Controlled expression of avian pre-migratory fattening influences indices of innate immunity.

While immunity is frequently dampened when birds engage in strenuous migratory flights, whether and how immunity changes during the rapid accumulation of energy stores in preparation for migration remains largely unknown. Here we induced pre-migratory fattening through controlled changes of daylight in common quails (Coturnix coturnix) and regularly assessed changes in three markers of constitutive innate immunity (leukocyte coping capacity or LCC, hemagglutination and hemolysis titres) and measures of body composition (lean and fat mass). All the three markers showed similar changes over the pre-migratory fattening process. LCC responses, hemagglutination titres, and hemolysis titres, were on average higher in the mid-fattening phase compared to the peak-fattening phase, when values were similar to those observed prior the start of pre-migratory fattening. At mid-fattening, we found that the birds that showed a larger accumulation of fat mass (as % of body mass) had lower LCC peak responses and hemolysis titres. Reversibly, at mid-fattening, we also found that the birds that kept a higher proportion of lean mass (as % of body mass) had the highest LCC peaks. Our results indicate that migratory birds undergo changes in immune indices (over 8 weeks) as they accumulate energy stores for migration and propose that this could be due to competing or trade-off processes between metabolic remodelling and innate immune system function.

How does early-life adversity shape telomere dynamics during adulthood? Problems and paradigms.

Although early-life adversity has been associated with negative consequences during adulthood, growing evidence shows that such adversity can also lead to subsequent stress resilience and positive fitness outcomes. Telomere dynamics are relevant in this context because of the link with developmental conditions and longevity. However, few studies have assessed whether the effects of early-life adversity on developmental telomere dynamics may relate to adult telomere dynamics. We propose that the potential links between early-life adversity and adult telomere dynamics could be driven by developmental constraints (the Constraint hypothesis), by the nature/severity of developmental adversity (the Resilience hypothesis), or by developmental-mediated changes in individual life-history strategies (the Pace of Life hypothesis). We discuss these non-mutually exclusive hypotheses, explore future research directions, and propose specific studies to test these hypotheses. Our article aims to expand our understanding of the evolutionary role of developmental conditions on adult telomere dynamics, stress resilience and ageing.

Ghrelin, not corticosterone, is associated with transitioning of phenotypic states in a migratory Galliform.

In both captive and free-living birds, the emergence of the migratory phenotype is signalled by rapid and marked increases in food intake and fuelling, as well as changes in amount of nocturnality or migratory restlessness. The metabolic hormone corticosterone and, as more recently suggested, the gut-derived hormone ghrelin have been suggested to play a role in mediating such phenomenal phenotypic flexibility given that they both regulate fuel metabolism and locomotion across vertebrate taxa. Here, using the Common quail (Coturnix coturnix) as our study species, we induced autumn migration followed by a non-migratory wintering phase through controlled changes in daylight. We thus compared plasma corticosterone and ghrelin concentrations between the two sampling phases and assessed whether these hormones might reflect the migratory state. While we found no differences in plasma corticosterone between the two sampling phases and no link of this hormone with changes in body mass, levels of food intake or migratory restlessness, the migratory birds had substantially higher levels of plasma ghrelin relative to the non-migratory birds. Furthermore, while ghrelin did not correlate with the gain in body mass over the entire pre-migratory fuelling phase (over an average of nine weeks preceding blood sampling), plasma ghrelin did positively correlate with the gain in body mass observed during the final fattening stages (over an average of three weeks preceding blood sampling). Again, variation in plasma ghrelin also reflected the amount of body mass depleted over both the long- and short-time frame as birds returned to their non-migratory baseline - lower levels of plasma ghrelin consistently correlated with larger losses in body mass. Thus, while our data do not highlight a role of the hormone corticosterone in sustaining pre-migratory fattening as shown in other bird species, they do add evidence for a potential role of ghrelin in mediating migratory behaviour and further suggest that this hormone might be important in regulating the transitioning of migratory states, possibly by promoting fuel mobilisation and usage.

Repeated exposure to challenging environmental conditions influences telomere dynamics across adult life as predicted by changes in mortality risk.

The effects of stress exposure are likely to vary depending on life-stage and stressor. While it has been postulated that mild stress exposure may have beneficial effects, the duration of such effects and the underlying mechanisms are unclear. While the long-term effects of early-life stress are relatively well studied, we know much less about the effects of exposure in adulthood since the early- and adult-life environments are often similar. We previously reported that repeated experimental exposure to a relatively mild stressor in female zebra finches, first experienced in young adulthood, initially had no effect on mortality risk, reduced mortality in middle age, but the apparently beneficial effects disappeared in old age. We show here that this is underpinned by differences between the control and stress-exposed group in the pattern of telomere change, with stress-exposed birds showing reduced telomere loss in middle adulthood. We thereby provide novel experimental evidence that telomere dynamics play a key role linking stress resilience and aging.

Controlled expression of the migratory phenotype affects oxidative status in birds.

High caloric intake can increase production of reactive oxygen and nitrogen species. We examined whether the emergence of the migratory phenotype, primarily signalled by increased food intake and fuelling, is accompanied by changes in oxidative status. We induced autumn migration followed by a non-migratory wintering phase in common quails (Coturnix coturnix). We compared three markers of oxidative status - oxidative damage to lipids expressed as thiobarbituric acid reactive substances (TBARS); superoxide dismutase (SOD); and glutathione peroxidase (GPx) - between birds sampled during the migratory and non-migratory phase. We found that the emergence of the migratory phenotype was associated with: (i) higher levels of TBARS in the liver; (ii) lower levels of SOD in red blood cells and, marginally, in the liver; (iii) higher levels of GPx in the pectoral muscle; and (iv) sex-specific changes in red blood cells and liver. We found no link between food intake and variation in markers of oxidative status in any of the tissues examined, despite food intake being higher in the migratory birds. However, the increase in body mass was positively correlated with muscle GPx activity as birds entered the pre-migratory fattening phase, while the amount of decrease in body mass was negatively correlated with muscle GPx as birds transitioned to the non-migratory phase. Such correlations were absent in red blood cells and liver. Our work suggests that during the emergence of the migratory phenotype, birds might strategically displace oxidative costs on the liver in order to safeguard the pectoral muscles, which have a fundamental role in successfully completing the migratory flight.

Data on the de novo transcriptome assembly for the migratory bird, the Common quail (Coturnix coturnix).

The Common or European quail (Coturnix coturnix) is a Galliform bird of ecological importance for research in the field of animal migration. The Common quail is also a game bird, thus, of great interest for recreational activities and conservation management. Here, we generated a high quality de novo transcriptome for the Common quail for which no reference genome is to date publicly available. The transcriptome was obtained from a population of Common quail originated from captive founders raised under laboratory conditions. Paired-end RNA-Sequencing reads were obtained from extracted total RNA of brain tissue punches (preoptic-hypothalamic region) of 23 quails, which yielded to 5.5-11.2 million reads per individual bird for a total of 236 million reads. After assembly optimization, we used a stringent filtering analysis pipeline to remove redundant and low confidence transcripts. The final transcriptome consisted of 22,293 transcripts of which 21,551 (97%) were provided with annotation data. Our data offers a high quality pipeline for compiling transcriptomes of complex non-genomic species. Our data also provide a robust reference for gene expression studies in this species or other related Galliform species, including the Japanese quail.

Intergenerational effects on offspring telomere length: interactions among maternal age, stress exposure and offspring sex.

Offspring produced by older parents often have reduced longevity, termed the Lansing effect. Because adults usually have similar-aged mates, it is difficult to separate effects of maternal and paternal age, and environmental circumstances are also likely to influence offspring outcomes. The mechanisms underlying the Lansing effect are poorly understood. Variation in telomere length and loss, particularly in early life, is linked to longevity in many vertebrates, and therefore changes in offspring telomere dynamics could be very important in this context. We examined the effect of maternal age and environment on offspring telomere length in zebra finches. We kept mothers under either control (ad libitum food) or more challenging (unpredictable food) circumstances and experimentally minimized paternal age and mate choice effects. Irrespective of the maternal environment, there was a substantial negative effect of maternal age on offspring telomere length, evident in longitudinal and cross-sectional comparisons (average of 39% shorter). Furthermore, in young mothers, sons reared by challenged mothers had significantly shorter telomere lengths than sons reared by control mothers. This effect disappeared when the mothers were old, and was absent in daughters. These findings highlight the importance of telomere dynamics as inter-generational mediators of the evolutionary processes determining optimal age-specific reproductive effort and sex allocation.

Leukocyte Coping Capacity: An Integrative Parameter for Wildlife Welfare Within Conservation Interventions.

Wildlife management, conservation interventions and wildlife research programs often involve capture, manipulation and transport of wild animals. Widespread empirical evidence across various vertebrate taxa shows that handling wildlife generally induces a severe stress response resulting in increased stress levels. The inability of individuals to appropriately respond to rapidly changing environmental conditions during and after manipulations may have deleterious and long-lasting implications on animal welfare. Therefore, mitigating stress responses in the frame of conservation interventions is a key animal welfare factor. However, we have a poor understanding of the metrics to adequately assess and monitor the dynamic physiological changes that animals undergo when subjected to stressful procedures in wild or captive conditions. A growing number of studies provide good evidence for reciprocal interactions between immune processes and stress. Here, we review the existing literature on a relatively new technique-Leukocyte Coping Capacity (LCC), a proxy for stress quantifying oxygen radical production by leukocytes. We discuss the strength and weaknesses of this immunological approach to evaluate stress, the individual capacity to cope with stress and the resulting potential implications for animal welfare. Additionally we present new data on LCC in captive roe deer (Capreolus capreolus) under long-time anesthesia and free-ranging Asiatic wild asses (Kulan; Equus hemionus kulan) were LCC was used to assess stress levels in animals captured for a reintroduction project.

Environmental conditions shape the temporal pattern of investment in reproduction and survival.

The relationship between environmental stress exposure and ageing is likely to vary with stressor severity, life-history stage and the time scale over which effects are measured. Such factors could influence whether stress exposure accelerates or slows the ageing process, but their interactions have not previously been experimentally investigated. We found that experimental exposure of zebra finches to mildly challenging environmental circumstances from young to old adulthood, which increased exposure to stress hormones, reduced breeding performance during early adulthood, but had positive effects when individuals were bred in old adulthood. This difference was not due to selective mortality, because the effects were evident within individuals, and no evidence of habituation in the response to the stressor was found. The more stressful environment had no effects on survival during young or old adulthood, but substantially improved survival during middle age. Changes in the effects at different ages could be due to the duration and nature of the challenging exposure, or to variation in coping capacity or strategy with age. These results show that living under challenging environmental circumstances can influence ageing trajectories in terms of both reproductive performance and longevity. Our results provide experimental support for the emerging idea that stress exposure needs to be optimized rather than minimized to obtain the best health outcomes.

Environmental conditions can modulate the links among oxidative stress, age, and longevity.

Understanding the links between environmental conditions and longevity remains a major focus in biological research. We examined within-individual changes between early- and mid-adulthood in the circulating levels of four oxidative stress markers linked to ageing, using zebra finches (Taeniopygia guttata): a DNA damage product (8-hydroxy-2'-deoxyguanosine; 8-OHdG), protein carbonyls (PC), non-enzymatic antioxidant capacity (OXY), and superoxide dismutase activity (SOD). We further examined whether such within-individual changes differed among birds living under control (ad lib food) or more challenging environmental conditions (unpredictable food availability), having previously found that the latter increased corticosterone levels when food was absent but improved survival over a three year period. Our key findings were: (i) 8-OHdG and PC increased with age in both environments, with a higher increase in 8-OHdG in the challenging environment; (ii) SOD increased with age in the controls but not in the challenged birds, while the opposite was true for OXY; (iii) control birds with high levels of 8-OHdG died at a younger age, but this was not the case in challenged birds. Our data clearly show that while exposure to the potentially damaging effects of oxidative stress increases with age, environmental conditions can modulate the pace of this age-related change.

Repeated exposure to stressful conditions can have beneficial effects on survival.

Repeated exposure to stressful circumstances is generally thought to be associated with increased pathology and reduced longevity. However, growing lines of evidence suggest that the effects of environmental stressors on survival and longevity depend on a multitude of factors and, under some circumstances, might be positive rather than negative. Here, using the zebra finch (Taeniopygia guttata), we show that repeated exposure to stressful conditions (i.e. unpredictable food availability), which induced no changes in body mass, was associated with a decrease in mortality rate and an increase in the age of death. As expected, the treated birds responded to the unpredictable food supply by increasing baseline glucocorticoid stress hormone secretion and there were no signs of habituation of this hormonal response to the treatment across time. Importantly, and consistent with previous literature, the magnitude of hormone increase induced by the treatment was significant, but relatively mild, since the baseline glucocorticoid concentrations in the treated birds were substantially lower than the peak levels that occur during an acute stress response in this species. Taken together, these data demonstrate that protracted exposure to relatively mild stressful circumstances can have beneficial lifespan effects.

Developmental post-natal stress can alter the effects of pre-natal stress on the adult redox balance.

Across diverse vertebrate taxa, stressful environmental conditions during development can shape phenotypic trajectories of developing individuals, which, while adaptive in the short-term, may impair health and survival in adulthood. Regardless, the long-lasting benefits or costs of early life stress are likely to depend on the conditions experienced across differing stages of development. Here, we used the Japanese quail (Coturnix coturnix japonica) to experimentally manipulate exposure to stress hormones in developing individuals. We tested the hypothesis that interactions occurring between pre- and post-natal developmental periods can induce long-term shifts on the adult oxidant phenotype in non-breeding sexually mature individuals. We showed that early life stress can induce long-term alterations in the basal antioxidant defences. The magnitude of these effects depended upon the timing of glucocorticoid exposure and upon interactions between the pre- and post-natal stressful stimuli. We also found differences among tissues with stronger effects in the erythrocytes than in the brain in which the long-term effects of glucocorticoids on antioxidant biomarkers appeared to be region-specific. Recent experimental work has demonstrated that early life exposure to stress hormones can markedly reduce adult survival (Monaghan et al., 2012). Our results suggest that long-term shifts in basal antioxidant defences might be one of the potential mechanisms driving such accelerated ageing processes and that post-natal interventions during development may be a potential tool to shape the effects induced by pre-natally glucococorticoid-exposed phenotypes.

Pre- and post-natal stress in context: effects on the stress physiology in a precocial bird.

Developmental stress can significantly influence physiology and survival in many species. Mammalian studies suggest that pre- and post-natal stress can have different effects (i.e. hyper- or hypo-responsiveness) on the hypothalamic-pituitary-adrenal (HPA) axis, the main mediator of the stress response. In mammals, the physiological intimacy between mother and offspring constrains the possibility to control, and therefore manipulate, maternal pre- and post-natal influences. Here, using the Japanese quail (Coturnix coturnix japonica) as our model, we elevated levels of the glucocorticoid stress hormone corticosterone in ovo and/or in the endogenous circulation of hatchlings. We examined the effects of treatments on corticosterone and glucose stress responses at two different ages, in juvenile and adult quail. In juveniles, corticosterone data revealed a sex-specific effect of post-natal treatment regardless of the previous pre-natal protocol, with post-natally treated females showing shorter stress responses in comparison with the other groups, while no differences were observed among males. In adulthood, birds previously stressed as embryos showed higher corticosterone concentrations over the stress response compared with controls. This effect was not evident in birds subjected to either post-natal treatment or the combined treatments. There were no effects on glucose in the juveniles. However, adult birds previously stressed in ovo showed opposite sex-specific basal glucose patterns compared with the other groups. Our results demonstrate that (1) early glucocorticoid exposure can have both transient and long-term effects on the HPA axis, depending upon the developmental stage and sex and (2) post-natal stress can modulate the effects of pre-natal stress on HPA activity.

Non-migratory stonechats show seasonal changes in the hormonal regulation of non-seasonal territorial aggression.

In many birds and mammals, male territorial aggression is modulated by elevated circulating concentrations of the steroid hormone testosterone (T) during the breeding season. However, many species are territorial also during the non-breeding season, when plasma T levels are basal. The endocrine control of non-breeding territorial aggression differs considerably between species, and previous studies on wintering birds suggest differences between migratory and resident species. We investigated the endocrine modulation of territorial aggression during the breeding and non-breeding season in a resident population of European stonechats (Saxicola torquata rubicola). We recorded the aggressive response to a simulated territorial intrusion in spring and winter. Then, we compared the territorial aggression between seasons and in an experiment in which we blocked the androgenic and estrogenic action of T. We found no difference in the aggressive response between the breeding and the non-breeding season. However, similarly to what is found in migratory stonechats, the hormonal treatment decreased aggressive behaviors in resident males in the breeding season, whereas no effects were recorded in the non-breeding season. When we compared the aggressive responses of untreated birds with those obtained from migratory populations in a previous study, we found that territorial aggression of resident males was lower than that of migratory males during the breeding season. Our results show that in a resident population of stonechats T and/or its metabolites control territorial aggression in the breeding but not in the non-breeding season. In addition, our study supports the hypothesis that migratory status does modulate the intensity of aggressive behavior.

A meta-analysis of glucocorticoids as modulators of oxidative stress in vertebrates.

Prolonged high secretion of glucocorticoids normally reflects a state of chronic stress, which has been associated with an increase in disease susceptibility and reduction in Darwinian fitness. Here, we hypothesize that an increase in oxidative stress accounts for the detrimental effects of prolonged high secretion of glucocorticoids. We performed a meta-analysis on studies where physiological stress was induced by administration of glucocorticoids to evaluate the magnitude of their effects on oxidative stress. Glucocorticoids have a significant effect on oxidative stress (Pearson r = 0.552), although this effect depends on the duration of treatment, and is larger in long-term experiments. Importantly, there was a significant effect on tissue, with brain and heart being the most and the least susceptible to GC-induced oxidative stress, respectively. Furthermore, effect size was larger (1) in studies using both sexes compared to males only, (2) when corticosterone rather than dexamethasone was administered and (3) in juveniles than in adults. These effects were not confounded by species, biochemical biomarker, or whether wild or laboratory animals were studied. In conclusion, our meta-analysis suggests that GC-induced oxidative stress could be a further mechanism underlying increases in disease susceptibility and decreases in Darwinian fitness observed under chronic stress.