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 (single methylation polymorphisms) are less effective than single nucleotide polymorphisms for identifying population differentiation in A. thaliana, they can classify phenotypically divergent B. distachyon subgroups that are otherwise genetically indistinguishable. The site frequency spectra generated using methylation sites from varied genomic locations and evolutionary conservation exhibit an excess of rare alleles. Nucleotide diversity estimates were three orders of magnitude higher for methylation variants than for single nucleotide polymorphisms in both species, driven by the higher epimutation rate. Correlations between single nucleotide polymorphisms and single methylation polymorphisms 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 100 bp for methylation variants in both plant species. Finally, we have developed a novel deep learning-based approach that infers demographic histories using methylation variation data alone. We identified recent population expansions in A. thaliana and B. distachyon using methylation variants that were not identified when using single nucleotide polymorphisms. Our study demonstrates the unique evolutionary insights methylomes provide that single nucleotide polymorphisms alone cannot reveal.