Lizards from warm and declining populations are born with extremely short telomeres

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...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2022-08, Vol.119 (33), p.e2201371119
Main Authors: Dupoué, Andréaz, Blaimont, Pauline, Angelier, Frédéric, Ribout, Cécile, Rozen-Rechels, David, Richard, Murielle, Miles, Donald, de Villemereuil, Pierre, Rutschmann, Alexis, Badiane, Arnaud, Aubret, Fabien, Lourdais, Olivier, Meylan, Sandrine, Cote, Julien, Clobert, Jean, Le Galliard, Jean-François
Format: Article
Language:English
Subjects:
Aging
Aging - genetics
Animal biology
Animals
Biodiversity and Ecology
Biological Sciences
Biomarkers
Climate change
Environmental Sciences
Extinction
Extinction, Biological
Female
Gene sequencing
Global Changes
Global Warming
Life history
Life Sciences
Lizards
Lizards - genetics
Neonates
Nucleotide sequence
Population Dynamics
Populations
Reproduction
Risk
Species extinction
Telomere - genetics
Telomere Shortening
Telomeres
Threshold limits
Vertebrate Zoology
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Summary: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 ( ) 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.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2201371119