Epigenetic inheritance of telomere length in wild birds

Abstract

Abstract:Telomere length (TL) predicts health and lifespan in humans and other organisms, making the identification of the causes of TL variation of interest. At conception, zygotes inherit genes that regulate TL during early development, but at the same time already express a phenotype, which is the TL of the parental gametes that formed the zygote. Whether the effect of gamete TL is transient or affects TL for life depends on the extent to which regulatory genes compensate for gamete TL variation during early development. A carry-over effect of parental TL, resulting in epigenetic inheritance, has been suggested to explain the observed relationship between parental age and offspring TL in humans and other species. However, reports of parental age effects are based on cross-sectional data, and age at reproduction has numerous confounds. Furthermore, parental age may affect offspring telomere dynamics between conception and sampling, which could also explain the paternal age effect. Using longitudinal telomere data of jackdaw parents and their chicks, we show that chicks hatched with shorter telomeres as individual fathers aged, whereas mother age had no effect. By crossfostering eggs, we confirmed the paternal age effect to be independent of paternal care after conception. The epigenetic effect accounted for 34% of the variance in offspring TL that was explained by paternal telomere length; the remaining 66% we ascribe to a combination of environmental and additive genetic effects. Thus, our results strongly indicate epigenetic inheritance of TL, with potential consequences for offspring fitness prospects.. CC-BY-NC-ND 4.0 International license not peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was . http://dx.doi.org/10.1101/284208 doi: bioRxiv preprint first posted online Mar. 18, 2018; Significance statement:Telomeres are DNA-protein structures at chromosome ends and their length predicts remaining lifespan in humans and other organisms. Variation in telomere length is thought to be largely of genetic origin, but telomere inheritance may be unusual because a fertilised cell already has a telomere length (most traits are first expressed later in life). Telomeres shorten with age, and, using long-term individual-based data of jackdaw families, we show that as fathers aged, they produced chicks with shorter telomeres. This shows that paternal telomere length directly affects offspring telomere length, i.e. is inherited genetically but without the involvement of genes. This is known as an epigenetic effect and explained a large part (≥34%) of the telomere resemblance between fathers and their offspring.

Associations of sperm telomere length with semen parameters, clinical outcomes and lifestyle factors in human normozoospermic samples

“…This elongation phenomenon is inherited from the father to offspring independently to the offspring sex 56 and seems to be conserved across species. 57,58 Interestingly, this paternal inheritance is also evident in leucocytes. 59 Older parental age at conception has been shown to have a negative effect on both offspring viability in mice 60 and the overall fitness of offspring in humans.…”

Telomere length is repeatable, shortens with age and reproductive success, and predicts remaining lifespan in a long‐lived seabird

“…Combined with the high within‐individual repeatability in telomere length, this raises the intriguing question of whether an individual's telomere length and lifespan are already partly determined early in life (Eastwood et al, ; Heidinger et al, ). In the same colony of common terns, we were previously unable to identify environmental factors that affected telomere length after hatching (Vedder, Verhulst, et al, ), but conditions during embryonic development (Vedder et al, ), as well as paternal age (Bouwhuis, Verhulst, Bauch, & Vedder, ; see also Bauch, Boonekamp, Korsten, Mulder, & Verhulst, for a longitudinal study in jackdaws Corvus monedula ), affected telomere length in common tern chicks. If both telomere length and adult lifespan are particularly susceptible to such factors early in life (Bouwhuis, Vedder, & Becker, ), this can explain the high within‐individual consistency in telomere length combined with its ability to predict adult lifespan.…”

Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets

“…The high heritability of telomere length suggests that the joint action of these mechanisms is heritable, resulting in a canalised, developmentally robust predetermined telomere length. At the same time epigenetic effects have also been observed showing that offspring telomere length decreases with paternal age (Bauch et al 2019). The presence of such epigenetic effects implies that telomere length regulatory mechanisms may be limited in their capacity to fully compensate for the telomere length that was physically inherited from the paternal gametes.…”