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Preprint: Exposure to food insecurity increases energy storage and reduces somatic maintenance in European starlings Abstract Birds exposed to food insecurity—defined as temporally variable access to food—respond adaptively by storing more energy. In order to do this, they may reduce energy allocation to other functions such as somatic maintenance and repair. To investigate this trade-off, we exposed juvenile European starlings (Sturnus vulgaris, n = 69) to 19 weeks of either uninterrupted food availability, or a regime where food was unpredictably unavailable for five hours on five days each week. Our measures of energy storage were repeated measurements of mass, and fat score at the end of the treatment. Our measures of somatic maintenance were growth rate of a repeatedly plucked tail feather, and erythrocyte telomere length, which we measured five times by analysis of the terminal restriction fragment. The insecure birds were heavier at all measurement points, but by an amount that varied across time points. They also had higher fat scores. We found no evidence that they consumed any more food overall, though our food consumption data was incomplete. Plucked tail feathers regrew more slowly in the insecure birds. Telomere length was reduced in the insecure birds, specifically, in the longer percentiles of the within-individual telomere length distribution. We conclude that increased energy storage in response to food insecurity is achieved at the expense of investment in somatic maintenance and repair.

Birds exposed to food insecurity—defined as temporally variable access to food—respond adaptively by storing more energy. To do this, they may reduce energy allocation to other functions such as somatic maintenance and repair. To investigate this trade-off, we exposed juvenile European starlings (Sturnus vulgaris, n = 69) to 19 weeks of either uninterrupted food availability or a regime where food was unpredictably unavailable for a 5-h period on 5 days each week. Our measures of energy storage were mass and fat scores. Our measures of somatic maintenance were the growth rate of a plucked feather, and erythrocyte telomere length (TL), measured by analysis of the terminal restriction fragment. The insecure birds were heavier than the controls, by an amount that varied over time. They also had higher fat scores. We found no evidence that they consumed more food overall, though our food consumption data were incomplete. Plucked feathers regrew more slowly in the insecure birds. TL was reduced in the insecure birds, specifically, in the longer percentiles of the within-individual TL distribution. We conclude that increased energy storage in response to food insecurity is achieved at the expense of investment in somatic maintenance and repair.

Lay Summary Although the evolution of parental care is a central topic in behavioral ecology, we know relatively little about how complex forms of care evolve. We studied elaborate parental care in the burying beetle N. vespilloides. Our results suggest that females differ in their parental quality, that some parental behaviors enhance offspring growth while others enhance offspring survival, and that there is little genetic variation in parental and offspring behaviors. Twitter: @persmiseth, The evolution of elaborate forms of parental care is an important topic in behavioral ecology, yet the factors shaping the evolution of complex suites of parental and offspring traits are poorly understood. Here, we use a multivariate quantitative genetic approach to study phenotypic and genetic correlations between parental and offspring traits in the burying beetle Nicrophorus vespilloides. To this end, we recorded 2 prenatal traits (clutch size and egg size), 2 postnatal parental behaviors (direct care directed toward larvae and indirect care directed toward resource maintenance), 1 offspring behavior (begging), and 2 measures of breeding success (larval dispersal mass and number of dispersing larvae). Females breeding on larger carcasses provided less direct care but produced larger larvae than females breeding on smaller carcasses. Furthermore, there were positive phenotypic correlations between clutch size, direct, and indirect care. Both egg size and direct care were positively correlated with dispersal mass, whereas clutch size was negatively correlated with dispersal mass. Clutch size and number of dispersed larvae showed genetic variance both in terms of differences between populations of origin and significant heritabilities. However, we found no evidence of genetic variance underlying other parental or offspring traits. Our results suggest that correlations between suites of parental traits are driven by variation in individual quality rather than trade-offs, that some parental traits promote offspring growth while others increase the number of offspring produced, and that parental and offspring traits might respond slowly to selection due to low levels of additive genetic variance.

Animals require strategies for coping with periods when food is scarce. Such strategies include storing fat as a buffer, and defending the rate of energy intake by changing foraging behaviour when food becomes difficult to obtain. Storage and behavioural defence may constitute alternative strategies for solving the same problem. We would thus expect any developmental influences that limit fat storage in adulthood to also induce a compensatory alteration in adult foraging behaviour, specifically when food is hard to obtain. In a cohort of hand-reared European starlings, we found that higher manipulated early-life begging effort caused individuals to maintain consistently lower adult body mass over a period of two years. Using an operant foraging task in which we systematically varied the costs of obtaining food, we show that higher early-life begging effort also caused stronger behavioural defence of the rate of energy intake when food was more costly to obtain. Among individuals with the same developmental history, however, those individuals who defended their rate of energy intake most strongly were also the heaviest. Our results are relevant to understanding why there are marked differences in body weight and foraging behaviour even among individuals inhabiting the same environment.

Why do some individuals gamble more than others? Existing theories, based on how close animals are to starvation, have been only weakly supported by evidence. We found that faster ageing birds were less likely to gamble while foraging. We measured biological ageing in starlings from the shortening of DNA sequences called telomeres. Birds’ whose telomeres shortened more had stronger preferences for a foraging option yielding a consistent amount of food over a variable amount., Why are some individuals more prone to gamble than others? Animals often show preferences between 2 foraging options with the same mean reward but different degrees of variability in the reward, and such risk preferences vary between individuals. Previous attempts to explain variation in risk preference have focused on energy budgets, but with limited empirical support. Here, we consider whether biological ageing, which affects mortality and residual reproductive value, predicts risk preference. We studied a cohort of European starlings (Sturnus vulgaris) in which we had previously measured developmental erythrocyte telomere attrition, an established integrative biomarker of biological ageing. We measured the adult birds’ preferences when choosing between a fixed amount of food and a variable amount with an equal mean. After controlling for change in body weight during the experiment (a proxy for energy budget), we found that birds that had undergone greater developmental telomere attrition were more risk averse as adults than were those whose telomeres had shortened less as nestlings. Developmental telomere attrition was a better predictor of adult risk preference than either juvenile telomere length or early-life food supply and begging effort. Our longitudinal study thus demonstrates that biological ageing, as measured via developmental telomere attrition, is an important source of lasting differences in adult risk preferences.

Link between our behavioural measures and Staddon's molar model of reinforcement

Early-life adversity is associated with increased vulnerability to depression in humans, and depression-like phenotypes in animals. However, different types of adverse experience may leave different signatures in adulthood. We experimentally manipulated the Amount of food delivered to European starling nestlings and the begging Effort required to obtain food during early development. Here, we report behavioural data in adulthood from a task that assessed sensitivity to shifts in reward magnitude characteristic of depression-like low mood. Birds that had experienced Hard Effort were more food motivated than birds that had experienced Easy Effort. Both Effort and Amount affected sensitivity to shifts in reward magnitude: Hard Effort birds showed an enhanced negative contrast effect following loss of reward ('disappointment'), and Lean Amount birds failed to show a normal positive contrast effect following gain in reward (a lack of 'elation'). Therefore, the feeding schedule experienced for just 10 days in early life caused enduring effects on feeding motivation and sensitivity to reward loss/gain consistent with human depression. Furthermore, the contrast effects were specific to different types of adversity. These results highlight the importance of early-life feeding schedules in the development of depression-like phenotypes.

For young birds in a nest, body size may have implications for other aspects of development such as telomere length and immune function. However, it is possible to predict associations in either direction. On the one hand, there may be trade‐offs between growth and telomere maintenance, and growth and investment in immune function, suggesting there will be negative correlations. On the other hand, relatively larger individuals might be advantaged in competition with their nest‐mates, allowing them to garner more resources overall, leading to positive correlations. We studied development over the nestling period in 34 nests of wild European starlings, Sturnus vulgaris. Intrabrood competition is typically more intense in larger broods. Hence, we predicted that body size should become an increasingly positive predictor of telomere length and immune functioning as brood size increases. In partial support of our prediction, there were significant interactions between brood size and body size in predicting both erythrocyte telomere length change and plasma levels of the cytokine interleukin‐6. The associations between body size and these outcomes went from negative in the smallest broods to positive in the largest. A further immune marker, high‐sensitivity C‐reactive protein, showed no systematic patterning with body size or brood size. Our results confirm that the size to which a nestling grows is important for telomere dynamics and the development of the immune system, but the phenotypic associations are moderated by the competitive context.

Early-life adversity is associated with accelerated cellular ageing during development and increased inflammation during adulthood. However, human studies can only establish correlation, not causation, and existing experimental animal approaches alter multiple components of early-life adversity simultaneously. We developed a novel hand-rearing paradigm in European starling nestlings (Sturnus vulgaris), in which we separately manipulated nutritional shortfall and begging effort for a period of 10 days. The experimental treatments accelerated erythrocyte telomere attrition and increased DNA damage measured in the juvenile period. For telomere attrition, amount of food and begging effort exerted additive effects. Only the combination of low food amount and high begging effort increased DNA damage. We then measured two markers of inflammation, high-sensitivity C-reactive protein and interleukin-6, when the birds were adults. The experimental treatments affected both inflammatory markers, though the patterns were complex and different for each marker. The effect of the experimental treatments on adult interleukin-6 was partially mediated by increased juvenile DNA damage. Our results show that both nutritional input and begging effort in the nestling period affect cellular ageing and adult inflammation in the starling. However, the pattern of effects is different for different biomarkers measured at different time points.

Preprint: Exposure to food insecurity increases energy storage and reduces somatic maintenance in European starlings Abstract Birds exposed to food insecurity—defined as temporally variable access to food—respond adaptively by storing more energy. In order to do this, they may reduce energy allocation to other functions such as somatic maintenance and repair. To investigate this trade-off, we exposed juvenile European starlings (Sturnus vulgaris, n = 69) to 19 weeks of either uninterrupted food availability, or a regime where food was unpredictably unavailable for five hours on five days each week. Our measures of energy storage were repeated measurements of mass, and fat score at the end of the treatment. Our measures of somatic maintenance were growth rate of a repeatedly plucked tail feather, and erythrocyte telomere length, which we measured five times by analysis of the terminal restriction fragment. The insecure birds were heavier at all measurement points, but by an amount that varied across time points. They also had higher fat scores. We found no evidence that they consumed any more food overall, though our food consumption data was incomplete. Plucked tail feathers regrew more slowly in the insecure birds. Telomere length was reduced in the insecure birds, specifically, in the longer percentiles of the within-individual telomere length distribution. We conclude that increased energy storage in response to food insecurity is achieved at the expense of investment in somatic maintenance and repair.

Preprint: Exposure to food insecurity increases energy storage and reduces somatic maintenance in European starlings Abstract Birds exposed to food insecurity—defined as temporally variable access to food—respond adaptively by storing more energy. In order to do this, they may reduce energy allocation to other functions such as somatic maintenance and repair. To investigate this trade-off, we exposed juvenile European starlings (Sturnus vulgaris, n = 69) to 19 weeks of either uninterrupted food availability, or a regime where food was unpredictably unavailable for five hours on five days each week. Our measures of energy storage were repeated measurements of mass, and fat score at the end of the treatment. Our measures of somatic maintenance were growth rate of a repeatedly plucked tail feather, and erythrocyte telomere length, which we measured five times by analysis of the terminal restriction fragment. The insecure birds were heavier at all measurement points, but by an amount that varied across time points. They also had higher fat scores. We found no evidence that they consumed any more food overall, though our food consumption data was incomplete. Plucked tail feathers regrew more slowly in the insecure birds. Telomere length was reduced in the insecure birds, specifically, in the longer percentiles of the within-individual telomere length distribution. We conclude that increased energy storage in response to food insecurity is achieved at the expense of investment in somatic maintenance and repair.