Stressors interact across generations to influence offspring telomeres and survival

Young, Rebecca C.; Westneat, David F.; Vangorder-Braid, Jennifer; Sirman, Aubrey E.; Siller, Stefanie J; Kittilson, Jeffrey D.; Ghimire, Ambika; Heidinger, Britt J.

doi:10.1098/rspb.2022.0868

Cited by 9 publications

(24 citation statements)

References 57 publications

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“…We identi ed one individual (a female from the Hestmannøy population) that showed signi cant consistent telomere elongation throughout life at a greater rate than might have been expected by measurement error (see Supporting Information). Recent studies on house sparrows in other populations have also showed instances of telomere lengthening within some individuals [84,103] and that house sparrows may experience rather transient TL shortening in response to stressors [104]. However, TL also generally declined with age in another long-term study of house sparrows [18,84].…”

Section: Discussionmentioning

confidence: 98%

Longitudinal telomere dynamics within natural lifespans of a wild bird

Pepke

Kvalnes

Wright

et al. 2022

Preprint

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Telomeres, the nucleotide sequences that protect the ends of eukaryotic chromosomes, shorten with each cell division and telomere loss may be increased by factors such as oxidative stress. Telomere length (TL) decreases with age in several species, and TL or the change in TL (∆TL) have emerged as biomarkers reflecting experienced stress. In this study, we tracked changes in TL throughout the natural lifespan (from a few months to almost 9 years) of free-living house sparrows (Passer domesticus) in two different island populations. TL was measured in nestlings and subsequently up to 4 times during their lifetime. TL generally decreased with age (senescence), but we also observed instances of telomere lengthening within individuals. We found some evidence for selective disappearance of individuals with shorter telomeres through life. Early-life TL positively predicted later-life TL, but the within-individual repeatability in TL was low (9.2%). Using genetic pedigrees, we found a moderate heritability of ∆TL (h2 = 0.21), which was higher than the heritabilities of early-life TL (h2 = 0.14) and later-life TL measurements (h2 = 0.15). Cohort effects explained considerable proportions of variation in early-life TL (60%), later-life TL (53%), and ∆TL (37%), which suggests persistent impacts of the early-life environment on lifelong telomere dynamics. Individual changes in TL were independent of early-life TL. Finally, there was weak evidence for population differences in ∆TL that may be linked to ecological differences in habitat types. Combined, our results show that individual telomere biology is highly dynamic and influenced by both genetic and environmental variation in natural conditions.

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Section: Discussionmentioning

confidence: 98%

Longitudinal telomere dynamics within natural lifespans of a wild bird

Pepke

Kvalnes

Wright

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…We identified one individual (a female from the Hestmannøy population) that showed significant consistent telomere elongation throughout life at a greater rate than might have been expected by measurement error (see Supporting Information). Recent studies on house sparrows in other populations have also showed instances of telomere lengthening within some individuals 90,112 and that house sparrows may experience rather transient TL shortening in response to stressors 113 . However, TL also generally declined with age in another long-term study of house sparrows 22,90 .…”

Section: Discussionmentioning

confidence: 99%

Longitudinal telomere dynamics within natural lifespans of a wild bird

Pepke

Kvalnes

Wright

et al. 2023

Sci Rep

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Telomeres, the nucleotide sequences that protect the ends of eukaryotic chromosomes, shorten with each cell division and telomere loss may be influenced by environmental factors. Telomere length (TL) decreases with age in several species, but little is known about the sources of genetic and environmental variation in the change in TL (∆TL) in wild animals. In this study, we tracked changes in TL throughout the natural lifespan (from a few months to almost 9 years) of free-living house sparrows (Passerdomesticus) in two different island populations. TL was measured in nestlings and subsequently up to four times during their lifetime. TL generally decreased with age (senescence), but we also observed instances of telomere lengthening within individuals. We found some evidence for selective disappearance of individuals with shorter telomeres through life. Early-life TL positively predicted later-life TL, but the within-individual repeatability in TL was low (9.2%). Using genetic pedigrees, we found a moderate heritability of ∆TL (h2 = 0.21), which was higher than the heritabilities of early-life TL (h2 = 0.14) and later-life TL measurements (h2 = 0.15). Cohort effects explained considerable proportions of variation in early-life TL (60%), later-life TL (53%), and ∆TL (37%), which suggests persistent impacts of the early-life environment on lifelong telomere dynamics. Individual changes in TL were independent of early-life TL. Finally, there was weak evidence for population differences in ∆TL that may be linked to ecological differences in habitat types. Combined, our results show that individual telomere biology is highly dynamic and influenced by both genetic and environmental variation in natural conditions.

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“…Any stress experienced by parents may also affect the telomere dynamics (i.e. telomere length and rate of loss) of the next generation via genetic and/or parental effects pathways ( Tarry-Adkins et al, 2009 ; Asghar et al, 2015 ; Marasco et al, 2019 ; Young et al, 2022 ), which in turn may depend on offspring sex ( Marasco et al, 2019 ) and/or offspring environment ( Young et al, 2022 ). While the estimation of telomere heritability is complicated by the fact that telomere lengths change through life and are under the influence of extrinsic factors, a recent meta-analysis reported an average heritability score of ~ 45% ( Chik et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Does pre-spawning catch and release angling affect offspring telomere dynamics in Atlantic salmon?

Duncan

Papatheodoulou

Metcalfe

et al. 2023

Conservation Physiology

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The practice of ‘catch and release’ (C&R) angling confers a balance between animal welfare, conservation efforts and preserving the socio-economic interests of recreational angling. However, C&R angling can still cause exhaustion and physical injury, and often exposes the captured fish to the stress of air exposure. Therefore, the true conservation success of C&R angling depends on whether the angled individuals then survive to reproduction and whether there are any persisting effects on subsequent generations. Here we tested the hypothesis that the stress of C&R angling is then passed on to offspring. We experimentally manipulated the C&R experience of wild adult salmon prior to the spawning season. These parental fish either underwent a C&R simulation (which involved exercise with/without air exposure) or were left as control individuals. We then measured the telomere length of the arising offspring (at the larval stage of development) since previous studies have linked a shorter telomere length with reduced fitness/longevity and the rate of telomere loss is thought to be influenced by stress. Family-level telomere length was positively related to rate of growth. However, the telomere lengths of the salmon offspring were unrelated to the C&R experience of their parents. This may be due to there being no intergenerational effect of parental stress exposure on offspring telomeres, or to any potential effects being buffered by the significant telomere elongation mechanisms that are thought to occur during the embryonic and larval stages of development. While this may suggest that C&R angling has a minimal intergenerational effect on offspring fitness, there have been numerous other reports of negative C&R effects, therefore we should still be aiming to mitigate and refine such practices, in order to minimize their impacts on fish populations.

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Stressors interact across generations to influence offspring telomeres and survival

Cited by 9 publications

References 57 publications

Longitudinal telomere dynamics within natural lifespans of a wild bird

Longitudinal telomere dynamics within natural lifespans of a wild bird

Longitudinal telomere dynamics within natural lifespans of a wild bird

Does pre-spawning catch and release angling affect offspring telomere dynamics in Atlantic salmon?

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