Fine‐scale population epigenetic structure in relation to gastrointestinal parasite load in red grouse (Lagopus lagopus scotica)

Abstract

Epigenetic modification of cytosine methylation states can be elicited by environmental stresses and may be a key process affecting phenotypic plasticity and adaptation. Parasites are potent stressors with profound physiological and ecological effects on their host, but there is little understanding in how parasites may influence host methylation states. Here, we estimate epigenetic diversity and differentiation among 21 populations of red grouse (Lagopus lagopus scotica) in north-east Scotland and test for association of gastrointestinal parasite load (caecal nematode Trichostrongylus tenuis) with hepatic genome-wide and locus-specific methylation states. Following methylation-sensitive AFLP (MSAP), 129 bands, representing 73 methylation-susceptible and 56 nonmethylated epiloci, were scored across 234 individuals. The populations differed significantly in genome-wide methylation levels and were also significantly epigenetically (FSC = 0.0227; P < 0.001) and genetically (FSC = 0.0058; P < 0.001) differentiated. Parasite load was not associated with either genome-wide methylation levels or epigenetic differentiation. Instead, we found eight disproportionately differentiated epilocus-specific methylation states (FST outliers) using bayescan software and significant positive and negative association of 35 methylation states with parasite load from bespoke generalized estimating equations (GEE), simple logistic regression (sam) and Bayesian environmental analysis (bayenv2). Following Sanger sequencing, genome mapping and geneontology (go) annotation, some of these epiloci were linked to genes involved in regulation of cell cycle, signalling, metabolism, immune system and notably rRNA methylation, histone acetylation and small RNAs. These findings demonstrate an epigenetic signature of parasite load in populations of a wild bird and suggest intriguing physiological effects of parasite-associated cytosine methylation.

Epigenetics in natural animal populations

“…In most wild animal populations examined to date, there has been an excess of DNA methylation variation relative to genetic variation (Massicotte et al, 2011;Mor an & P erez-Figueroa, 2011;Liu et al, 2012;Massicotte & Angers, 2012;Schrey et al, 2012;Liebl et al, 2013;Skinner et al, 2014;Wenzel & Piertney, 2014). First investigations into epigenetic variation in wild animal populations involved the salmonid, Oncorhynchus mykiss (Blouin et al, 2010).…”

“…The authors tested if distinct levels of DNA methylation variation could explain differential survival rates between fish in two different habitats, but found no significant differences, possibly due to small sample size (six fish in total) and low-resolution methods (MS-AFLP). However, recent studies in clonal fish (Chrosomus eos-neogaeus) (Massicotte et al, 2011;Massicotte & Angers, 2012), round-leaf bats (Hipposideros armiger) (Liu et al, 2012), house sparrows (Passer domesticus) Liebl et al, 2013), Atlantic salmon (Salmo salar) (Mor an & P erez-Figueroa, 2011), Darwin's finches (Skinner et al, 2014), red grouse (Lagopus lagopus scotica) (Wenzel & Piertney, 2014), Daphnia (Schield et al, 2015), yellow baboon (Papio cynocephalus) (Lea et al, 2016), Tessellated darter (Etheostoma olmstedi) (Smith et al, 2016) and threespine stickleback (Gasterosteus aculeatus) (Smith et al, 2015;Trucchi et al, 2016) all showed population, habitat or species-specific DNA methylation patterns. These patterns may indicate that epigenetic variation is both environmentally sensitive and common among wild animal populations, and could play an important role in regulating phenotypic traits during local adaptation.…”

Population cycles: generalities, exceptions and remaining mysteries

“…This points to the need to know what triggers changes in reproduction associated with outbreak density. As suggested for snowshoe hares, epigenetic changes to genes related to stress responses [46,94] or for grouse [95] and insects [96] to disease resistance, might be occurring.…”

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

“…Unlike an individual's genotype, the epigenetic state of an individual is dynamic and can change throughout its lifespan (Horvath, 2013). Such changes can be mediated by environmental variation, exposure to parasites (Wenzel & Piertney, 2014) and hormones (Dhiman, Attwood, Campbell, & Smiraglia, 2015). …”

“…There are now a growing number of studies that have examined DNA methylation in wild organisms, mainly in birds (great tits Parus major ; Riyahi, Sánchez‐Delgado, Calafell, Monk, & Senar, 2015; Derks et al., 2016; Laine et al., 2016; Verhulst et al., 2016; eastern blue birds Sialia sialis; Bentz, Sirman, Wada, Navara, & Hood, 2016; red grouse Lagopus lagopus ; Wenzel & Piertney, 2014; house sparrows Passer domesitcus : Liebl, Schrey, Richards, & Martin, 2013; superb starlings Lamprotornis superbus ; Rubenstein et al., 2016). These and other studies have begun to support a role for DNA methylation in mediating ecological effects on phenotypic traits in the wild (e.g., personality and cognition: Laine et al., 2016; Verhulst et al., 2016) and emphasize the dynamic environmental sensitivity of DNA methylation levels across the life course.…”