Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse

Maternal behaviour has profound, long-lasting implications for the health and well-being of developing offspring. In the monogamous California mouse (Peromyscus californicus), care by both parents is critical for offspring survival. We tested the hypothesis that similar to maternal care in rodents, paternal huddling and grooming (HG) behaviour can be transmitted to future generations via behavioural mechanisms. In California mice, testosterone maintains paternal HG behaviour. In the present study, we randomly assigned a group of male California mice to castration or sham-operated conditions and allowed them to raise their offspring normally. Adult sons of these males were paired with a female, and they were observed interacting with their own offspring. We found that like their fathers, the sons of castrated males huddled and groomed their young at lower levels than the sons of sham-operated fathers. The sons of castrates also retrieved pups more frequently. When both parents were present, the sons of castrates also showed a trend towards engaging in less exploratory behaviour. These data support the hypothesis that paternal behaviour, like maternal behaviour, can be transferred to future generations via epigenetic mechanisms and suggest that in a biparental species both parents contribute to offspring behavioural development.