Michael Briga

Oxidative stress and life histories: unresolved issues and current needs

Abstract Life‐history theory concerns the trade‐offs that mold the patterns of investment by animals between reproduction, growth, and survival. It is widely recognized that physiology plays a role in the mediation of life‐history trade‐offs, but the details remain obscure. As life‐history theory concerns aspects of investment in the soma that influence survival, understanding the physiological basis of life histories is related, but not identical, to understanding the process of aging. One idea from the field of aging that has gained considerable traction in the area of life histories is that life‐history trade‐offs may be mediated by free radical production and oxidative stress. We outline here developments in this field and summarize a number of important unresolved issues that may guide future research efforts. The issues are as follows. First, different tissues and macromolecular targets of oxidative stress respond differently during reproduction. The functional significance of these changes, however, remains uncertain. Consequently there is a need for studies that link oxidative stress measurements to functional outcomes, such as survival. Second, measurements of oxidative stress are often highly invasive or terminal. Terminal studies of oxidative stress in wild animals, where detailed life‐history information is available, cannot generally be performed without compromising the aims of the studies that generated the life‐history data. There is a need therefore for novel non‐invasive measurements of multi‐tissue oxidative stress. Third, laboratory studies provide unrivaled opportunities for experimental manipulation but may fail to expose the physiology underpinning life‐history effects, because of the benign laboratory environment. Fourth, the idea that oxidative stress might underlie life‐history trade‐offs does not make specific enough predictions that are amenable to testing. Moreover, there is a paucity of good alternative theoretical models on which contrasting predictions might be based. Fifth, there is an enormous diversity of life‐history variation to test the idea that oxidative stress may be a key mediator. So far we have only scratched the surface. Broadening the scope may reveal new strategies linked to the processes of oxidative damage and repair. Finally, understanding the trade‐offs in life histories and understanding the process of aging are related but not identical questions. Scientists inhabiting these two spheres of activity seldom collide, yet they have much to learn from each other.

Bill Redness Is Positively Associated with Reproduction and Survival in Male and Female Zebra Finches

Sexual traits can serve as honest indicators of phenotypic quality when they are costly. Brightly coloured yellow to red traits, which are pigmented by carotenoids, are relatively common in birds, and feature in sexual selection. Carotenoids have been linked to immune and antioxidant function, and the trade-off between ornamentation and these physiological functions provides a potential mechanism rendering carotenoid based signals costly. Mutual ornamentation is also common in birds and can be maintained by mutual mate choice for this ornament or by a correlated response in one sex to selection on the other sex. When selection pressures differ between the sexes this can cause intralocus sexual conflict. Sexually antagonistic selection pressures have been demonstrated for few sexual traits, and for carotenoid-dependent traits there is a single example: bill redness was found to be positively associated with survival and reproductive output in male zebra finches, but negatively so in females. We retested these associations in our captive zebra finch population without two possible limitations of this earlier study. Contrary to the earlier findings, we found no evidence for sexually antagonistic selection. In both sexes, individuals with redder bills showed higher survival. This association disappeared among the females with the reddest bills. Furthermore, females with redder bills achieved higher reproductive output. We conclude that bill redness of male and female zebra finches honestly signals phenotypic quality, and discuss the possible causes of the differences between our results and earlier findings.

Large diurnal temperature range increases bird sensitivity to climate change

Climate variability is changing on multiple temporal scales, and little is known of the consequences of increases in short-term variability, particularly in endotherms. Using mortality data with high temporal resolution of zebra finches living in large outdoor aviaries (5 years, 359.220 bird-days), we show that mortality rate increases almost two-fold per 1°C increase in diurnal temperature range (DTR). Interestingly, the DTR effect differed between two groups with low versus high experimentally manipulated foraging costs, reflecting a typical laboratory ‘easy’ foraging environment and a ‘hard’ semi-natural environment respectively. DTR increased mortality on days with low minimum temperature in the easy foraging environment, but on days with high minimum temperature in the semi-natural environment. Thus, in a natural environment DTR effects will become increasingly important in a warming world, something not detectable in an ‘easy’ laboratory environment. These effects were particularly apparent at young ages. Critical time window analyses showed that the effect of DTR on mortality is delayed up to three months, while effects of minimum temperature occurred within a week. These results show that daily temperature variability can substantially impact the population viability of endothermic species.

Effects of early developmental conditions on innate immunity are only evident under favourable adult conditions in zebra finches

Long-term effects of unfavourable conditions during development can be expected to depend on the quality of the environment experienced by the same individuals during adulthood. Yet, in the majority of studies, long-term effects of early developmental conditions have been assessed under favourable adult conditions only. The immune system might be particularly vulnerable to early environmental conditions as its development, maintenance and use are thought to be energetically costly. Here, we studied the interactive effects of favourable and unfavourable conditions during nestling and adult stages on innate immunity (lysis and agglutination scores) of captive male and female zebra finches (Taeniopygia guttata). Nestling environmental conditions were manipulated by a brood size experiment, while a foraging cost treatment was imposed on the same individuals during adulthood. This combined treatment showed that innate immunity of adult zebra finches is affected by their early developmental conditions and varies between both sexes. Lysis scores, but not agglutination scores, were higher in individuals raised in small broods and in males. However, these effects were only present in birds that experienced low foraging costs. This study shows that the quality of the adult environment may shape the long-term consequences of early developmental conditions on innate immunity, as long-term effects of nestling environment were only evident under favourable adult conditions.

Food availability affects adult survival trajectories depending on early developmental conditions

Food availability modulates survival in interaction with (for example) competition, disease and predators, but to what extent food availability in natural populations affects survival independent of these factors is not well known. We tested the effect of food availability on lifespan and actuarial senescence in a large population of captive zebra finches by increasing the effort required to obtain food, reflecting natural contrasts in food availability. Food availability may not affect all individuals equally and we therefore created heterogeneity in phenotypic quality by raising birds with different numbers of siblings. Low food availability had no effect on lifespan for individuals from benign developmental conditions (raised in small broods), but shortened lifespan for individuals from harsh developmental conditions. The lifespan difference arose through higher baseline mortality rate of individuals from harsh developmental conditions, despite a decrease in the rate of actuarial senescence. We found no evidence for sex-specific environmental sensitivity, but females lived shorter than males due to increased actuarial senescence. Thus, low food availability by itself shortens lifespan, but only in individuals from harsh developmental conditions. Our food availability manipulation resembles dietary restriction as applied to invertebrates, where it extends lifespan in model organisms and we discuss possible reasons for the contrasting results.

What can long-lived mutants tell us about mechanisms causing aging and lifespan variation in natural environments?

Long-lived mutants of model organisms have brought remarkable progress in our understanding of aging mechanisms. However, long-lived mutants are usually maintained in optimal standardized laboratory environments (SLEs), and it is not obvious to what extent insights from long-lived mutants in SLEs can be generalized to more natural environments. To address this question, we reviewed experiments that compared the fitness and lifespan advantage of long-lived mutants relative to wild type controls in SLEs and more challenging environments in various model organisms such as yeast Saccharomyces cerevisiae, the nematode worm Caenorhabditis elegans, the fruitfly Drosophila melanogaster and the mouse Mus musculus. In competition experiments over multiple generations, the long-lived mutants had a lower fitness relative to wild type controls, and this disadvantage was the clearest when the environment included natural challenges such as limited food (N=6 studies). It is well known that most long-lived mutants have impaired reproduction, which provides one reason for the fitness disadvantage. However, based on 12 experiments, we found that the lifespan advantage of long-lived mutants is diminished in more challenging environments, often to the extent that the wild type controls outlive the long-lived mutants. Thus, it appears that information on aging mechanisms obtained from long-lived mutants in SLEs may be specific to such environments, because those same mechanisms do not extend lifespan in more natural environments. This suggests that different mechanisms cause variation in aging and lifespan in SLEs compared to natural populations.

Individual variation in metabolic reaction norms over ambient temperature causes low correlation between basal and standard metabolic rate

ABSTRACT Basal metabolic rate (BMR) is often assumed to be indicative of the energy turnover at ambient temperatures (Ta) below the thermoneutral zone (SMR), but this assumption has remained largely untested. Using a new statistical approach, we quantified the consistency in nocturnal metabolic rate across a temperature range in zebra finches (N=3213 measurements on 407 individuals) living permanently in eight outdoor aviaries. Foraging conditions were either benign or harsh, and body mass and mass-adjusted BMR (BMRm) and SMR (SMRm) were lower in individuals living in a harsh foraging environment. The correlation between SMRm at different Ta was high (r=0.91), independent of foraging environment, showing that individuals are consistently ranked according to their SMRm. However, the correlations between BMRm and SMRm were always lower (average: r=0.29; range: 0<r<0.50), in particular in the benign foraging environment. Variation in metabolic response to lower Ta at least in part reflected differential body temperature (Tb) regulation: early morning Tb was lower at low Ta, and more so in individuals with a weaker metabolic response to lower Ta. Our findings have implications for the use of BMR in the estimation of time–energy budgets and comparative analyses: we suggest that the use of metabolic rates at ecologically relevant Ta, such as the easily tractable SMR, will be more informative than the use of BMR as a proxy for energy turnover. Summary: Individual differences in cold response mean that minimal energy expenditure can be better quantified at ecologically relevant ambient temperatures.

Effects of developmental conditions on glucocorticoid concentrations in adulthood depend on sex and foraging conditions

Abstract Developmental conditions in early life frequently have long‐term consequences on the adult phenotype, but the adult environment can modulate such long‐term effects. Glucocorticoid hormones may be instrumental in mediating developmental effects, but the permanency of such endocrine changes is still debated. Here, we manipulated environmental conditions during development (small vs. large brood size, and hence sibling competition) and in adulthood (easy vs. hard foraging conditions) in a full factorial design in zebra finches, and studied effects on baseline (Bas‐CORT) and stress‐induced (SI‐CORT) corticosterone in adulthood. Treatments affected Bas‐CORT in females, but not in males. Females reared in small broods had intermediate Bas‐CORT levels as adults, regardless of foraging conditions in adulthood, while females reared in large broods showed higher Bas‐CORT levels in hard foraging conditions and lower levels in easy foraging conditions. Female Bas‐CORT was also more susceptible than male Bas‐CORT to non‐biological variables, such as ambient temperature. In line with these results, repeatability of Bas‐CORT was higher in males (up to 51%) than in females (25%). SI‐CORT was not responsive to the experimental manipulations in either sex and its repeatability was high in both sexes. We conclude that Bas‐CORT responsiveness to intrinsic and extrinsic conditions is higher in females than in males, and that the expression of developmental conditions may depend on the adult environment. The latter finding illustrates the critical importance of studying of causes and consequences of long‐term developmental effects in other environments in addition to standard laboratory conditions. HighlightsWe studied environmental effects on baseline and SI‐CORT in zebra finches.Environmental conditions were manipulated early and late in life in a 2 × 2 design.Effects of developmental conditions were dependent on the adult environment.Responsiveness to environmental conditions was significantly higher in females.SI‐CORT was highly repeatable and not responsive to the experimental conditions.

The heuristic value of redundancy models of aging

Molecular studies of aging aim to unravel the cause(s) of aging bottom-up, but linking these mechanisms to organismal level processes remains a challenge. We propose that complementary top-down data-directed modelling of organismal level empirical findings may contribute to developing these links. To this end, we explore the heuristic value of redundancy models of aging to develop a deeper insight into the mechanisms causing variation in senescence and lifespan. We start by showing (i) how different redundancy model parameters affect projected aging and mortality, and (ii) how variation in redundancy model parameters relates to variation in parameters of the Gompertz equation. Lifestyle changes or medical interventions during life can modify mortality rate, and we investigate (iii) how interventions that change specific redundancy parameters within the model affect subsequent mortality and actuarial senescence. Lastly, as an example of data-directed modelling and the insights that can be gained from this, (iv) we fit a redundancy model to mortality patterns observed by Mair et al. (2003; Science 301: 1731-1733) in Drosophila that were subjected to dietary restriction and temperature manipulations. Mair et al. found that dietary restriction instantaneously reduced mortality rate without affecting aging, while temperature manipulations had more transient effects on mortality rate and did affect aging. We show that after adjusting model parameters the redundancy model describes both effects well, and a comparison of the parameter values yields a deeper insight in the mechanisms causing these contrasting effects. We see replacement of the redundancy model parameters by more detailed sub-models of these parameters as a next step in linking demographic patterns to underlying molecular mechanisms.

Male but not female zebra finches with high plasma corticosterone have lower survival

The glucocorticoid axis is essential for coping with predictable and unpredictable environmental variation. Despite this vital function, attempts to link individual variation in the glucocorticoid axis to survival have yielded mixed results, which may be due to endocrine variation caused by uncontrolled variation in environment and life-history traits such as reproductive effort. We therefore studied the link between the glucocorticoid axis and long-term survival using captive non-breeding zebra finches. We quantified the relationship between survival over a three-year period and plasma corticosterone concentrations: (1) baseline, (2) stress-induced, (3) after induction of negative feedback via dexamethasone injection and (4) after maximal adrenal stimulation via adrenocorticotropin hormone injection. Only stress-induced corticosterone predicted survival, with higher concentrations being associated with lower survival. However, this effect differed significantly between the sexes, being present only in males. Stress-induced corticosterone concentration is the sum of baseline corticosterone and the corticosterone increase in response to the standardized stressor, and both components were similarly associated with male survival in a model that included both variables. This implies that baseline corticosterone itself also exerts an effect on male survival, but this was only revealed when the stress-induced corticosterone increase was included in the model, presumably because this increased statistical power. Given that corticosterone concentrations are highly repeatable in our study population and independent of manipulated foraging conditions, these data suggest that endocrine stress reactivity may be a major component determining male life span, presumably also in wild populations.