Paternal and grandpaternal ages at conception and descendant telomere lengths in chimpanzees and humans

Eisenberg, Dan T. A.; Tackney, Justin; Cawthon, Richard M.; Cloutier, Christina T; Hawkes, Kristen

doi:10.1002/ajpa.23109

Cited by 37 publications

(60 citation statements)

References 59 publications

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“…The reduction in TL in the embryos fathered by old males that we have found supports recent experimental evidence in mice [40], and correlative studies in other bird and lizard species [28][29][30]. These results, however, contrast with previous epidemiological studies in other vertebrate species such as humans or apes [24][25][26][27]33] where the opposite relationship between paternal age and offspring TL was found. It is possible that, in contrast to long-lived mammals such as humans or apes, sperm TL in short-lived vertebrates such as the zebra finch decreases with male age so that embryos fathered by older males inherit shorter telomeres.…”

Section: Discussionsupporting

confidence: 86%

Experimental demonstration that offspring fathered by old males have shorter telomeres and reduced lifespans

2018

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Offspring of older parents frequently show reduced longevity, but the mechanisms driving this so-called 'Lansing effect' are unknown. While inheritance of short telomeres from older parents could underlie this effect, studies to date in different species have found mixed results, reporting positive, negative or no association between parental age and offspring telomere length (TL). However, most of the existing evidence is from non-experimental studies in which it is difficult to exclude alternative explanations such as differential survival of parents with different telomere lengths. Here we provide evidence in the zebra finch that offspring from older parents have reduced lifespans. As a first step in disentangling possible causes, we used an experimental approach to examine whether or not we could detect pre-natal paternal effects on offspring TL. We found that zebra finch embryos fathered by old males have shorter telomeres than those produced by the same mothers but with younger fathers. Since variation in embryonic TL persists into post-natal life, and early life TL is predictive of longevity in this species, this experimental study demonstrates that a paternally driven pre-natal TL reduction could at least in part underlie the reduced lifespan of offspring from older parents.

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Section: Discussionsupporting

confidence: 86%

Experimental demonstration that offspring fathered by old males have shorter telomeres and reduced lifespans

2018

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“…Finally, our closest living relatives, chimpanzees, show a similar PAC-TL association despite having very different mating, rearing (e.g. no paternal care) and social systems than humans [48]. Collectively, these findings suggest that these other sources of confounding are unlikely to account for the PAC-TL association.…”

Section: Is the Pac Association With Tl Causal In Humans?mentioning

confidence: 69%

The paternal age at conception effect on offspring telomere length: mechanistic, comparative and adaptive perspectives

Eisenberg

Kuzawa

2018

Phil. Trans. R. Soc. B

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104

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Telomeres are repeating DNA found at the ends of chromosomes that, in the absence of restorative processes, shorten with cell replications and are implicated as a cause of senescence. It appears that sperm telomere length (TL) increases with age in humans, and as a result offspring of older fathers inherit longer telomeres. We review possible mechanisms underlying this paternal age at conception (PAC) effect on TL, including sperm telomere extension due to telomerase activity, age-dependent changes in the spermatogonial stem cell population (possibly driven by 'selfish' spermatogonia) and non-causal confounding. In contrast to the lengthening of TL with PAC, higher maternal age at conception appears to predict shorter offspring TL in humans. We review evidence for heterogeneity across species in the PAC effect on TL, which could relate to differences in statistical power, sperm production rates or testicular telomerase activity. Finally, we review the hypothesis that the PAC effect on TL may allow a gradual multi-generational adaptive calibration of maintenance effort, and reproductive lifespan, to local demographic conditions: descendants of males who reproduced at a later age are likely to find themselves in an environment where increased maintenance effort, allowing later reproduction, represents a fitness improving resource allocation.This article is part of the theme issue 'Understanding diversity in telomere dynamics'.

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“…This result is surprising, given that paternal age at conception is typically positively associated with offspring telomeres (e.g. in humans [63] and chimpanzees (Pan troglodytes) [64]). It is possible that older male meerkats lose condition faster than humans or chimpanzees, with concomitant decreases in sperm and pup telomere lengths, but further work would be needed to clarify the role of paternal age at conception in meerkat telomere dynamics.…”

Section: Discussionmentioning

confidence: 98%

Effects of early-life competition and maternal nutrition on telomere lengths in wild meerkats

et al. 2017

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Effects of early-life competition and maternal nutrition on telomere lengths in wild meerkats. Proceedings of the Royal Society of London Series B: Biological Sciences, 284(1861), 20171383. (doi:10.1098/rspb.2017.1383 This is the author's final accepted version.There may be differences between this version and the published version. You are advised to consult the publisher's version if you wish to cite from it.http://eprints.gla.ac.uk/147697/ Here, we investigate the link between early-life competition and telomere length in wild 23 meerkats. Our results show that, when multiple females breed concurrently, increases in the 24 number of pups in the group are associated with shorter telomeres in pups. Given that pups 25 from different litters compete for access to milk, we tested whether this effect is due to 26 nutritional constraints on maternal milk production, by experimentally supplementing 27 females' diets during gestation and lactation. While control pups facing high competition had 28 shorter telomeres, the negative effects of pup number on telomere lengths were absent when 29 maternal nutrition was experimentally improved. Shortened pup telomeres were associated 30 with reduced survival to adulthood, suggesting that early-life competition for nutrition has 31 detrimental fitness consequences that are reflected in telomere lengths. Dominant females 32 commonly kill pups born to subordinates, thereby reducing competition and increasing 33 growth rates of their own pups. Our work suggests an additional benefit of infanticide may be 34 that it also reduces telomere shortening caused by competition for resources, with associated 35 benefits for offspring ageing profiles and longevity. 36 37 KEY WORDS 38telomeres, early-life adversity, early-life stress, Suricata suricatta, meerkats, infanticide 39 40 41Introduction 42

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Paternal and grandpaternal ages at conception and descendant telomere lengths in chimpanzees and humans

Cited by 37 publications

References 59 publications

Experimental demonstration that offspring fathered by old males have shorter telomeres and reduced lifespans

Experimental demonstration that offspring fathered by old males have shorter telomeres and reduced lifespans

The paternal age at conception effect on offspring telomere length: mechanistic, comparative and adaptive perspectives

Effects of early-life competition and maternal nutrition on telomere lengths in wild meerkats

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