Telomere attrition rates are associated with weather conditions and predict productive lifespan in dairy cattle

Seeker, Luise A.; Underwood, Sarah; Wilbourn, Rachael V.; Dorrens, Jennifer; Froy, Hannah; Holland, Rebecca; Ilska, Joanna J.; Psifidi, Androniki; Bagnall, Ainsley; Whitelaw, Bruce; Coffey, Mike; Banos, Georgios; Nussey, Daniel H.

doi:10.1038/s41598-021-84984-2

Cited by 20 publications

(31 citation statements)

References 70 publications

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“…However, both short and long early‐life TL tended to be weakly associated with the lowest mortality rates over the lifespan in that study (Pepke, Kvalnes, et al, 2022 ), suggesting disruptive selection on TL. Furthermore, some studies have showed that early‐life TL was a poor predictor of survival, which was instead predicted by changes in TL (Boonekamp et al, 2014 ; Seeker et al, 2021 ; Wood & Young, 2019 ), which we did not measure in this study.…”

Section: Discussionmentioning

confidence: 75%

“…Similarly, TL decreased with higher temperatures experienced by common lizards (Dupoué et al, 2017), desert toad-headed agamas (Phrynocephalus przewalskii, Zhang et al, 2018), and dairy cattle (Bos taurus, Seeker et al, 2021), but not in Gouldian finches (Chloebia gouldiae, Fragueira et al, 2019). However, TL increased with higher temperature in Eastern mosquitofish (Gambusia holbrooki, Rollings et al, 2014), spotted snow skinks (Niveoscincus ocellatus, Fitzpatrick et al, 2019), and dark-eyed juncos (Graham et al, 2019) and there was no effect of temperature manipulation on TL in Atlantic salmon (Salmo salar, McLennan et al, 2018) or three-spined sticklebacks (Gasterosteus aculeatus, Kim et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

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Causes and consequences of variation in early‐life telomere length in a bird metapopulation

Pepke

Kvalnes

Ranke

et al. 2022

Ecology and Evolution

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Environmental conditions during early‐life development can have lasting effects shaping individual heterogeneity in fitness and fitness‐related traits. The length of telomeres, the DNA sequences protecting chromosome ends, may be affected by early‐life conditions, and telomere length (TL) has been associated with individual performance within some wild animal populations. Thus, knowledge of the mechanisms that generate variation in TL, and the relationship between TL and fitness, is important in understanding the role of telomeres in ecology and life‐history evolution. Here, we investigate how environmental conditions and morphological traits are associated with early‐life blood TL and if TL predicts natal dispersal probability or components of fitness in 2746 wild house sparrow ( Passer domesticus ) nestlings from two populations sampled across 20 years (1994–2013). We retrieved weather data and we monitored population fluctuations, individual survival, and reproductive output using field observations and genetic pedigrees. We found a negative effect of population density on TL, but only in one of the populations. There was a curvilinear association between TL and the maximum daily North Atlantic Oscillation index during incubation, suggesting that there are optimal weather conditions that result in the longest TL. Dispersers tended to have shorter telomeres than non‐dispersers. TL did not predict survival, but we found a tendency for individuals with short telomeres to have higher annual reproductive success. Our study showed how early‐life TL is shaped by effects of growth, weather conditions, and population density, supporting that environmental stressors negatively affect TL in wild populations. In addition, shorter telomeres may be associated with a faster pace‐of‐life, as individuals with higher dispersal rates and annual reproduction tended to have shorter early‐life TL.

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Section: Discussionmentioning

confidence: 75%

Section: Discussionmentioning

confidence: 99%

Causes and consequences of variation in early‐life telomere length in a bird metapopulation

Pepke

Kvalnes

Ranke

et al. 2022

Ecology and Evolution

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“…It is important to note that studies based on both laboratory and natural populations indicate that a significant proportion of an individual's telomere length can be explained by environmental variation, i.e. harsher or unpredictable environments are linked to shorter telomeres or faster telomere shortening rate (Watson et al 2015, McLennan et al 2016, Angelier et al 2018, Seeker et al 2021; meta‐analysed in Chatelain et al 2020). Telomeres seem to be particularly sensitive to environmental variation at early life stages, including prior to birth or hatching (Haussmann et al 2012, Noguera et al 2020, Stier et al 2020) or via maternal effects and parental life histories (Haussmann et al 2012, McLennan et al 2018).…”

Section: The Use Of Telomeres In Eco‐evolutionary Studiesmentioning

confidence: 99%

Telomeres in a spatial context: a tool for understanding ageing pattern variation in wild populations

2021

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Ageing refers to the loss of organismal functionality with age, a process that is characterised by decreased reproduction and survival probability. In natural populations, it is expected that environmental conditions influence an individual's ageing trajectory. Understanding the role of environmental heterogeneity on ageing variation could provide critical insights into population resilience and species distribution but remains overlooked. Telomeres, the end cap of chromosomes, are a promising integrative physiological marker of an individual's health and a possible proxy to aid the understanding of variation in ageing trajectories. Here, we review the existing information on telomere length and its dynamics in wild populations distributed across spatial scales. Despite a relative scarcity of information, there is evidence for divergence in telomere length between populations facing contrasting environments. Nonetheless, a higher spatial resolution and temporal replication are needed to fully understand the role that environmental conditions play on telomere length variation. Since most of the existing studies are correlational, future field and laboratory experiments are required. For the first time, we demonstrate the use of population telomere data to predict species habitat suitability through species distribution models (SDMs). This represents a promising new research area in the study of ageing pattern variation in wild populations. Furthermore, the inclusion of telomere data in future physiological SDMs may improve our understanding of species distribution and population resilience. However, the use of telomeres within this context could be limited if no previous knowledge on the relevance of telomeres as markers of health and survival at the species level is available. Finally, we suggest some key practical and theoretical considerations that, ideally, future studies combining biogeographic and telomere data should pay attention.

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“…This is supported by a recent study which took repeated measurement of the relative leukocyte telomere length in a dairy herd. Higher rates of telomere attrition in individual cows was predictive of a shorter productive lifespan, suggesting a link between telomere loss and health [ 58 ].…”

Section: Discussionmentioning

confidence: 99%

Comparison of the transcriptome in circulating leukocytes in early lactation between primiparous and multiparous cows provides evidence for age-related changes

et al. 2021

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Background Previous studies have identified many immune pathways which are consistently altered in humans and model organisms as they age. Dairy cows are often culled at quite young ages due to an inability to cope adequately with metabolic and infectious diseases, resulting in reduced milk production and infertility. Improved longevity is therefore a desirable trait which would benefit both farmers and their cows. This study analysed the transcriptome derived from RNA-seq data of leukocytes obtained from Holstein cows in early lactation with respect to lactation number. Results Samples were divided into three lactation groups for analysis: i) primiparous (PP, n = 53), ii) multiparous in lactations 2–3 (MP 2–3, n = 121), and iii) MP in lactations 4–7 (MP > 3, n = 55). Leukocyte expression was compared between PP vs MP > 3 cows with MP 2–3 as background using DESeq2 followed by weighted gene co-expression network analysis (WGCNA). Seven modules were significantly correlated (r ≥ 0.25) to the trait lactation number. Genes from the modules which were more highly expressed in either the PP or MP > 3 cows were pooled, and the gene lists subjected to David functional annotation cluster analysis. The top three clusters from modules more highly expressed in the PP cows all involved regulation of gene transcription, particularly zinc fingers. Another cluster included genes encoding enzymes in the mitochondrial beta-oxidation pathway. Top clusters up-regulated in MP > 3 cows included the terms Glycolysis/Gluconeogenesis, C-type lectin, and Immunity. Differentially expressed candidate genes for ageing previously identified in the human blood transcriptome up-regulated in PP cows were mainly associated with T-cell function (CCR7, CD27, IL7R, CAMK4, CD28), mitochondrial ribosomal proteins (MRPS27, MRPS9, MRPS31), and DNA replication and repair (WRN). Those up-regulated in MP > 3 cows encoded immune defence proteins (LYZ, CTSZ, SREBF1, GRN, ANXA5, ADARB1). Conclusions Genes and pathways associated with lactation number in cows were identified for the first time to date, and we found that many were comparable to those known to be associated with ageing in humans and model organisms. We also detected changes in energy utilization and immune responses in leukocytes from older cows.

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Telomere attrition rates are associated with weather conditions and predict productive lifespan in dairy cattle

Cited by 20 publications

References 70 publications

Causes and consequences of variation in early‐life telomere length in a bird metapopulation

Causes and consequences of variation in early‐life telomere length in a bird metapopulation

Telomeres in a spatial context: a tool for understanding ageing pattern variation in wild populations

Comparison of the transcriptome in circulating leukocytes in early lactation between primiparous and multiparous cows provides evidence for age-related changes

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