Epigenetic inheritance of telomere length in wild birds

Abstract

Telomere length (TL) predicts health and survival across taxa. Variation in TL between individuals is thought to be largely of genetic origin, but telomere inheritance is unusual, because zygotes already express a TL phenotype, the TL of the parental gametes. Offspring TL changes with paternal age in many species including humans, presumably through age-related TL changes in sperm, suggesting an epigenetic inheritance mechanism. However, present evidence is based on cross-sectional analyses, and age at reproduction is confounded with between-father variation in TL. Furthermore, the quantitative importance of epigenetic TL inheritance is unknown. Using longitudinal data of free-living jackdaws Corvus monedula , we show that erythrocyte TL of subsequent offspring decreases with parental age within individual fathers, but not mothers. By cross-fostering eggs, we confirmed the paternal age effect to be independent of paternal age dependent care. Epigenetic inheritance accounted for a minimum of 34% of the variance in offspring TL that was explained by paternal TL. This is a minimum estimate, because it ignores the epigenetic component in paternal TL variation and sperm TL heterogeneity within ejaculates. Our results indicate an important epigenetic component in the heritability of TL with potential consequences for offspring fitness prospects.

Estimation of environmental and genetic contributions to telomere length variation in a wild mammal

“…Studies in wild populations have provided mixed evidence for PAC and MAC effects. Studies from different taxa, with a variety of mating systems, have shown a negative PAC effect (Bouwhuis et al, 2018;Criscuolo, Zahn, & Bize, 2017;Olsson et al, 2011), including a longitudinal (Bauch, Boonekamp, Korsten, Mulder, & Verhulst, 2019) and an experimental manipulation (Noguera, Metcalfe, & Monaghan, 2018) study. However, other studies have reported no PAC or MAC effect on offspring telomere length (Heidinger et al, 2016;McLennan et al, 2018;Froy et al, 2017;Belmaker, Hallinger, Glynn, Winkler, & Haussmann, 2019) or a positive MAC effect (Asghar et al, 2015).…”

The deteriorating soma and the indispensable germline: gamete senescence and offspring fitness

“…Studies to date in non-human species indicate that this might not be a simple restoration to the average telomere length of the parents. Most importantly in the context of this review, studies of birds, reptiles, and non-human mammals have reported that older fathers have offspring with shorter telomeres [24,91,[109][110][111], though a positive correlation between male and female age within a breeding pair often makes it difficult to separate maternal and paternal effects in natural populations [112]. In controlled conditions using laboratory mice, offspring from older fathers have been reported to have shorter telomeres [91].…”

Cross‐Generational Effects of Parental Age on Offspring Longevity: Are Telomeres an Important Underlying Mechanism?

“…[ 24 ] One mechanism that may be particularly important in these contexts is telomeres. [ 23,25–28 ] Telomeres are highly conserved, repetitive, sequences of DNA at chromosome ends that enhance genome integrity, but shorten during normal cell division and in response to stress. [ 29 ] Once telomeres become critically short, cells stop dividing and both cell loss and the accumulation of senescent cells are expected to contribute to organismal aging.…”

“…[35]. Telomere length is heritable, but accumulating evidence suggests that the age of the parents at the time of offspring production can also influence offspring telomeres, [ 27,36,37 ] which may have important consequences for offspring longevity.…”

“…To further illustrate this idea, a longitudinal study in jackdaws ( Corvus monedula ) (i.e., offspring produced by the same parents were sampled at multiple time points across the parents’ lives) found that although there was no significant effect of a father's average age on offspring telomeres (mimicking a cross‐sectional study), there was a significant negative effect of paternal age on offspring telomeres within individual fathers. [ 27 ] To date, only two studies have used longitudinal sampling designs. Both of these studies were conducted in birds and in both cases there was a negative relationship between either paternal [ 27 ] or maternal [ 28 ] age and offspring telomeres.…”