Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 119, Issue 33, Pages -Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.2201371119
Keywords
aging; ectotherms; population extinction; telomeres; life-history tradeoffs
Categories
Funding
- National Center for Scientific Research (France)
- Agence Nationale de la Recherche [ANR-13-JSV7-001 DESTRESS, ANR-17-CE02-0013 AQUATHERM]
- European Research Council under the European Union [817779]
- National Science Foundation [EF1241848, DEB1950636]
- French Research Institute for Exploitation of the Sea
- Interreg-POCTEFA [EFA031/15 ECTOPYR]
- TULIP (Laboratory of Excellence) [ANR-10 LABX-41]
- European Research Council (ERC) [817779] Funding Source: European Research Council (ERC)
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This study investigated the relationship between life history, telomere length (TL), and extinction risk in a cold-adapted ectotherm (Zootoca vivipara) facing climate-induced extirpations. The results suggest intergenerational accumulation of accelerated aging rate in declining populations, with most neonates inheriting short telomeres and unlikely to reach recruitment. TL also explained females' reproductive performance at adulthood.
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.
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