Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird

Exposure to stressors early in life is associated with faster ageing and reduced longevity. One important mechanism that could underlie these late life effects is increased telomere loss. Telomere length in early post-natal life is an important predictor of subsequent lifespan, but the factors underpinning its variability are poorly understood. Recent human studies have linked stress exposure to increased telomere loss. These studies have of necessity been non-experimental and are consequently subjected to several confounding factors; also, being based on leucocyte populations, where cell composition is variable and some telomere restoration can occur, the extent to which these effects extend beyond the immune system has been questioned. In this study, we experimentally manipulated stress exposure early in post-natal life in nestling European shags (Phalacrocorax aristotelis) in the wild and examined the effect on telomere length in erythrocytes. Our results show that greater stress exposure during early post-natal life increases telomere loss at this life-history stage, and that such an effect is not confined to immune cells. The delayed effects of increased telomere attrition in early life could therefore give rise to a ‘time bomb’ that reduces longevity in the absence of any obvious phenotypic consequences early in life

Protracted treatment with corticosterone reduces breeding success in a long-lived bird

Determining the physiological mechanisms underpinning life-history decisions is essential for understanding the constraints under which life-history strategies can evolve. In long-lived species, where the residual reproductive value of breeders is high, adult survival is a key contributor to lifetime reproductive success. We therefore expect that when adult survival is compromised during reproduction, mechanisms will evolve to redirect resources away from reproduction, with implications for reproductive hormones, adult body mass, nest attendance behaviour and breeding success. We investigated whether manipulating corticosterone, to simulate exposure to an environmental stressor, affected the secretion of prolactin and breeding success in the black-legged kittiwake Rissa tridactyla. We used implanted Alzet® osmotic pumps to administer corticosterone to incubating kittiwakes at a constant rate over a period of approximately eight days. Manipulated birds were compared with sham implanted birds and control birds, which had no implants. There was no significant difference in the body mass of captured individuals at the time of implantation and implant removal. Corticosterone-implanted males showed lower nest attendance during the chick rearing period compared to sham-implanted males; the opposite pattern was found in females. Corticosterone treated birds showed a marginally significant reduction in breeding success compared to sham-implanted individuals, with all failures occurring at least one week after implant removal. However, prolactin concentrations at implant removal were not significantly different from initial values. We were unable to measure the profile of change in corticosterone during the experiment. However, our results suggest a delayed effect of elevated corticosterone on breeding success rather than an immediate suppression of prolactin concentrations causing premature failure

Parental age influences offspring telomere loss

1. The age of the parents at the time of offspring production can influence offspring longevity, but the underlying mechanisms remain poorly understood. The effect of parental age on offspring telomere dynamics (length and loss rate) is one mechanism that could be important in this context. 2. Parental age might influence the telomere length that offspring inherit or age-related differences in the quality of parental care could influence the rate of offspring telomere loss. However, these routes have generally not been disentangled. 3. Here, we investigated whether parental age was related to offspring telomere dynamics using parents ranging in age from 2 to 22 years old in a free-living population of a long-lived seabird, the European shag (Phalacrocorax aristotelis). By measuring the telomere length of offspring at hatching and towards the end of the post-natal growth period, we could assess whether any potential parental age effect was confined to the post-natal rearing period. 4. There was no effect of maternal or paternal age on the initial telomere length of their chicks. However, chicks produced by older mothers and fathers experienced significantly greater telomere loss during the post-natal nestling growth period. We had relatively few nests in which the ages of both parents were known, and individuals in this population mate assortatively with respect to age. Thus, we could not conclusively determine whether the parental age effect was due to maternal age, paternal age, or both; however, it appears that the effect is stronger in mothers. 5. These results demonstrate that in this species, there was no evidence that parental age was related to offspring hatching telomere length. However, telomere loss during nestling growth was reduced in the offspring of older parents. This could be due to an age-related deterioration in the quality of the environment that parents provide, or because parents that invest less in offspring rearing live to an older age

Maternal condition but not corticosterone is linked to brood sex ratio adjustment in a passerine bird

There is evidence of offspring sex ratio adjustment in a range of species, but the potential mechanisms remain largely unknown. Elevated maternal corticosterone (CORT) is associated with factors that can favour brood sex ratio adjustment, such as reduced maternal condition, food availability and partner attractiveness. Therefore, the steroid hormone has been suggested to play a key role in sex ratio manipulation. However, despite correlative and causal evidence CORT is linked to sex ratio manipulation in some avian species, the timing of adjustment varies between studies. Consequently, whether CORT is consistently involved in sex-ratio adjustment, and how the hormone acts as a mechanism for this adjustment remains unclear. Here we measured maternal baseline CORT and body condition in free-living blue tits (Cyanistes caeruleus) over three years and related these factors to brood sex ratio and nestling quality. In addition, a non-invasive technique was employed to experimentally elevate maternal CORT during egg laying, and its effects upon sex ratio and nestling quality were measured. We found that maternal CORT was not correlated with brood sex ratio, but mothers with elevated CORT fledged lighter offspring. Also, experimental elevation of maternal CORT did not influence brood sex ratio or nestling quality. In one year, mothers in superior body condition produced male biased broods, and maternal condition was positively correlated with both nestling mass and growth rate in all years. Unlike previous studies maternal condition was not correlated with maternal CORT. This study provides evidence that maternal condition is linked to brood sex ratio manipulation in blue tits. However, maternal baseline CORT may not be the mechanistic link between the maternal condition and sex ratio adjustment. Overall, this study serves to highlight the complexity of sex ratio adjustment in birds and the difficulties associated with identifying sex biasing mechanisms

Early-life telomere dynamics differ between the sexes and predict growth in the barn swallow (Hirundo rustica)

Telomeres are conserved DNA-protein structures at the termini of eukaryotic chromosomes which contribute to maintenance of genome integrity, and their shortening leads to cell senescence, with negative consequences for organismal functions. Because telomere erosion is influenced by extrinsic and endogenous factors, telomere dynamics may provide a mechanistic basis for evolutionary and physiological trade-offs. Yet, knowledge of fundamental aspects of telomere biology under natural selection regimes, including sex- and context-dependent variation in early-life, and the covariation between telomere dynamics and growth, is scant. In this study of barn swallows (Hirundo rustica) we investigated the sex-dependent telomere erosion during nestling period, and the covariation between relative telomere length and body and plumage growth. Finally, we tested whether any covariation between growth traits and relative telomere length depends on the social environment, as influenced by sibling sex ratio. Relative telomere length declined on average over the period of nestling maximal growth rate (between 7 and 16 days of age) and differently covaried with initial relative telomere length in either sex. The frequency distribution of changes in relative telomere length was bimodal, with most nestlings decreasing and some increasing relative telomere length, but none of the offspring traits predicted the a posteriori identified group to which individual nestlings belonged. Tail and wing length increased with relative telomere length, but more steeply in males than females, and this relationship held both at the within- and among-broods levels. Moreover, the increase in plumage phenotypic values was steeper when the sex ratio of an individual's siblings was female-biased. Our study provides evidence for telomere shortening during early life according to subtly different dynamics in either sex. Furthermore, it shows that the positive covariation between growth and relative telomere length depends on sex as well as social environment, in terms of sibling sex ratio

Telomere Dynamics May Link Stress Exposure and Ageing across Generations

Although exposure to stressors is known to increase disease susceptibility and accelerate ageing, evidence is accumulating that these effects can span more than one generation. Stressors experienced by parents have been reported to negatively influence the longevity of their offspring and even grand offspring. The mechanisms underlying these long-term, cross-generational effects are still poorly understood, but we argue here that telomere dynamics are likely to play an important role. In this review, we begin by surveying the current connections between stress and telomere dynamics. We then lay out the evidence that exposure to stressors in the parental generation influences telomere dynamics in offspring and potentially subsequent generations. We focus on evidence in mammalian and avian studies and highlight several promising areas where our understanding is incomplete and future investigations are critically needed. Understanding the mechanisms that link stress exposure across generations requires interdisciplinary studies and is essential to both the biomedical community seeking to understand how early adversity impacts health span and evolutionary ecologists interested in how changing environmental conditions are likely to influence age-structured population dynamics. 2015 The Author(s)

Effects of human disturbance on postnatal growth and baseline corticosterone in a long-lived bird

Prolonged or repeated episodes of environmental stress could be especially detrimental for developing young, via impaired growth or development. Despite this, most studies investigating the effects of human recreational and tourism activities have focused on adults. An increasing demand for nature-based tourism in remote locations means that many seabirds, which have evolved largely in the absence of predators and humans, are being exposed to novel pressures. The slow-growing semi-precocial nestlings of the European storm petrel Hydrobates pelagicus experience higher mortality rates in nests exposed to human recreational disturbance. Here, we examine whether surviving nestlings reared in disturbed areas are also affected via changes in growth trajectories and baseline circulating glucocorticoids. Nestlings reared in high-disturbance areas displayed delayed mass growth, and we found weak evidence for slower rates of mass gain and tarsus growth, compared with nestlings reared in undisturbed areas. There were no differences in wing growth, consistent with prioritization of long wings, important for post-fledging survival. A tendency for a less marked age-related decline in corticosterone (CORT) in disturbed nestlings offers limited evidence that changes in growth trajectories were mediated by baseline CORT. However, disturbed nestlings could have experienced overall higher GC exposure if the acute GC response was elevated. ‘Catch-up’ growth enabled high-disturbance nestlings to overcome early constraints and achieve a similar, or even larger, asymptotic body size and mass as low-disturbance nestlings. While catch-up growth has been shown to carry costs for parents and offspring, the effects of disturbance were slight and considerably smaller than growth alterations driven by variation in environmental conditions between years. Nonetheless, effects of human recreational activities could be exacerbated under higher levels of human disturbance or in the presence of multiple pressures, as imposed by present rapid rates of environmental change