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.
Highlights
Telomeres are evolutionarily conserved DNA sequence repeats, which form the ends of chromosomes together with associated proteins and contribute to genome stability [1]
Using longterm individual-based data of jackdaw families, we found that as fathers aged, they produced chicks with shorter telomeres. This suggests that telomere length inheritance has an epigenetic component
The negative, non-significant effect of maternal age on offspring telomere length we observed (Table 2B) we attribute to the age of their mates, because pair bonds in jackdaws are maintained over many years and maternal and paternal age are correlated
Summary
Telomeres are evolutionarily conserved DNA sequence repeats, which form the ends of chromosomes together with associated proteins and contribute to genome stability [1]. Inheritance of TL is unusual in that the TL phenotype is directly expressed in the zygote without any effect of its own genome This is because the zygote’s set of chromosomes carries the telomeres of the two parental gametes. The latter case would imply the inheritance of parental TL, which is independent of DNA sequence variation (in vertebrates (TTAGGG)n [15]), but a change in telomere sequence length (n). We interpret this as a form of epigenetic inheritance component on TL [16,17]. Note that this epigenetic inheritance mechanism differs from better known epigenetic mechanisms such as DNA methylation in that it does not affect the phenotype (TL) by modulating gene expression, but instead through direct inheritance of the phenotype itself and has been referred to as “epigenetic-like” [17]
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