Age‐ and quality‐dependent DNA methylation correlate with melanin‐based coloration in a wild bird

Abstract

Secondary sexual trait expression can be influenced by fixed individual factors (such as genetic quality) as well as by dynamic factors (such as age and environmentally induced gene expression) that may be associated with variation in condition or quality. In particular, melanin‐based traits are known to relate to condition and there is a well‐characterized genetic pathway underpinning their expression. However, the mechanisms linking variable trait expression to genetic quality remain unclear. One plausible mechanism is that genetic quality could influence trait expression via differential methylation and differential gene expression. We therefore conducted a pilot study examining DNA methylation at a candidate gene (agouti‐related neuropeptide: AgRP) in the black grouse Lyrurus tetrix. We specifically tested whether CpG methylation covaries with age and multilocus heterozygosity (a proxy of genetic quality) and from there whether the expression of a melanin‐based ornament (ultraviolet‐blue chroma) correlates with DNA methylation. Consistent with expectations, we found clear evidence for age‐ and heterozygosity‐specific patterns of DNA methylation, with two CpG sites showing the greatest DNA methylation in highly heterozygous males at their peak age of reproduction. Furthermore, DNA methylation at three CpG sites was significantly positively correlated with ultraviolet‐blue chroma. Ours is the first study to our knowledge to document age‐ and quality‐dependent variation in DNA methylation and to show that dynamic sexual trait expression across the lifespan of an organism is associated with patterns of DNA methylation. Although we cannot demonstrate causality, our work provides empirical support for a mechanism that could potentially link key individual factors to variation in sexual trait expression in a wild vertebrate.

Mite load predicts the quality of sexual color and locomotor performance in a sexually dichromatic lizard

“…Studies exploring sexual color evolution in lizards often determine that older and larger lizards have decreased sexual color expression (Christian & Bedford, ; Schall & Marghoob, ). Because melanin production is also negatively correlated with age (Soulsbury et al, ), and mass and age are positively correlated in lizards (Shine & Charnov, ), it might then be expected that as mass in scrub lizards increases, melanin production decreases, leading to increases in the brightness of sexual colors (i.e., decreased color expression). However, results presented herein show that mass, as a stand‐alone predictor variable, does not predict the brightness of badge color or black borders of male scrub lizards.…”

An ecologist's guide for studying DNA methylation variation in wild vertebrates

“…Other studies aim to provide insights into the link between epigenetic variation and ecologically relevant phenotypic variation. So far, studies have focused on exploratory behaviour (van Oers et al, 2020;Verhulst et al, 2016), novelty-seeking behaviour (Riyahi et al, 2015), salinity tolerance (Heckwolf et al, 2020), stress resilience (Taff et al, 2019), plumage characteristics (Soulsbury et al, 2018;Taff et al, 2019) and patterns of scutes (Caracappa et al, 2016).…”

“…Another popular topic in ecological studies is how DNA methylation levels change over time due to, for example, ageing (Ito et al, 2018;Paoli-Iseppi et al, 2019;Parrott et al, 2014;Polanowski et al, 2014;Soulsbury et al, 2018;Thompson et al, 2017;Wilkinson et al, 2021), where methylation might accumulate over time or in the context of regulation of temporal plastic changes, such as regulation of timing of migration and reproduction (Baerwald et al, 2016;Lindner et al, 2021;Mäkinen et al, 2019;Saino et al, 2017;Viitaniemi et al, 2019) and hibernation (Alvarado et al, 2015).…”

Epigenetic Measurement of Key Vertebrate Population Biology Parameters

“…Follow-up research, however, was able to successfully identify age-related genomic regions and develop the first epigenetic age estimation assay for birds (De Paoli-Iseppi et al, 2019). The other bird-focused study found DNAm relationships between age and heterozygosity in black grouse (Lyrurus tetrix), but their goal was not to develop an assay for age determination (Soulsbury et al, 2018). In reptiles, age negatively correlated with global DNAm in wild alligators (Alligator mississippiensis) in two studies, a trend related to the process of epigenetic drift, but age estimation was not the objective of either study (Parrott et al, 2014;Jones et al, 2015;Nilsen et al, 2016).…”

“…Most studies into epigenetic control of vertebrate sexual mechanisms and development are performed under controlled laboratory conditions (Wen et al, 2014;Laing et al, 2018;Ortega-Recalde et al, 2019). Recently, however, research has begun to also focus upon wild animal populations (Domingos et al, 2018;Martín-del-campo et al, 2018;Soulsbury et al, 2018). The first such study assessed Atlantic salmon (Salmo salar) and DNAm levels during maturation, finding high DNAm variation between two of three analyzed tissue types (gonads and brain, though not in liver) between maturation states (Morán and Pérez-figueroa, 2011).…”