Transcription and DNA methylation signatures of paternal care in hippocampal dentate gyrus of prairie voles

In socially monogamous prairie voles (Microtus ochrogaster), parental behaviors not only occur in mothers and fathers, but also can exist in virgin males (“parental”). However, some virgin males display aggressive behaviors towards conspecific pups (“attacker”). Although this behavioral dichotomy in response to pup exposure has been well documented, little is known about the gene expression changes underlie the parental behavioral differences and their regulatory mechanisms. To address this, we profiled the transcriptome and DNA methylome of hippocampal dentate gyrus of four prairie vole groups, attacker virgin males, parental virgin males, fathers, and mothers. We found a concordant pattern of gene transcription in parental virgin males and fathers, when comparing to the attacker group. The methylome analysis also revealed signaling pathways enriched for epigenetic changes involving both receptor-mediated and secondary messenger signaling across both behavioral phenotypes and sexual experiences. Furthermore, we found correlations between gene expression changes and DNA methylation differences between attacker and parental virgin males, which suggests a canonical gene expression regulatory role of DNA methylation in paternal care. Therefore, our study presents an integrated view of transcriptome and epigenome that provides a DNA epigenetic based molecular insight of paternal behavior.