Effects of persistent organic pollutants on telomere dynamics are sex and age-specific in a wild long-lived bird

• Published in: The Science of the total environment 2024-09, Vol.943, p.173785, Article 173785
• Main Authors: Colominas-Ciuró, Roger, Gray, Francesca E., Arikan, Kalender, Zahn, Sandrine, Meier, Christoph, Criscuolo, François, Bize, Pierre
• Format: Article
• Language: English
• Subjects: Long-lived species; Persistent organic pollutants; Senescence; Tachymarptis (Apus) melba; Telomere dynamics; Telomere length; Wildlife ecotoxicology
• ISSN: 0048-9697; 1879-1026; 1879-1026
• DOI: 10.1016/j.scitotenv.2024.173785

Chemical pollution is a major man-made environmental threat to ecosystems and natural animal populations. Of concern are persistent organic pollutants (POPs), which can persist in the environment for many years. While bioaccumulating throughout the lives of wild animals, POPs can affect their health, reproduction, and survival. However, measuring long-term effects of POPs in wild populations is challenging, and therefore appropriate biomarkers are required in wildlife ecotoxicology. One potential target is telomere length, since telomere preservation has been associated to survival and longevity, and stressors as chemical pollution can disrupt its maintenance. Here, we investigated the effects of different classes of POPs on relative telomere length (RTL) and its rate of change (TROC) in wild long-lived Alpine swifts (Tachymarptis melba). As both RTL and TROC are often reported to differ between sexes and with chronological age, we tested for sex- and age-specific (pre-senescent vs. senescent, ≥ 9 age of years, individuals) effects of POPs. Our results showed that senescent females presented longer RTL and elongated telomeres over time compared to pre-senescent females and males. These sex- and age-related differences in RTL and TROC were influenced by POPs, but differently depending on whether they were organochlorine pesticides (OCPs) or industrial polychlorinated biphenyls (PCBs). OCPs (particularly drins) were negatively associated with RTL, with the strongest negative effects being found in senescent females. Conversely, PCBs led to slower rates of telomere shortening, especially in females. Our study indicates diametrically opposed effects of OCPs on RTL and PCBs on TROC, and these effects were more pronounced in females and senescent individuals. The mechanisms behind these effects (e.g., increased oxidative stress by OCPs; upregulation of telomerase activity by PCBs) remain unknown. Our results highlight the importance in wildlife ecotoxicology to account for sex- and age-related effects when investigating the health effects of pollutants on biomarkers such as telomeres. [Display omitted] •POPs effects on Alpine swift telomeres accounting for senescence status and sex.•Senescent females presented longer RTL and elongated telomeres over time.•OCPs negatively associated with RTL, particularly in senescent females.•PCBs led to slower rates of telomere shortening, especially in females.•Life-history traits (sex & age) are required to disentangle POPs e