Mathilde Tissier

and 5 more

Understanding ageing and the diversity of life histories is a cornerstone in biology. Telomeres, the protecting caps of chromosomes, are thought to be involved in ageing, cancer risks and to modulate life-history strategies. They shorten with cell division and age in somatic tissues of most species, possibly limiting lifespan. The resource allocation trade-off hypothesis predicts that short telomeres have thus co-evolved with early reproduction, proactive behaviour and reduced lifespan: a fast Pace-of-Life Syndrome (POLS). Conversely, since short telomeres may also reduce the risks of cancer, the anti-cancer hypothesis advances that they should be associated with slow POLS. Conclusion on which hypothesis best supports the role of telomeres as mediators of life-history strategies is hampered by a lack of study on wild short-lived vertebrates, apart from birds. Using seven years of data on wild Eastern chipmunks Tamias striatus, we highlighted that telomeres elongate with age and do not limit lifespan in this species. Furthermore, short telomeres correlated with a slow POLS in a sex-specific way. Females with short telomeres had a delayed age at first breeding and a lower fecundity rate than females with long telomeres, whereas those differences were not recorded in males. Our findings support most predictions adapted from the anti-cancer hypothesis, but none of those made under the resource allocation trade-off hypothesis. Results are in line with an increasing body of evidence suggesting that other evolutionary forces than resource allocation trade-offs shape the diversity of telomere length in adult somatic cells and the relationships between telomeres and life-histories.

Mathilde Tissier

and 5 more

Understanding ageing and the diversity of life histories is a cornerstone in biology. Telomeres, the protecting caps of chromosomes, are thought to be involved in ageing, cancer risks and to modulate life-history strategies. They shorten with cell division and age in somatic tissues of most species, possibly limiting lifespan. The resource allocation trade-off hypothesis predicts that short telomeres have thus co-evolved with early reproduction, proactive behaviour and reduced lifespan, i.e. a fast Pace-of-Life Syndrome (POLS). Conversely, since short telomeres may also reduce the risks of cancer, the anti-cancer hypothesis advances that they should be associated with slow POLS. Conclusion on which hypothesis best supports the role of telomeres as mediators of life-history strategies is hampered by a lack of study on wild short-lived vertebrates, apart from birds. Using seven years of data on wild Eastern chipmunks Tamias striatus, we highlighted that telomeres elongate with age and do not limit lifespan in this species. Furthermore, short telomeres correlated with a slow POLS in a sex-specific way. Females with short telomeres had a delayed age at first breeding and a lower fecundity rate than females with long telomeres, whereas those differences were not recorded in males. Our findings support most predictions adapted from the anti-cancer hypothesis, but none of those made under the resource allocation trade-off hypothesis. Results are in line with an increasing body of evidence suggesting that resource allocation trade-offs alone cannot explaining the diversity of telomere length in adult somatic cells and life-histories observed across the tree of life.

François Criscuolo

and 2 more

Longevity is highly variable among animal species, and has coevolved with other of life-history traits, like body size and rates of reproduction. Telomeres, through their erosion over time, are one of the cell mechanisms that produce senescence at the cell level, and might even have an influence on the rate of ageing in whole organisms. However, uneroded telomeres are also risk factors of cell immortalization. The associations of telomere lengths, their rate of change, and life-history traits independent of body size are largely underexplored for birds. To test associations of life-history traits and telomere dynamics, we conducted a phylogenetic meta-analysis using studies of 53 species of birds. We restricted analyses to studies that applied the telomere restriction fragment length (TRF) method, and examined relationships between mean telomere length at the chick (Chick TL) and adult (Adult TL) stages, the mean rate of change in telomere length during life (TROC), and life-history traits. We examined 3 principal components of 12 life-history variables that represented: body size (PC1), the slow-fast continuum of pace-of-life (PC2) and post-fledging parental care (PC3). Phylogeny had at best a small-to-medium influence on Adult and Chick TL (r² = 0.190 and 0.138, respectively), but a substantial influence on TROC (r² = 0.688). Phylogeny strongly influenced life histories: PC1 (r² = 0.828), PC2 (0.838), and PC3 (0.613). Adult TL and Chick TL were poorly associated with the life-history variables. TROC, however, was negatively and moderate-to-strongly associated with PC2 (unadjusted r = -0.340; with phylogenetic correction, r = -0.490). Independent of body size, long-lived species with smaller clutches and slower embryonic rate of growth may exhibited less change in telomere length over their lifetimes. We suggest that telomere lengths may have diverged even among closely avian related species, yet telomere dynamics are strongly linked to the pace of life.