (qPCR) are used to measure telomeres in birds, but with limitations. TRF analysis is time consuming, while relative qPCR gives a within-study relative value making it difficult to compare across experiments. Utilising an approach first developed in humans of using synthetic oligomer telomeric (TTAGGG)n and normaliser gene standards of known length to calibrate qPCR values, we describe a methodological adaptation to the avian qPCR telomere assay to make results comparable within, and potentially between, bird species. We evaluate this absolute qPCR method in the Seychelles warbler Acrocephalus sechellensis against relative qPCR measurements on the same samples. Telomere estimates from both methods showed an age-related decline in telomere length, and were highly correlated (r = 0.99). Absolute qPCR avian telomere analysis may prove a useful means of estimating telomere lengths in a calibrated, sensitive, and efficient way using small amounts of archived bird sample.

Telomere length predicts survival in birds, and many stressors that presumably reduce fitness have also been linked to telomere length. The response to selection of telomere length will be largely determined by the heritability of this trait; however, little is known about the genetic component of telomere length variation in animals other than humans. Moreover, published heritability estimates of telomere length are based on telomere measurements with techniques that do not distinguish between terminal telomeres, which are susceptible to age and stress, and the interstitial telomeric repeats, which are relatively inert. Heritability estimates that combine interstitial and terminal telomeres are difficult to interpret in species such as birds, where interstitial telomeres are often numerous. We estimated the heritability of terminal telomere length in a captive Zebra Finch population of cross-fostered (half-)siblings using data obtained with an electrophoresis technique that excludes the interstitial repeats from the measurements. We used both a Bayesian quantitative genetic 'animal' model and a frequentist sibling regression approach to estimate heritability. With the animal model, we estimated a high heritability of telomere length (h (2) = 0.99, 95 % credible interval = 0.87-1), but had insufficient statistical power to separate parental and permanent environment effects. The frequentist approach yielded similar heritability estimates, although with large confidence intervals. We used general linear mixed models to disentangle variance components of telomere length. The relative contributions of the individual, mother and father to telomere length variation were statistically indistinguishable at 23-31 %. Chicks were cross-fostered 4-days after hatching, and no effect of rearing nest was found, indicating that any undetected environmental effects exerted their influence prior to, or soon after, hatching. Thus, we conclude that telomere length resemblance between relatives is high and proportional to their relatedness, but we cannot conclusively distinguish between genetic and other forms of inheritance.

Background Circadian organisation of behavioural and physiological rhythms in mammals is largely driven by the clock in the suprachiasmatic nuclei (SCN) of the hypothalamus. In this clock, a molecular transcriptional repression and activation mechanism generates near 24 hour rhythms. One of the outputs of the molecular clock in specific SCN neurons is arginine-vasopressin (AVP), which is responsive to transcriptional activation by clock gene products. As negative regulators, the protein products of the period genes are thought to repress transcriptional activity of the positive limb after heterodimerisation with CRYPTOCHROME. When both the Per1 and Per2 genes are dysfunctional by targeted deletion of the PAS heterodimer binding domain, mice lose circadian organization of behaviour upon release into constant environmental conditions. To which degree the period genes are involved in the control of AVP output is unknown. Methods Using an in vitro slice culture setup, SCN-AVP release of cultures made of 10 wildtype and 9 Per1/2 double-mutant mice was assayed. Mice were sacrificed in either the early light phase of the light-dark cycle, or in the early subjective day on the first day of constant dark. Results Here we report that in arrhythmic homozygous Per1/2 double-mutant mice there is still a diurnal peak in in vitro AVP release from the SCN similar to that of wildtypes but distinctively different from the release pattern from the paraventricular nucleus. Such a modulation of AVP release is unexpected in mice where the circadian clockwork is thought to be disrupted. Conclusion Our results suggest that the circadian clock in these animals, although deficient in (most) behavioural and molecular rhythms, may still be (partially) functional, possibly as an hourglass mechanism. The level of perturbation of the clock in Per1/2 double mutants may therefore be less than was originally thought.