Experimental biology can inform our understanding of food insecurity.

Food insecurity is a major public health issue. Millions of households worldwide have intermittent and unpredictable access to food and this experience is associated with greater risk for a host of negative health outcomes. While food insecurity is a contemporary concern, we can understand its effects better if we acknowledge that there are ancient biological programs that evolved to respond to the experience of food scarcity and uncertainty, and they may be particularly sensitive to food insecurity during development. Support for this conjecture comes from common findings in several recent animal studies that have modeled insecurity by manipulating predictability of food access in various ways. Using different experimental paradigms in different species, these studies have shown that experience of insecure access to food can lead to changes in weight, motivation and cognition. Some of these studies account for changes in weight through changes in metabolism, while others observe increases in feeding and motivation to work for food. It has been proposed that weight gain is an adaptive response to the experience of food insecurity as 'insurance' in an uncertain future, while changes in motivation and cognition may reflect strategic adjustments in foraging behavior. Animal studies also offer the opportunity to make in-depth controlled studies of mechanisms and behavior. So far, there is evidence that the experience of food insecurity can impact metabolic efficiency, reproductive capacity and dopamine neuron synapses. Further work on behavior, the central and peripheral nervous system, the gut and liver, along with variation in age of exposure, will be needed to better understand the full body impacts of food insecurity at different stages of development.

Assessing the emotional states of dairy cows housed with or without their calves.

The practice of keeping dairy cows with their calves continues to gain interest. Cow-calf contact, or lack thereof, is expected to affect emotional states, but this requires empirical testing. Different types of cow-calf contact may also affect the emotional states of cows. The primary objective of this study was to assess the emotional state of dairy cows with full-time (23 h/d), part-time (10 h/d), or no-contact with their calves (separated 48 h after birth), using a visual judgment bias test (JBT) about one month after calving; JBT is the current gold-standard method to assess emotional state in animals by evaluating optimism or pessimism (illustrated by the proverbial half-full or half-empty water glass). The secondary objective was to compare outcomes of color- versus shape-based visual JBT. Fifty dairy cows were trained to approach a positive image on a screen (rewarded with food) and to avoid a negative image (else punished with waving bag). Once learned (>80% correct over 2 consecutive days), cows were presented with 3 ambiguous images (each presented once per day among 4 positive and 3 negative images, repeated over 4 d), and their approach responses recorded. For the color method (10 full-time, 9 part-time and 11 no-contact cows), positive and negative images were a solid red or white background; ambiguous images were shades of pink. For the shape method (8 full-time, 6 part-time and 6 no-contact cows), positive and negative images were a white circle or cross on a black background; ambiguous images were overlaid circle and cross in varying shades of gray. Cows learned to discriminate colors quicker than shapes (7.3 d, confidence limits [CL]: 6.6-8.2 d; vs. 9.3 d, CL: 8.1-10.6 d). Approaches to ambiguous colors followed a generalization curve (81.0, 33.1, and 5.0 ± 3.7% for near-positive, middle, and near-negative images, respectively), but not approaches to ambiguous shapes (31.9%, 25.7%, and 21.9% ± 4.8%, respectively), indicating colors over shapes should be used in visual JBT for cattle. Part-time cows approached fewer ambiguous color images than full-time cows (23.5%, CL: 13.4%-34.4%; vs. 44.8%, CL; 32.8%-57.1%) whereas no-contact cows were intermediate, but not different from full-time or part-time cows (37.8%, CL; 26.8%-49.5%). The color JBT results show a pessimistic bias (indicating a negative emotional state) in cows with part-time calf contact, possibly due to repeated daily separation from her young calf, relative to cows with full-time calf contact. Thus, cow-calf contact systems appear to influence the emotional state of cows depending on the practice. Cows without calf contact showed no difference in judgment bias between cows with full- or part-time calf contact, suggesting these cows probably do not experience a pervasive negative emotional state (relative to those with calf contact) approximately 30 d after calf separation. However, individual variability in judgment bias was evident for all treatments. The visual judgment bias test is a useful methodology for assessing emotional states of dairy cows; future research should prioritize understanding the emotional states of dairy cows in alternative management systems.

Maternal behavior of dairy cows and suckling behavior of dairy calves in different cow-calf-contact conditions.

Cow-calf contact (CCC) has been suggested as an alternative to the common practice of early separation of dairy cow and calf. Increasing CCC poses challenges by reducing the machine milk yield and increasing separation stress. Part-time CCC may prove more feasible than full-time contact for farmers but may affect the maternal behavior of the cows. Gradually reducing the daily contact could gradually wean the calf off milk, preparing it for separation. This study aims to investigate 1) how cows' maternal behaviors toward their own calf are affected by part-time contact, and 2) whether calves' suckling behavior is reduced by reducing daily cow contact. Fifty-six dairy cows and their calves were assigned to either full-time (23 h/d) or part-time (10 h/d) cow-calf contact for 7 weeks (main rearing period). This was followed by 2 weeks of either reduced contact (50% in wk 8, then 25% of original contact time in wk 9) or unchanged contact. First, the maternal behavior of full and part-time cows was observed for 24 h in the third week of the main rearing period. Part-time cows spent less time nursing and grooming their own calf than full-time cows did. However, the amount of nursing in the inverse parallel position and the probability of a cow nursing a calf other than her own did not differ between the 2 treatments. Second, calf suckling behavior was observed for 24 h in both weeks of the reduced contact period. Averaged across both observations, total suckling time (i.e., time spent suckling any cow) was lower in part-time calves that experienced reduced contact compared with part-time calves with unchanged contact. In wk 9, time spent suckling only the dam was lower for full-time calves with reduced contact compared with part-time calves with unchanged contact. In conclusion, although we found a lower nursing and grooming time in part-time cows compared with full-time, we found no difference between treatments with regards to nursing in the inverse parallel position and nursing a calf other than the cow's own. The effect of gradually reducing cow-calf contact on calves' suckling time requires more research.

Concurrent invasions of European starlings in Australia and North America reveal population-specific differentiation in shared genomic regions.

A species' success during the invasion of new areas hinges on an interplay between the demographic processes common to invasions and the specific ecological context of the novel environment. Evolutionary genetic studies of invasive species can investigate how genetic bottlenecks and ecological conditions shape genetic variation in invasions, and our study pairs two invasive populations that are hypothesized to be from the same source population to compare how each population evolved during and after introduction. Invasive European starlings (Sturnus vulgaris) established populations in both Australia and North America in the 19th century. Here, we compare whole-genome sequences among native and independently introduced European starling populations to determine how demographic processes interact with rapid evolution to generate similar genetic patterns in these recent and replicated invasions. Demographic models indicate that both invasive populations experienced genetic bottlenecks as expected based on invasion history, and we find that specific genomic regions have differentiated even on this short evolutionary timescale. Despite genetic bottlenecks, we suggest that genetic drift alone cannot explain differentiation in at least two of these regions. The demographic boom intrinsic to many invasions as well as potential inversions may have led to high population-specific differentiation, although the patterns of genetic variation are also consistent with the hypothesis that this infamous and highly mobile invader adapted to novel selection (e.g., extrinsic factors). We use targeted sampling of replicated invasions to identify and evaluate support for multiple, interacting evolutionary mechanisms that lead to differentiation during the invasion process.

Historical museum samples enable the examination of divergent and parallel evolution during invasion.

During the Anthropocene, Earth has experienced unprecedented habitat loss, native species decline and global climate change. Concurrently, greater globalization is facilitating species movement, increasing the likelihood of alien species establishment and propagation. There is a great need to understand what influences a species' ability to persist or perish within a new or changing environment. Examining genes that may be associated with a species' invasion success or persistence informs invasive species management, assists with native species preservation and sheds light on important evolutionary mechanisms that occur in novel environments. This approach can be aided by coupling spatial and temporal investigations of evolutionary processes. Here we use the common starling, Sturnus vulgaris, to identify parallel and divergent evolutionary change between contemporary native and invasive range samples and their common ancestral population. To do this, we use reduced-representation sequencing of native samples collected recently in northwestern Europe and invasive samples from Australia, together with museum specimens sampled in the UK during the mid-19th century. We found evidence of parallel selection on both continents, possibly resulting from common global selective forces such as exposure to pollutants. We also identified divergent selection in these populations, which might be related to adaptive changes in response to the novel environment encountered in the introduced Australian range. Interestingly, signatures of selection are equally as common within both invasive and native range contemporary samples. Our results demonstrate the value of including historical samples in genetic studies of invasion and highlight the ongoing and occasionally parallel role of adaptation in both native and invasive ranges.

Food insecurity and patterns of dietary intake in a sample of UK adults.

The aim of this study was to identify the dietary intake correlates of food insecurity (FI) in UK adults. We recruited groups of low-income participants who were classified as food insecure (n 196) or food secure (n 198). Participants completed up to five 24 h dietary recalls. There was no difference in total energy intake by FI status (ßFI = -0·06, 95 % CI - 0·25, 0·13). Food insecure participants consumed a less diverse diet, as evidenced by fewer distinct foods per meal (ßFI = -0·27, 95 % CI - 0·47, -0·07), and had more variable time gaps between meals (ßFI = 0·21, 95 % CI 0·01, 0·41). These associations corresponded closely to those found in a recent US study using similar measures, suggesting that the dietary intake signature of FI generalises across populations. The findings suggest that the consequences of FI for weight gain and health are not due to increased energy intake. We suggest that there may be important health and metabolic effects of temporal irregularity in dietary intake, which appears to be an important component of FI.

Measurement of Telomere Length for Longitudinal Analysis: Implications of Assay Precision.

Researchers increasingly wish to test hypotheses concerning the impact of environmental or disease exposures on telomere length (TL), and they use longitudinal study designs to do so. In population studies, TL is usually measured with a quantitative polymerase chain reaction (qPCR)-based method. This method has been validated by calculating its correlation with a gold standard method such as Southern blotting (SB) in cross-sectional data sets. However, in a cross-section, the range of true variation in TL is large, and measurement error is introduced only once. In a longitudinal study, the target variation of interest is small, and measurement error is introduced at both baseline and follow-up. In this paper, we present results from a small data set (n = 20) in which leukocyte TL was measured twice 6.6 years apart by means of both qPCR and SB. The cross-sectional correlations between qPCR and SB were high at both baseline (r = 0.90) and follow-up (r = 0.85), yet their correlation for TL change was poor (r = 0.48). Moreover, the qPCR data but not the SB data showed strong signatures of measurement error. Through simulation, we show that the statistical power gain from performing a longitudinal analysis is much greater for SB than for qPCR. We discuss implications for optimal study design and analysis.

Time perception and patience: individual differences in interval timing precision predict choice impulsivity in European starlings, Sturnus vulgaris.

Impulsivity, in the sense of the extent rewards are devalued as the time until their realization increases, is linked to various negative outcomes in humans, yet understanding of the cognitive mechanisms underlying it is limited. Variation in the imprecision of interval timing is a possible contributor to variation in impulsivity. We use a numerical model to generate predictions concerning the effect of timing imprecision on impulsivity. We distinguish between fixed imprecision (the imprecision that applies even when timing the very shortest time intervals) and proportional imprecision (the rate at which imprecision increases as the interval becomes longer). The model predicts that impulsivity should increase with increasing fixed imprecision, but decrease with increasing proportional imprecision. We present data from a cohort of European starlings (Sturnus vulgaris, n = 28) in which impulsivity had previously been measured through an intertemporal choice paradigm. We tested interval timing imprecision in the same individuals using a tri-peak temporal reproduction procedure. We found repeatable individual differences in both fixed and proportional imprecision. As predicted, birds with greater proportional imprecision in interval timing made fewer impulsive choices, whilst those with greater fixed imprecision tended to make more. Contradictory observations in the literature regarding the direction of association between timing imprecision and impulsivity might be clarified by distinguishing between fixed and proportional components of imprecision.

Developmental history, energetic state and choice impulsivity in European starlings, Sturnus vulgaris.

Impulsivity-the extent to which a reward is devalued by the amount of time until it is realized-can be affected by an individual's current energetic state and long-term developmental history. In European starlings (Sturnus vulgaris), a previous study found that birds that were lighter for their skeletal size, and birds that had undergone greater shortening of erythrocyte telomeres over the course of development, were more impulsive as adults. Here, we studied the impulsivity of a separate cohort of 29 starlings hand-reared under different combinations of food amount and begging effort. The task involved repeated choice between a key yielding one pellet after 3 s and another key yielding two pellets after 8 s. Impulsivity was operationalised as the proportion of choices for the short-delay option. We found striking variation in impulsivity. We did not replicate the results of the previous study concerning developmental telomere attrition, though combining all the evidence to date in a meta-analysis did support that robustness of that association. We also found that early-life conditions and mass for skeletal size interacted in predicting impulsivity. Specifically, birds that had experienced the combination of high begging effort and low food amount were less impulsive than other groups, and the usual negative relationship between impulsivity and body mass was abolished in birds that had experienced high begging effort. We discuss methodological differences between our study and studies that measure impulsivity using an adjusting-delay procedure.

Developmental history and stress responsiveness are related to response inhibition, but not judgement bias, in a cohort of European starlings (Sturnus vulgaris).

Judgement bias tasks are designed to provide markers of affective states. A recent study of European starlings (Sturnus vulgaris) demonstrated modest familial effects on judgement bias performance, and found that adverse early experience and developmental telomere attrition (an integrative marker of biological age) both affected judgement bias. Other research has shown that corticosterone levels affect judgement bias. Here, we investigated judgement bias using a modified Go/No Go task in a new cohort of starlings (n = 31) hand-reared under different early-life conditions. We also measured baseline corticosterone and the corticosterone response to acute stress in the same individuals. We found evidence for familial effects on judgement bias, of a similar magnitude to the previous study. We found no evidence that developmental treatments or developmental telomere attrition were related to judgement bias per se. We did, however, find that birds that experienced the most benign developmental conditions, and birds with the greatest developmental telomere attrition, were significantly faster to probe the learned unrewarded stimulus. We also found that the birds whose corticosterone levels were faster to return towards baseline after an acute stressor were slower to probe the learned unrewarded stimulus. Our results illustrate the potential complexities of relationships between early-life experience, stress and affectively mediated decision making. For judgement bias tasks, they demonstrate the importance of clearly distinguishing factors that affect patterns of responding to the learned stimuli (i.e. response inhibition in the case of the Go/No Go design) from factors that influence judgements under ambiguity.

Opportunistic food consumption in relation to childhood and adult food insecurity: An exploratory correlational study.

Food insecurity is associated with high body weight for women but not men in affluent Western societies. However, it is not currently known what behavioural or psychological mechanisms drive this association. Moreover, it is also unknown whether only current experience of food insecurity in adulthood is important, or there are lasting effects of childhood experience. We carried out a mock 'taste test' where 126 adult volunteers had the opportunity to consume and rate senergy-dense snack foods. Current food insecurity was measured using the standard USDA measure, and in addition, we used a novel measure that also captures childhood experience of food insecurity. As well as the expected gender-specific association between current food insecurity and body weight, we found some evidence for associations between food insecurity and calorie consumption in the taste test, and liking of one of the foods, chocolate. However, associations between current food insecurity and the outcomes were moderated by childhood experience of food insecurity, with greater childhood food insecurity enhancing the positive effect of current food insecurity on body weight, but attenuating the positive effect of food insecurity on calorie consumption and liking for chocolate. These findings are exploratory, but they suggest that any effects of food insecurity in adulthood on eating and the hedonic value of foods may be moderated by childhood experience.

Cumulative stress in research animals: Telomere attrition as a biomarker in a welfare context?

Progress in improving animal welfare is currently limited by the lack of objective methods for assessing lifetime experience. I propose that telomere attrition, a cellular biomarker of biological age, provides a molecular measure of cumulative experience that could be used to assess the welfare impact of husbandry regimes and/or experimental procedures on non-human animals. I review evidence from humans that telomere attrition is accelerated by negative experiences in a cumulative and dose-dependent manner, but that this attrition can be mitigated or even reversed by positive life-style interventions. Evidence from non-human animals suggests that despite some specific differences in telomere biology, stress-induced telomere attrition is a robust phenomenon, occurring in a range of species including mice and chickens. I conclude that telomere attrition apparently integrates positive and negative experience in an accessible common currency that translates readily to novel species--the Holy Grail of a cumulative welfare indicator.

Adaptive principles of weight regulation: Insufficient, but perhaps necessary, for understanding obesity.

We reflect on the major issues raised by a thoughtful and diverse set of commentaries on our target article. We draw attention to the need to differentiate between ultimate and proximate explanation; the insurance hypothesis (IH) needs to be understood as an ultimate-level argument, although we welcome the various suggestions made about proximate mechanisms. Much of this response is concerned with clarifying the interrelationships between adaptationist explanations like the IH, constraint explanations, and dysfunction explanations, in understanding obesity. We also re-examine the empirical evidence base, concurring that it is equivocal and only partially supportive. Several commentators offer additional supporting evidence, whereas others propose alternative explanations for the evidence we reviewed and suggest ways that our current knowledge could be strengthened. Finally, we take the opportunity to clarify some of the assumptions and predictions of our formal model.

Food insecurity as a driver of obesity in humans: The insurance hypothesis.

Integrative explanations of why obesity is more prevalent in some sectors of the human population than others are lacking. Here, we outline and evaluate one candidate explanation, the insurance hypothesis (IH). The IH is rooted in adaptive evolutionary thinking: The function of storing fat is to provide a buffer against shortfall in the food supply. Thus, individuals should store more fat when they receive cues that access to food is uncertain. Applied to humans, this implies that an important proximate driver of obesity should be food insecurity rather than food abundance per se. We integrate several distinct lines of theory and evidence that bear on this hypothesis. We present a theoretical model that shows it is optimal to store more fat when food access is uncertain, and we review the experimental literature from non-human animals showing that fat reserves increase when access to food is restricted. We provide a meta-analysis of 125 epidemiological studies of the association between perceived food insecurity and high body weight in humans. There is a robust positive association, but it is restricted to adult women in high-income countries. We explore why this could be in light of the IH and our theoretical model. We conclude that although the IH alone cannot explain the distribution of obesity in the human population, it may represent a very important component of a pluralistic explanation. We also discuss insights it may offer into the developmental origins of obesity, dieting-induced weight gain, and anorexia nervosa.

Attention bias to threat indicates anxiety differences in sheep.

Humans and animals show increased attention towards threatening stimuli when they are in increased states of anxiety. The few animal studies that have examined this phenomenon, known as attention bias, have applied environmental manipulations to induce anxiety but the effects of drug-induced anxiety levels on attention bias have not been demonstrated. Here, we present an attention bias test to identify high and low anxiety states in sheep using pharmacological manipulation. Increased anxiety was induced using 1-methyl-chlorophenylpiperazine (m-CPP) and decreased anxiety with diazepam, and then we examined the behaviour of sheep in response to the presence of a dog as a threat. Increased attention towards the threat and increased vigilance were shown in sheep that received the m-CPP and reduced in sheep receiving the diazepam. The modulated attention towards a threat displayed by the m-CPP and diazepam animals suggests that attention bias can assess different levels of anxiety in sheep. Measuring attention bias has the potential to improve animal welfare assessment protocols.

Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve?

Developmental plasticity describes situations where a specific input during an individual's development produces a lasting alteration in phenotype. Some instances of developmental plasticity may be adaptive, meaning that the tendency to produce the phenotype conditional on having experienced the developmental input has been under positive selection. We discuss the necessary assumptions and predictions of hypotheses concerning adaptive developmental plasticity (ADP) and develop guidelines for how to test empirically whether a particular example is adaptive. Central to our analysis is the distinction between two kinds of ADP: informational, where the developmental input provides information about the future environment, and somatic state-based, where the developmental input enduringly alters some aspect of the individual's somatic state. Both types are likely to exist in nature, but evolve under different conditions. In all cases of ADP, the expected fitness of individuals who experience the input and develop the phenotype should be higher than that of those who experience the input and do not develop the phenotype, while the expected fitness of those who do not experience the input and do not develop the phenotype should be higher than those who do not experience the input and do develop the phenotype. We describe ancillary predictions that are specific to just one of the two types of ADP and thus distinguish between them.

Developmental telomere attrition predicts impulsive decision-making in adult starlings.

Animals in a poor biological state face reduced life expectancy, and as a consequence should make decisions that prioritize immediate survival and reproduction over long-term benefits. We tested the prediction that if, as has been suggested, developmental telomere attrition is a biomarker of state and future life expectancy, then individuals who have undergone greater developmental telomere attrition should display greater choice impulsivity as adults. We measured impulsive decision-making in a cohort of European starlings (Sturnus vulgaris) in which we had previously manipulated developmental telomere attrition by cross-fostering sibling chicks into broods of different sizes. We show that as predicted by state-dependent optimality models, individuals who had sustained greater developmental telomere attrition and who had shorter current telomeres made more impulsive foraging decisions as adults, valuing smaller, sooner food rewards more highly than birds with less attrition and longer telomeres. Our findings shed light on the biological embedding of early adversity and support a functional explanation for its consequences that could be applicable to other species, including humans.

An experimental demonstration that early-life competitive disadvantage accelerates telomere loss.

Adverse experiences in early life can exert powerful delayed effects on adult survival and health. Telomere attrition is a potentially important mechanism in such effects. One source of early-life adversity is the stress caused by competitive disadvantage. Although previous avian experiments suggest that competitive disadvantage may accelerate telomere attrition, they do not clearly isolate the effects of competitive disadvantage from other sources of variation. Here, we present data from an experiment in European starlings (Sturnus vulgaris) that used cross-fostering to expose siblings to divergent early experience. Birds were assigned either to competitive advantage (being larger than their brood competitors) or competitive disadvantage (being smaller than their brood competitors) between days 3 and 12 post-hatching. Disadvantage did not affect weight gain, but it increased telomere attrition, leading to shorter telomere length in disadvantaged birds by day 12. There were no effects of disadvantage on oxidative damage as measured by plasma lipid peroxidation. We thus found strong evidence that early-life competitive disadvantage can accelerate telomere loss. This could lead to faster age-related deterioration and poorer health in later life.

Humans are not fooled by size illusions in attractiveness judgements.

Could signallers use size contrast illusions to dishonestly exaggerate their attractiveness to potential mates? Using composite photographs of women from three body mass index (BMI) categories designed to simulate small groups, we show that target women of medium size are judged as thinner when surrounded by larger women than when surrounded by thinner women. However, attractiveness judgements of the same target women were unaffected by this illusory change in BMI, despite small true differences in the BMIs of the target women themselves producing strong effects on attractiveness. Thus, in the context of mate choice decisions, the honesty of female body size as a signal of mate quality appears to have been maintained by the evolution of assessment strategies that are immune to size contrast illusions. Our results suggest that receiver psychology is more flexible than previously assumed, and that illusions are unlikely to drive the evolution of exploitative neighbour choice in human sexual displays.

Better the devil you know: avian predators find variation in prey toxicity aversive.

Toxic prey that signal their defences to predators using conspicuous warning signals are called 'aposematic'. Predators learn about the toxic content of aposematic prey and reduce their attacks on them. However, through regulating their toxin intake, predators will include aposematic prey in their diets when the benefits of gaining the nutrients they contain outweigh the costs of ingesting the prey's toxins. Predators face a problem when managing their toxin intake: prey sharing the same warning signal often vary in their toxicities. Given that predators should avoid uncertainty when managing their toxin intake, we tested whether European starlings (Sturnus vulgaris) preferred to eat fixed-defence prey (where all prey contained a 2% quinine solution) to mixed-defence prey (where half the prey contained a 4% quinine solution and the other half contained only water). Our results support the idea that predators should be more 'risk-averse' when foraging on variably defended prey and suggest that variation in toxicity levels could be a form of defence.