Epigenetic inheritance of telomere length in wild birds

Epigenetic inheritance of telomere length in wild birds
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DOI:
10.1371/journal.pgen.1007827
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发表时间:
2019-02-01
期刊:
影响因子:
4.5
通讯作者:
Verhulst, Simon
Verhulst, Simon
中科院分区:
生物学2区
文献类型:
--
作者:
Bauch, Christina;Boonekamp, Jelle J.;Verhulst, Simon

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端粒长度(TL)预测健康和生存跨类群。个体之间的TL变异被认为主要是遗传起源,但端粒遗传是不寻常的,因为合子已经表达了TL表型,即亲本配子的TL。在包括人类在内的许多物种中,后代TL随父代年龄的变化而变化,可能是通过精子中与年龄相关的TL变化,这表明了一种表观遗传遗传机制。然而,目前的证据是基于横截面分析,和年龄在生殖与父亲之间的TL变化混淆。此外,表观遗传TL遗传的数量重要性是未知的。使用纵向数据的自由生活寒鸦monedula,我们发现,红细胞TL随后的后代随着父母的年龄在个别父亲,但不是母亲。通过交叉培养卵子,我们证实了父亲的年龄效应是独立的父亲的年龄依赖的照顾。表观遗传遗传占最低的34%的后代TL的方差,这是由父亲的TL解释。这是一个最小的估计,因为它忽略了表观遗传的组成部分,在父亲的TL变异和精子的TL异质性内射精。我们的研究结果表明,一个重要的表观遗传组成部分的遗传TL与后代健身prospects.Author摘要端粒是DNA-蛋白质结构在染色体末端和短端粒长度预测减少生存在人类,鸟类和其他生物体的潜在后果。个体之间端粒长度的变化被认为主要是遗传起源,但端粒遗传可能是不寻常的,因为不仅调节端粒长度的基因被遗传,而且受精细胞已经具有端粒长度(来自亲本配子)。利用寒鸦家族(一种小型鸦科鸟类)的长期个体数据,我们发现随着父亲年龄的增长,他们生出的小鸡端粒更短。这表明端粒长度遗传具有表观遗传成分。为了研究受精细胞中的端粒长度在多大程度上影响出生后的端粒长度,我们将父亲的端粒长度与他们连续后代的端粒长度进行了比较。这种表观遗传成分解释了端粒长度遗传的很大一部分(三分之一),而母体端粒长度则没有这种影响。性别差异符合终身精子形成导致精子细胞端粒长度变化的观点,而女性配子都是在出生前形成的,它们的端粒长度不会随着时间的推移而变化。
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.Author summary Telomeres are DNA-protein structures at chromosome ends and a short telomere length predicts reduced survival in humans, birds and other organisms. Variation in telomere length between individuals is thought to be largely of genetic origin, but telomere inheritance may be unusual because not only genes regulating telomere length are inherited, but a fertilised cell already has a telomere length (from the parental gametes). Using long-term individual-based data of jackdaw families (a small corvid species), we found that as fathers aged, they produced chicks with shorter telomeres. This suggests that telomere length inheritance has an epigenetic component. To investigate to what extent telomere length in the fertilised cell affects telomere length after birth, we compared telomere length over years within fathers with the telomere length of their consecutive offspring. This epigenetic component explained a substantial part ( one third) of the telomere length inheritance; whereas there was no such effect of maternal telomere length. The sex difference fits the idea that lifelong sperm formation leads to change in telomere length of the sperm cells, whereas female gametes are all formed before birth and their telomere length does not change over time.