Conventional physiological research has focused on elucidating the endogenous mechanisms that underly the adaptations of species to life in extreme habitats, such as polar regions or deserts. In this review article, we argue that even habitats that are not considered extremes are facing unpredictable, rapid, and strong modifications due to human activities that expose animals to novel extreme conditions. Thus, physiological research on these animals can offer insight on the role of physiological plasticity in driving their resilience and adaptation. To this end, we discuss how stress physiology (with a particular focus on oxidative stress) has a central role in mediating the interaction between the exposome (measure of all the environmental exposures of an individual in a lifetime) and cellular processes (bio-exposome) in the contexts of relevant extreme anthropogenic changes to the habitat conditions. We also provide concrete examples on the relationship between oxidative stress and the bio-exposome in free-living animals, and how this research can be relevant to human health. Finally, we propose future research directions integrating the bio-exposome and the One Health framework to achieve a holistic understanding of the proximate mechanisms underlying individual responses to extreme anthropogenic environmental changes.

Salinization is predicted to intensify due to climate change, impacting biodiversity and ecosystem functioning. Amphibians, particularly embryos and larvae, are highly susceptible to environmental salinity. Yet, local adaptation may cause differing vulnerabilities between coastal and inland populations. In this study, we investigated the physiological, behavioural, and life-history responses to environmental salinity (0, 2 and 4 g l-1) of embryos and larvae of a widespread amphibian species (spined toad, Bufo spinosus) from salt-exposed (coastal) and salt-free (inland) populations. Moderate salinity (4 g l-1) altered embryonic and larval development in both populations, causing increased malformations, decreased body size and survival, and altered behavior, but did not affect telomere length or oxidative status. Individuals exposed to low salinity (2 g l-1) performed better across most traits. However, moderate salinity had stronger negative effects on coastal individuals, indicating a lack of local adaptation and overall lower performance compared to their inland counterparts. These findings suggest that increasing salinity will have varied impacts on organisms depending on their population origins and developmental stages.

We investigate a historical experience to measure the long-term effect of malaria on lifespan among infected survivors and identify a factor that mitigates malaria's effect. Using a sample of Union Army veterans born during the mid-19th century and their lifetime records, we show that exposure to high risk of malaria at birth or in early life substantially shortened their lifespan. The legacy of exposure to malaria is robust while controlling for lifetime socioeconomic and health conditions, fixed effects, and considering selection bias. Additionally, we include the US Colored Troops sample of black veterans to analyze racial differences in the effect of malaria exposure on lifespan. Exposure to malaria did not lead to a shorter lifespan among black veterans. Evidence suggests that genetic immunity to malaria in black veterans might contribute this heterogeneity.

The biological mechanisms that explain how adverse early life events influence adult disease risk are poorly understood. One proposed mechanism is via the induction of accelerated biological aging, for which telomere length is considered a biomarker. We aimed to determine if maternal depression pre- and post-partum was associated with telomere length in children at 4 years of age (n = 4299). Mothers completed structured questionnaires assessing depression during pregnancy (Edinburgh Depression Scale), at 9 months (Edinburgh Depression Scale), and at 54 months postpartum (Patient Health Questionnaire 9). Regression methods were used to investigate the relationship between telomere length (DNA from saliva) and maternal depression score recorded at each stage. Significant covariates included in the final model were: maternal age at pregnancy; child sex; child ethnicity; gestational age group, and rurality group. Child telomere length was found to be longer if their mother had a higher depression score at both postpartum time points tested (9 months of age; coefficient 0.003, SE = 0.001, P = 0.01, 54 months of age; coefficient 0.003, SE = 0.002, P = 0.02). Although these findings seem paradoxical, increased telomere length may be an adaptive response to early life stressors. We propose several testable hypotheses for these results and to determine if the positive association between depression and telomere length is a developmental adaptation or an indirect consequence of environmental factors.

The early stages of life, especially the period from conception to two years, are crucial for shaping metabolic health and the risk of obesity in adulthood. Adipose tissue (AT) plays a crucial role in regulating energy homeostasis and metabolism, and brown AT (BAT) and the browning of white AT (WAT) are promising targets for combating weight gain. Nutritional factors during prenatal and early postnatal stages can influence the development of AT, affecting the likelihood of obesity later on. This narrative review focuses on the nutritional programming of AT features. Research conducted across various animal models with diverse interventions has provided insights into the effects of specific compounds on AT development and function, influencing the development of crucial structures and neuroendocrine circuits responsible for energy balance. The hormone leptin has been identified as an essential nutrient during lactation for healthy metabolic programming against obesity development in adults. Studies have also highlighted that maternal supplementation with polyunsaturated fatty acids (PUFAs), vitamin A, nicotinamide riboside, and polyphenols during pregnancy and lactation, as well as offspring supplementation with myo-inositol, vitamin A, nicotinamide riboside, and resveratrol during the suckling period, can impact AT features and long-term health outcomes and help understand predisposition to obesity later in life.

Telomere length and dynamics are commonly used biomarkers of somatic state, yet the role of telomeres underlying the aging process is still debated. Indeed, to date, empirical evidence for an association between age and telomere length is mixed. Here, we test if the age-dependency of the association between age and telomere length can provide a potential explanation for the reported inconsistencies across studies. To this end, we quantified telomere length by telomere restriction fragment analysis in two groups of Japanese quail (Coturnix japonica) that differed in their age distribution. One group consisted of young adults only, whereas the second group consisted of adults across a wide range of ages. In the young adults group, there was a highly significant negative association between telomere length and age, whereas no association between age and telomere length was found in the all-ages adults group. This difference between groups was not due to telomere length-dependent selective disappearance. Our results shows that the association between telomere length and age is age-dependent and suggest that the costs and benefits associated with telomere maintenance are dynamic across an individual's life course.

In evolutionary ecology, two classes of explanations are frequently invoked to explain "early life effects" on adult outcomes. Developmental constraints (DC) explanations contend that costs of early adversity arise from limitations adversity places on optimal development. Adaptive response (AR) hypotheses propose that later life outcomes will be worse when early and adult environments are poorly "matched." Here, we use recently proposed mathematical definitions for these hypotheses and a quadratic-regression based approach to test the long-term consequences of variation in developmental environments on fertility in wild baboons. We evaluate whether low rainfall and/or dominance rank during development predict three female fertility measures in adulthood, and whether any observed relationships are consistent with DC and/or AR. Neither rainfall during development nor the difference between rainfall in development and adulthood predicted any fertility measures. Females who were low-ranking during development had an elevated risk of losing infants later in life, and greater change in rank between development and adulthood predicted greater risk of infant loss. However, both effects were statistically marginal and consistent with alternative explanations, including adult environmental quality effects. Consequently, our data do not provide compelling support for either of these common explanations for the evolution of early life effects.

Telomeres are short repetitive DNA sequences capping the ends of chromosomes. Telomere shortening occurs during cell division and may be accelerated by oxidative damage or ameliorated by telomere maintenance mechanisms. Consequently, telomere length changes with age, which was recently confirmed in a large meta-analysis across vertebrates. However, based on the correlation between telomere length and age, it was concluded that telomere length can be used as a tool for chronological age estimation in animals. Correlation should not be confused with predictability, and the current data and studies suggest that telomeres cannot be used to reliably predict individual chronological age. There are biological reasons for why there is large individual variation in telomere dynamics, which is mainly due to high susceptibility to a wide range of environmental, but also genetic factors, rendering telomeres unfeasible as a tool for age estimation. The use of telomeres for chronological age estimation is largely a misguided effort, but its occasional reappearance in the literature raises concerns that it will mislead resources in wildlife conservation.

Telomeres, the repetitive DNA regions that protect the ends of chromosomes, and their shortening have been linked to key life history trade-offs among growth, reproduction and lifespan. In contrast to most endotherms, many ectotherms can compensate for telomere shortening throughout life by upregulation of telomerase in somatic tissues. However, during development, marked by rapid growth and an increased sensitivity to extrinsic factors, the upregulation of telomerase may be overwhelmed, resulting in long-term impacts on telomere dynamics. In ectotherms, one extrinsic factor that may play a particularly important role in development is temperature. Here, we investigated the influence of developmental temperature and sex on early-life telomere dynamics in an oviparous ectotherm, Lacerta agilis. While there was no effect of developmental temperature on telomere length at hatching, there were subsequent effects on telomere maintenance capacity, with individuals incubated at warm temperatures exhibiting less telomere maintenance compared with cool-incubated individuals. Telomere dynamics were also sexually dimorphic, with females having longer telomeres and greater telomere maintenance compared with males. We suggest that selection drives this sexual dimorphism in telomere maintenance, in which females maximise their lifetime reproductive success by investing in traits promoting longevity such as maintenance, while males invest in short-term reproductive gains through a polygynous mating behaviour. These early-life effects, therefore, have the potential to mediate life-long changes to life histories.

Telomere length and telomere shortening are thought to be critical cellular attributes and processes that are related to an individual's life span and fitness. The general pattern across most taxa is that after birth telomere length gradually decreases with age. Telomere protection and restoration mechanisms are usually assumed to reduce the rate of shortening or at most keep telomere length constant. However, here we have compiled a list of 26 articles showing that there is an increasing number of studies reporting apparent elongation of telomeres (i.e., a net increase in TL from timet to timet+1) often in a considerable proportion of the individuals studied. Moreover, the few studies which have studied telomere elongation in detail show that increases in telomere length are unlikely to be due to measurement error alone. In this article, we argue that episodes of telomere elongation deserve more attention as they could reflect individual strategies to optimise life histories and maximise fitness, which may not be reflected in the overall telomere dynamics patterns. We propose that patterns of telomere (net) elongation may be partly determined by other factors than those causing telomere shortening, and therefore deserve analyses specifically targeted to investigate the occurrence of telomere elongation. We elaborate on two ecological hypotheses that have been proposed to explain patterns of telomere elongation (the 'excess resources elongation' and the 'last resort elongation' hypothesis) and we discuss the current evidence for (or against) these hypotheses and propose ways to test them.

Telomere dynamics in hibernating species are known to reflect seasonal changes in somatic maintenance. Throughout hibernation, the periodic states of rewarming, known as inter-bout euthermia or arousals, are associated with high metabolic costs including shortening of telomeres. In the active season, if high energetic resources are available, telomere length can be restored in preparation for the upcoming winter. The mechanism for telomere elongation has not been clearly demonstrated, although the action of the ribonucleoprotein complex, telomerase, has been implicated in many species. Here we tested for levels of telomerase activity in the garden dormouse (Eliomys quercinus) at different seasonal time points throughout the year and across ages from liver tissues of male juveniles to adults. We found that telomerase is active at high levels across seasons (during torpor and inter-bout euthermia, plus in the active season) but that there was a substantial decrease in activity in the month prior to hibernation. Telomerase levels were consistent across age groups and were independent of feeding regime and time of birth (early or late born). The changes in activity levels that we detected were broadly associated with changes in telomere lengths measured in the same tissues. We hypothesise that i) telomerase is the mechanism used by garden dormice for maintenance of telomeres and that ii) activity is kept at high levels throughout the year until pre-hibernation when resources are diverted to increasing fat reserves for overwintering. We found no evidence for a decrease in telomerase activity with age or a final increase in telomere length which has been detected in other hibernating rodents.

In wild vertebrates, the increase of breeding success with advancing age has been extensively studied through laying date, clutch size, hatching success, and fledging success. However, to better evaluate the influence of age on reproductive performance in species with high reproductive success, assessing not only reproductive success but also other proxies of reproductive performance appear crucial. For example, the quality of developmental conditions and offspring phenotype can provide robust and complementary information on reproductive performance. In long-lived vertebrate species, several proxies of developmental conditions can be used to estimate the quality of the produced offspring (i.e., body size, body condition, corticosterone levels, and telomere length), and therefore, their probability to survive. By sampling chicks reared by known-aged mothers, we investigated the influence of maternal age on reproductive performance and offspring quality in a long-lived bird species, the snow petrel (Pagodroma nivea). Older females bred and left their chick alone earlier. Moreover, older females had larger chicks that grew faster, and ultimately, those chicks had a higher survival probability at the nest. In addition, older mothers produced chicks with a higher sensitivity to stress, as shown by moderately higher stress-induced corticosterone levels. Overall, our study demonstrated that maternal age is correlated to reproductive performance (hatching date, duration of the guarding period and survival) and offspring quality (body size, growth rate and sensitivity to stress), suggesting that older individuals provide better parental cares to their offspring. These results also demonstrate that maternal age can affect the offspring phenotype with potential long-term consequences.

Telomeres are chromosome protectors that shorten during eukaryotic cell replication and in stressful conditions. Developing individuals are susceptible to telomere erosion when their growth is fast and resources are limited. This is critical because the rate of telomere attrition in early life is linked to health and life span of adults. The metabolic telomere attrition hypothesis (MeTA) suggests that telomere dynamics can respond to biochemical signals conveying information about the organism's energetic state. Among these signals are glucocorticoids, hormones that promote catabolic processes, potentially impairing costly telomere maintenance, and nucleotides, which activate anabolic pathways through the cellular enzyme target of rapamycin (TOR), thus preventing telomere attrition. During the energetically demanding growth phase, the regulation of telomeres in response to two contrasting signals - one promoting telomere maintenance and the other attrition - provides an ideal experimental setting to test the MeTA. We studied nestlings of a rapidly developing free-living passerine, the great tit (Parus major), that either received glucocorticoids (Cort-chicks), nucleotides (Nuc-chicks) or a combination of both (NucCort-chicks), comparing these with controls (Cnt-chicks). As expected, Cort-chicks showed telomere attrition, while NucCort- and Nuc-chicks did not. NucCort-chicks was the only group showing increased expression of a proxy for TOR activation (the gene TELO2), of mitochondrial enzymes linked to ATP production (cytochrome oxidase and ATP-synthase) and a higher efficiency in aerobically producing ATP. NucCort-chicks had also a higher expression of telomere maintenance genes (shelterin protein TERF2 and telomerase TERT) and of enzymatic antioxidant genes (glutathione peroxidase and superoxide dismutase). The findings show that nucleotide availability is crucial for preventing telomere erosion during fast growth in stressful environments.

Telomere length (TL) attrition is related to chronic disease risk. However, less is known on whether TL predicts infectious outcomes, especially in childhood. We examined whether leukocyte TL (LTL) was associated with subsequent infectious morbidity in schoolchildren.

We assessed LTL in 717 Colombian children 5-12 years-old at the beginning of a school year and followed them through the year for daily occurrence of common infection symptoms and doctor visits. We estimated adjusted incidence rate ratios (IRR) with 95% confidence intervals (CI) of gastrointestinal and respiratory syndromes for quartiles of standardized LTL Z score and per unit LTL Z score.

A longer LTL was associated with increased incidence of all infectious morbidity syndromes considered. Adjusted IRR (95% CI) per unit LTL Z score were 1.55 (1.20, 2.00) for diarrhea with vomiting, 1.34 (1.13, 1.60) for cough with fever, 1.70 (1.28, 2.28) for ear infection, and 1.66 (1.36, 2.02) for doctor visits with symptoms.

Longer LTL is related to increased incidence of common infectious morbidities in middle childhood.

In many species, individuals that experience harsh conditions during development have poor health and fitness outcomes in adulthood, compared with peers that do not. These early-life contributions to inequality are often attributed to two classes of evolutionary hypotheses: Developmental Constraints (DC) models, which focus on the deleterious effects of low-quality early-life environments, and Predictive Adaptive Response (PAR) hypotheses, which emphasize the costs individuals incur when they make incorrect predictions about conditions in adulthood. Testing these hypotheses empirically is difficult for conceptual and analytical reasons. Here, we help resolve some of these difficulties by providing mathematical definitions for DC, PAR (particularly focusing on 'external' PAR) and related concepts. We propose a novel, quadratic regression-based statistical test derived from these definitions. Our simulations show that this approach markedly improves the ability to discriminate between DC and PAR hypotheses relative to the status quo approach, which uses interaction effects. Simulated data indicate that the interaction effects approach often conflates PAR with DC, while the quadratic regression approach yields high sensitivity and specificity for detecting PAR. Our results highlight the value of linking verbal and visual models to a formal mathematical treatment for understanding the developmental origins of inequitable adult outcomes. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Understanding if and how individuals and populations cope with environmental change is an enduring question in evolutionary ecology that has renewed importance given the pace of change in the Anthropocene. Two evolutionary strategies of coping with environmental change may be particularly important in rapidly changing environments: adaptive phenotypic plasticity and/or bet hedging. Adaptive plasticity could enable individuals to match their phenotypes to the expected environment if there is an accurate cue predicting the selective environment. Diversifying bet hedging involves the production of seemingly random phenotypes in an unpredictable environment, some of which may be adaptive. Here, I review the central role of the hypothalamic-pituitary-adrenal (HPA) axis and glucocorticoids (GCs) in enabling vertebrates to cope with environmental change through adaptive plasticity and bet hedging. I first describe how the HPA axis mediates three types of adaptive plasticity to cope with environmental change (evasion, tolerance, recovery) over short timescales (e.g., 1-3 generations) before discussing how the implications of GCs on phenotype integration may depend upon the timescale under consideration. GCs can promote adaptive phenotypic integration, but their effects on phenotypic co-variation could also limit the dimensions of phenotypic space explored by animals over longer timescales. Finally, I discuss how organismal responses to environmental stressors can act as a bet hedging mechanism and therefore enhance evolvability by increasing genetic or phenotypic variability or reducing patterns of genetic and phenotypic co-variance. Together, this emphasizes the crucial role of the HPA axis in understanding fundamental questions in evolutionary ecology.

Telomeres, the nucleotide sequences that protect the ends of eukaryotic chromosomes, shorten with each cell division and telomere loss may be influenced by environmental factors. Telomere length (TL) decreases with age in several species, but little is known about the sources of genetic and environmental variation in the change in TL (∆TL) in wild animals. In this study, we tracked changes in TL throughout the natural lifespan (from a few months to almost 9 years) of free-living house sparrows (Passer domesticus) in two different island populations. TL was measured in nestlings and subsequently up to four times during their lifetime. TL generally decreased with age (senescence), but we also observed instances of telomere lengthening within individuals. We found some evidence for selective disappearance of individuals with shorter telomeres through life. Early-life TL positively predicted later-life TL, but the within-individual repeatability in TL was low (9.2%). Using genetic pedigrees, we found a moderate heritability of ∆TL (h² = 0.21), which was higher than the heritabilities of early-life TL (h² = 0.14) and later-life TL measurements (h² = 0.15). Cohort effects explained considerable proportions of variation in early-life TL (60%), later-life TL (53%), and ∆TL (37%), which suggests persistent impacts of the early-life environment on lifelong telomere dynamics. Individual changes in TL were independent of early-life TL. Finally, there was weak evidence for population differences in ∆TL that may be linked to ecological differences in habitat types. Combined, our results show that individual telomere biology is highly dynamic and influenced by both genetic and environmental variation in natural conditions.