Epigenetic inheritance of telomere length in wild birds

PLoS Genet. 2019 Feb 14;15(2):e1007827. doi: 10.1371/journal.pgen.1007827. eCollection 2019 Feb.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Wild / genetics*
  • Birds / genetics*
  • Cross-Sectional Studies
  • Epigenesis, Genetic / genetics*
  • Epigenomics / methods
  • Fathers
  • Female
  • Heredity / genetics*
  • Male
  • Paternal Age
  • Reproduction / genetics
  • Spermatozoa / physiology
  • Telomere / genetics*

Grants and funding

CB was supported by a research fellowship of the German Research Foundation, DFG (grant no. BA 5422/1-1; www.dfg.de). JJB was funded by a grant of the Netherlands Organisation for Scientific Research, NWO (grant no. 823.01.009; www.nwo.nl) awarded to SV. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.