Allele-specific DNA methylation in the livebearing fish Poeciliopsis gracilis

DNA methylation is an important process that is involved in gene regulation. In a diploid organism, the two haplotypes are expected to have the same methylation state for the majority of the genome. However, differences in methylation between the two haplotypes can occur at certain genomic regions, which can result in allele-specific expression of genes. Allele-specific methylation has been studied in mammals and flowering plants, but studies in other organisms are scarce. Here we look for allele-specific methylation in the genome of the livebearing fish Poeciliopsis gracilis by sequencing four individuals: two parents and two of their offspring. For this, we developed a new approach that is based on Oxford Nanopore long read sequencing. We find that allele-specific methylation is widespread across the genome of Poeciliopsis gracilis, affecting CpG sites around 3.4-16.2% of all predicted genes, depending on the individual. We show that heterozygous positions in CpG sites can partly explain these observations, although most CpG sites showing allele-specific methylation do not contain heterozygosity. We also show that allele-specific methylation in the offspring is not random in terms of parent-of-origin, with the methylated allele more often than expected originating from the parent of the opposite sex. Genes that are nearby CpG sites showing allele-specific methylation are significantly enriched for neurological function. We hypothesize that patterns of allele-specific methylation can evolve if different selective pressures exist for both sexes on the same locus, and that sexual selection as observed throughout the genus Poeciliopsis can explain these results.