Baseline glucocorticoids alone do not predict reproductive success across years, but in interaction with enzymatic antioxidants.

Glucocorticoids are known to adjust organismal functions, such as metabolism, in response to environmental conditions. Therefore, these hormones are thought to play a key role in regulating the metabolically demanding aspects of reproduction, especially in variable environments. However, support for the hypothesis that variation in glucocorticoid concentrations predicts reproductive success is decidedly mixed. Two explanations may account for this discrepancy: (i) Glucocorticoids might not act independently but could interact with other physiological traits, jointly influencing reproduction, and (ii) such an association could become apparent primarily in challenging environments when glucocorticoid concentrations increase. To address these two possibilities, we determined natural variation in circulating baseline glucocorticoid concentrations in parental great tits (Parus major) alongside two physiological systems known to be related with an individual's metabolism: oxidative status parameters (i.e., concentrations of pro-oxidants, dietary, and enzymatic antioxidants) and body condition. These systems interact with glucocorticoids and can also influence reproductive success. We measured these variables in two breeding seasons that differed in environmental conditions. When accounting for the interaction of baseline glucocorticoids with other physiological traits, we found a positive relationship between baseline glucocorticoids and the number of fledglings in adult great tits. The strength of this relationship was more pronounced for those individuals who also had high concentrations of the enzymatic antioxidant glutathione peroxidase. When studied independently, glucocorticoids were not related to fitness proxies, even in the year with more challenging environmental conditions. Together, our study lend to support the hypothesis that glucocorticoids do not influence fitness alone, but in association with other physiological systems.

Endocrine flexibility can facilitate or constrain the ability to cope with global change.

Global climate change has increased average environmental temperatures world-wide, simultaneously intensifying temperature variability and extremes. Growing numbers of studies have documented phenological, behavioural and morphological responses to climate change in wild populations. As systemic signals, hormones can contribute to orchestrating many of these phenotypic changes. Yet little is known about whether mechanisms like hormonal flexibility (reversible changes in hormone concentrations) facilitate or limit the ability of individuals, populations and species to cope with a changing climate. In this perspective, we discuss different mechanisms by which hormonal flexibility, primarily in glucocorticoids, could promote versus hinder evolutionary adaptation to changing temperature regimes. We focus on temperature because it is a key gradient influenced by climate change, it is easy to quantify, and its links to hormones are well established. We argue that reaction norm studies that connect individual responses to population-level and species-wide patterns will be critical for making progress in this field. We also develop a case study on urban heat islands, where several key questions regarding hormonal flexibility and adaptation to climate change can be addressed. Understanding the mechanisms that allow animals to cope when conditions become more challenging will help in predicting which populations are vulnerable to ongoing climate change. This article is part of the theme issue 'Endocrine responses to environmental variation: conceptual approaches and recent developments'.

Mitochondrial metabolism in blood more reliably predicts whole-animal energy needs compared to other tissues.

Understanding energy metabolism in free-ranging animals is crucial for ecological studies. In birds, red blood cells (RBCs) offer a minimally invasive method to estimate metabolic rate (MR). In this study with European starlings Sturnus vulgaris, we examined how RBC oxygen consumption relates to oxygen use in key tissues (brain, liver, heart, and pectoral muscle) and versus the whole organism measured at basal levels. The pectoral muscle accounted for 34%-42% of organismal MR, while the heart and liver, despite their high mass-specific metabolic rate, each contributed 2.5%-3.0% to organismal MR. Despite its low contribution to organismal MR (0.03%-0.04%), RBC MR best predicted organismal MR (r = 0.70). Oxygen consumption of the brain and pectoralis was also associated with whole-organism MR, unlike that of heart and liver. Overall, our findings demonstrate that the metabolism of a systemic tissue like blood is a superior proxy for organismal energy metabolism than that of other tissues.

Dietary nucleotides can prevent glucocorticoid-induced telomere attrition in a fast-growing wild vertebrate.

Telomeres are chromosome protectors that shorten during eukaryotic cell replication and in stressful conditions. Developing individuals are susceptible to telomere erosion when their growth is fast and resources are limited. This is critical because the rate of telomere attrition in early life is linked to health and life span of adults. The metabolic telomere attrition hypothesis (MeTA) suggests that telomere dynamics can respond to biochemical signals conveying information about the organism's energetic state. Among these signals are glucocorticoids, hormones that promote catabolic processes, potentially impairing costly telomere maintenance, and nucleotides, which activate anabolic pathways through the cellular enzyme target of rapamycin (TOR), thus preventing telomere attrition. During the energetically demanding growth phase, the regulation of telomeres in response to two contrasting signals - one promoting telomere maintenance and the other attrition - provides an ideal experimental setting to test the MeTA. We studied nestlings of a rapidly developing free-living passerine, the great tit (Parus major), that either received glucocorticoids (Cort-chicks), nucleotides (Nuc-chicks) or a combination of both (NucCort-chicks), comparing these with controls (Cnt-chicks). As expected, Cort-chicks showed telomere attrition, while NucCort- and Nuc-chicks did not. NucCort-chicks was the only group showing increased expression of a proxy for TOR activation (the gene TELO2), of mitochondrial enzymes linked to ATP production (cytochrome oxidase and ATP-synthase) and a higher efficiency in aerobically producing ATP. NucCort-chicks had also a higher expression of telomere maintenance genes (shelterin protein TERF2 and telomerase TERT) and of enzymatic antioxidant genes (glutathione peroxidase and superoxide dismutase). The findings show that nucleotide availability is crucial for preventing telomere erosion during fast growth in stressful environments.

Great tits differ in glucocorticoid plasticity in response to spring temperature.

Fluctuations in environmental temperature affect energy metabolism and stimulate the expression of reversible phenotypic plasticity in vertebrate behavioural and physiological traits. Changes in circulating concentrations of glucocorticoid hormones often underpin environmentally induced phenotypic plasticity. Ongoing climate change is predicted to increase fluctuations in environmental temperature globally, making it imperative to determine the standing phenotypic variation in glucocorticoid responses of free-living populations to evaluate their potential for coping via plastic or evolutionary changes. Using a reaction norm approach, we repeatedly sampled wild great tit (Parus major) individuals for circulating glucocorticoid concentrations during reproduction across five years to quantify individual variation in glucocorticoid plasticity along an environmental temperature gradient. As expected, baseline and stress-induced glucocorticoid concentrations increased with lower environmental temperatures at the population and within-individual level. Moreover, we provide unique evidence that individuals differ significantly in their plastic responses to the temperature gradient for both glucocorticoid traits, with some displaying greater plasticity than others. Average concentrations and degree of plasticity covaried for baseline glucocorticoids, indicating that these two reaction norm components are linked. Hence, individual variation in glucocorticoid plasticity in response to a key environmental factor exists in a wild vertebrate population, representing a crucial step to assess their potential to endure temperature fluctuations.

Glucocorticoids in a warming world: Do they help birds to cope with high environmental temperatures?

Climate change is threatening biodiversity world-wide. One of its most prominent manifestations are rising global temperatures and higher frequencies of heat waves. High environmental temperatures may be particularly challenging for endotherms, which expend considerable parts of their energy budget and water resources on thermoregulation. Thermoregulation involves phenotypic plasticity in behavioral and physiological traits. Information on causal mechanisms that support plastic thermoregulatory strategies is key to understand how environmental information is transmitted and whether they impose trade-offs or constraints that determine how endotherms cope with climate warming. In this review, we focus on glucocorticoids, metabolic hormones that orchestrate plastic responses to various environmental stimuli including temperature. To evaluate how they may mediate behavioral and physiological responses to high environmental temperatures, we 1) briefly review the major thermoregulatory strategies in birds; 2) summarize the functions of baseline and stress-induced glucocorticoid concentrations; 3) synthesize the current knowledge of the relationship between circulating glucocorticoids and high environmental temperatures in birds; 4) generate hypotheses for how glucocorticoids may support plastic thermoregulatory responses to high environmental temperatures that occur over different time-frames (i.e., acute, short- and longer-term); and 5) discuss open questions on how glucocorticoids, and their relationship with thermoregulation, may evolve. Throughout this review we highlight that our knowledge, particularly on free-living populations, is really limited and outline promising avenues for future research. As evolutionary endocrinologists we now need to step up and identify the costs, benefits, and evolution of glucocorticoid plasticity to elucidate how they may help birds cope with a warming world.

Quantifying Glucocorticoid Plasticity Using Reaction Norm Approaches: There Still is So Much to Discover!

Hormones are highly responsive internal signals that help organisms adjust their phenotype to fluctuations in environmental and internal conditions. Our knowledge of the causes and consequences of variation in circulating hormone concentrations has improved greatly in the past. However, this knowledge often comes from population-level studies, which generally tend to make the flawed assumption that all individuals respond in the same way to environmental changes. Here, we advocate that we can vastly expand our understanding of the ecology and evolution of hormonal traits once we acknowledge the existence of individual differences by quantifying hormonal plasticity at the individual level, where selection acts. In this review, we use glucocorticoid (GC) hormones as examples of highly plastic endocrine traits that interact intimately with energy metabolism but also with other organismal traits like behavior and physiology. First, we highlight the insights gained by repeatedly assessing an individual's GC concentrations along a gradient of environmental or internal conditions using a "reaction norm approach." This study design should be followed by a hierarchical statistical partitioning of the total endocrine variance into the among-individual component (individual differences in average hormone concentrations, i.e., in the intercept of the reaction norm) and the residual (within-individual) component. The latter is ideally further partitioned by estimating more precisely hormonal plasticity (i.e., the slope of the reaction norm), which allows to test whether individuals differ in the degree of hormonal change along the gradient. Second, we critically review the published evidence for GC variation, focusing mostly on among- and within-individual levels, finding only a good handful of studies that used repeated-measures designs and random regression statistics to investigate GC plasticity. These studies indicate that individuals can differ in both the intercept and the slope of their GC reaction norm to a known gradient. Third, we suggest rewarding avenues for future work on hormonal reaction norms, for example to uncover potential costs and trade-offs associated with GC plasticity, to test whether GC plasticity varies when an individual's reaction norm is repeatedly assessed along the same gradient, whether reaction norms in GCs covary with those in other traits like behavior and fitness (generating multivariate plasticity), or to quantify GC reaction norms along multiple external and internal gradients that act simultaneously (leading to multidimensional plasticity). Throughout this review, we emphasize the power that reaction norm approaches offer for resolving unanswered questions in ecological and evolutionary endocrinology.

Inferring Whole-Organism Metabolic Rate From Red Blood Cells in Birds.

Metabolic rate is a key ecological variable that quantifies the energy expenditure needed to fuel almost all biological processes in an organism. Metabolic rates are typically measured at the whole-organism level (woMR) with protocols that can elicit stress responses due to handling and confinement, potentially biasing resulting data. Improved, non-stressful methodology would be especially valuable for measures of field metabolic rate, which quantifies the energy expenditure of free-living individuals. Recently, techniques to measure cellular metabolic rate (cMR) in mitochondria of blood cells have become available, suggesting that blood-based cMR can be a proxy of organismal aerobic performance. Aerobic metabolism actually takes place in the mitochondria. Quantifying cMR from blood samples offers several advantages such as direct estimates of metabolism and minimized disturbance of individuals. To our knowledge, the hypothesis that blood-based cMR correlates with woMR has not yet been directly tested. We measured cMR in red blood cells of captive great tits (Parus major), first during their morning activity period and second after subjecting them to a 2.5 h day-time respirometry protocol to quantify woMR. We predicted cMR to decrease as individuals transitioned from an active to a resting state. In the two blood samples we also assessed circulating corticosterone concentrations to determine the perceived disturbance of individuals. From respirometry traces we extracted initial and final woMR measures to test for a predicted positive correlation with cMR measures, while accounting for corticosterone concentrations. Indeed, cMR declined from the first to the second measurement. Furthermore, woMR and cMR were positively related in individuals that had relatively low corticosterone concentrations and displayed little locomotor activity throughout respirometry. By contrast, woMR and cMR covaried negatively in birds that increased corticosterone concentrations and activity levels substantially. Our results show that red blood cell cMR represents a proxy for woMR when birds do not display signs of stress, i.e., either before increases in hormonal or behavioral parameters have occurred or after they have abated. This method represents a valuable tool for obtaining metabolic data repeatedly and in free-living individuals. Our findings also highlight the importance of accounting for individual stress responses when measuring metabolic rate at any level.

Natural variation in yolk fatty acids, but not androgens, predicts offspring fitness in a wild bird.

BACKGROUND: In egg-laying animals, mothers can influence the developmental environment and thus the phenotype of their offspring by secreting various substances into the egg yolk. In birds, recent studies have demonstrated that different yolk substances can interactively affect offspring phenotype, but the implications of such effects for offspring fitness and phenotype in natural populations have remained unclear. We measured natural variation in the content of 31 yolk components known to shape offspring phenotypes including steroid hormones, antioxidants and fatty acids in eggs of free-living great tits (Parus major) during two breeding seasons. We tested for relationships between yolk component groupings and offspring fitness and phenotypes. RESULTS: Variation in hatchling and fledgling numbers was primarily explained by yolk fatty acids (including saturated, mono- and polyunsaturated fatty acids) - but not by androgen hormones and carotenoids, components previously considered to be major determinants of offspring phenotype. Fatty acids were also better predictors of variation in nestling oxidative status and size than androgens and carotenoids. CONCLUSIONS: Our results suggest that fatty acids are important yolk substances that contribute to shaping offspring fitness and phenotype in free-living populations. Since polyunsaturated fatty acids cannot be produced de novo by the mother, but have to be obtained from the diet, these findings highlight potential mechanisms (e.g., weather, habitat quality, foraging ability) through which environmental variation may shape maternal effects and consequences for offspring. Our study represents an important first step towards unraveling interactive effects of multiple yolk substances on offspring fitness and phenotypes in free-living populations. It provides the basis for future experiments that will establish the pathways by which yolk components, singly and/or interactively, mediate maternal effects in natural populations.

Early nighttime testosterone peaks are correlated with GnRH-induced testosterone in a diurnal songbird.

Experimental manipulation has established testosterone as a potent, pleiotropic regulator coordinating morphology, physiology and behavior. However, the relationship of field-sampled, unmanipulated testosterone concentrations with traits of interest is often equivocal. Circulating testosterone varies over the course of the day, and recent reports indicate that testosterone is higher during the night in diurnal songbirds. Yet, most field studies sample testosterone during the morning. Sampling at times when levels and individual variation are low may be one reason relationships between testosterone and other traits are not always observed. Testosterone is regulated by the hypothalamic-pituitary-gonadal axis, with gonadotropin-releasing hormone (GnRH) initiating the endocrine cascade. Research has examined GnRH-induced testosterone levels with traits of interest, yet the relevance of these induced levels and their relationship with endogenously produced levels are not fully clear. Using photostimulated male great tits (Parus major) we tested the hypotheses that circulating testosterone levels peak during the night and that GnRH-induced testosterone concentrations are positively related to nightly testosterone peaks. Blood was sampled during first, middle or last third of night. One week later, baseline and GnRH-induced testosterone levels were sampled during mid-morning. Morning baseline testosterone levels were low compared with night-sampled levels that peaked during the first third of the night. Further, GnRH-induced testosterone was strongly positively correlated with levels observed during the first third of the night. These data suggest that morning testosterone samples likely do not reflect an individual's endogenous peak. Instead, GnRH-induced testosterone levels do approximate an individual's nightly peak and may be an alternative for birds that cannot easily be sampled at night in the field. These findings are likely to have implications for research aimed at relating traits of interest with natural variation in sex steroid hormone levels.

Life history and environment predict variation in testosterone across vertebrates.

Endocrine systems act as key intermediaries between organisms and their environments. This interaction leads to high variability in hormone levels, but we know little about the ecological factors that influence this variation within and across major vertebrate groups. We study this topic by assessing how various social and environmental dynamics influence testosterone levels across the entire vertebrate tree of life. Our analyses show that breeding season length and mating system are the strongest predictors of average testosterone concentrations, whereas breeding season length, environmental temperature, and variability in precipitation are the strongest predictors of within-population variation in testosterone. Principles from small-scale comparative studies that stress the importance of mating opportunity and competition on the evolution of species differences in testosterone levels, therefore, likely apply to the entire vertebrate lineage. Meanwhile, climatic factors associated with rainfall and ambient temperature appear to influence variability in plasma testosterone, within a given species. These results, therefore, reveal how unique suites of ecological factors differentially explain scales of variation in circulating testosterone across mammals, birds, reptiles, amphibians, and fishes.

Sex steroids modulate circadian behavioral rhythms in captive animals, but does this matter in the wild?

Nearly all organisms alter physiological and behavioral activities across the twenty-four-hour day. Endogenous timekeeping mechanisms, which are responsive to environmental and internal cues, allow organisms to anticipate predictable environmental changes and time their daily activities. Among-individual variation in the chronotype, or phenotypic output of these timekeeping mechanisms (i.e. timing of daily behaviors), is often observed in organisms studied under naturalistic environmental conditions. The neuroendocrine system, including sex steroids, has been implicated in the regulation and modulation of endogenous clocks and their behavioral outputs. Numerous studies have found clear evidence that sex steroids modulate circadian and daily timing of activities in captive animals under controlled conditions. However, little is known about how sex steroids influence daily behavioral rhythms in wild organisms or what, if any, implication this may have for survival and reproductive fitness. Here we review the evidence that sex steroids modulate daily timing in vertebrates under controlled conditions. We then discuss how this relationship may be relevant for the reproductive success and fitness of wild organisms and discuss the limited evidence that sex steroids modulate circadian rhythms in wild organisms.

Increased glucocorticoid concentrations in early life cause mitochondrial inefficiency and short telomeres.

Telomeres are DNA structures that protect chromosome ends. However, telomeres shorten during cell replication and at critically low lengths can reduce cell replicative potential, induce cell senescence and decrease fitness. Stress exposure, which elevates glucocorticoid hormone concentrations, can exacerbate telomere attrition. This phenomenon has been attributed to increased oxidative stress generated by glucocorticoids ('oxidative stress hypothesis'). We recently suggested that glucocorticoids could increase telomere attrition during stressful periods by reducing the resources available for telomere maintenance through changes in the metabolic machinery ('metabolic telomere attrition hypothesis'). Here, we tested whether experimental increases in glucocorticoid levels affected telomere length and mitochondrial function in wild great tit (Parus major) nestlings during the energy-demanding early growth period. We monitored resulting corticosterone (Cort) concentrations in plasma and red blood cells, telomere lengths and mitochondrial metabolism (metabolic rate, proton leak, oxidative phosphorylation, maximal mitochondrial capacity and mitochondrial inefficiency). We assessed oxidative damage caused by reactive oxygen species (ROS) metabolites as well as the total non-enzymatic antioxidant protection in plasma. Compared with control nestlings, Cort-nestlings had higher baseline corticosterone, shorter telomeres and higher mitochondrial metabolic rate. Importantly, Cort-nestlings showed increased mitochondrial proton leak, leading to a decreased ATP production efficiency. Treatment groups did not differ in oxidative damage or antioxidants. Hence, glucocorticoid-induced telomere attrition is associated with changes in mitochondrial metabolism, but not with ROS production. These findings support the hypothesis that shortening of telomere length during stressful periods is mediated by glucocorticoids through metabolic rearrangements.

Baseline and stress-induced corticosterone levels across birds and reptiles do not reflect urbanization levels.

Rates of human-induced environmental change continue increasing with human population size, potentially altering animal physiology and negatively affecting wildlife. Researchers often use glucocorticoid concentrations (hormones that can be associated with stressors) to gauge the impact of anthropogenic factors (e.g. urbanization, noise and light pollution). Yet, no general relationships between human-induced environmental change and glucocorticoids have emerged. Given the number of recent studies reporting baseline and stress-induced corticosterone (the primary glucocorticoid in birds and reptiles) concentrations worldwide, it is now possible to conduct large-scale comparative analyses to test for general associations between disturbance and baseline and stress-induced corticosterone across species. Additionally, we can control for factors that may influence context, such as life history stage, environmental conditions and urban adaptability of a species. Here, we take a phylogenetically informed approach and use data from HormoneBase to test if baseline and stress-induced corticosterone are valid indicators of exposure to human footprint index, human population density, anthropogenic noise and artificial light at night in birds and reptiles. Our results show a negative relationship between anthropogenic noise and baseline corticosterone for birds characterized as urban avoiders. While our results potentially indicate that urban avoiders are more sensitive to noise than other species, overall our study suggests that the relationship between human-induced environmental change and corticosterone varies across species and contexts; we found no general relationship between human impacts and baseline and stress-induced corticosterone in birds, nor baseline corticosterone in reptiles. Therefore, it should not be assumed that high or low levels of exposure to human-induced environmental change are associated with high or low corticosterone levels, respectively, or that closely related species, or even individuals, will respond similarly. Moving forward, measuring alternative physiological traits alongside reproductive success, health and survival may provide context to better understand the potential negative effects of human-induced environmental change.

Host dispersal shapes the population structure of a tick-borne bacterial pathogen.

Birds are hosts for several zoonotic pathogens. Because of their high mobility, especially of longdistance migrants, birds can disperse these pathogens, affecting their distribution and phylogeography. We focused on Borrelia burgdorferi sensu lato, which includes the causative agents of Lyme borreliosis, as an example for tick-borne pathogens, to address the role of birds as propagation hosts of zoonotic agents at a large geographical scale. We collected ticks from passerine birds in 11 European countries. B. burgdorferi s.l. prevalence in Ixodes spp. was 37% and increased with latitude. The fieldfare Turdus pilaris and the blackbird T. merula carried ticks with the highest Borrelia prevalence (92 and 58%, respectively), whereas robin Erithacus rubecula ticks were the least infected (3.8%). Borrelia garinii was the most prevalent genospecies (61%), followed by B. valaisiana (24%), B. afzelii (9%), B. turdi (5%) and B. lusitaniae (0.5%). A novel Borrelia genospecies "Candidatus Borrelia aligera" was also detected. Multilocus sequence typing (MLST) analysis of B. garinii isolates together with the global collection of B. garinii genotypes obtained from the Borrelia MLST public database revealed that: (a) there was little overlap among genotypes from different continents, (b) there was no geographical structuring within Europe, and (c) there was no evident association pattern detectable among B. garinii genotypes from ticks feeding on birds, questing ticks or human isolates. These findings strengthen the hypothesis that the population structure and evolutionary biology of tick-borne pathogens are shaped by their host associations and the movement patterns of these hosts.

Developmental conditions modulate DNA methylation at the glucocorticoid receptor gene with cascading effects on expression and corticosterone levels in zebra finches.

Developmental conditions can impact the adult phenotype via epigenetic changes that modulate gene expression. In mammals, methylation of the glucocorticoid receptor gene Nr3c1 has been implicated as mediator of long-term effects of developmental conditions, but this evidence is limited to humans and rodents, and few studies have simultaneously tested for associations between DNA methylation, gene expression and phenotype. Adverse environmental conditions during early life (large natal brood size) or adulthood (high foraging costs) exert multiple long-term phenotypic effects in zebra finches, and we here test for effects of these manipulations on DNA methylation and expression of the Nr3c1 gene in blood. Having been reared in a large brood induced higher DNA methylation of the Nr3c1 regulatory region in adulthood, and this effect persisted over years. Nr3c1 expression was negatively correlated with methylation at 2 out of 8 CpG sites, and was lower in hard foraging conditions, despite foraging conditions having no effect on Nr3c1 methylation at our target region. Nr3c1 expression also correlated with glucocorticoid traits: higher expression level was associated with lower plasma baseline corticosterone concentrations and enhanced corticosterone reactivity. Our results suggest that methylation of the Nr3c1 regulatory region can contribute to the mechanisms underlying the emergence of long-term effects of developmental conditions in birds, but in our system current adversity dominated over early life experiences with respect to receptor expression.

Macroevolutionary Patterning in Glucocorticoids Suggests Different Selective Pressures Shape Baseline and Stress-Induced Levels.

Glucocorticoid (GC) hormones are important phenotypic mediators across vertebrates, but their circulating concentrations can vary markedly. Here we investigate macroevolutionary patterning in GC levels across tetrapods by testing seven specific hypotheses about GC variation and evaluating whether the supported hypotheses reveal consistent patterns in GC evolution. If selection generally favors the "supportive" role of GCs in responding effectively to challenges, then baseline and/or stress-induced GCs may be higher in challenging contexts. Alternatively, if selection generally favors "protection" from GC-induced costs, GCs may be lower in environments where challenges are more common or severe. The predictors of baseline GCs were all consistent with supportive effects: levels were higher in smaller organisms and in those inhabiting more energetically demanding environments. During breeding, baseline GCs were also higher in populations and species with fewer lifetime opportunities to reproduce. The predictors of stress-induced GCs were instead more consistent with the protection hypothesis: during breeding, levels were lower in organisms with fewer lifetime reproductive opportunities. Overall, these patterns indicate a surprising degree of consistency in how some selective pressures shape GCs across broad taxonomic scales; at the same time, in challenging environments selection appears to operate on baseline and stress-induced GCs in distinct ways.

Telomere attrition: metabolic regulation and signalling function?

Stress exposure can leave long-term footprints within the organism, like in telomeres (TLs), protective chromosome caps that shorten during cell replication and following exposure to stressors. Short TLs are considered to indicate lower fitness prospects, but why TLs shorten under stressful conditions is not understood. Glucocorticoid hormones (GCs) increase upon stress exposure and are thought to promote TL shortening by increasing oxidative damage. However, evidence that GCs are pro-oxidants and oxidative stress is causally linked to TL attrition is mixed . Based on new biochemical findings, we propose the metabolic telomere attrition hypothesis: during times of substantially increased energy demands, TLs are shortened as part of the transition into an organismal 'emergency state', which prioritizes immediate survival functions over processes with longer-term benefits. TL attrition during energy shortages could serve multiple roles including amplified signalling of cellular energy debt to re-direct critical resources to immediately important processes. This new view of TL shortening as a strategy to resolve major energetic trade-offs can improve our understanding of TL dynamics. We suggest that TLs are master regulators of cell homeostasis and propose future research avenues to understand the interactions between energy homeostasis, metabolic regulators and TL.

Enzymatic antioxidants but not baseline glucocorticoids mediate the reproduction-survival trade-off in a wild bird.

The trade-off between reproductive investment and survival is central to life-history theory, but the relative importance and the complex interactions among the physiological mechanisms mediating it are still debated. Here we experimentally tested whether baseline glucocorticoid hormones, the redox system or their interaction mediate reproductive investment-survival trade-offs in wild great tits (Parus major). We increased the workload of parental males by clipping three feathers on each wing, and 5 days later determined effects on baseline corticosterone concentrations (Cort), redox state (reactive oxygen metabolites, protein carbonyls, glutathione peroxidase [GPx], total non-enzymatic antioxidants), body mass, body condition, reproductive success and survival. Feather-clipping did not affect fledgling numbers, chick body condition, nest provisioning rates or survival compared with controls. However, feather-clipped males lost mass and increased both Cort and GPx concentrations. Within feather-clipped individuals, GPx increases were positively associated with reproductive investment (i.e. male nest provisioning). Furthermore, within all individuals, males that increased GPx suffered reduced survival rates. Baseline Cort increases were related to mass loss but not to redox state, nest provisioning or male survival. Our findings provide experimental evidence that changes in the redox system are associated with the trade-off between reproductive investment and survival, while baseline Cort may support this trade-off indirectly through a link with body condition. These results also emphasize that plastic changes in individuals, rather than static levels of physiological signals, may mediate life-history trade-offs.

Glucocorticoid-temperature association is shaped by foraging costs in individual zebra finches.

Glucocorticoid (GC) levels vary with environmental conditions, but the functional interpretation of GC variation remains contentious. A primary function is thought to be metabolic, mobilizing body reserves to match energetic demands. This view is supported by temperature-dependent GC levels, although reports of this effect show unexplained heterogeneity. We hypothesized that the temperature effect on GC concentrations will depend on food availability through its effect on the energy spent to gather the food needed for thermoregulation. We tested this hypothesis in zebra finches living in outdoor aviaries with manipulated foraging conditions (i.e. easy versus hard), by relating within-individual differences in baseline GCs between consecutive years to differences in ambient temperature. In agreement with our hypothesis, we found the GC-temperature association to be significantly steeper in the hard foraging environment. This supports the metabolic explanation of GC variation, underlining the importance of accounting for variation in energy expenditure when interpreting GC variation.