Inter-generational resemblance of methylation levels at circadian genes and associations with phenology in the barn swallow

Abstract

Regulation of gene expression can occur via epigenetic effects as mediated by DNA methylation. The potential for epigenetic effects to be transmitted across generations, thus modulating phenotypic variation and affecting ecological and evolutionary processes, is increasingly appreciated. However, the study of variation in epigenomes and inter-generational transmission of epigenetic alterations in wild populations is at its very infancy. We studied sex- and age-related variation in DNA methylation and parent-offspring resemblance in methylation profiles in the barn swallows. We focused on a class of highly conserved ‘clock’ genes (clock, cry1, per2, per3, timeless) relevant in the timing of activities of major ecological importance. In addition, we considerably expanded previous analyses on the relationship between methylation at clock genes and breeding date, a key fitness trait in barn swallows. We found positive assortative mating for methylation at one clock locus . Methylation varied between the nestling and the adult stage, and according to sex. Individuals with relatively high methylation as nestlings also had high methylation levels when adults. Extensive parent-nestling resemblance in methylation levels was observed. Occurrence of extra-pair fertilizations allowed to disclose evidence hinting at a prevalence of paternal germline or sperm quality effects over common environment effects in generating father-offspring resemblance in methylation. Finally, we found an association between methylation at the clock poly-Q region, but not at other loci , and breeding date. We thus provided evidence for sex-dependent variation and the first account of parent-offspring resemblance in methylation in any wild vertebrate. We also showed that epigenetics may influence phenotypic plasticity of timing of life cycle events, thus having a major impact on fitness.

Candidate gene polymorphisms are linked to dispersive and migratory behaviour: Searching for a mechanism behind the “paradox of the great speciators”

“…In birds, different associations (negative, positive or no correlation) in different populations, species and candidate genes are often reported (Table S1). Furthermore, few studies have considered candidate gene–environment interactions (but see Bourret & Garant, 2015; Liedvogel & Sheldon, 2010; Liedvogel et al, 2009) or methylation patterns that have been found to explain diverse complex behaviours in birds (Saino et al, 2019). The lack of replicability even within the same species could also be a product of sampling in different locations with a low number of individuals leading to a lack of statistical power, choosing different variables and proxies to measure migration and dispersiveness, using different methodologies to analyse data, publication bias or a combination of all of these (Yang et al, 2022).…”

Time trees and clock genes: a systematic review and comparative analysis of contemporary avian migration genetics

“…Firstly, it assumes equal bi‐allelic expression from a single locus, an absence of parental imprinting (Jang et al ., 2013), and identical regulation of both alleles. This contradicts the central hypothesis of altered entrainment cycles in the presence of a length polymorphism as well as some existing evidence for heritable patterns of methylation in birds (Romano et al ., 2017; Saino et al ., 2019). Secondly it assumes knowledge of the copy number variation for the studied genes (Skinner et al ., 2014), which may be particularly complex in birds given that different karyotypes where chromosome numbers ranging between 78 and 82 can be found in most species (Degrandi et al ., 2020).…”

Candidate gene length polymorphisms are linked to dispersive behaviour: searching for a mechanism behind the “paradox of the great speciators”

“…In birds, different associations (negative, positive or no correlation) in different populations, species and candidate genes are often reported (Table S1). Furthermore, few studies have considered candidate geneenvironment interactions (but see Liedvogel et al, 2009; Liedvogel and Sheldon, 2010; Bourret and Garant, 2015) or methylation patterns that have been found to explain diverse complex behaviours in birds (Saino et al, 2019). The lack of replicability even within the same species could also be a product of sampling in different locations with a low number of individuals leading to a lack of statistical power, choosing different variables and proxies to measure migration and dispersiveness, using different methodologies to analyse data, publication bias or a combination of all of these (Yang et al, 2022).…”