Climate change should lead to massive loss of biodiversity in most taxa, but the detailed physiological mechanisms underlying population extinction remain largely elusive so far. In vertebrates, baseline levels of hormones such as glucocorticoids (GCs) may be indicators of population state as their secretion to chronic stress can impair survival and reproduction. However, the relationship between GC secretion, climate change and population extinction risk remains unclear. In this study, we investigated whether levels of baseline corticosterone (the main GCs in reptiles) correlate with environmental conditions and associated extinction risk across wild populations of the common lizard Zootoca vivipara. First, we performed a cross-sectional comparison of baseline corticosterone levels along an altitudinal gradient among 14 populations. Then, we used a longitudinal study in eight populations to examine the changes in corticosterone levels following the exposure to a heatwave period. Unexpectedly, baseline corticosterone decreased with increasing thermal conditions at rest in females and was not correlated with extinction risk. In addition, baseline corticosterone levels decreased after exposure to an extreme heatwave period. This seasonal corticosterone decrease was more pronounced in populations without access to standing water. We suggest that low basal secretion of corticosterone may entail downregulating activity levels and limit exposure to adverse climatic conditions, especially to reduce water loss. These new insights suggest that rapid population decline might be preceded by a downregulation of the corticosterone secretion.

1. Reproduction involves considerable reorganization in an organism's physiology that incurs potential toxicity for cells (e.g., oxidative stress) and decrease in fitness. This framework has been the cornerstone of the so-called 'oxidative cost of reproduction', a theory that remains controversial and relatively overlooked in non-model ectotherms.2. Here, we used two complementary approaches in natural and controlled conditions to test whether altered access to climate conditions (water and temperature resources) alters oxidative status and mediates reproductive trade-offs in viviparous populations of the common lizard (Zootoca vivipara).3. First, we examined whether access to free-standing water and differences in ambient temperature across 12 natural populations could be related to variation in oxidative status, reproductive effort and reproductive success. Second, we determined whether an experimental restriction to water triggers higher oxidative cost of reproduction and correlates with fitness measures (reproductive success, future survival rate and probability of future reproduction). 4. Pregnant females exhibited higher sensitivity than males to natural or experimental limitations in temperature and water access. That is, in restricted environments, pregnant females with higher reproductive effort exhibited stronger oxidative damage despite enhanced non-enzymatic antioxidant capacity. 5. Enhanced antioxidant defensive capacity in pregnant females was positively correlated with higher reproductive success, whereas elevated oxidative damage negatively correlated with offspring annual survival.6. Altogether, our results revealed a context-dependent oxidative cost of reproduction that was concomitant with a conflict in water demand from offspring. These new insights should be critical for understanding ectotherm responses to heat waves and summer droughts that are increasing in frequency and duration.

Aging is the price to pay for acquiring and processing energy through cellular activity and life history productivity. Climate warming can exacerbate the inherent pace of aging, as illustrated by a faster erosion of protective telomere DNA sequences. This biomarker integrates individual pace of life and parental effects through the germline, but whether intra- and intergenerational telomere dynamics underlies population trends remains an open question. Here, we investigated the covariation between life history, telomere length (TL), and extinction risk among three age classes in a cold-adapted ectotherm ( Zootoca vivipara ) facing warming-induced extirpations in its distribution limits. TL followed the same threshold relationships with population extinction risk at birth, maturity, and adulthood, suggesting intergenerational accumulation of accelerated aging rate in declining populations. In dwindling populations, most neonates inherited already short telomeres, suggesting they were born physiologically old and unlikely to reach recruitment. At adulthood, TL further explained females’ reproductive performance, switching from an index of individual quality in stable populations to a biomarker of reproductive costs in those close to extirpation. We compiled these results to propose the aging loop hypothesis and conceptualize how climate-driven telomere shortening in ectotherms may accumulate across generations and generate tipping points before local extirpation.

In the past decades, nocturnal temperatures have been playing a disproportionate role in the global warming of the planet. Yet, they remain a neglected factor in studies assessing the impact of global warming on natural populations. Here, we question whether an intense augmentation of nocturnal temperatures is beneficial or deleterious to ectotherms. Physiological performance is influenced by thermal conditions in ectotherms and an increase in temperature by only 2°C is sufficient to induce a disproportionate increase in metabolic expenditure. Warmer nights may expand ectotherms' species thermal niche and open new opportunities for prolonged activities and improve foraging efficiency. However, increased activity may also have deleterious effects on energy balance if exposure to warmer nights reduces resting periods and elevates resting metabolic rate. We assessed whether warmer nights affected an individual's growth, dorsal skin colouration, thermoregulation behaviour, oxidative stress status and parasite load by exposing yearling common lizards (Zootoca vivipara) from four populations to either ambient or high nocturnal temperatures for approximately 5 weeks. Warmer nocturnal temperatures increased the prevalence of ectoparasitic infestation and altered allocation of resources towards structural growth rather than storage. We found no change in markers for oxidative stress. The thermal treatment did not influence thermal preferences, but influenced dorsal skin brightness and luminance, in line with a predicted acclimation response in colder environments to enhance heat gain from solar radiation. Altogether, our results highlight the importance of considering nocturnal warming as an independent factor affecting ectotherms' life history in the context of global climate change. ​