Gene expression divergence between closely related species could be attributed to both cis- and trans- DNA sequence changes during evolution, but it is unclear how the evolutionary dynamics of epigenetic marks are regulated. In eutherian mammals, biparental DNA methylation marks are erased and reset during gametogenesis, resulting in paternal or maternal imprints, which lead to genomic imprinting. Whether DNA methylation reprogramming exists in insects is not known. Wasps of the genus Nasonia are non-social parasitoids that are emerging as a model for studies of epigenetic processes in insects. In this study, we quantified allele-specific expression and methylation genome-wide in Nasonia vitripennis and Nasonia giraulti and their reciprocal F1 hybrids. No parent-of-origin effect in allelic expression was found for >8,000 covered genes, suggesting a lack of genomic imprinting in adult Nasonia. As we expected, both significant cis- and trans- effects are responsible for the expression divergence between N. vitripennis and N. giraulti. Surprisingly, all 178 differentially methylated genes are also differentially methylated between the two alleles in F1 hybrid offspring, recapitulating the parental methylation status with nearly 100% fidelity, indicating the presence of strong cis-elements driving the target of gene body methylation. In addition, we discovered that total and allele-specific expression are positively correlated with allele-specific methylation in a subset of the differentially methylated genes. The 100% cis-regulation in F1 hybrids suggests the methylation machinery is conserved and DNA methylation is targeted by cis features in Nasonia. The lack of genomic imprinting and parent-of-origin differentially methylated regions in Nasonia, together with the stable inheritance of methylation status between generations, suggests either a cis-regulatory motif for methylation at the DNA level or highly stable inheritance of an epigenetic signal in Nasonia.
RNA-sequencing and whole-genome bisulfite sequencing in the hybrid offspring of two Nasonia parasitoid wasp species revealed strong cis-regulation of methylation and allele-specific expression. No gene was found to display genomic imprinting.
The relationship between methylation of genomic DNA and expression of the genes that it encodes—and how this relationship changes during evolution—has been widely studied in mammals, but remains less well understood for insects. Here we analyze the expressed mRNA transcripts and genomic DNA methylation of the hybrid offspring of a pair of Nasonia parasitoid wasp species, producing a wealth of information about the regulation of gene expression. We find that variation in DNA sequence impacts expression on the same strand (called “ cis-regulation”), and that cytosine methylation state is also associated in cis with the regulatory consequences of this base alteration. We show that these wasp species lack differential expression dependent on parent-of-origin (called “genomic imprinting”), and that in the hybrids the alleles retain the methylation status of the parental species in a strong cis-regulated fashion. Transcript abundances were also largely driven in a cis-regulated manner, consistent with a correlation between methylation status and expression levels. Despite the many differences between Nasonia and mammals in the impact of genomic DNA methylation, in both groups the use of methylated cytosine has been co-opted in ways that help tune gene expression.