Abstract

DNA methylation could shape phenotypic responses to environmental cues and underlie developmental plasticity. Environmentally induced changes in DNA methylation during development can give rise to stable phenotypic traits and thus affect fitness. In the laboratory, it has been shown that the vertebrate methylome undergoes dynamic reprogramming during development, creating a critical window for environmentally induced epigenetic modifications. Studies of DNA methylation in the wild are lacking, yet are essential for understanding how genes and the environment interact to affect phenotypic development and ultimately fitness. Furthermore, our knowledge of the establishment of methylation patterns during development in birds is limited. We quantified genome‐wide DNA methylation at various stages of embryonic and postnatal development in an altricial passerine bird, the great tit Parus major. While, there was no change in global DNA methylation in embryonic tissue during the second half of embryonic development, a twofold increase in DNA methylation in blood occurred between 6 and 15 days posthatch. Though not directly comparable, DNA methylation levels were higher in the blood of nestlings compared with embryonic tissue at any stage of prenatal development. This provides the first evidence that DNA methylation undergoes global change during development in a wild bird, supporting the hypothesis that methylation mediates phenotypic development. Furthermore, the plasticity of DNA methylation demonstrated during late postnatal development, in the present study, suggests a wide window during which DNA methylation could be sensitive to environmental influences. This is particularly important for our understanding of the mechanisms by which early‐life conditions influence later‐life performance. While, we found no evidence for differences in genome‐wide methylation in relation to habitat of origin, environmental variation is likely to be an important driver of variation in methylation at specific loci.

Highlights

  • There is increasing interest among ecologists and evolutionary bi‐ ologists in the potential for epigenetic mechanisms to shape envi‐ ronmentally induced phenotypic responses (Angers, Castonguay, & Massicotte, 2010; Bossdorf, Richards, & Pigliucci, 2008; Hu & Barrett, 2017; Verhoeven, VonHoldt, & Sork, 2016)

  • We present the first evidence for within‐individual changes in ge‐ nome‐wide DNA methylation during development of an altricial bird

  • The observed develop‐ mental change in DNA methylation is of great significance, as it is among the first evidence that DNA methylation could play a funda‐ mental role in shaping phenotypic plasticity during early life in altri‐ cial birds (Rubenstein et al, 2016; Sheldon et al, 2018)

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Summary

| INTRODUCTION

There is increasing interest among ecologists and evolutionary bi‐ ologists in the potential for epigenetic mechanisms to shape envi‐ ronmentally induced phenotypic responses (Angers, Castonguay, & Massicotte, 2010; Bossdorf, Richards, & Pigliucci, 2008; Hu & Barrett, 2017; Verhoeven, VonHoldt, & Sork, 2016). DNA methylation—the most widely studied epigenetic mark—plays a crucial role in regulating gene expression and genomic stability (Klose & Bird, 2006; Weber et al, 2007) It has been shown in a number of vertebrates, in the laboratory, that the methylome undergoes reprogramming during development. The established patterns of methylation are subsequently main‐ tained through mitotic cell division and can create permanent changes in gene expression and stable phenotypic traits (Jablonka & Raz, 2009; Weaver et al, 2004) This cycle of epi‐ genetic reprogramming appears to be critical in directing embryonic development and determining patterns of DNA methylation in so‐ matic cells (Bird, 2002). Using embryos and nestlings originating from both urban and rural environments, we investigated the potential for environmen‐ tally induced variation in genome‐wide DNA methylation levels

| MATERIALS AND METHODS
| DISCUSSION
Findings
ETHICAL APPROVAL
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