Sex-specific expression and DNA methylation in a species with extreme sexual dimorphism and paternal genome elimination

Abstract

Sexual dimorphism is exhibited in many species across the tree of life with many phenotypic differences mediated by differential expression and alternative splicing of genes present in both sexes. However, the mechanisms that regulate these sex-specific expression and splicing patterns remain poorly understood. The mealybug, Planococcus citri, displays extreme sexual dimorphism and exhibits an unusual instance of sex-specific genomic imprinting, Paternal Genome Elimination (PGE), in which the paternal chromosomes in males are highly condensed and eliminated from the sperm. P. citri also has no sex chromosomes and as such both sexual dimorphism and PGE are predicted to be under epigenetic control. We recently showed that P. citri females display a highly unusual DNA methylation profile for an insect species, with the presence of promoter methylation associated with lower levels of gene expression. In this study we therefore decided to explore genome-wide differences in DNA methylation between male and female P. citri using whole genome bisulfite sequencing. We have identified extreme differences in genome-wide levels and patterns between the sexes. Males display overall higher levels of DNA methylation which manifests as more uniform low-levels across the genome. Whereas females display more targeted high levels of methylation. We suggest these unique sex-specific differences are due to chromosomal differences caused by PGE and may be linked to possible ploidy compensation. Using RNA-Seq we identified extensive sex-specific gene expression and alternative splicing. We found cis-acting DNA methylation is not directly associated with differentially expressed or differentially spliced genes, indicating a broader role for chromosome-wide trans-acting DNA methylation in this species.