Abstract
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.
Highlights
Expression divergence between orthologous genes in closely related species could be attributed to species-specific DNA sequence changes in cis-regulatory elements and/or trans-factors
We find that variation in DNA sequence impacts expression on the same strand, and that cytosine methylation state is 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, and that in the hybrids the alleles retain the methylation status of the parental species in a strong cis-regulated fashion
Summary
Expression divergence between orthologous genes in closely related species could be attributed to species-specific DNA sequence changes in cis-regulatory elements and/or trans-factors. The bulk of CpG methylation in mammals occurs in intergenic regions [7], while Drosophila lacks symmetrical CpG methylation [8,9]. Eusocial insects such as honey bees and ants have gene body DNA methylation [10,11,12,13,14], but caste-specific methylation patterns are often found, necessitating a careful control of caste in experimental designs [15,16]. There are substantial DNA polymorphisms in social insects that can complicate DNA methylation calling
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