Hannah Watson

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

ABSTRACT 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 it is 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. Summary: The environment strongly influences early-life telomere attrition, suggesting that telomere dynamics may underlie cohort effects often observed in natural populations and may mechanistically link early-life stress and later-life performance.

Transcriptome analysis of a wild bird reveals physiological responses to the urban environment

Identifying the molecular basis of environmentally induced phenotypic variation presents exciting opportunities for furthering our understanding of how ecological processes and the environment can shape the phenotype. Urban and rural environments present free-living organisms with different challenges and opportunities, which have marked consequences for the phenotype, yet little is known about responses at the molecular level. We characterised transcriptomes from an urban and a rural population of great tits Parus major, demonstrating striking differences in gene expression profiles in both blood and liver tissues. Differentially expressed genes had functions related to immune and inflammatory responses, detoxification, protection against oxidative stress, lipid metabolism, and regulation of gene expression. Many genes linked to stress responses were expressed at higher levels in the urban birds, in accordance with our prediction that urban animals are exposed to greater environmental stress. This is one of the first studies to reveal transcriptional differences between urban- and rural-dwelling animals and suggests an important role for epigenetics in mediating environmentally induced physiological variation. The study provides valuable resources for developing further in-depth studies of the mechanisms driving phenotypic variation in the urban context at larger spatial and temporal scales.

Fatty acid profiles of great tit ( Parus major ) eggs differ between urban and rural habitats, but not between coniferous and deciduous forests

Early-life nutrition is an important determinant of both short- and long-term performance and fitness. The avian embryo develops within an enclosed package of nutrients, of which fatty acids (FA) are essential for many aspects of development. The FA composition of yolk depends on maternal nutrition and condition prior to egg formation, which may be affected by the external environment. To test if maternal environment affects yolk FA composition, we investigated whether the FA composition of great tit (Parus major) egg yolks differed between urban and rural habitats, and between deciduous and coniferous habitats. The results reveal differences in FA composition between eggs laid in urban and rural habitats, but not between eggs from the coniferous and deciduous habitats. To a large extent, this difference likely reflects dietary differences associated with urban habitats rather than dominating vegetation type. Specifically, urban yolks contained lower proportions of both ω-3 and ω-6 polyunsaturated FAs (PUFA), which are important for chick development. We also found a positive association between the proportion of saturated fatty acids and laying date, and a negative association between the proportion of ω-6 PUFA and clutch size. Given that urbanization is expanding rapidly, future studies should investigate whether factors such as anthropogenic food in the urban environment underlie these differences and whether they impair chick development.

Selective disappearance of great tits with short telomeres in urban areas

Urban environments pose novel challenges, as well as opportunities, for urban-dwelling wildlife. Although differences have been reported in several phenotypic traits (e.g. morphology, physiology and behaviour) between urban and rural populations, it is poorly understood whether this affects individual fitness. Telomere dynamics are posited as one possible mechanism underlying senescence and mortality. It was recently shown that telomere shortening is accelerated when growing up in an urban, compared with a rural, environment. However, the implications of accelerated telomere attrition for fitness are still unclear. Here, we examine the relationship between telomere length (TL) and survival in a bird common to urban and rural environments, and during both early and later life. The results reveal that TL is a strong predictor of post-fledging survival and recruitment in both habitats but, crucially, selective disappearance of individuals with short telomeres early in life is more pronounced in the urban environment, resulting in a longer average TL among the adult population. However, following recruitment, we found no difference in the relationship between TL and survival between the urban and rural environments. This indicates that the urban environment has negative effects in early life, while during later life the benefits could potentially outweigh the costs.

A theoretical model of the evolution of actuarial senescence under environmental stress.

Free-living organisms are exposed to a wide range of stressors, all of which can disrupt components of stress-related and detoxification physiology. The subsequent accumulation of somatic damage is widely believed to play a major role in the evolution of senescence. Organisms have evolved sophisticated physiological regulatory mechanisms to maintain homeostasis in response to environmental perturbations, but these systems are likely to be constrained in their ability to optimise robustness to multiple stressors due to functional correlations among related traits. While evolutionary change can accelerate due to human ecological impacts, it remains to be understood how exposure to multiple environmental stressors could affect senescence rates and subsequently population dynamics and fitness. We used a theoretical evolutionary framework to quantify the potential consequences for the evolution of actuarial senescence in response to exposure to simultaneous physiological stressors – one versus multiple and additive versus synergistic – in a hypothetical population of avian “urban adapters”. In a model in which multiple stressors have additive effects on physiology, species may retain greater capacity to recover, or respond adaptively, to environmental challenges. However, in the presence of high synergy, physiological dysregulation suddenly occurs, leading to a rapid increase in age-dependent mortality and subsequent population collapse. Our results suggest that, if the synergistic model is correct, population crashes in environmentally-stressed species could happen quickly and with little warning, as physiological thresholds of stress resistance are overcome.

Maternally derived yolk antioxidants buffer the developing avian embryo against oxidative stress induced by hyperoxia

ABSTRACT In oviparous animals, maternally transferred antioxidants protect the embryo from oxidative damage from high rates of reactive oxygen species (ROS) production incurred by rapid growth. Elevated ROS exposure, beyond that incurred by normal growth, can occur as a result of exposure to exogenous factors (e.g. pollutants, toxins, radiation), increasing the risk of oxidative damage, with potentially adverse consequences for embryonic development and long-term fitness. The capacity of the avian embryos antioxidant protection system to counter an increased exogenous oxidative threat is poorly understood. We induced an external oxidative challenge via experimental increase in ambient oxygen concentration throughout incubation of wild great tit Parus major eggs in the laboratory. At day 11 of incubation, brain tissue revealed no consistent differences in oxidative stress status [as measured by antioxidant levels (superoxide dismutase and total glutathione), lipid peroxidation and telomere length] between control (21% oxygen) and hyperoxic (40% oxygen) embryos. However, the level of vitamin E was significantly lower and lipid peroxidation was significantly higher in yolks of eggs reared under elevated oxygen concentrations. The results suggest that maternally derived yolk antioxidants successfully buffer developing embryonic tissues against an increased exogenous oxidative threat. Furthermore, vitamin E plays a more important role in protecting the embryo than carotenoids. However, the depletion of antioxidants and increased peroxidation of lipids in the yolk could have negative consequences for embryonic development, in particular for the brain and heart that require highly unsaturated fatty acids, and protection against the oxidative burst following hatching. Summary: The avian yolk bears the burden of an elevated oxidative challenge, without the embryo having to compromise its endogenous antioxidant supply or suffer oxidative damage itself.

Effects of the Urban Environment on Oxidative Stress in Early Life : Insights from a Cross-fostering Experiment

Abstract As urban areas expand rapidly worldwide, wildlife is exposed to a wide range of novel environmental stressors, such as increased air pollution and artificial light at night. Birds in highly polluted and/or urbanized habitats have been found to have increased antioxidant protection, which is likely important to avoid accumulation of oxidative damage, which can have negative fitness consequences. Yet, the current knowledge about the ontogeny of antioxidant protection in urban areas is limited; i.e., is the capacity to up-regulate the antioxidant defences already established during pre-natal development, or does it manifest itself during post-natal development? We cross-fostered great tit (Parus major) nestlings within and between urban and rural habitats, to determine if oxidative stress (measured as non-enzymatic total antioxidant capacity, superoxide dismutase (SOD), and plasma lipid peroxidation) is affected by habitat of origin and/or by habitat of rearing. The results demonstrate that being reared in the urban environment triggers an increase in SOD (an intracellular, enzymatic antioxidant) independent of natal habitat. Oxidative damage increased with hatching date in urban-reared nestlings, but there was little seasonal change in rural-reared nestlings. Total antioxidant capacity was neither affected by habitat of rearing or habitat of origin, but we observed a decline with hatching date in both rearing habitats. Taken together, our results support the growing evidence that the urban environment induces a direct plastic adjustment in antioxidant protection, but that up-regulation is not sufficient to avoid increased oxidative damage in late-hatched broods. Future studies should explore the underlying causes for this effect in late-hatched broods and whether it has any negative long-term implications, both at the individual- and the population level.

Assessing the effects of repeated handling on the physiology and condition of semi‐precocial nestlings

Repeated exposure to elevated levels of glucocorticoids during development can have long‐term detrimental effects on survival and fitness, potentially associated with increased telomere attrition. Nestling birds are regularly handled for ecological research, yet few authors have considered the potential for handling‐induced stress to influence hormonally mediated phenotypic development or bias interpretations of subsequent focal measurements. We experimentally manipulated the handling experience of the semi‐precocial nestlings of European Storm Petrel Hydrobates pelagicus to simulate handling in a typical field study and examined cumulative effects on physiology and condition in late postnatal development. Neither baseline corticosterone (the primary glucocorticoid in birds), telomere length nor body condition varied with the number of handling episodes. The absence of a response could be explained if Storm Petrels did not perceive handling to be stressful or if there is dissociation of the hypothalamic–pituitary–adrenal axis from stressful stimuli in early life. Eliciting a response to a stressor may be maladaptive for cavity‐dwelling young that are unable to escape or defend themselves. Furthermore, avoiding elevated overall glucocorticoid exposure may be particularly important in a long‐lived species, in which accelerated early‐life telomere erosion could impact negatively upon longevity. We propose that the level of colony‐wide disturbance induced by investigator handling of young could be important in underlining species‐specific responses. Storm Petrel nestlings appear unresponsive to investigator handling within the limits of handling in a typical field study and handling at this level should not bias physiological and morphological measurements.