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

Type Article
Date 2022-08
Language English
Author(s) Dupoué AndreazORCID1, Blaimont Pauline2, 3, Angelier Frédéric4, Ribout Cécile4, Rozen-Rechels David5, Richard MurielleORCID6, Miles DonaldORCID7, de Villemereuil PierreORCID8, Rutschmann Alexis9, Badiane ArnaudORCID5, Aubret FabienORCID6, 10, Lourdais Olivier4, Meylan Sandrine5, Cote Julien11, Clobert Jean6, Le Gallard Jean-François5, 12
Affiliation(s) 1 : Laboratoire des sciences de l’environnement marin, Centre National de la Recherche Scientifique, Universite Bretagne Occidentale, Institut de recherche pour le developpement, Institut Francais de Recherche pour l’Exploitation de la Mer, UMR 6539, Plouzane, 29280, France
2 : Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064, USA
3 : Department of Biology, Rider University, Lawrenceville, NJ 08648, USA
4 : Centre d’Etudes Biologiques de Chize, Universite de La Rochelle, CNRS, UMR 7372, Beauvoir sur Niort, 79360, France
5 : Institut d’ecologie et des sciences de l’environnement de Paris, CNRS, UMR 7618, Sorbonne Universite, Paris, 75005, France
6 : Station d’Ecologie Theorique et Experimentale de Moulis, CNRS, UMR 5321, Saint Girons, 09200, France
7 : Department of Biological Sciences, Ohio University, Athens, OH 45701, Greece
8 : Institut de Systematique,Evolution, Biodiversite, CNRS, Museum national d’Histoire naturelle, Sorbonne Universite, Ecole Pratique des Hautes Etudes and Universite des Antilles, UMR 72
9 : School of Biological Sciences, University of Auckland, Auckland, 1142, New Zealand
10 : School of Agricultural, Environmental and Veterinary Sciences, Faculty of Science and Health, Charles Sturt University, Port Macquarie NSW 2444, Australia
11 : Laboratoire Evolution et Diversite Biologique, CNRS, UMR 5174, Toulouse, 31077, France
12 : Centre de recherche en ecologie experimentale et predictive-Ecotron IleDeFrance, CNRS, Ecole Normale Superieure, UMS 3194, Saint-Pierre-les-Nemours, 77140, France
Source Proceedings Of The National Academy Of Sciences Of The United States Of America (0027-8424) (Proceedings of the National Academy of Sciences), 2022-08 , Vol. 119 , N. 33 , P. e2201371119 (7p.)
DOI 10.1073/pnas.2201371119
WOS© Times Cited 17
Keyword(s) aging, ectotherms, population extinction, telomeres, life-history tradeoffs
Abstract

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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Dupoué Andreaz, 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 Gallard Jean-François (2022). Lizards from warm and declining populations are born with extremely short telomeres. Proceedings Of The National Academy Of Sciences Of The United States Of America, 119(33), e2201371119 (7p.). Publisher's official version : https://doi.org/10.1073/pnas.2201371119 , Open Access version : https://archimer.ifremer.fr/doc/00787/89946/