Epigenetic inheritance of telomere length in wild birds.

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 i...

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Main Authors: Christina Bauch, Jelle J Boonekamp, Peter Korsten, Ellis Mulder, Simon Verhulst
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-02-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1007827
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spelling doaj-ae9b65e032bf42b783d2302c17898d9d2021-04-21T13:49:07ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042019-02-01152e100782710.1371/journal.pgen.1007827Epigenetic inheritance of telomere length in wild birds.Christina BauchJelle J BoonekampPeter KorstenEllis MulderSimon VerhulstTelomere 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.https://doi.org/10.1371/journal.pgen.1007827
collection DOAJ
language English
format Article
sources DOAJ
author Christina Bauch
Jelle J Boonekamp
Peter Korsten
Ellis Mulder
Simon Verhulst
spellingShingle Christina Bauch
Jelle J Boonekamp
Peter Korsten
Ellis Mulder
Simon Verhulst
Epigenetic inheritance of telomere length in wild birds.
PLoS Genetics
author_facet Christina Bauch
Jelle J Boonekamp
Peter Korsten
Ellis Mulder
Simon Verhulst
author_sort Christina Bauch
title Epigenetic inheritance of telomere length in wild birds.
title_short Epigenetic inheritance of telomere length in wild birds.
title_full Epigenetic inheritance of telomere length in wild birds.
title_fullStr Epigenetic inheritance of telomere length in wild birds.
title_full_unstemmed Epigenetic inheritance of telomere length in wild birds.
title_sort epigenetic inheritance of telomere length in wild birds.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2019-02-01
description 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.
url https://doi.org/10.1371/journal.pgen.1007827
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AT jellejboonekamp epigeneticinheritanceoftelomerelengthinwildbirds
AT peterkorsten epigeneticinheritanceoftelomerelengthinwildbirds
AT ellismulder epigeneticinheritanceoftelomerelengthinwildbirds
AT simonverhulst epigeneticinheritanceoftelomerelengthinwildbirds
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