Individual variation in survival probability due to differential responses to early‐life environmental conditions is important in the evolution of life histories and senescence. A biomarker allowing quantification of such individual variation, and which links early‐life environmental conditions with survival by providing a measure of conditions experienced, is telomere length. Here, we examined telomere dynamics among 24 cohorts of European badgers (Meles meles). We found a complex cross‐sectional relationship between telomere length and age, with no apparent loss over the first 29 months, but with both decreases and increases in telomere length at older ages. Overall, we found low within‐individual consistency in telomere length across individual lifetimes. Importantly, we also observed increases in telomere length within individuals, which could not be explained by measurement error alone. We found no significant sex differences in telomere length, and provide evidence that early‐life telomere length predicts lifespan. However, while early‐life telomere length predicted survival to adulthood (≥1 year old), early‐life telomere length did not predict adult survival probability. Furthermore, adult telomere length did not predict survival to the subsequent year. These results show that the relationship between early‐life telomere length and lifespan was driven by conditions in early‐life, where early‐life telomere length varied strongly among cohorts. Our data provide evidence for associations between early‐life telomere length and individual life history, and highlight the dynamics of telomere length across individual lifetimes due to individuals experiencing different early‐life environments.
Understanding individual variation in fitness‐related traits requires separating the environmental and genetic determinants. Telomeres are protective caps at the ends of chromosomes that are thought to be a biomarker of senescence as their length predicts mortality risk and reflect the physiological consequences of environmental conditions. The relative contribution of genetic and environmental factors to individual variation in telomere length is, however, unclear, yet important for understanding its evolutionary dynamics. In particular, the evidence for transgenerational effects, in terms of parental age at conception, on telomere length is mixed. Here, we investigate the heritability of telomere length, using the ‘animal model’, and parental age at conception effects on offspring telomere length in a wild population of European badgers (Meles meles). Although we found no heritability of telomere length and low evolvability (<0.001), our power to detect heritability was low and a repeatability of 2% across individual lifetimes provides a low upper limit to ordinary narrow‐sense heritability. However, year (32%) and cohort (3%) explained greater proportions of the phenotypic variance in telomere length, excluding qPCR plate and row variances. There was no support for cross‐sectional or within‐individual parental age at conception effects on offspring telomere length. Our results indicate a lack of transgenerational effects through parental age at conception and a low potential for evolutionary change in telomere length in this population. Instead, we provide evidence that individual variation in telomere length is largely driven by environmental variation in this wild mammal.
Early-life environmental conditions can provide a source of individual variation in life-history strategies and senescence patterns. Conditions experienced in early life can be quantified by measuring telomere length, which can act as a biomarker of survival probability. Here, we investigate whether seasonal changes, weather conditions, and group size are associated with early-life and/or early-adulthood telomere length in a wild population of European badgers (Meles meles). We found substantial intraannual changes in telomere length during the first three years of life (both between and within individuals), with shorter telomere lengths from spring to winter and longer telomere lengths over the 2 winter torpor period. In terms of weather conditions, linked to food availability and foraging success, cubs born in warmer, wetter springs with low rainfall variability had longer early-life (<1 year old) telomere lengths. Additionally, cubs born in groups with more cubs did not have significantly shorter early-life telomeres, providing no evidence of resource constraint from cub competition. We also found that our previously documented positive association between early-life telomere length and cub survival probability remained when social and weather variables were included. Finally, after sexual maturity, in early adulthood (i.e. 12-36 months) we found no significant association between same-sex adult group size and telomere length (i.e. no effect of intra-sexual competition). Overall we show that controlling for seasonal effects is important in telomere length analyses, and that badger telomere length functions as a biomarker that reflects the physiological consequences of early-life adversity and subsequent effects on cub survival probability.
Evidence for age-related changes in innate and adaptive immune responses is increasing in wild populations. Such changes have been linked to fitness, and knowledge of the factors driving immune response variation is important for understanding the evolution of immunity. Age-related changes in immune profiles may be owing to factors such as immune system development, sex-specific behaviour and responses to environmental conditions. Social environments may also contribute to variation in immunological responses, for example, through transmission of pathogens and stress arising from resource and mate competition. Yet, the impact of the social environment on age-related changes in immune cell profiles is currently understudied in the wild. Here, we tested the relationship between leukocyte cell composition (proportion of neutrophils and lymphocytes [innate and adaptive immunity, respectively] that were lymphocytes) and age, sex and group size in a wild population of European badgers ( Meles meles ). We found that the proportion of lymphocytes in early life was greater in males in smaller groups compared to larger groups, but with a faster age-related decline in smaller groups. By contrast, the proportion of lymphocytes in females was not significantly related to age or group size. Our results provide evidence of sex-specific age-related changes in immune cell profiles in a wild mammal, which are influenced by the social environment.
Evidence for age-related changes in innate and adaptive immune responses is increasing in wild populations. Such changes have been linked to fitness, and understanding the factors driving variation in immune responses is important for the evolution of immunity and senescence. Age-related changes in immune profiles may be due to sex-specific behaviour, physiology and responses to environmental conditions. Social conditions may also contribute to variation in immunological responses, for example, through transmission of pathogens and stress from resource and mate competition. Yet, the impact of the social environment on age-related changes in immune cell profile requires further investigation in the wild. Here, we tested the relationship between leukocyte cell composition (agranulocyte proportion, i.e. adaptive and innate immunity) and age, sex, and group size in a wild population of European badgers (Meles meles). We found that the proportion of agranulocytes decreased with age only in males living in small groups. In contrast, females in larger groups exhibited a greater age-related decline in the proportion of agranulocytes compared to females in smaller groups. Our results provide evidence for age-related changes in immune cell profiles in a wild mammal, which are influenced by both the sex of the individual and their social environment.
The longitudinal study of populations is a core tool for understanding ecological and evolutionary processes. Long‐term studies typically collect samples repeatedly over individual lifetimes and across generations. These samples are then analysed in batches (e.g. qPCR plates) and clusters (i.e. group of batches) over time in the laboratory. However, these analyses are constrained by cross‐classified data structures introduced biologically or through experimental design. The separation of biological variation from the confounding among‐batch and among‐cluster variation is crucial, yet often ignored. The commonly used approaches to structuring samples for analysis, sequential and randomization, generate bias due to the non‐independence between time of collection and the batch and cluster they are analysed in. We propose a new sample structuring strategy, called slicing, designed to separate confounding among‐batch and among‐cluster variation from biological variation. Through simulations, we tested the statistical power and precision to detect within‐individual, between‐individual, year and cohort effects of this novel approach. Our slicing approach, whereby recently and previously collected samples are sequentially analysed in clusters together, enables the statistical separation of collection time and cluster effects by bridging clusters together, for which we provide a case study. Our simulations show, with reasonable slicing width and angle, similar precision and similar or greater statistical power to detect year, cohort, within‐ and between‐individual effects when samples are sliced across batches, compared with strategies that aggregate longitudinal samples or use randomized allocation. While the best approach to analysing long‐term datasets depends on the structure of the data and questions of interest, it is vital to account for confounding among‐cluster and batch variation. Our slicing approach is simple to apply and creates the necessary statistical independence of batch and cluster from environmental or biological variables of interest. Crucially, it allows sequential analysis of samples and flexible inclusion of current data in later analyses without completely confounding the analysis. Our approach maximizes the scientific value of every sample, as each will optimally contribute to unbiased statistical inference from the data. Slicing thereby maximizes the power of growing biobanks to address important ecological, epidemiological and evolutionary questions.
Understanding individual variation in fitness-related traits requires separating the environmental and genetic determinants. Telomeres are protective caps at the ends of chromosomes that are thought to be a biomarker of senescence as their length predicts mortality risk and reflect the physiological consequences of environmental conditions. The relative contribution of genetic and environmental factors to individual variation in telomere length is however unclear, yet important for understanding its evolutionary dynamics. In particular, the evidence for transgenerational effects, in terms of parental age at conception, on telomere length is mixed. Here, we investigate the heritability of telomere length, using the ‘animal model’, and parental age at conception effects on offspring telomere length in a wild population of European badgers (Meles meles). While we found no heritability of telomere length, our power to detect heritability was low and a repeatability of 2% across individual lifetimes provides a low upper limit to ordinary heritability. However, year (25%) and cohort (3%) explained greater proportions of the phenotypic variance in telomere length. There was no support for parental age at conception effects, or for longitudinal within-parental age effects on offspring telomere length. Our results indicate a lack of transgenerational effects through parental age at conception and a low potential for evolutionary change in telomere length in this population. Instead, we provide evidence that individual variation in telomere length is largely driven by environmental variation in this wild mammal.
Early-life environmental conditions can provide a source of individual variation in life-history strategies and senescence patterns. Conditions experienced in early life can be quantified by measuring telomere length, which can act as a biomarker of survival probability. Here, we investigate whether seasonal changes, weather conditions, and group size are associated with early-life and/or early-adulthood telomere length in a wild population of European badgers (Meles meles). We found substantial intra-annual changes in telomere length during the first three years of life (both between and within individuals), with shorter telomere lengths from spring to winter and longer telomere lengths over the winter torpor period. In terms of weather conditions, linked to food availability and foraging success, cubs born in warmer, wetter springs with low rainfall variability had longer early-life (<1 year old) telomere lengths. Additionally, cubs born in groups with more cubs did not have significantly shorter early-life telomeres, providing no evidence of resource constraint from cub competition. We also found that our previously documented positive association between early-life telomere length and cub survival probability remained when social and weather variables were included. Finally, after sexual maturity, in early adulthood (i.e. 12–36 months) we found no significant association between same-sex adult group size and telomere length (i.e. no effect of intra-sexual competition). Overall we show that controlling for seasonal effects is important in telomere length analyses, and that badger telomere length functions as a biomarker that reflects the physiological consequences of early-life adversity and subsequent effects on cub survival probability.
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