Identifying the early warning signals of catastrophic extinctions has recently become a central focus for ecologists, but species’ functional responses to environmental changes remain an untapped source for the sharpening of such warning signals. Telomere length (TL) analysis represents a promising molecular tool with which to raise the alarm regarding early population decline, since telomere attrition is associated with aging processes and accelerates after a recurrent exposure to environmental stressors. In the southern margin of their range, populations of the common lizard (Zootoca vivipara) recently became extinct at lowest elevations due to changes in climate conditions. However, the proximal signals involved in these demographic declines are still unknown. Here, we sampled 100 yearling lizards from 10 natural populations (n = 10 per population) along an extinction risk gradient. Relative lizard abundance dramatically dropped over 12 years in low-altitude populations characterized by warmer ambient temperatures and higher body growth of lizards early in life. A non-linear relationship was found between TL and population extinction risk, with shorter telomeres in populations facing high risk of extinction when compared to non-threatened ones. Our results identify TL as a promising biomarker and imply that population extinctions might be preceded by a loop of physiological aging.

Urban sprawl is associated with deep and intense modifications of the natural habitats of wild vertebrates. Although, many species are unable to cope with such an environment, a few species can be found in cities and can help us assessing the impact of urbanization on wildlife. Urban-related environmental modifications are multiple and some of them seem beneficial while others seem rather detrimental to wild vertebrates. Moreover, the impact of these modifications on wild vertebrates is likely to vary depending on the phase of the annual life-cycle. Therefore, it is challenging to get a comprehensive picture of the impact of urbanization on wild vertebrates. Overall, urbanization is usually associated with reduced breeding performances in wild birds, but the impact of urbanization on the phenotype and quality of developing offspring has been less studied. In this study, we specifically investigated the impact of urbanization on several proxies of individual quality in great tits (Parus major). We concomitantly measured body size (tarsus length and body mass), plumage coloration, and telomere length in 14-days old chicks issued from 4 populations (two pairs of urban/rural populations located in two different geographical areas of France). First, rural chicks were significantly taller and heavier than urban birds although this impact of urbanization on body size/body mass appears only true for the most urbanized site. Interestingly, body size was also affected by the geographical area of capture, suggesting that regional environmental conditions may attenuate or exacerbate the influence of urbanization on nestling growth. Second, the carotenoid-based yellow plumage of rural nestlings was more colorful than that of urban birds, independently of the area of capture. This suggests that urban birds probably have a low-carotenoid diet relative to rural birds. Finally, telomere length did not differ between rural and urban chicks. These results suggest that urbanization probably imposes large developmental constraints in wild vertebrates and that this impact may primarily be related to constraining nutritional conditions.

Telomeres are DNA-protein complexes located at the end of chromosomes, which play an important role in maintaining the genomic integrity. Telomeres shorten at each cell division and previous studies have shown that telomere length is related to health and lifespan and can be affected by a wide range of environmental factors. Among them, some persistent organic pollutants (POPs) have the potential to damage DNA. However, the effect of POPs on telomeres is poorly known for wildlife. Here, we investigated the relationships between some legacy POPs (organochlorine pesticides and polychlorobiphenyls) and telomere length in breeding adult black-legged kittiwakes (Rissa tridactyla), an arctic seabird species. Our results show that among legacy POPs, only blood concentration of oxychlordane, the major metabolite of chlordane mixture, is associated with shorter telomere length in females but not in males. This suggests that female kittiwakes could be more sensitive to oxychlordane, potentially explaining the previously reported lower survival rate in most oxychlordane-contaminated kittiwakes from the same population. This study is the first to report a significant and negative relationship between POPs and telomere length in a free-living bird and highlights sex-related susceptibility to banned pesticides.