Methylation patterns reveal cryptic structure and a pathway for adaptation in a panmictic carnivore

Abstract

Determining the molecular signatures of adaptive differentiation is a fundamental component of evolutionary biology. A key challenge remains for identifying such signatures in wild organisms, particularly between populations of highly mobile species that undergo substantial gene flow. The Canada lynx (Lynx canadensis) is one species where mainland populations appear largely undifferentiated at traditional genetic markers, despite inhabiting diverse environments and displaying phenotypic variation. Here, we used high-throughput sequencing to investigate both neutral genetic structure and epigenetic differentiation across the distributional range of Canada lynx. Using a customized bioinformatics pipeline we scored both neutral SNPs and methylated nucleotides across the lynx genome. Newfoundland lynx were identified as the most differentiated population at neutral genetic markers, with diffusion approximations of allele frequencies indicating that divergence from the panmictic mainland occurred at the end of the last glaciation, with minimal contemporary admixture. In contrast, epigenetic structure revealed hidden levels of differentiation across the range coincident with environmental determinants including winter conditions, particularly in the peripheral Newfoundland and Alaskan populations. Several biological pathways related to morphology were differentially methylated between populations, with Newfoundland being disproportionately methylated for genes that could explain the observed island dwarfism. Our results indicate that epigenetic modifications, specifically DNA methylation, are powerful markers to investigate population differentiation and functional plasticity in wild and non-model systems.\n\nSIGNIFICANCEPopulations experiencing high rates of gene flow often appear undifferentiated at neutral genetic markers, despite often extensive environmental and phenotypic variation. We examined genome-wide genetic differentiation and DNA methylation between three interconnected regions and one insular population of Canada lynx (Lynx canadensis) to determine if epigenetic modifications characterized climatic associations and functional molecular plasticity. Demographic approximations indicated divergence of Newfoundland during the last glaciation, while cryptic epigenetic structure identified putatively functional differentiation that might explain island dwarfism. Our study suggests that DNA methylation is a useful marker for differentiating wild populations, particularly when faced with functional plasticity and low genetic differentiation.