During range expansions, epigenetic mechanisms may mediate phenotypic responses to environmental cues, enabling organisms to adjust to novel conditions at novel sites. Here, we predicted that the number of CpG sites within the genome, one form of epigenetic potential, would be important for success during range expansions because DNA methylation can modulate gene expression and hence facilitate adaptive plasticity. Previously, we found that this same form of epigenetic potential was higher in introduced compared to native populations of house sparrows (Passer domesticus) for two immune genes (Toll-like receptors 2A and 4). Here, we took a reduced-representation sequencing approach (ddRadSeq and EpiRadSeq) to investigate how CpG site number, as well as resultant DNA methylation, varied across five sites in the ~70 year-old Kenyan house sparrow range expansion. We found that the number of CpG sites increased towards the vanguard of the invasion, even when accounting for variation in genetic diversity among sites. This pattern was driven by more losses of CpG sites towards the core of the invasion (the initial site of introduction). Across all sequenced loci, DNA methylation decreased but became more variable towards the range-edge. However, in the subset CpG sites proximal to mutated CpG sites, DNA methylation increased and variation declined. These results indicate that epigenetic potential influenced the Kenyan house sparrow range expansion, likely by providing greater phenotypic plasticity which is genetically assimilated as populations adapt to local conditions. Similar mechanisms might underlie the successes and failures of other natural and anthropogenic range expansions.
Introduction:Epigenetic modifications, such as DNA methylation, play a critical role in linking environmental variation to phenotypic variation by modifying how genes are expressed (1). In vertebrates, these processes are instrumental to cellular and tissue differentiation during development, but these same modifications can also affect evolutionarily-relevant behavioral, morphological, and physiological plasticity (2, 3). As epigenetic variation, including DNA methylation patterns, predominates in particular genomic regions (e.g., CpG dinucleotides), genomes might differ in their capacity to be modified epigenetically (4). When genomic variation associated with epigenetic marks occurs in genes that affect fitness, natural (and neutral) selection should follow, leading to differences in epigenetic potential among individuals, populations, and