Transcriptomic analysis of paternal behaviors in prairie voles

The importance of fathers' engagement in care and its critical role in the offspring’s cognitive and emotional development is now well established. Yet, little is known on the underlying neurobiology due to the lack of appropriate animal models. In the socially monogamous and bi-parental prairie vole (Microtus ochrogaster), while most virgin males show spontaneous paternal behaviors (Paternal), others display pup-directed aggression (Attackers). Here we took advantage of this phenotypic dichotomy and used RNA-sequencing in three important brain areas to characterize gene expression associated with paternal behaviors of Paternal males and compare it to experienced fathers and mothers. This strategy allowed the identification of spontaneous paternal behaviors independently from fatherhood and pair-bonding. While Paternal males displayed the same range and extent of paternal behaviors than experienced Fathers, the nucleus accumbens (NAc) and medial preoptic area (MPOA) transcriptomes mainly reflected pair-bonded status or sex differences, respectively. The lateral septum (LS) transcriptome, however, primarily reflected phenotypic differences between Paternal and Attackers and suggested the involvement of the mitochondria, RNA translation, and protein degradation processes. Altogether, these observations highlight a marked structure- and phenotype-specific pattern of gene expression underlying paternal behaviors in prairie voles and highlight similarities and differences from those underlying fatherhood. A total of 24 prairie voles were used: 6 Mothers (6 MPOA, 6 NAc, 6 LS libraries), 6 Fathers (6 MPOA, 6 NAc, 6 LS libraries), 6 Paternal (4 MPOA, 6 NAc, 6 LS libraries), and 6 Attackers (6 MPOA, 6 NAc, 5 LS libraries).