Variation in DNA Methylation in Avian Nestlings Is Largely Determined by Genetic Effects

Sepers, Bernice; Chen, Rebecca Shuhua; Memelink, Michelle; Verhoeven, Koen; Oers, Kees van

doi:10.1093/molbev/msad086

Cited by 19 publications

(14 citation statements)

References 163 publications

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“…Songbirds lay multiple clutches in a season; egg composition, development, and fledging rates vary across clutches, with productivity declining across successive clutches (Monaghan & Nager, 1997; Sockman et al., 2006). Recent work in birds suggests that DNA methylation differences between individuals are due to a genetic basis and vary little due to the postnatal rearing environment (egg cross‐fostering experiment; Sepers et al., 2023). However, given that our study manipulates early developmental exposure to CORT, the prenatal rearing environment may well be an important factor in determining offspring DNA methylation differences.…”

Section: Discussionmentioning

confidence: 99%

Maternally derived avian corticosterone affects offspring genome‐wide DNA methylation in a passerine species

Miltiadous,

Callahan,

Dujon

et al. 2024

Molecular Ecology

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Avian embryos develop in an egg composition which reflects both maternal condition and the recent environment of their mother. In birds, yolk corticosterone (CORT) influences development by impacting pre‐ and postnatal growth, as well as nestling stress responses and development. One possible mechanism through which maternal CORT may affect offspring development is via changes to offspring DNA methylation. We sought to investigate this, for the first time in birds, by quantifying the impact of manipulations to maternal CORT on offspring DNA methylation. We non‐invasively manipulated plasma CORT concentrations of egg‐laying female zebra finches (Taeniopygia castanotis) with an acute dose of CORT administered around the time of ovulation and collected their eggs. We then assessed DNA methylation in the resulting embryonic tissue and in their associated vitelline membrane blood vessels, during early development (5 days after lay), using two established methods – liquid chromatography–mass spectrometry (LC–MS) and methylation‐sensitive amplification fragment length polymorphism (MS‐AFLP). LC–MS analysis showed that global DNA methylation was lower in embryos from CORT‐treated mothers, compared to control embryos. In contrast, blood vessel DNA from eggs from CORT‐treated mothers showed global methylation increases, compared to control samples. There was a higher proportion of global DNA methylation in the embryonic DNA of second clutches, compared to first clutches. Locus‐specific analyses using MS‐AFLP did not reveal a treatment effect. Our results indicate that an acute elevation of maternal CORT around ovulation impacts DNA methylation patterns in their offspring. This could provide a mechanistic understanding of how a mother's experience can affect her offspring's phenotype.

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Section: Discussionmentioning

confidence: 99%

Maternally derived avian corticosterone affects offspring genome‐wide DNA methylation in a passerine species

Miltiadous,

Callahan,

Dujon

et al. 2024

Molecular Ecology

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“…The birds used in this study were part of a brood size manipulation experiment as described in detail in Sepers, Chen, et al. ( 2023 ) and Sepers, Mateman, et al. ( 2023 ).…”

Section: Methodsmentioning

confidence: 99%

“…This study was conducted from April to September 2018, using a long-term nest box population of great tits (P. major) in Westerheide, a mixed wood forest near Arnhem, the Netherlands (52°01′00 N, 05°50′30 E). The birds used in this study were part of a brood size manipulation experiment as described in detail in Sepers, Chen, et al (2023) and Sepers, Mateman, et al (2023). In short, we conducted a partial cross-foster design and manipulated the original brood sizes in 32 broods.…”

Section: Subjects the Study Site And The Sample Sizementioning

confidence: 99%

“…Few studies have examined the effects of the postnatal rearing environment on DNA methylation in wild nestlings (Sepers et al., 2021 ; Sepers, Chen, et al., 2023 ; Sepers, Mateman, et al., 2023 ; Sheldon et al., 2018 ; von Holdt et al., 2023 ), but none examined (lasting) effects in fledglings or adults. Using a cross‐fostering and brood size manipulation experiment in wild great tits, we previously showed that nestlings from enlarged and reduced broods differ in biometric and behavioural traits, but they differed in methylation level in one CpG site only.…”

Section: Introductionmentioning

confidence: 99%

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Early developmental carry‐over effects on exploratory behaviour and DNA methylation in wild great tits (Parus major)

Sepers,

Verhoeven,

van Oers

2024

Evolutionary Applications

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Adverse, postnatal conditions experienced during development are known to induce lingering effects on morphology, behaviour, reproduction and survival. Despite the importance of early developmental stress for shaping the adult phenotype, it is largely unknown which molecular mechanisms allow for the induction and maintenance of such phenotypic effects once the early environmental conditions are released. Here we aimed to investigate whether lasting early developmental phenotypic changes are associated with post‐developmental DNA methylation changes. We used a cross‐foster and brood size experiment in great tit (Parus major) nestlings, which induced post‐fledging effects on biometric measures and exploratory behaviour, a validated personality trait. We investigated whether these post‐fledging effects are associated with DNA methylation levels of CpG sites in erythrocyte DNA. Individuals raised in enlarged broods caught up on their developmental delay after reaching independence and became more explorative as days since fledging passed, while the exploratory scores of individuals that were raised in reduced broods remained stable. Although we previously found that brood enlargement hardly affected the pre‐fledging methylation levels, we found 420 CpG sites that were differentially methylated between fledged individuals that were raised in small versus large sized broods. A considerable number of the affected CpG sites were located in or near genes involved in metabolism, growth, behaviour and cognition. Since the biological functions of these genes line up with the observed post‐fledging phenotypic effects of brood size, our results suggest that DNA methylation provides organisms the opportunity to modulate their condition once the environmental conditions allow it. In conclusion, this study shows that nutritional stress imposed by enlarged brood size during early development associates with variation in DNA methylation later in life. We propose that treatment‐associated DNA methylation differences may arise in relation to pre‐ or post‐fledging phenotypic changes, rather than that they are directly induced by the environment during early development.

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“…However, profiling these patterns in the common myna lays important groundwork for future studies into genome-methylome interactions (e.g. Sun et al 2021;Sepers et al 2023).…”

Section: Genomic Landscapementioning

confidence: 99%

The genome of a globally invasive passerine, the common myna (Acridotheres tristis)

Stuart,

Johnson,

Major

et al. 2023

Preprint

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In an era of global climate change and massive environmental disturbance, biodiversity conservation is receiving increased attention. Conservation efforts are being greatly aided by genetic tools and approaches, which seek to understand patterns of genetic diversity and how they impact species health and ability to persist under future climate regimes. Invasive species offer vital model systems in which to investigate questions around adaptive potential, with a particular focus on how changes in genetic diversity and effective population size interact with the novel selection regime of the invaded range to drive rapid evolution. The common myna (Acridotheres tristis) is a globally invasive passerine, which has undergone multiple concurrent and sequential bottlenecks across its globally invasive range, and yet has established itself across a diverse array of ecological conditions. It is therefore an excellent model species for research both into the persistence of low-diversity populations and the mechanics of biological invasion. To underpin research on the invasion genetics of this species, we present the genome assembly of the common myna, assembled using a backbone of Oxford Nanopore Technologies long reads, alongside an RNA-seq based transcriptome and genome annotation. To provide genomic context for future studies, we describe the genomic landscape of this species, including genome wide allelic diversity, methylation, repeats, and recombination rate, as well as an examination of gene family expansions and contractions. Finally, we use demographic analysis to identify that some native regions underwent a dramatic population increase between the two most recent periods of glaciation, but also reveal artefactual impacts of genetic bottlenecks on demographic analysis.

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Variation in DNA Methylation in Avian Nestlings Is Largely Determined by Genetic Effects

Cited by 19 publications

References 163 publications

Maternally derived avian corticosterone affects offspring genome‐wide DNA methylation in a passerine species

Maternally derived avian corticosterone affects offspring genome‐wide DNA methylation in a passerine species

Early developmental carry‐over effects on exploratory behaviour and DNA methylation in wild great tits (Parus major)

The genome of a globally invasive passerine, the common myna (Acridotheres tristis)

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