Leach's storm-petrel (Hydrobates leucorhous), a long-lived seabird shows flexible, condition-dependent, feeding strategies in response to poor chick condition.

BACKGROUND: Parent-offspring conflict represents the sensitive balance of resource allocation between self-maintenance and reproduction. Two strategies have been proposed to better understand how species manage this conflict. In fixed-level feeding behavior, parents feed offspring consistent quantities of food; while flexible feeding shows plasticity in parental allocation based on offspring need. Life-history theory predicts that parents of long-lived species prioritize their survival and may favor the fixed-level hypothesis to maximize lifetime reproductive success. In this study, we highlight the natural variation of parent-offspring allocation strategies within a unique population of Leach's storm-petrels (Hydrobates leucorhous), and through month-long food supplementation and restriction manipulations, we investigate how chick condition affects parental provisioning during the chick-rearing period of reproduction. RESULTS: We show that the parents upregulated chick feeding frequency of nutritionally deprived chicks, resulting in a larger total amount of food delivered during the study period. Additionally, the proportion of nights when both parents fed was highest in restricted chicks, and the proportion of nights when neither parents fed was lowest in restricted chicks, suggesting that storm-petrel parents shorten their foraging bouts to deliver food more often when their chicks are in relatively poor condition. CONCLUSIONS: Our results support that Leach's storm-petrels use a flexible-level feeding strategy, suggesting that parents can assess offspring condition, and respond by feeding chicks at higher frequencies. These data provide insight on how a long-lived seabird balances its own energetic demands with that of their offspring during the reproductive period.

Birds of a feather age together: telomere dynamics and social behavior predict life span in female Japanese quail (Coturnix japonica).

Social support is vital for mental and physical health and is linked to lower rates of disease and early mortality. Conversely, anti-social behavior can increase mortality risks, both for the initiator and target of the behavior. Chronic stress, which also can increase mortality, may serve as an important link between social behavior and healthy lifespan. There is a growing body of literature in both humans, and model organisms, that chronic social stress can result in more rapid telomere shortening, a measure of biological aging. Here we examine the role of anti-social behavior and social support on physiological markers of stress and aging in the social Japanese quail, Coturnix Japonica. Birds were maintained in groups for their entire lifespan, and longitudinal measures of antisocial behavior (aggressive agonistic behavior), social support (affiliative behavior), baseline corticosterone, change in telomere length, and lifespan were measured. We found quail in affiliative relationships both committed less and were the targets of less aggression compared to birds who were not in these relationships. In addition, birds displaying affiliative behavior had longer telomeres, and longer lifespans. Our work suggests a novel pathway by which social support may buffer against damage at the cellular level resulting in telomere protection and subsequent longer lifespans.

The association between age and telomere length is age-dependent: Evidence for a threshold model of telomere length maintenance.

Telomere length and dynamics are commonly used biomarkers of somatic state, yet the role of telomeres underlying the aging process is still debated. Indeed, to date, empirical evidence for an association between age and telomere length is mixed. Here, we test if the age-dependency of the association between age and telomere length can provide a potential explanation for the reported inconsistencies across studies. To this end, we quantified telomere length by telomere restriction fragment analysis in two groups of Japanese quail (Coturnix japonica) that differed in their age distribution. One group consisted of young adults only, whereas the second group consisted of adults across a wide range of ages. In the young adults group, there was a highly significant negative association between telomere length and age, whereas no association between age and telomere length was found in the all-ages adults group. This difference between groups was not due to telomere length-dependent selective disappearance. Our results shows that the association between telomere length and age is age-dependent and suggest that the costs and benefits associated with telomere maintenance are dynamic across an individual's life course.

Oxytocin prevents dysregulation of the acute stress response and glucocorticoid-induced oxidative stress in chronically isolated prairie voles.

Chronic social isolation can lead to dysregulation of many physiological and psychological processes, including the ability to respond to acute stressors. Previous work in our lab reported that six weeks of social isolation in prairie voles (Microtus ochrogaster) caused increased glucocorticoid levels, oxidative damage, telomere degradation and anhedonia, and that oxytocin treatment prevented all of these changes. Following these results, we investigated how chronic social isolation with and without oxytocin treatment affected glucocorticoid (CORT) and oxidative stress responses to an acute stressor, a 5-min resident-intruder (R-I) test at the end of the social isolation period. To investigate the effect of a brief acute stressor on CORT and oxidative stress, baseline blood samples were collected following six weeks of social isolation, 24-hrs before the R-I test. Two more blood samples were collected 15-min after the end of the R-I test, and again 25-min later to measure peak and recovery responses, respectively. Isolated animals had higher baseline, peak, recovery, and integrated levels of CORT and reactive oxygen metabolites (ROMs, a measure of oxidative stress), compared to animals that did not experience isolation. Importantly, oxytocin treatment throughout the isolation period prevented these elevations in CORT and ROMs. No significant changes were observed in total antioxidant capacity (TAC). Levels of CORT and ROMs at the peak and recovery time points were positively correlated. These data show that acute stress in chronically isolated prairie voles, then, is associated with increased glucocorticoid-induced oxidative stress (GiOS), and that oxytocin mitigates isolation-induced dysregulation of glucocorticoid and oxidative stress acute stress responses.

The response to stressors in adulthood depends on the interaction between prenatal exposure to glucocorticoids and environmental context.

Maternal stress during reproduction can influence how offspring respond to stress later in life. Greater lifetime exposure to glucocorticoid hormones released during stress is linked to greater risks of behavioral disorders, disease susceptibility, and mortality. The immense variation in individual's stress responses is explained, in part, by prenatal glucocorticoid exposure. To explore the long-term effects of embryonic glucocorticoid exposure, we injected Japanese quail (Coturnix japonica) eggs with corticosterone. We characterized the endocrine stress response in offspring and measured experienced aggression at three different ages. We found that prenatal glucocorticoid exposure affected (1) the speed at which the stress response was terminated suggesting dysregulated negative feedback, (2) baseline corticosterone levels in a manner dependent on current environmental conditions with higher levels of experienced aggression associated with higher levels of baseline corticosterone, (3) the magnitude of an acute stress response based on baseline concentrations. We finish by proposing a framework that can be used to test these findings in future work. Overall, our findings suggest that the potential adaptive nature of prenatal glucocorticoid exposure is likely dependent on environmental context and may also be tempered by the negative effects of longer exposure to glucocorticoids each time an animal faces a stressor.

Reproductive Strategies Affect Telomere Dynamics across the Life Course.

AbstractBecause parental care has a heritable basis, the benefits of receiving increased parental provisioning early in life are genetically linked to the costs of providing increased parental provisioning at adulthood. Reproductive strategies thus result in distinct cost-benefit syndromes across the life course that may shape individual health and aging trajectories. Here we used an artificial selection approach in Japanese quail (Coturnix japonica) to test how reproductive strategies affect telomere length, a biomarker of somatic state, at different life stages. We show that males but not females from lines selected for low maternal investment (i.e., developing in a relatively small egg) had shorter telomeres at birth. These patterns were still weakly present at the end of the juvenile growth period. In contrast, significantly shorter telomeres were found in reproductively active adult birds from the high-investment lines, suggesting that telomere attrition was accelerated in these individuals once they had become reproductively active. Our study shows that reproductive strategies differentially affect telomere dynamics across the life course, highlighting the role of cross-generational constraints in shaping individual aging trajectories.

Maternal glucocorticoids promote offspring growth without inducing oxidative stress or shortening telomeres in wild red squirrels.

Elevations in glucocorticoid (GC) levels in breeding females may induce adaptive shifts in offspring life histories. Offspring produced by mothers with elevated GCs may be better prepared to face harsh environments, where a faster pace of life is beneficial. We examined how experimentally elevated GCs in pregnant or lactating North American red squirrels (Tamiasciurus hudsonicus) affected offspring postnatal growth, structural size and oxidative stress levels (two antioxidants and oxidative protein damage) in three different tissues (blood, heart and liver) and liver telomere lengths. We predicted that offspring from mothers treated with GCs would grow faster but would also have higher levels of oxidative stress and shorter telomeres, which may predict reduced longevity. Offspring from mothers treated with GCs during pregnancy were 8.3% lighter around birth but grew (in body mass) 17.0% faster than those from controls, whereas offspring from mothers treated with GCs during lactation grew 34.8% slower than those from controls and did not differ in body mass around birth. Treating mothers with GCs during pregnancy or lactation did not alter the oxidative stress levels or telomere lengths of their offspring. Fast-growing offspring from any of the treatment groups did not have higher oxidative stress levels or shorter telomere lengths, indicating that offspring that grew faster early in life did not exhibit oxidative costs after this period of growth. Our results indicate that elevations in maternal GCs may induce plasticity in offspring growth without long-term oxidative costs to the offspring that might result in a shortened lifespan.

Is there an oxidative cost of acute stress? Characterization, implication of glucocorticoids and modulation by prior stress experience.

Acute rises in glucocorticoid hormones allow individuals to adaptively respond to environmental challenges but may also have negative consequences, including oxidative stress. While the effects of chronic glucocorticoid exposure on oxidative stress have been well characterized, those of acute stress or glucocorticoid exposure have mostly been overlooked. We examined the relationship between acute stress exposure, glucocorticoids and oxidative stress in Japanese quail (Coturnix japonica). We (i) characterized the pattern of oxidative stress during an acute stressor in two phenotypically distinct breeds; (ii) determined whether corticosterone ingestion, in the absence of acute stress, increased oxidative stress, which we call glucocorticoid-induced oxidative stress (GiOS); and (iii) explored how prior experience to stressful events affected GiOS. Both breeds exhibited an increase in oxidative stress in response to an acute stressor. Importantly, in the absence of acute stress, ingesting corticosterone caused an acute rise in plasma corticosterone and oxidative stress. Lastly, birds exposed to no previous acute stress or numerous stressful events had high levels of GiOS in response to acute stress, while birds with moderate prior exposure did not. Together, these findings suggest that an acute stress response results in GiOS, but prior experience to stressors may modulate that oxidative cost.

The environmental and genetic determinants of chick telomere length in Tree Swallows (Tachycineta bicolor).

Conditions during early life can have dramatic effects on adult characteristics and fitness. However, we still know little about the mechanisms that mediate these relationships. Telomere shortening is one possibility. Telomeres are long sequences of DNA that protect the ends of chromosomes. They shorten naturally throughout an individual's life, and individuals with short telomeres tend to have poorer health and reduced survival. Given this connection between telomere length (TL) and fitness, natural selection should favor individuals that are able to retain longer telomeres for a greater portion of their lives. However, the ability of natural selection to act on TL depends on the extent to which genetic and environmental factors influence TL. In this study, we experimentally enlarged broods of Tree Swallows (Tachycineta bicolor) to test the effects of demanding early-life conditions on TL, while simultaneously cross-fostering chicks to estimate heritable genetic influences on TL. In addition, we estimated the effects of parental age and chick sex on chick TL. We found that TL is highly heritable in Tree Swallow chicks, and that the maternal genetic basis for TL is stronger than is the paternal genetic basis. In contrast, the experimental manipulation of brood size had only a weak effect on chick TL, suggesting that the role of environmental factors in influencing TL early in life is limited. There was no effect of chick sex or parental age on chick TL. While these results are consistent with those reported in some studies, they are in conflict with others. These disparate conclusions might be attributable to the inherent complexity of telomere dynamics playing out differently in different populations or to study-specific variation in the age at which subjects were measured.

Exogenous glucocorticoids amplify the costs of infection by reducing resistance and tolerance, but effects are mitigated by co-infection.

Individual variation in parasite defences, such as resistance and tolerance, can underlie heterogeneity in fitness and could influence disease transmission dynamics. Glucocorticoid hormone concentrations often change in response to fluctuating environmental conditions and mediate changes in immune function, resource allocation and tissue repair. Thus, changes in glucocorticoid hormone concentrations might mediate individual variation in investment in resistance versus tolerance. In this study, we experimentally increased glucocorticoid concentrations in red-winged blackbirds ( Agelaius phoeniceus) that were naturally infected with haemosporidian parasites, and assessed changes in resistance and tolerance of infection. Glucocorticoid treatment increased burdens of Plasmodium, the parasite causing avian malaria, but only in the absence of co-infection with another Haemosporidian, Haemoproteus. Thus, glucocorticoids might reduce resistance to infection, but co-infection can mitigate the negative consequences of increased hormone concentrations. Glucocorticoid treatment also decreased tolerance of infection. We found no evidence that the inflammatory immune response or rate of red blood cell production underlie the effects of glucocorticoids on resistance and tolerance. Our findings suggest that exogenous glucocorticoids can increase the costs of haemosporidian infections by both increasing parasite numbers and reducing an individual's ability to cope with infection. These effects could scale up to impact populations of both host and parasite.

Brief Increases in Corticosterone Affect Morphology, Stress Responses, and Telomere Length but Not Postfledging Movements in a Wild Songbird.

Organisms are frequently exposed to challenges during development, such as poor weather and food shortage. Such challenges can initiate the hormonal stress response, which involves secretion of glucocorticoids. Although the hormonal stress response helps organisms deal with challenges, long-term exposure to high levels of glucocorticoids can have morphological, behavioral, and physiological consequences, especially during development. Glucocorticoids are also associated with telomere shortening, and they have a complex relationship with survival. To investigate whether brief, acute exposures to glucocorticoids can also produce these phenotypic effects in free-living birds, we exposed wild tree swallow (Tachycineta bicolor) nestlings to a brief exogenous dose of corticosterone once per day for 5 d and then measured their morphology, baseline and stress-induced corticosterone levels, and telomere length. We also deployed radio tags on a subset of nestlings, which allowed us to determine the age at which tagged nestlings left the nest (fledged) and their pattern of presence and absence at the natal site during the postbreeding period. Corticosterone-treated nestlings had lower mass, higher baseline and stress-induced corticosterone, and reduced telomeres; other metrics of morphology were affected weakly or not at all. Our treatment resulted in no significant effect on survival to fledging, fledge age, or age at first departure from the natal site, and we found no negative effect of corticosterone on interannual return rate. These results show that brief acute corticosterone exposure during development can have measurable effects on phenotype in free-living tree swallows. Corticosterone may therefore mediate correlations between rearing environment and phenotype in developing organisms, even in the absence of prolonged stressors.

Traffic noise exposure alters nestling physiology and telomere attrition through direct, but not maternal, effects in a free-living bird.

Anthropogenic impacts, such as noise pollution from transportation networks, can serve as stressors to some wildlife species. For example, increased exposure to traffic noise has been found to alter baseline and stress-induced corticosterone levels, reduce body condition and reproductive success, and increase telomere attrition in free-living birds. However, it remains unknown if alterations in nestling phenotype are due to direct or indirect effects of noise exposure. For example, indirect (maternal) effects of noise may occur if altered baseline and stress-induced corticosterone in mothers results in differential deposition of yolk steroids or other components in eggs. Noise exposure may also alter nestling corticosterone levels directly, given that nestlings cannot escape the nest during development. Here, we examined maternal versus direct effects of traffic noise exposure on baseline and stress-induced corticosterone levels, and body condition (as measured by size-corrected mass) in nestling tree swallows (Tachycineta bicolor). We used a two-way factorial design and partially cross-fostered eggs between nests exposed to differing levels (i.e. amplitudes) of traffic noise. For nestlings that were not cross-fostered, we also investigated the effects of traffic noise on telomere dynamics. Our results show a positive relationship between nestling baseline and stress-induced corticosterone and nestling noise exposure, but not maternal noise exposure. While we did not find a relationship between noise and body condition in nestlings, nestling baseline corticosterone was negatively associated with body condition. We also found greater telomere attrition for nestlings from nests with greater traffic noise amplitudes. These results suggest that direct, rather than maternal, effects result in potentially long-lasting consequences of noise exposure. Reduced nestling body condition and increased telomere attrition have been shown to reduce post-fledging survival in this species. Given that human transportation networks continue to expand, strategies to mitigate noise exposure on wildlife during critical periods (i.e. breeding) may be needed to maintain local population health in free-living passerines, such as tree swallows.

Divergent patterns of telomere shortening in tropical compared to temperate stonechats.

Telomeres have emerged as important biomarkers of health and senescence as they predict chances of survival in various species. Tropical birds live in more benign environments with lower extrinsic mortality and higher juvenile and adult survival than temperate birds. Therefore, telomere biology may play a more important role in tropical compared to temperate birds. We measured mean telomere length of male stonechats (Saxicola spp.) at four age classes from tropical African and temperate European breeding regions. Tropical and temperate stonechats had similarly long telomeres as nestlings. However, while in tropical stonechats pre-breeding first-years had longer telomeres than nestlings, in temperate stonechats pre-breeding first-years had shorter telomeres than nestlings. During their first breeding season, telomere length was again similar between tropical and temperate stonechats. These patterns may indicate differential survival of high-quality juveniles in tropical environments. Alternatively, more favorable environmental conditions, that is, extended parental care, may enable tropical juveniles to minimize telomere shortening. As suggested by previous studies, our results imply that variation in life history and life span may be reflected in different patterns of telomere shortening rather than telomere length. Our data provide first evidence that distinct selective pressures in tropical and temperate environments may be reflected in diverging patterns of telomere loss in birds.

Oxytocin administration prevents cellular aging caused by social isolation.

Chronic stressors, such as chronic isolation in social mammals, can elevate glucocorticoids, which can affect cellular mechanisms of aging, including increased levels of oxidative stress and shortened telomere lengths. Recent work in the selectively social prairie vole (Microtus ochrogaster) suggests that oxytocin and social support may mitigate some of the negative consequences of social isolation, possibly by reducing glucocorticoid levels. We investigated the influences of isolation, social support, and daily oxytocin injections in female prairie voles. Glucocorticoid levels, oxidative damage, telomere length, and anhedonia, a behavioral index of depression, were measured throughout the study. We found that six weeks of chronic isolation led to increased glucocorticoid levels, oxidative damage, telomere degradation and anhedonia. However, daily oxytocin injections in isolated voles prevented these negative consequences. These findings demonstrate that chronic social isolation in female prairie voles is a potent stressor that results in depression-like behavior and accelerated cellular aging. Importantly, oxytocin can completely prevent the negative consequences of social isolation.

Longevity and life history coevolve with oxidative stress in birds.

1. The mechanisms that underpin the evolution of ageing and life histories remain elusive. Oxidative stress, which results in accumulated cellular damages, is one of the mechanisms suggested to play a role. 2. In this paper, we set out to test the "oxidative stress theory of ageing" and the "oxidative stress hypothesis of life histories" using a comprehensive phylogenetic comparison based on an unprecedented dataset of oxidative physiology in 88 free-living bird species. 3. We show for the first time that bird species with longer lifespan have higher non-enzymatic antioxidant capacity and suffer less oxidative damage to their lipids. We also found that bird species featuring a faster pace-of-life either have lower non-enzymatic antioxidant capacity or are exposed to higher levels of oxidative damage, while adult annual mortality does not relate to oxidative state. 4. These results reinforce the role of oxidative stress in the evolution of lifespan and also corroborate the role of oxidative state in the evolution of life histories among free-living birds.

In ovo metabolism and yolk glucocorticoid concentration interact to influence embryonic glucocorticoid exposure patterns.

Vertebrates release glucocorticoids during stressful events. If stress occurs during reproduction, the resulting offspring can show altered phenotypes that are thought to arise from increased exposure to maternal glucocorticoids. Developing offspring can metabolize maternal glucocorticoids, which can alter the pattern of exposure they encounter. For egg laying vertebrates, we are just beginning to understand how embryonic steroid metabolism impacts embryonic exposure to maternal glucocorticoids. Here we injected three doses of radioactive corticosterone into Japanese quail (Coturnix japonica) eggs to determine the degree of embryonic exposure at days six and nine of development. We found that increasing injection dose increased the amount of radioactivity found in the embryo at day six but by day nine the effect of injection dose disappeared as the amount of radioactivity within the embryo dropped to equivalent levels for all three doses. Interestingly, when examined as a percentage of initial dose, there were no differences between treatment groups at any time points. Importantly, using thin-layer chromatography we characterized that some free steroid, putatively identified as corticosterone, does reach the developing embryo. Together, our data suggest that the in ovo metabolism of maternal corticosterone can eventually eliminate it from the egg, but before this happens, embryos developing in eggs with elevated amounts of maternal corticosterone are exposed to higher levels early in development. This has important implications for how we understand the developmental steroid environment and the mechanisms underlying maternal stress effects.

The rate of telomere loss is related to maximum lifespan in birds.

Telomeres are highly conserved regions of DNA that protect the ends of linear chromosomes. The loss of telomeres can signal an irreversible change to a cell's state, including cellular senescence. Senescent cells no longer divide and can damage nearby healthy cells, thus potentially placing them at the crossroads of cancer and ageing. While the epidemiology, cellular and molecular biology of telomeres are well studied, a newer field exploring telomere biology in the context of ecology and evolution is just emerging. With work to date focusing on how telomere shortening relates to individual mortality, less is known about how telomeres relate to ageing rates across species. Here, we investigated telomere length in cross-sectional samples from 19 bird species to determine how rates of telomere loss relate to interspecific variation in maximum lifespan. We found that bird species with longer lifespans lose fewer telomeric repeats each year compared with species with shorter lifespans. In addition, phylogenetic analysis revealed that the rate of telomere loss is evolutionarily conserved within bird families. This suggests that the physiological causes of telomere shortening, or the ability to maintain telomeres, are features that may be responsible for, or co-evolved with, different lifespans observed across species.This article is part of the theme issue 'Understanding diversity in telomere dynamics'.

An experimental test of the physiological consequences of avian malaria infection.

Chronic, low-intensity parasite infections can reduce host fitness through negative impacts on reproduction and survival, even if they produce few overt symptoms. As a result, these parasites can influence the evolution of host morphology, behaviour and physiology. The physiological consequences of chronic infection can provide insight into the processes underlying parasite-driven natural selection. Here, we evaluate the physiological consequences of natural, low-intensity infection in an avian host-parasite system: adult male red-winged blackbirds (Agelaius phoeniceus) infected with haemosporidian parasites. Chronic haemosporidian infection has previously been shown to reduce both reproductive success and survival in several avian species. We used antimalarial medications to experimentally reduce haemosporidian parasitaemia (the proportion of blood cells infected with haemosporidian parasites) and measured the effect of treatment on body condition, haematology, immune function, physiological stress and oxidative state. Treatment with an antimalarial medication reduced parasitaemia for the most prevalent haemosporidian parasites from the genus Plasmodium. Treatment also increased haemoglobin and haematocrit, and decreased red blood cell production rates. We detected no effect of treatment on body condition, immune metrics, plasma corticosterone concentrations, total antioxidant capacity or reactive oxygen metabolites. Our results suggest that the damage and replacement of red blood cells during infection could be important costs of chronic haemosporidian infection. Strong links between parasitaemia and the physiological consequences of infection indicate that even for relatively low-intensity infections, measuring parasitaemia rather than only presence/absence could be important when evaluating the role of infection in influencing hosts' behaviour, physiology or fitness.

Restless roosts: Light pollution affects behavior, sleep, and physiology in a free-living songbird.

The natural nighttime environment is increasingly polluted by artificial light. Several studies have linked artificial light at night to negative impacts on human health. In free-living animals, light pollution is associated with changes in circadian, reproductive, and social behavior, but whether these animals also suffer from physiologic costs remains unknown. To fill this gap, we made use of a unique network of field sites which are either completely unlit (control), or are artificially illuminated with white, green, or red light. We monitored nighttime activity of adult great tits, Parus major, and related this activity to within-individual changes in physiologic indices. Because altered nighttime activity as a result of light pollution may affect health and well-being, we measured oxalic acid concentrations as a biomarker for sleep restriction, acute phase protein concentrations and malaria infection as indices of immune function, and telomere lengths as an overall measure of metabolic costs. Compared to other treatments, individuals roosting in the white light were much more active at night. In these individuals, oxalic acid decreased over the course of the study. We also found that individuals roosting in the white light treatment had a higher probability of malaria infection. Our results indicate that white light at night increases nighttime activity levels and sleep debt and affects disease dynamics in a free-living songbird. Our study offers the first evidence of detrimental effects of light pollution on the health of free-ranging wild animals.