Telomeres are regarded as important biomarkers of ageing and serve as useful tools in revealing how stress acts at the cellular level. However, the effects of social and ecological factors on telomere length remain poorly understood, particularly in free-ranging mammals. Here, we investigated the influences of within-group dominance rank and group membership on telomere length in wild adult spotted hyenas (Crocuta crocuta). We found large effects of both factors; high-ranking hyenas exhibited significantly greater mean telomere length than did subordinate animals, and group membership significantly predicted mean telomere length within high-ranking females. We further inquired whether prey availability mediates the observed effect of group membership on telomere length, but this hypothesis was not supported. Interestingly, adult telomere length was not predicted by age. Our work shows for the first time, to the best of our knowledge, the effects of social rank on telomere length in a wild mammal and enhances our understanding of how social and ecological variables may contribute to organismal senescence.
Elevated levels of maternal androgens in avian eggs affect numerous traits, including oxidative stress. However, current studies disagree as to whether prenatal androgen exposure enhances or ameliorates oxidative stress. Here, we tested how prenatal testosterone exposure affects oxidative stress in female domestic chickens (Gallus gallus) during the known oxidative challenge of an acute stressor. Prior to incubation, eggs were either injected with an oil vehicle or 5 ng testosterone. At either 17 or 18 days post-hatch, several oxidative stress markers were assessed from blood taken before and after a 20 min acute stressor, as well as following a 25 min recovery from the stressor. We found that, regardless of yolk treatment, during both stress and recovery all individuals were in a state of oxidative stress, with elevated levels of oxidative damage markers accompanied by a reduced total antioxidant capacity. In addition, testosterone-exposed individuals exhibited poorer DNA damage repair efficiencies in comparison with control individuals. Our work suggests that while yolk androgens do not alter oxidative stress directly, they may impair mechanisms of oxidative damage repair.
Flight of nocturnal insects may be limited by cool nighttime environmental temperatures. We used laboratory and field experiments to explore the thermal basis of nocturnal flight in wing‐polymorphic Gryllus lineaticeps crickets consisting of long‐winged (LW), flight‐capable morphs and short‐winged (SW), flight‐incapable morphs. These crickets are a model for life history evolution and loss of flight, but their thermal requirements for flight have been unknown. We hypothesized that LW crickets achieve warm body temperatures required for flight through a combination of behavioural thermoregulation, producing heat endogenously (either by initiating muscular thermogenesis or increasing resting metabolic rate) and minimizing heat loss (by circulatory adjustments or insulation). Summer evening air temperatures in the field gradually declined from 25 to 18°C during the hours of nighttime cricket activity. Laboratory LW crickets did not fly at a body temperature of 18°C, and 60% flew at 25°C. In an experimental thermal gradient, spontaneous flight did not occur until body temperature exceeded 35°C, confirming that nocturnal field air temperature limits flight in this species. In a thermal gradient, LW crickets preferred higher temperatures (~36°C) than SW crickets (~32.5°C). In the field, all crickets were warmer than air temperature but considerably cooler than their preferred temperatures. LW crickets had higher field body temperatures (24.3°C) than SW crickets (22.3°C). LW crickets spontaneously initiated muscular thermogenesis through wing vibrations, increasing body temperature to a pre‐flight maximum of 35°C. Muscular thermogenesis was limited below 25°C. LW crickets cooled more slowly and had higher metabolic rates than SW crickets. We conclude that LW crickets prepare to fly on cool nights by gaining heat from warm substrates, activating endogenous muscular thermogenesis and reducing their cooling rate. These mechanisms are absent or less pronounced in SW crickets. The overall thermoregulatory strategy we report represents a previously unrecognized component of insect dispersal polymorphism. We suggest that thermal constraints on nocturnal flight may have contributed to evolutionary loss of flight in other insect groups. A free Plain Language Summary can be found within the Supporting Information of this article.
Animals adjust resource acquisition throughout life to meet changing physiological demands of growth, reproduction, activity and somatic maintenance. Wing-polymorphic crickets invest in either dispersal or reproduction during early adulthood, providing a system in which to determine how variation in physiological demands, determined by sex and life history strategy, impact nutritional targets, plus the consequences of nutritionally imbalanced diets across life stages. We hypothesized that high demands of biosynthesis (especially oogenesis in females) drive elevated resource acquisition requirements and confer vulnerability to imbalanced diets. Nutrient targets and allocation into key tissues associated with life history investments were determined for juvenile and adult male and female field crickets (Gryllus lineaticeps) when given a choice between two calorically equivalent but nutritionally imbalanced (protein- or carbohydrate-biased) artificial diets, or when restricted to one imbalanced diet. Flight muscle synthesis drove elevated general caloric requirements for juveniles investing in dispersal, but flight muscle quality was robust to imbalanced diets. Testes synthesis was not costly, and life history investments by males were insensitive to diet composition. In contrast, costs of ovarian synthesis drove elevated caloric and protein requirements for adult females. When constrained to a carbohydrate-biased diet, ovary synthesis was reduced in reproductive morph females, eliminating their advantage in early life fecundity over the dispersal morph. Our findings demonstrate that nutrient acquisition modulates dispersal–reproduction trade-offs in an age- and sex-specific manner. Declines in food quality will thus disproportionately affect specific cohorts, potentially driving demographic shifts and altering patterns of life history evolution.
Organismal performance directly depends on an individual's ability to cope with a wide array of physiological challenges. For social animals, social isolation is a stressor that has been shown to increase oxidative stress. Another physiological challenge, routine locomotor activity, has been found to decrease oxidative stress levels. Because we currently do not have a good understanding of how diverse physiological systems like stress and locomotion interact to affect oxidative balance, we studied this interaction in the prairie vole (Microtus ochrogaster). Voles were either pair housed or isolated and within the isolation group, voles either had access to a moving wheel or a stationary wheel. We found that chronic periodic isolation caused increased levels of oxidative stress. However, within the vole group that was able to run voluntarily, longer durations of locomotor activity were associated with less oxidative stress. Our work suggests that individuals who demonstrate increased locomotor activity may be better able to cope with the social stressor of isolation.
Our understanding of how oxidative stress resistance phenotypes are affected by the developmental environment is limited. One component of the developmental environment, which is likely central to early life oxidative stress among ectothermic and oviparous species, is that of temperature. We investigated how incubation temperature manipulations affect oxidative damage and total antioxidant capacity (TAC) in red-eared slider turtle (Trachemys scripta elegans) hatchlings. First, to determine whether temperature fluctuations elicit oxidative stress, eggs from clutches were randomly assigned to either a constant (29.5°C) or daily fluctuating temperature incubation (28.7±3°C) treatment. Second, to assess the effect of temperature fluctuation frequency on oxidative stress, eggs were incubated in one of three fluctuating incubation regimes: 28.7±3°C fluctuations every 12 h (hyper), 24 h (normal) or 48 h (hypo). Third, we tested the influence of average incubation temperature by incubating eggs in a daily fluctuating incubation temperature regime with a mean temperature of 26.5°C (low), 27.1°C (medium) or 27.7°C (high). Although the accumulation of oxidative damage in hatchlings was unaffected by any thermal manipulation, TAC was affected by both temperature fluctuation frequency and average incubation temperature. Individuals incubated with a low frequency of temperature fluctuations had reduced TAC, while incubation at a lower average temperature was associated with enhanced TAC. These results indicate that although sufficient to prevent oxidative damage, TAC is influenced by developmental thermal environments, potentially because of temperature-mediated changes in metabolic rate. The observed differences in TAC may have important future consequences for hatchling fitness and overwinter survival.
The emergency life-history stage (ELHS) can be divided into two subcategories that describe distinct, coordinated responses to disease- or non-disease-related physiological challenges. Whether an individual can simultaneously express aspects of both subcategories when faced with multiple challenges is poorly understood. Emergency life-history theory suggests that disease- and non-disease-related responses are coordinated at the level of the whole organism and therefore cannot be expressed simultaneously. However, the reactive scope and physiological regulatory network models suggest that traits can be independently regulated, allowing for components of both disease- and non-disease-related responses to be simultaneously expressed within a single organism. To test these ideas experimentally, we subjected female zebra finches to food deprivation, an immune challenge, both, or neither, and measured a suite of behavioural and physiological traits involved in the ELHS. We examined whether the trait values expressed by birds experiencing simultaneous challenges resembled trait values of birds experiencing a single challenge or if birds could express a mixture of trait values concurrently. We find that birds can respond to simultaneous challenges by regulating components of the behavioural and immune responses independently of one another. Modularity within these physio-behavioural networks adds additional dimensions to how we evaluate the intensity or quality of an ELHS. Whether modularity provides fitness advantages or costs in nature remains to be determined.
Life history and metabolism covary, but the mechanisms and individual traits responsible for these linkages remain unresolved. Dispersal capability is a critical component of life history that is constrained by metabolic capacities for energy production. Conflicting relationships between metabolism and life histories may be explained by accounting for variation in dispersal and maximal metabolic rates. We used female wing‐polymorphic sand field crickets, Gryllus firmus, selected either for long wings (LW, flight‐capable) or short wings (SW, flightless) to test the hypothesis that selection on dispersal capability drives the evolution of metabolic capacities. While resting metabolic rates were similar, long‐winged crickets reached higher maximal metabolic rates than short‐winged crickets, resulting in improved running performance. We further provided insight into the mechanisms responsible for covariation between life history and metabolism by comparing mitochondrial content of tissues involved in powering locomotion and assessing the function of mitochondria isolated from long‐ and short‐winged crickets. Our results demonstrated that larger metabolic capacities in long‐winged crickets were underpinned by increases in mitochondrial content of dorsoventral flight muscle and enhanced bioenergetic capacities of mitochondria within the fat body, a tissue responsible for fuel storage and mobilization. Thus, selection on flight capability correlates with increases in maximal, but not resting metabolic rates, through modifications of tissues powering locomotion at the cellular and organelle levels. This allows organisms to meet high energetic demands of activity for life history. Dispersal capability should therefore explicitly be considered as a potential factor driving the evolution of metabolic capacities.
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