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.
Highlights
The traditional paradigm that phenotypic variability and evolutionary change are consequences solely of DNA sequence variation is becoming increasingly challenged (Jablonka & Lamb 2007; Bonduriansky & Day2008; Danchin et al 2011; Mesoudi et al 2013)
Parasite load was not associated with either genome-wide methylation levels or epigenetic differentiation
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)
Summary
The traditional paradigm that phenotypic variability and evolutionary change are consequences solely of DNA sequence variation is becoming increasingly challenged (Jablonka & Lamb 2007; Bonduriansky & Day2008; Danchin et al 2011; Mesoudi et al 2013). From a molecular ecology perspective, these phenomena complement the DNA sequence-based systems hitherto examined and are likely to provide new insights into the underpinning, regulation and evolution of phenotypic traits The most intensively studied epigenetic mechanism is enzymatically mediated attachment of a methyl group to cytosine or adenine nucleotides (Angers et al 2010) POPULATION EPIGENETIC STRUCTURE IN RED GROUSE et al 2008; Angers et al 2010; Richards et al 2010; Duncan et al 2014).
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