Methylomes reveal recent evolutionary changes in populations of two plant species

Plant DNA methylation changes occur hundreds to thousands of times faster than DNA mutations and can be transmitted transgenerationally, making them useful for studying population-scale patterns in clonal or selfing species. However, a state-of-the-art approach to use them for inferring population genetic processes and demographic histories is lacking. To address this, we compare evolutionary signatures extracted from CG methylomes and genomes in Arabidopsis thaliana and Brachypodium distachyon . While methylation variants (SMPs) are less effective than genetic variants (SNPs) for identifying population differentiation in A. thaliana , they can classify phenotypically divergent B. distachyon subgroups that are otherwise genetically undistinguishable. The site frequency spectra generated using methylation sites from varied genomic locations and evolutionary conservation exhibit similar shapes, indicating minimal noise when all CG sites are analyzed jointly. Nucleotide diversity is three orders of magnitude higher for methylation variants than for genetic variants in both species, driven by the higher epimutation rate. Correlations between SNPs and SMPs in nucleotide diversity and allele frequencies at gene exons are weak or absent in A. thaliana , possibly because the two sources of variation reflect evolutionary forces acting at different timescales. Linkage disequilibrium quickly decays within 250 bp for methylation variants in both plant species. Finally, we developed a deep learning-based demographic inference approach. We identified recent population expansions in A. thaliana and B. distachyon using methylation variants that were not identified when using genetic variants. Our study demonstrates the unique evolutionary insights methylomes provide that genetic variation alone cannot reveal.