State-Dependent and Social Modulation of Circulating Glucocorticoids in a Nomadic Songbird, the Red Crossbill (Loxia Curvirostra)

食物限制对黑线仓鼠免疫功能的影响

Theoretical models about the relationship between food restriction and individual differences in risk-taking behavior (i.e., boldness) have led to conflicting predictions: some models predict that food restriction increases boldness, while other models predict that food restriction decreases boldness. This discrepancy may be partially attributable to an underappreciation for animals' complex physiological responses to food restriction. To understand the proximate mechanisms mediating state-dependent boldness, we used freshwater snails (Helisoma trivolvis) to examine the relationships among food availability, body condition, boldness (latency to reemerge from shell and exploration), and mRNA expression of three genes (adenosine monophosphate-activated protein kinase [AMPK], molluscan insulin-like peptide [MIP], and serotonin receptor [5-HT]) involved in maintaining energy homeostasis during periods of moderate food restriction. Latency to reemerge and exploratory behavior decreased over time, but fed snails were bolder than fasted snails, suggesting that food restriction reduces bold behavior. Although food restriction decreased body condition, there was not a relationship between body condition and latency to reemerge from shell. However, expression of MIP was positively correlated with latency to reemerge from shell. Furthermore, AMPK was positively correlated with MIP and negatively correlated with body condition and 5-HT. Therefore, individual differences in physiological responses to food restriction, not overall body condition per se, appear to be more closely associated with state-dependent bold behavior. Finally, snails that experienced a novel assay environment returned to their initial "shy" behavior, suggesting that habituation to the assay environment may contribute to snails expressing bolder behavior over time.

Animals prepare for fluctuations in resources through advance storage of energy, planned reduction in energy costs or by moving elsewhere. Unpredictable fluctuations in food, however, may be particularly challenging if animals cannot avoid negative impacts on body condition. Social information may help animals to cope with unpredictable resources if cues from individuals with low foraging success give advance warning about deteriorating conditions. This study investigates the impact of social information on behaviour and physiology of food-restricted captive red crossbills (Loxia curvirostra). Birds were restricted to two short feeding periods per day to simulate a decline in resources and were given social information from food-restricted neighbours either before (i.e. predictive) or during (i.e. parallel) the food-restriction period. Focal birds better conserved body mass during food restriction if social information was predictive of the decline in resources. Crossbills with predictive information ate more food, had larger intestinal mass and better conserved pectoral muscle size at the end of the restriction period compared to those with parallel social information. These data suggest that birds can use social information to alter behavioural and physiological responses during food shortage in ways that may confer an adaptive advantage for survival.

Temperate winters can impose severe conditions on songbirds that threaten survival, including shorter days and often lower temperatures and food availability. One well-studied mechanism by which songbirds cope with such conditions is seasonal acclimatization of thermal metabolic traits, with strong evidence for both preparative and responsive changes in thermogenic capacity (i.e., the ability to generate heat) to low winter temperatures. However, a bird's ability to cope with seasonal extremes or unpredictable events is likely dependent on a combination of behavioral and physiological traits that function to maintain allostatic balance. The ability to cope with reduced food availability may be an important component of organismal response to temperate winters in songbirds. Here, we compare responses to experimentally reduced food availability at different times of year in captive red crossbills (Loxia curvirostra) and pine siskins (Spinus pinus)-two species that cope with variable food resources and live in cold places-to investigate seasonal changes in the organismal response to food availability. Further, red crossbills are known to use social information to improve responses to reduced food availability, so we also examine whether the use of social information in this context varies seasonally in this species. We find that pine siskins and red crossbills lose less body mass during time-restricted feedings in late winter compared to summer, and that red crossbills further benefit from social information gathered from observing other food-restricted red crossbills in both seasons. Observed changes in body mass were only partially explained by seasonal differences in food intake. Our results demonstrate seasonal acclimation to food stress and social information use across seasons in a controlled captive environment and highlight the importance of considering diverse physiological systems (e.g., thermogenic, metabolic, digestive, etc.) to understand organismal responses to environmental challenges.

Small mammals in the temperate area often face fluctuations in food availability. Changes in food availability may have a great influence on an animals' immunity, which is important to their survival. We tested the hypothesis that cellular and humoral immunity would be suppressed by food restriction and restored to control levels by refeeding in Mongolian gerbils Meriones unguiculatus. Forty adult male gerbils were randomly divided into food-restricted (80% of baseline food intake) and food ad lib. groups. Similarly, another 40 adult male gerbils were also randomly assigned to two groups: a group for which food was restricted for 36 d and then provided ad lib. and a group that was continuously fed ad lib. Half of the gerbils in each group were injected with phytohemagglutinin (PHA) and keyhole limpet hemocyanin solution to assess cellular and humoral immunity, respectively; the others were injected with sterile saline as control groups. Food-restricted gerbils had significantly lower body mass, body fat mass, dry thymus mass, wet and dry spleen mass, and serum leptin levels than those of the controls, whereas refeeding restored these parameters to the controls. Both food restriction and refeeding had no significant effect on PHA response indicative of cellular immunity, immunoglobulin G and immunoglobulin M concentrations, and white blood cells. We also found that food restriction decreased corticosterone levels in food-restricted gerbils, while refeeding increased corticosterone levels in refed gerbils compared with the controls. Our results suggest that cellular and humoral immunity were not affected by food restriction and refeeding in gerbils.

Food restriction is a common environmental stressor, and it can have beneficial effects such as increased longevity when applied to non-reproducing adults. At the molecular level, food restriction can have beneficial effects through increased DNA repair, reduced DNA damage and longer telomeres, but a lack of food may also hinder the ability to utilize carotenoids, or antioxidants obtained from diet. When food restriction overlaps with a period of high energetic demand, such as during offspring provisioning, a combination of the two may instigate reproductive trade-offs. In this study, adult zebra finches (Taeniopygia guttata castanotis) were exposed to either ad libitum (control) or 40% restricted (food-restricted) diet while raising their young. Blood samples and beak pictures of parents were taken when birds were paired (before treatment), when their offspring fledged (~13 days on treatment), and when their offspring reached nutritional independence (~40 days on treatment). DNA was extracted from red blood cells to quantify telomere length and DNA damage, RNA was extracted from whole blood to quantify expression of DNA repair genes, and beak pictures were used to quantify beak color as a measure of carotenoids. We found that while provisioning their offspring, food-restricted birds increased the length of their telomeres, while controls did not alter telomere length. However, there was no effect of food restriction on DNA damage, gene expression of Pot1, Neil3, Aptx, or Hspa2, or beak color, and DNA damage and telomere length were not significantly associated with each other. The results of this study suggest that food-restricted parents provisioning offspring are behaviorally calorically restricting themselves and promoting genomic maintenance. Furthermore, the lack of significance in DNA damage and repair under food restriction suggests the relationship between telomeres, oxidative stress, repair mechanisms, and morphometric indicators of antioxidants under food restriction is complex and requires further exploration.

An organism's investment in immune function often varies seasonally but understanding of how fluctuations in environmental conditions directly modulate investment remains limited. This experiment investigated how changes in photoperiod and food availability affect investment in constitutive innate immunity and the acute phase response induced by lipopolysaccharide (LPS) injections in captive red crossbills (Loxia curvirostra). Crossbills are reproductively flexible songbirds that specialize on an unpredictably available food resource and display temporal variation in immunity in the wild. Birds were separated into four treatments and exposed to long or short day lengths for 6weeks before continuing on an ad libitum diet or experiencing a 20% food reduction for 10 days. Birds were un-injected or injected with LPS both before and after diet change. Innate immunity was quantified throughout the experiment to assess effects of photoperiod, food availability and their interactions on hemolysis-hemagglutination, haptoglobin, bacterial killing ability and leukocyte counts. Overall, increasing day length significantly increased both bacterial killing ability and leukocyte counts. Surprisingly, food restriction had little effect on the immune parameters, potentially owing to the 'low-cost' environment of captivity and suggesting that investment in innate immunity is prioritized and maintained whenever possible. LPS injections induced stereotypical sickness behaviors and increased bacterial killing ability in short day birds and complement activity (hemolysis) both before and after food restriction. These results demonstrate robust seasonal modulation of immune investment and an ability to maintain innate immunity in the face of limited resources in these temporally flexible songbirds.

Hematocrit-or the percent volume of red blood cells in whole blood-is thought to fluctuate adaptively in response to changing oxygen demands that occur during different life activities and in different environments. Because red blood cells are made from materials that can be limiting, however, it is thought that hematocrit may also reflect general body condition and access to resources. We tested the effect of hydration state, resource restriction (i.e., time available to forage), and activity (i.e., different cage sizes) on hematocrit in captive red crossbills (Loxia curvirostra). We found no evidence that a mild dehydration protocol impacts hematocrit and only weak support that mild food restriction impacts hematocrit. Food restriction did, however, reduce fat deposits and fat loss was more significant in birds that were also sampled for hematocrit. Furthermore, food-restricted birds housed in flight aviaries recovered hematocrit but not fat stores following repeated blood sampling, whereas birds housed in small cages lost additional hematocrit but mitigated fat loss following successive bleeds. Together these results suggest that different flight demands may determine response to blood loss during food restriction, potentially revealing a trade-off between fat storage and red blood cell development. Our results also demonstrate the need for scientists to carefully record hematocrit data and the time course across which multiple tubes of blood are collected to avoid confounding real patterns with variation generated by sampling protocol.

Abstract:Lizards of the genusAnolishave been widely studied, however, little is known about the effects of environmental seasonality, food availability and geographic isolation on body condition, growth rate and habitat use of lizards. The existence of an insular and a continental population ofAnolis nebulosus(clouded anole), separated by only 0.47 km, represents an ideal opportunity to address this topic. We compared seasonal fluctuations in food availability (arthropod density) for anoles, as well as body condition, growth rate and habitat use in the two populations. Food availability throughout the year was sampled every 2 mo by trapping arthropods at each site. Lizards were also monitored and measured every 2 mo by surveying three quadrats in each site over 2 y giving a total of 30 visits for each quadrat. Results suggested that composition and density of food supply was similar for the two populations. Nevertheless, food supply responded to seasonality of rainfall, with an increase of 1.5 times during the rainy season. Despite similarity in food availability, insular anoles had body condition that was 5–10 times better, with growth rate twice as fast, and used similar perches. The role of predation, and inter- and intraspecific competition are discussed as possible drivers.

Variation in state, which is any factor that alters the value of decision options, is likely one of the most common drivers of personality differences. However, the general relationship between individuals’ body state and various personality metrics/average behavioral type, repeatability of behavior, and behavioral syndrome structure is still poorly resolved. Here, we manipulate body condition in three spider species (Agelenopsis aperta, Latrodectus hesperus, and Anelosimus studiosus) using contrasting feeding schedules. We then assessed the effects of historic feeding regime on individuals’ body condition, boldness, and foraging aggressiveness. We further assessed the effects of feeding regimes on the repeatability of boldness and aggressiveness and the presence/absence of correlations between these two traits. We found that feeding treatment impacted individuals’ average boldness and aggressiveness in two species (A. aperta and A. studiosus). We also noted that among-individual variance in both boldness and aggressiveness was severely reduced when A. aperta and A. studiosus were subjected to prolonged food restriction, steeply reducing repeatability in these traits. Finally, we noted that correlations between boldness and foraging aggressiveness were detectable only in one case, revealing no compelling relationship between food restriction and the presence/absence of behavioral correlations. Taken together, our results suggest that food restriction has only weak, circumstantial effects on individuals’ average personality type and the correlations between behavioral traits. However, there appears to be a robust positive relationship between food availability and the signature of consistent individual differences in behavior. Under laboratory conditions, we found that lower feeding rates sharply decreased the repeatability of aggressiveness and boldness in two spider species. In doing so, we provide the second body of evidence suggesting that a highly prevalent and ecologically relevant state variable, higher body condition, can increase the repeatability of foraging-related behavioral traits. Additionally, under some feeding regimes, we found that hunger levels could alter the average individual aggressiveness and boldness but not correlations between these traits. This work highlights the importance of state variables such as hunger in eroding behavioral repeatability, the defining trait of personality.

Variation in state, which is any factor that alters the value of decision options, is likely one of the most common drivers of personality differences. However, the general relationship between individuals’ body state and various personality metrics/average behavioral type, repeatability of behavior, and behavioral syndrome structure is still poorly resolved. Here, we manipulate body condition in three spider species (Agelenopsis aperta, Latrodectus hesperus, and Anelosimus studiosus) using contrasting feeding schedules. We then assessed the effects of historic feeding regime on individuals’ body condition, boldness, and foraging aggressiveness. We further assessed the effects of feeding regimes on the repeatability of boldness and aggressiveness and the presence/absence of correlations between these two traits. We found that feeding treatment impacted individuals’ average boldness and aggressiveness in two species (A. aperta and A. studiosus). We also noted that among-individual variance in both boldness and aggressiveness was severely reduced when A. aperta and A. studiosus were subjected to prolonged food restriction, steeply reducing repeatability in these traits. Finally, we noted that correlations between boldness and foraging aggressiveness were detectable only in one case, revealing no compelling relationship between food restriction and the presence/absence of behavioral correlations. Taken together, our results suggest that food restriction has only weak, circumstantial effects on individuals’ average personality type and the correlations between behavioral traits. However, there appears to be a robust positive relationship between food availability and the signature of consistent individual differences in behavior. Under laboratory conditions, we found that lower feeding rates sharply decreased the repeatability of aggressiveness and boldness in two spider species. In doing so, we provide the second body of evidence suggesting that a highly prevalent and ecologically relevant state variable, higher body condition, can increase the repeatability of foraging-related behavioral traits. Additionally, under some feeding regimes, we found that hunger levels could alter the average individual aggressiveness and boldness but not correlations between these traits. This work highlights the importance of state variables such as hunger in eroding behavioral repeatability, the defining trait of personality.

Environmental challenges, such as fluctuations in food availability, could influence reproductive investment. If resource availability is poor, individuals need to decide in which life‐history process they invest more energy and vital compounds, which determine the cost of reproduction. In resource allocation, the physiological pathways have important roles. The aim of our study was to examine whether food availability influenced physiological traits (insulin‐like growth factor‐1 (IGF‐1) concentration, antioxidant capacity (OXY), level of oxidative damage (ROM) and haematocrit value) prior to egg‐laying in female canaries Serinus canaria. We also tested whether these physiological traits were associated with traits reflecting the reproductive investment in egg macro‐ (egg mass and yolk mass) and micronutrient content (eggshell biliverdin‐ and protoporphyrin‐based colouration). To test these questions we conducted a food restriction experiment with control and food‐restricted (72% of control food) groups. Our study showed that food‐restricted canary females delayed egg‐laying and the physiological traits differed between the groups. At the pre‐laying period, after 9–11 days of treatment, a reduction in plasma IGF‐1 concentration, ROM level and haematocrit value was detected in the control group, whereas in the food‐restricted group plasma IGF‐1 concentration increased, while ROM level and haematocrit value did not change. Plasma level of OXY was not influenced by treatment or breeding period. Plasma concentration of IGF‐1, haematocrit value and oxidative status before egg laying did not affect the egg characteristics. Our study highlights the importance of breeding stage when studying and interpreting the effects of food restriction on physiological traits of breeding birds. Moreover, our data suggest that nutritional limitation had an effect on the timing of egg‐laying that could be mediated by changes in physiological variables.

Phenotypic flexibility is a central way that organisms cope with challenging and changing environments. As endocrine signals mediate many phenotypic traits, heritable variation in hormone levels, or their context-dependent flexibility, could present an important target for selection. Several studies have estimated the heritability of circulating glucocorticoid levels under acute stress conditions, but little is known about the potential for either baseline hormone levels or rapid endocrine flexibility to evolve. Here, we assessed the potential for selection to operate on the elevation (circulating hormone levels) and flexibility of glucocorticoid reaction norms to acute restraint stress. Multivariate animal models revealed low but significant heritability in baseline (h2 =0.13-0.14) and stress-induced glucocorticoids (h2 =0.18), and moderate heritability in glucocorticoid flexibility in response to acute stress (h2 =0.38) in free-living juvenile tree swallows (Tachycineta bicolor; n=408). Baseline glucocorticoids were not genetically correlated with either stress-induced glucocorticoids or glucocorticoid flexibility. These findings indicate that baseline glucocorticoids and the acute stress response are distinct traits that can be independently shaped by selection. Microevolutionary changes that influence the expression or flexibility of these endocrine mediators of phenotype may be an important way that populations adapt to changing environments and novel threats.

Animals go through different life history stages such as reproduction, moult, or migration, of which some are more energy-demanding than others. Baseline concentrations of glucocorticoid hormones increase during moderate, predictable challenges and thus are expected to be higher when seasonal energy demands increase, such as during reproduction. By contrast, stress-induced glucocorticoids prioritize a survival mode that includes reproductive inhibition. Thus, many species down-regulate stress-induced glucocorticoid concentrations during the breeding season. Interspecific variation in glucocorticoid levels during reproduction has been successfully mapped onto reproductive investment, with species investing strongly in current reproduction (fast pace of life) showing higher baseline and lower stress-induced glucocorticoid concentrations than species that prioritize future reproduction over current attempts (slow pace of life). Here we test the "glucocorticoid seasonal plasticity hypothesis", in which we propose that interspecific variation in seasonal changes in glucocorticoid concentrations from the non-breeding to the breeding season will be related to the degree of reproductive investment (and thus pace of life). We extracted population means for baseline (for 54 species) and stress-induced glucocorticoids (for 32 species) for the breeding and the non-breeding seasons from the database "HormoneBase", also calculating seasonal glucocorticoid changes. We focused on birds because this group offered the largest sample size. Using phylogenetic comparative methods, we first showed that species differed consistently in both average glucocorticoid concentrations and their changes between the two seasons, while controlling for sex, latitude, and hemisphere. Second, as predicted seasonal changes in baseline glucocorticoids were explained by clutch size (our proxy for reproductive investment), with species laying larger clutches showing a greater increase during the breeding season-especially in passerine species. In contrast, changes in seasonal stress-induced levels were not explained by clutch size, but sample sizes were more limited. Our findings highlight that seasonal changes in baseline glucocorticoids are associated with a species' reproductive investment, representing an overlooked physiological trait that may underlie the pace of life.

Glucocorticoid (GC) hormones are important phenotypic mediators across vertebrates, but their circulating concentrations can vary markedly. Here we investigate macroevolutionary patterning in GC levels across tetrapods by testing seven specific hypotheses about GC variation and evaluating whether the supported hypotheses reveal consistent patterns in GC evolution. If selection generally favors the "supportive" role of GCs in responding effectively to challenges, then baseline and/or stress-induced GCs may be higher in challenging contexts. Alternatively, if selection generally favors "protection" from GC-induced costs, GCs may be lower in environments where challenges are more common or severe. The predictors of baseline GCs were all consistent with supportive effects: levels were higher in smaller organisms and in those inhabiting more energetically demanding environments. During breeding, baseline GCs were also higher in populations and species with fewer lifetime opportunities to reproduce. The predictors of stress-induced GCs were instead more consistent with the protection hypothesis: during breeding, levels were lower in organisms with fewer lifetime reproductive opportunities. Overall, these patterns indicate a surprising degree of consistency in how some selective pressures shape GCs across broad taxonomic scales; at the same time, in challenging environments selection appears to operate on baseline and stress-induced GCs in distinct ways.