Paternal predatory risk alters parental behavior and offspring phenotypes in biparental Brandt's voles

Paternal predation risk can program offspring phenotypes via maternal responses and epigenetic marks of spermatozoa. However, the processes and consequences of this experience in biparental species are unknown. Here, we examined how preconception and postconception paternal cat odor (CO) exposure affects anxiety-like behavior and antipredator response in Brandt's voles (Lasiopodomys brandtii). We found that preconception paternal CO exposure inhibited maternal investment when offspring were raised by mothers alone, while postconception exposure increased paternal investment towards the offspring raised by both parents. The increased paternal behavior may be associated with an increasing grooming behavior received from their mates, which alleviated the anxiety-like behavior in CO-exposed males. Both paternal experiences increased the levels of anxiety-like behavior in adolescent offspring but differentially altered adult phenotypes. Specifically, adult females from preconception CO-exposed fathers spent less time in defensive concealing, whereas the offspring of postconception CO-exposed fathers showed more in response to acute cat urine exposure. Correspondingly, baseline corticosterone levels were decreased and increased in these offspring, respectively. Our results indicate that in biparental species, paternal predation risk exposure affects offspring phenotypes in pathway-dependent and age-specific manners and that only the presence of both parents can elicit adaptive responses to a high predation-risk environment.