Abstract

Telomeres are conserved DNA-protein structures at the termini of eukaryotic chromosomes which contribute to maintenance of genome integrity, and their shortening leads to cell senescence, with negative consequences for organismal functions. Because telomere erosion is influenced by extrinsic and endogenous factors, telomere dynamics may provide a mechanistic basis for evolutionary and physiological trade-offs. Yet, knowledge of fundamental aspects of telomere biology under natural selection regimes, including sex- and context-dependent variation in early-life, and the covariation between telomere dynamics and growth, is scant. In this study of barn swallows (Hirundo rustica) we investigated the sex-dependent telomere erosion during nestling period, and the covariation between relative telomere length and body and plumage growth. Finally, we tested whether any covariation between growth traits and relative telomere length depends on the social environment, as influenced by sibling sex ratio. Relative telomere length declined on average over the period of nestling maximal growth rate (between 7 and 16 days of age) and differently covaried with initial relative telomere length in either sex. The frequency distribution of changes in relative telomere length was bimodal, with most nestlings decreasing and some increasing relative telomere length, but none of the offspring traits predicted the a posteriori identified group to which individual nestlings belonged. Tail and wing length increased with relative telomere length, but more steeply in males than females, and this relationship held both at the within- and among-broods levels. Moreover, the increase in plumage phenotypic values was steeper when the sex ratio of an individual’s siblings was female-biased. Our study provides evidence for telomere shortening during early life according to subtly different dynamics in either sex. Furthermore, it shows that the positive covariation between growth and relative telomere length depends on sex as well as social environment, in terms of sibling sex ratio.

Highlights

  • Telomeres are nucleoproteins located at the termini of eukaryotic chromosomes [1,2,3,4] which play an essential role in the maintenance of chromosome integrity [5,6,7]

  • The results of the analyses where morphological traits at age 16 were modelled in relation to relative TL7 were qualitatively similar to those obtained based on relative TL16. In this correlational study we analyzed sex-dependent variation of relative telomere length (TL) and telomere shortening of nestling barn swallows and whether any covariation between morphological traits and relative TL or telomere shortening depended on social effects

  • Telomere length measurements were carried out in peripheral blood; these are considered to provide a good evaluation of telomere length and dynamics in the entire organism [70,71]

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Summary

Introduction

Telomeres are nucleoproteins located at the termini of eukaryotic chromosomes [1,2,3,4] which play an essential role in the maintenance of chromosome integrity [5,6,7]. Telomeric repeat tracts vary considerably in length between organisms [8]; in humans, double stranded telomeric DNA extends for a few Kb (up to 10) and ends with a G-rich 3’ overhang [9] which folds back and invades the double stranded DNA forming a peculiar structure called T-loop [3]. Because of its role in controlling cell loss and renewal, progressive erosion of telomeres and cellular replicative senescence are one of the main candidate mechanisms for organismal loss of function with age [7,8]. Rapid deletion in size of telomeric sequences through recombination based mechanisms was reported in the yeast Saccharomyces cerevisiae [12] and in human cells during apoptosis, senescence and tumorigenesis [13]. Telomere length and shortening may depend on genetic differences among individuals, available estimates of genetic variance in telomere length are few [15]

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