Variation in early-life telomere dynamics in a long-lived bird: links to environmental conditions and survival

Conditions experienced during early life can have profound consequences for both short and long-term fitness. Variation in the natal environment has been shown to influence survival and reproductive performance of entire cohorts in wild vertebrate populations. Telomere dynamics potentially provide a link between the early environment and long-term fitness outcomes, yet we know little about how the environment can influence telomere dynamics in early life. We found that environmental conditions during growth have an important influence on early-life telomere length (TL) and attrition in nestlings of a long-lived bird, the European storm petrel Hydrobates pelagicus. Nestlings reared under unfavourable environmental conditions experienced significantly greater telomere loss during postnatal development compared with nestlings reared under more favourable natal conditions, which displayed a negligible change in TL. There was, however, no significant difference in pre-fledging TL between cohorts. The results suggest that early-life telomere dynamics could contribute to the marked differences in life-history traits that can arise among cohorts reared under different environmental conditions. Early-life TL was also found to be a significant predictor of survival during the nestling phase, providing further evidence for a link between variation in TL and individual fitness. To what extent the relationship between early-life TL and mortality during the nestling phase is a consequence of genetic, parental and environmental factors is currently unknown, but an interesting area for future research. Accelerated telomere attrition under unfavourable conditions, as observed in this study, might play a role in mediating the effects of the early-life environment on later-life performance

Experimental demonstration that offspring fathered by old males have shorter telomeres and reduced lifespans

Offspring of older parents frequently show reduced longevity, but the mechanisms driving this so-called 'Lansing effect' are unknown. While inheritance of short telomeres from older parents could underlie this effect, studies to date in different species have found mixed results, reporting positive, negative or no association between parental age and offspring telomere length (TL). However, most of the existing evidence is from non-experimental studies in which it is difficult to exclude alternative explanations such as differential survival of parents with different telomere lengths. Here we provide evidence in the zebra finch that offspring from older parents have reduced lifespans. As a first step in disentangling possible causes, we used an experimental approach to examine whether or not we could detect pre-natal paternal effects on offspring TL. We found that zebra finch embryos fathered by old males have shorter telomeres than those produced by the same mothers but with younger fathers. Since variation in embryonic TL persists into post-natal life, and early life TL is predictive of longevity in this species, this experimental study demonstrates that a paternally driven pre-natal TL reduction could at least in part underlie the reduced lifespan of offspring from older parents

Variation in population synchrony in a multi-species seabird community: response to changes in predator abundance

Ecologically similar sympatric species, subject to typical environmental conditions, may be expected to exhibit synchronous temporal fluctuations in demographic parameters, while populations of dissimilar species might be expected to show less synchrony. Previous studies have tested for synchrony in different populations of single species, and those including data from more than one species have compared fluctuations in only one demographic parameter. We tested for synchrony in inter-annual changes in breeding population abundance and productivity among four tern species on Coquet Island, northeast England. We also examined how manipulation of one independent environmental variable (predator abundance) influenced temporal changes in ecologically similar and dissimilar tern species. Changes in breeding abundance and productivity of ecologically similar species (Arctic Sterna paradisaea, Common S. hirundo and Roseate Terns S. dougallii) were synchronous with one another over time, but not with a species with different foraging and breeding behaviour (Sandwich Terns Thalasseus sandvicensis). With respect to changes in predator abundance, there was no clear pattern. Roseate Tern abundance was negatively correlated with that of large gulls breeding on the island from 1975 to 2013, while Common Tern abundance was positively correlated with number of large gulls, and no significant correlations were found between large gull and Arctic and Sandwich Tern populations. Large gull abundance was negatively correlated with productivity of Arctic and Common Terns two years later, possibly due to predation risk after fledging, while no correlation with Roseate Tern productivity was found. The varying effect of predator abundance is most likely due to specific differences in the behaviour and ecology of even these closely-related species. Examining synchrony in multi-species assemblages improves our understanding of how whole communities react to long-term changes in the environment and suggests that changes in predator abundance may differentially affect populations of sympatric seabird species

Bottom of the heap: having heavier competitors accelerates early-life telomere loss in the European starling, sturnus vulgaris

Early-life adversity is associated with poorer health and survival in adulthood in humans and other animals. One pathway by which early-life environmental stressors could affect the adult phenotype is via effects on telomere dynamics. Several studies have shown that early-life adversity is associated with relatively short telomeres, but these are often cross-sectional and usually correlational in design. Here, we present a novel experimental system for studying the relationship between early-life adversity and telomere dynamics using a wild bird, the European starling (Sturnus vulgaris). We used cross-fostering to experimentally assign sibling chicks to either small or large broods for twelve days of the growth period. We measured telomere length in red blood cells using quantitative PCR near the beginning of the experimental manipulation (4 days old), at the end of the experimental manipulation (15 days old), and once the birds were independent (55 days old). Being in a larger brood slowed growth and retarded wing development and the timing of fledging. We found no evidence that overall brood size affected telomere dynamics. However, the greater the number of competitors above the focal bird in the within-brood size hierarchy, the greater was the telomere loss during the period of the experimental manipulation. The number of competitors below the focal in the hierarchy had no effect. The effect of heavier competitors was still evident when we controlled for the weight of the focal bird at the end of the manipulation, suggesting it was not due to retarded growth per se. Moreover, the impact of early competition on telomeres was still evident at independence, suggesting persistence beyond early life. Our study provides experimental support for the hypothesis that social stress, in this case induced by the presence of a greater number of dominant competitors, accelerates the rate of telomere loss

The deteriorating soma and the indispensable germline: gamete senescence and offspring fitness

The idea that there is an impenetrable barrier that separates the germline and soma has shaped much thinking in evolutionary biology and in many other disciplines. However, recent research has revealed that the so-called ‘Weismann Barrier’ is leaky, and that information is transferred from soma to germline. Moreover, the germline itself is now known to age, and to be influenced by an age-related deterioration of the soma that houses and protects it. This could reduce the likelihood of successful reproduction by old individuals, but also lead to long-term deleterious consequences for any offspring that they do produce (including a shortened lifespan). Here, we review the evidence from a diverse and multidisciplinary literature for senescence in the germline and its consequences; we also examine the underlying mechanisms responsible, emphasizing changes in mutation rate, telomere loss, and impaired mitochondrial function in gametes. We consider the effect on life-history evolution, particularly reproductive scheduling and mate choice. Throughout, we draw attention to unresolved issues, new questions to consider, and areas where more research is needed. We also highlight the need for a more comparative approach that would reveal the diversity of processes that organisms have evolved to slow or halt age-related germline deterioration

Linking telomere dynamics to evolution, life history and environmental change: perspectives, predictions and problems

This perspectives paper considers the value of studying telomere biology outside of a biomedical context. I provide illustrative examples of the kinds of questions that evolutionary ecologists have addressed in studies of telomere dynamics in non-model species, primarily metazoan animals, and what this can contribute to our understanding of their evolution, life histories and health. I also discuss why the predicted relationships between telomere dynamics and life history traits, based on the detailed cellular studies in humans and model organisms, are not always found in studies in other species

A marker of biological ageing predicts adult risk preference in European starlings, Sturnus vulgaris

Why are some individuals more prone to gamble than others? Animals often show preferences between 2 foraging options with the same mean reward but different degrees of variability in the reward, and such risk preferences vary between individuals. Previous attempts to explain variation in risk preference have focused on energy budgets, but with limited empirical support. Here, we consider whether biological ageing, which affects mortality and residual reproductive value, predicts risk preference. We studied a cohort of European starlings (Sturnus vulgaris) in which we had previously measured developmental erythrocyte telomere attrition, an established integrative biomarker of biological ageing. We measured the adult birds’ preferences when choosing between a fixed amount of food and a variable amount with an equal mean. After controlling for change in body weight during the experiment (a proxy for energy budget), we found that birds that had undergone greater developmental telomere attrition were more risk averse as adults than were those whose telomeres had shortened less as nestlings. Developmental telomere attrition was a better predictor of adult risk preference than either juvenile telomere length or early-life food supply and begging effort. Our longitudinal study thus demonstrates that biological ageing, as measured via developmental telomere attrition, is an important source of lasting differences in adult risk preferences

Intergenerational transfer of ageing: Parental age and offspring lifespan

The extent to which the age of parents at reproduction can affect offspring lifespan and other fitness-related traits is important in our understanding of the selective forces shaping life history evolution. In this article, the widely reported negative effects of parental age on offspring lifespan (the ‘Lansing effect’) is examined. Outlined herein are the potential routes whereby a Lansing effect can occur, whether effects might accumulate across multiple generations, and how the Lansing effect should be viewed as part of a broader framework, considering how parental age affects offspring fitness. The robustness of the evidence for a Lansing effect produced so far, potential confounding variables, and how the underlying mechanisms might best be unravelled through carefully designed experimental studies are discussed

Postnatal nutrition influences male attractiveness and promotes plasticity in male mating preferences

Poor early-life nutrition could reduce adult reproductive success by negatively affecting traits linked to sexual attractiveness such as song complexity. If so, this might favor strategic mate choice, allowing males with less complex songs to tailor their mating tactics to maximize the reproductive benefits. However, this possibility has been ignored in theoretical and empirical studies. By manipulating the micronutrient content of the diet (e.g., low or high) during the postnatal period of male zebra finches, we show for the first time (1) that males reared on a poor (low) micronutrient diet had less complex songs as adults; (2) that these males, in contrast to the high micronutrient diet group, were more selective in their mating strategies, discriminating against those females most likely to reduce their clutch size when paired with males having less complex songs; and (3) that by following different mating strategies, males reared on the contrasting diets obtained similar reproductive benefits. These results suggest that early-life dietary conditions can induce multiple and long-lasting effects on male and female reproductive traits. Moreover, the results seem to reflect a previously unreported case of adaptive plasticity in mate choice in response to a nutritionally mediated reduction in sexual attractiveness