<scp>DNA</scp> methylation markers of age(ing) in non‐model animals

Tangili, Marianthi; Slettenhaar, Annabel; Sudyka, Joanna; Dugdale, Hannah L.; Pen, Ido; Palsbøll, Per J.; Verhulst, Simon

doi:10.1111/mec.17065

Cited by 9 publications

(14 citation statements)

References 118 publications

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“…Telomere length and dynamics are proving a useful tool for this purpose (e.g. Eastwood et al (2022)); DNA methylation is another promising candidate in this context (Tangili et al, 2023). For example, it might be that extrinsic stressors have an additive effect on survival, further confirming the impact that early-life adversity can have on fitness prospects (Cooper & Kruuk, 2018).…”

Section: Discussionmentioning

confidence: 99%

Ectoparasite presence and brood size manipulation interact to accelerate telomere shortening in nestling jackdaws

Badás,

Bauch,

Boonekamp

et al. 2023

Molecular Ecology

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Early‐life conditions impact fitness, but whether the combined effect of extrinsic stressors is additive or synergistic is not well known. This is a major knowledge gap because exposure to multiple stressors is frequent. Telomere dynamics may be instrumental when testing how stressors interact because many factors affect telomere shortening, and telomere shortening predicts survival. We evaluated the effect of manipulated brood size and natural infestation by the carnid fly Carnus hemapterus on nestling growth and telomere shortening of wild jackdaws (Corvus monedula). Telomere length, measured in blood using TRF, shortened on average by 264 bp, and on average, Carnus infection induced more telomere shortening. Further analyses showed that in enlarged broods, nestlings' telomeres shortened more when parasitized, while in reduced broods there was no effect of infection on telomere shortening. We conclude that there is a synergistic effect of number of siblings and Carnus infection on telomere shortening rate: blood‐sucking parasites may negatively impact telomeres by increasing cell proliferation and/or physiological stress, and coping with infection may be less successful in enlarged broods with increased sibling competition. Larger nestlings had shorter telomeres independent of age, brood manipulation or infection. Growth was independent of infestation but in enlarged broods, nestlings were lighter at fledging. Our findings indicate that (i) evaluating consequences of early‐life environmental conditions in isolation may not yield a full picture due to synergistic effects, and (ii) effects of environmental conditions may be cryptic, for example, on telomeres, with fitness consequences expressed beyond the temporal framework of the study.

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Section: Discussionmentioning

confidence: 99%

Ectoparasite presence and brood size manipulation interact to accelerate telomere shortening in nestling jackdaws

Badás,

Bauch,

Boonekamp

et al. 2023

Molecular Ecology

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“…This clock was validated on an additional 30 samples from C57BL/6 mice ( n =15 mice, two samples per animal). We assessed clock performance for estimating chronological age of lab mice using mean absolute error (MAE; Tangili et al, 2023). We then built another epigenetic clock as described above using only those CpG sites that (1) showed parallel trends in their methylation rates against body mass in lab and wild mice (i.e., ones that increased in methylation with body mass in both systems; Fig.…”

Section: Methodsmentioning

confidence: 99%

“…Such epigenetic clocks can provide a more accurate estimate of chronological age among wild animals than visible characteristics (Mayne et al, 2022; Larison et al, 2021). Epigenetic clocks have now been developed for a wide range of animal species including baboons, chimpanzees, humpback whales, wolves, green turtles, and zebras (Jarman et al, 2015; Anderson et al, 2021; Pinho et al, 2022; De Paoli-Iseppi et al, 2017; Polanowski et al, 2014; Thompson et al, 2017; Wright et al, 2018; Mayne et al, 2022; Larison et al, 2021; Bors et al, 2021; Sullivan et al, 2022; Tangili et al, 2023; Ito et al, 2018; Fairfield et al, 2021; Wilkinson et al, 2021), as well as plants (Gardner et al, 2023).…”

Section: Introductionmentioning

confidence: 99%

Elevated epigenetic age in wild compared to lab-raised house mice

Hanski,

Joseph,

Raulo

et al. 2023

Preprint

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Age is a key parameter in population ecology, with myriad biological processes changing with age as organisms develop early in life and later senesce. As age is often hard to accurately measure with non-lethal methods, epigenetic methods of age estimation (epigenetic clocks) have become a popular tool in animal ecology, and are often developed or calibrated using captive animals of known age. However, few studies have directly compared epigenetic age estimates between wild and captive or lab-reared animals of the same species, even though age-related epigenetic changes can be influenced by environmental conditions. Here, we built an epigenetic clock from standard laboratory house mice (C57BL/6, Mus musculus) and then used it to estimate age in a population of wild mice (Mus musculus domesticus) of unknown age. We show that this clock accurately predicts adult wild mice to be older than juveniles and that wild mice typically increase in epigenetic age over time, but with wide variation in epigenetic ageing rate among wild individuals. We further show that, for a given body mass, wild mice are epigenetically older than lab mice, and that this difference is not explained by accelerated ageing post-capture but is observed even among the smallest juvenile mice. This suggests different epigenetic age profiles in mice with contrasting genetic and environmental backgrounds arise very early in life and may be driven by peri- and postnatal effects on offspring DNA methylation.

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“…This clock was validated on an additional 15 C57BL/6 mice from facility B. Using one sample per animal, we first measured the correlation between epigenetic age and chronological age and assessed clock performance for estimating chronological age of laboratory mice using mean absolute error (MAE; Tangili et al, 2023). We then ran a linear mixed effects model using lmer function from lme4 R package (Bates et al, 2015) to measure the influence of sex and sequencing batch on epigenetic age predictions.…”

Section: Analysesmentioning

confidence: 99%

“…Such epigenetic clocks can provide a more accurate estimate of chronological age among wild animals than visible characteristics (Larison et al, 2021;Mayne et al, 2022). Epigenetic clocks have now been developed for a wide range of animal species including baboons, chimpanzees, humpback whales, wolves, green turtles and zebras (Anderson et al, 2021;Bors et al, 2021;De Paoli-Iseppi et al, 2017;Fairfield et al, 2021;Ito et al, 2018;Jarman et al, 2015;Larison et al, 2021;Mayne et al, 2022;Pinho et al, 2022;Polanowski et al, 2014;Sullivan et al, 2022;Tangili et al, 2023;Thompson et al, 2017;Wilkinson et al, 2021;Wright et al, 2018), as well as plants (Gardner et al, 2023).…”

mentioning

confidence: 99%

Epigenetic age estimation of wild mice using faecal samples

Hanski,

Joseph,

Raulo

et al. 2024

Molecular Ecology

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Age is a key parameter in population ecology, with a myriad of biological processes changing with age as organisms develop in early life then later senesce. As age is often hard to accurately measure with non‐lethal methods, epigenetic methods of age estimation (epigenetic clocks) have become a popular tool in animal ecology and are often developed or calibrated using captive animals of known age. However, studies typically rely on invasive blood or tissue samples, which limit their application in more sensitive or elusive species. Moreover, few studies have directly assessed how methylation patterns and epigenetic age estimates compare across environmental contexts (e.g. captive or laboratory‐based vs. wild animals). Here, we built a targeted epigenetic clock from laboratory house mice (strain C57BL/6, Mus musculus) using DNA from non‐invasive faecal samples, and then used it to estimate age in a population of wild mice (Mus musculus domesticus) of unknown age. This laboratory mouse‐derived epigenetic clock accurately predicted adult wild mice to be older than juveniles and showed that wild mice typically increased in epigenetic age over time, but with wide variation in epigenetic ageing rate among individuals. Our results also suggested that, for a given body mass, wild mice had higher methylation across targeted CpG sites than laboratory mice (and consistently higher epigenetic age estimates as a result), even among the smallest, juvenile mice. This suggests wild and laboratory mice may display different CpG methylation levels from very early in life and indicates caution is needed when developing epigenetic clocks on laboratory animals and applying them in the wild.

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DNA methylation markers of age(ing) in non‐model animals

Cited by 9 publications

References 118 publications

Ectoparasite presence and brood size manipulation interact to accelerate telomere shortening in nestling jackdaws

Ectoparasite presence and brood size manipulation interact to accelerate telomere shortening in nestling jackdaws

Elevated epigenetic age in wild compared to lab-raised house mice

Epigenetic age estimation of wild mice using faecal samples

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