Longitudinal evidence that older parents produce offspring with longer telomeres in a wild social bird

Brown, Andy; Wood, E. J.; Capilla‐Lasheras, Pablo; Harrison, Xavier A.; Young, Andrew J.

doi:10.1098/rsbl.2021.0409

Cited by 9 publications

(7 citation statements)

References 43 publications

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“…While we expected that old parents would produce chicks with shorter telomeres, as found in other short-lived bird species in line with predictions of the Lansing effect ( Criscuolo et al, 2017 ; Bauch et al, 2019 ), our experimental approach found that old fathers produced daughters with longer telomeres, but only 3 months after hatching, potentially indicating an environmental or an age-dependent epigenetic effect ( Matsushima et al, 2019 ). Positive relationships between parental age and offspring telomere length have previously been foundin long- and short-lived bird species ( Asghar et al, 2015 ; Dupont et al, 2018 ; Brown A. M et al, 2021 ). Such effects may arise indirectly, for example, through improved parental care that older individuals provide compared to inexperienced, younger breeders.…”

Section: Discussionmentioning

confidence: 81%

“…This increase disagrees with much of the published literature, which generally finds a decrease in telomere length in early life ( De Meyer et al, 2007 ; Salomons et al, 2009 ; Boonekamp et al, 2014 ; Hoelzl et al, 2016 ; Cerchiara et al, 2017 ). While a population level increase in telomere length has previously been found in some long-lived bird species ( Haussmann et al, 2007 ; Pauliny et al, 2012 ), other studies have found that telomere elongation for a proportion of chicks is more common in shorter-lived species ( Eisenberg, 2019 ; Brown A. M et al, 2021 ; Brown T et al, 2021 ) and few longer-lived species ( Cerchiara et al, 2017 ). For example, a study on jackdaws Corvus monedula found that between 5 and 30 days post-hatching, telomere lengths increased for 25% of sampled offspring ( Grasman et al, 2011 ).…”

Section: Discussionmentioning

confidence: 85%

“…In further support of our findings is Schroeder et al (2015) which identified a sex-specific heritable parental age effect on offspring fitness in house sparrows with daughters of older fathers having higher lifetime reproductive success than sons of older fathers. There is also increasing evidence demonstrating the potential positive effect of father age on offspring telomere lengths (sons and daughters: Brown A. M et al, 2021 , daughters only: Dupont et al, 2018 ). A combined effect of z-linked inheritance and improved parental care or father quality for offspring of older fathers in our study may then explain why we find a positive effect of father age on daughter telomere lengths.…”

Section: Discussionmentioning

confidence: 99%

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Evidence of Paternal Effects on Telomere Length Increases in Early Life

et al. 2022

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Offspring of older parents in many species have decreased longevity, a faster ageing rate and lower fecundity than offspring born to younger parents. Biomarkers of ageing, such as telomeres, that tend to shorten as individuals age, may provide insight into the mechanisms of such parental age effects. Parental age may be associated with offspring telomere length either directly through inheritance of shortened telomeres or indirectly, for example, through changes in parental care in older parents affecting offspring telomere length. Across the literature there is considerable variation in estimates of the heritability of telomere length, and in the direction and extent of parental age effects on telomere length. To address this, we experimentally tested how parental age is associated with the early-life telomere dynamics of chicks at two time points in a captive population of house sparrows Passer domesticus. We experimentally separated parental age from sex effects, and removed effects of age-assortative mating, by allowing the parent birds to only mate with young, or old partners. The effect of parental age was dependent on the sex of the parent and the chicks, and was found in the father-daughter relationship only; older fathers produced daughters with longer telomere lengths post-fledging. Overall we found that chick telomere length increased between the age of 0.5 and 3 months at the population and individual level. This finding is unusual in birds with such increases more commonly associated with non-avian taxa. Our results suggest parental age effects on telomere length are sex-specific either through indirect or direct inheritance. The study of similar patterns in different species and taxa will help us further understand variation in telomere length and its evolution.

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Section: Discussionmentioning

confidence: 81%

Section: Discussionmentioning

confidence: 85%

Section: Discussionmentioning

confidence: 99%

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Evidence of Paternal Effects on Telomere Length Increases in Early Life

et al. 2022

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“…If strong evidence exists for genetic inheritance of TL, conclusions on relationship between parental age at conception and TL of offspring depend on the species studied. In several studies (mostly birds), TL shortens as parents age and predicts offspring TL with sex-specific differences in TL inheritance [4,6,[37][38][39][40][41]. By constrast, a weak or no relationships between TL and parental TL has been observed in other species [42][43][44][45].…”

Section: Discussionmentioning

confidence: 99%

Parental age at conception on mouse lemur’s offspring longevity: sex-specific maternal effects

Perret

Aude

2022

Preprint

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Parental age at conception often influences offspring’s longevity, a phenomenon referred as the “Lansing effect” described in large variety of organisms. But, the majority of the results refer to the survival of juveniles, mainly explained by an inadequate parental care by the elderly parents, mostly the mothers. Studies on the effect of parental age on offspring’s longevity in adulthood remain few, excepted in humans for whom effects of parental age are variable according to statistical models or socioeconomic environments. In a small primate which the longevity reaches up to 12 years, we investigated the effects of parental age at conception on the longevity of offspring (N = 278) issued from parents with known longevity. None of the postnatal parameters, including body mass, influenced offspring’s longevity. Mothers’ age at conception significantly affected offspring’s longevity in males but not females. By contrast, fathers’ age at conception did not influence offspring’s longevity. When considering the age of the breeding pairs at conception, the older the mother, the lower the longevity of male offspring with a minimum when the father was aged. No such correlation was observed for female offspring. Lastly, the longevity of female offspring was significantly positively related to the longevity of both parents. Compared with current studies, the surprisingly minor effect of fathers ‘age and the major impact of mothers’ age on male offspring survival, despite favourable conditions, were discussed in relation with the highly seasonal reproduction in mouse lemurs.

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“…However, there is currently no robust evidence that the decline in offspring speed with maternal age is mediated by effects on offspring size. Besides, older mothers can influence offspring independent of maternal care and offspring weight [21,56].…”

Section: Discussionmentioning

confidence: 99%

Evidence of maternal and paternal age effects on speed in thoroughbred racehorses

2022

Self Cite

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Effects of parental age on offspring viability have been reported in a wide range of species. However, to what extent parental age influences offspring traits beyond viability remains unclear. Moreover, previous research has primarily focused on maternal age effects. The purpose of this study was to test for paternal and maternal age effects on offspring speed in thoroughbred racehorses. We analysed over 900 000 race performances by over 100 000 horses on British racecourses between 1996 and 2019. With knowledge of the age of all 41 107 dams and 2 887 sires at offspring conception, we jointly modelled maternal and paternal age effects using a ‘within-individual centring’ approach. Within-parents, we identified a significant effect of maternal age on offspring speed of −0.017 yards s −1 yr −1 and a corresponding paternal age effect of −0.011 yards s −1 yr −1 . Although maternal age effects were stronger (more negative), the existence and magnitude of paternal effects is particularly noteworthy, given thoroughbred sires have no involvement in parental care. Our results also suggest that the selective disappearance of both sires and dams is ongoing. These findings could potentially be used to optimize thoroughbred racehorse breeding decisions, and more generally, add to the increasing body of evidence that both maternal and paternal age affect a range of offspring characteristics.

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Longitudinal evidence that older parents produce offspring with longer telomeres in a wild social bird

Cited by 9 publications

References 43 publications

Evidence of Paternal Effects on Telomere Length Increases in Early Life

Evidence of Paternal Effects on Telomere Length Increases in Early Life

Parental age at conception on mouse lemur’s offspring longevity: sex-specific maternal effects

Evidence of maternal and paternal age effects on speed in thoroughbred racehorses

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