Telomere length and dynamics predict mortality in a wild longitudinal study

Barrett, Emma; Burke, Terry; Hammers, Martijn; Komdeur, Jan; Richardson, David S.

doi:10.1111/mec.12110

Cited by 193 publications

(282 citation statements)

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“…Critically short telomeres trigger a signal prompting the cell to permanently stop dividing, which leads to the induction of cellular senescence (Herbig et al, 2006). Furthermore, long telomeres have been found to correlate with good health and higher life expectancies in several species, thereby also serving as an indicator of somatic fitness, which represents the boundary of aging diseases (Bize et al, 2009;Horn et al, 2010;Barrett et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Long telomeres are associated with clonality in wild populations of the fissiparous starfish Coscinasterias tenuispina

et al. 2015

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Telomeres usually shorten during an organism's lifespan and have thus been used as an aging and health marker. When telomeres become sufficiently short, senescence is induced. The most common method of restoring telomere length is via telomerase reverse transcriptase activity, highly expressed during embryogenesis. However, although asexual reproduction from adult tissues has an important role in the life cycles of certain species, its effect on the aging and fitness of wild populations, as well as its implications for the long-term survival of populations with limited genetic variation, is largely unknown. Here we compare relative telomere length of 58 individuals from four populations of the asexually reproducing starfish Coscinasterias tenuispina. Additionally, 12 individuals were used to compare telomere lengths in regenerating and non-regenerating arms, in two different tissues (tube feet and pyloric cecum). The level of clonality was assessed by genotyping the populations based on 12 specific microsatellite loci and relative telomere length was measured via quantitative PCR. The results revealed significantly longer telomeres in Mediterranean populations than Atlantic ones as demonstrated by the Kruskal-Wallis test (K = 24.17, significant value: P-valueo0.001), with the former also characterized by higher levels of clonality derived from asexual reproduction. Telomeres were furthermore significantly longer in regenerating arms than in non-regenerating arms within individuals (pyloric cecum tissue: Mann-Whitney test, V = 299, P-valueo10 − 6 ; and tube feet tissue Student's t = 2.28, P-value = 0.029). Our study suggests that one of the mechanisms responsible for the long-term somatic maintenance and persistence of clonal populations is telomere elongation.

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Section: Introductionmentioning

confidence: 99%

Long telomeres are associated with clonality in wild populations of the fissiparous starfish Coscinasterias tenuispina

et al. 2015

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“…Short telomeres are strongly associated with cellular senescence, shortened lifespan, and reduced future reproductive success (20). Although long telomeres are maintained in the germ line through replenishment during meiosis, there is some evidence that telomere length is heritable and that such inheritance is sex specific (21)(22)(23) in birds, potentially resulting in daughters of older mothers having shorter telomeres (24)(25)(26), and, in turn, reduced fitness (27). The cellular consequences of aging and stress are similar, because both lead to oxidative damage that causes telomeres to shorten (20,28).…”

Section: Significancementioning

confidence: 99%

Reduced fitness in progeny from old parents in a natural population

Schroeder

Nakagawa

Rees

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

138

206

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A nongenetic, transgenerational effect of parental age on offspring fitness has been described in many taxa in the laboratory. Such a transgenerational fitness effect will have important influences on population dynamics, population age structure, and the evolution of aging and lifespan. However, effects of parental age on offspring lifetime fitness have never been demonstrated in a natural population. We show that parental age has sex-specific negative effects on lifetime fitness, using data from a pedigreed insular population of wild house sparrows. Birds whose parents were older produced fewer recruits annually than birds with younger parents, and the reduced number of recruits translated into a lifetime fitness difference. Using a long-term cross-fostering experiment, we demonstrate that this parental age effect is unlikely to be the result of changes in the environment but that it potentially is epigenetically inherited. Our study reveals the hidden consequences of late-life reproduction that persist into the next generation.aging | epigenetic | indirect effects | senescence | transgenerational R eproducing at old age is known to incur costs such as an increased risk of polysomy and higher infant and maternal mortality. One potential cost that is hard to estimate occurs when parental age influences the lifespan or fertility of the next generation and beyond. First described by Alexander Graham Bell (1), this negative influence of parental age on offspring fitness [known as the "Lansing effect" (2-6)] has been observed in humans and in many taxa in the laboratory. Such transgenerational effects might have an epigenetic cause and are critical for understanding the evolution of late reproduction and longevity (7-11). However, to our knowledge, an effect of parental age on fitness in the next generation has not yet been shown conclusively in the wild, perhaps because its detection requires an exact knowledge of parental age and of the lifetime fate of offspring, data that are difficult to gather in natural populations (12). We have data from a natural, pedigreed population of passerines, house sparrows (Passer domesticus), in which we know the life history and precise fitness estimates of nearly all individuals (13). We use these data to demonstrate that parental age has a negative effect on fitness. We complement this study with a long-term cross-fostering experiment (14) that allows us to demonstrate that this effect is not environmentally induced. Our study reveals the hidden consequences of late-life reproduction for the next generation. Such transgenerational effects have the potential to help us better understand the evolution of aging and lifespan. ResultsWe found no statistically significant effect of a parent's age at reproduction on its offspring's longevity (Table 1). However, we found significant, sex-specific evidence for a negative effect of the age of the focal individual's parents on its lifetime reproductive success (the number of genetic recruits over a lifetime, LRS; Fig. 1). Sparrow females ...

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“…Telomeres appear to shorten throughout the life of individuals (Pauliny et al 2006;Bize et al 2009;Salomons et al 2009;Heidinger et al 2012;Angelier et al 2013;Barrett et al 2013;Bauch et al 2013;Boonekamp et al 2014) and, importantly, telomere length (TL) has been shown to be a reliable predictor of survival under some circumstances (Haussmann et al 2005;Pauliny et al 2006;Bize et al 2009;Salomons et al 2009;Heidinger et al 2012;Angelier et al 2013;Barrett et al 2013) but not others (Pauliny et al 2006;Beaulieu et al 2011;Caprioli et al 2013;Boonekamp et al 2014). Therefore, specific attention has been paid to the determinants of TL in wild vertebrates.…”

Section: Introductionmentioning

confidence: 99%

“…During adulthood, different individuals experience different environmental conditions and this can result in variable rates of telomere shortening between individuals Salomons et al 2009;Angelier et al 2013;Barrett et al 2013). Importantly, and contrary to TL, body size does not change after the developmental phase since birds have determinate growth, suggesting that telomere dynamics will become independent of structural body size in adults.…”

Section: Introductionmentioning

confidence: 99%

Bill size correlates with telomere length in male American Redstarts

et al. 2015

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Telomere length (TL) has been shown to be a potential predictor of survival in wild vertebrates, and, as a consequence, there is growing interest in understanding the causes of inter-individual variability in TL. In that context, developmental conditions deserve a specific attention because they are thought to be a major driver of telomere shortening. Because poor developmental conditions can accelerate telomere shortening and impair growth (resulting in a small adult size), a positive correlation between TL and body size is expected. However, and surprisingly, the relationship between body size and telomere length has rarely been described in wild vertebrates. Here, we specifically examined this question in hatch-year (HY) and after hatch-year (AHY) male wintering American Redstarts (Setophaga ruticilla). Although tarsus size was not related to TL, we found a significant positive correlation between bill size and TL in HY male Redstarts, therefore supporting the idea that determinants of some components of individual size are also important determinants of TL in young birds. Moreover, this positive relationship between bill size and TL was also found for AHY birds, suggesting that adult TL may be, at least partly, explained by the telomere dynamics that occurred during the developmental phase. Abstract Telomere length (TL) has been shown to be a potential predictor of survival in wild vertebrates, and, as a consequence, there is growing interest in understanding the causes of inter-individual variability in TL. In that context, developmental conditions deserve a specific attention because they are thought to be a major driver of telomere shortening. Because poor developmental conditions can accelerate telomere shortening and impair growth (resulting in a small adult size), a positive correlation between TL and body size is expected. However, and surprisingly, the relationship between body size and telomere length has rarely been described in wild vertebrates. Here, we specifically examined this question in hatch-year (HY) and after hatch-year (AHY) male wintering American Redstarts (Setophaga ruticilla). Although tarsus size was not related to TL, we found a significant positive correlation between bill size and TL in HY male Redstarts, therefore supporting the idea that determinants of some components of individual size are also important determinants of TL in young birds. Moreover, this positive relationship between bill size and TL was also found for AHY birds, suggesting that adult TL may be, at least partly, explained by the telomere dynamics that occurred during the developmental phase.

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Telomere length and dynamics predict mortality in a wild longitudinal study

Cited by 193 publications

References 59 publications

Long telomeres are associated with clonality in wild populations of the fissiparous starfish Coscinasterias tenuispina

Long telomeres are associated with clonality in wild populations of the fissiparous starfish Coscinasterias tenuispina

Reduced fitness in progeny from old parents in a natural population

Bill size correlates with telomere length in male American Redstarts

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