Maternal predation risk during pregnancy alters various social behaviors in the offspring of Brandt's voles

Predation risk can affect offspring phenotype and fitness via maternal effects. However, most studies have mainly focused on the effect of maternal exposure to predation risk on offspring anti-predator traits, and evidence of its impact on social behavior is still weak. We explored this using social Brandt's voles (Lasiopodomys brandtii). To this end, we exposed pregnant female voles to one of three treatments: distilled water (DW), rabbit odor (RO, non-predator odor), or cat odor (CO, predator odor) for 60 min daily from gestation day 1-18 and compared the range of social behaviors of their offspring. The levels of anxiety-like behaviors and serum adrenocorticotropic hormone (ACTH) and corticosterone (CORT) were also measured. Our data showed that maternal CO exposure had no effect on sibling play behavior, but female adolescent offspring displayed increased contact with their siblings. During the social interaction test, adult male offspring of CO mothers engaged in less aggression toward unfamiliar same-sex individuals. Additionally, they exhibited slightly shorter latency and longer duration of mounting behavior with a novel opposite-sex individual than the offspring of DW mothers. Following 72 h of cohabitation, both male and female CO offspring exhibited selective aggression toward strangers related to their partners. In addition, the offspring of the CO mothers spent less time in the central area of the open-field and entered the light box less often. Finally, we observed higher serum ACTH and CORT levels in offspring. These findings suggest that maternal exposure to predator risk during pregnancy can influence the social behavior of Brandt's voles in a sex- and behavior-specific manner. Anxiety and HPA axis activity may play modulatory roles in the expression of these social behaviors. Further studies should examine this transgenerational effect in the natural environment. Predation risk is an important environmental factor for animal populations and can trigger transgenerational responses, ultimately influencing the phenotype and fitness prospects of prey offspring. However, in social animals, the extent to which this non-genetic maternal effect influences the offspring's social behavior is unclear. Brandt's voles are typical social and grassland rodents. Owing to their complex social behavior, Brandt's voles may respond to predation risk in a variety of ways. We found increased contact behavior in adolescent females, decreased aggression and increased sexual motivation in adult males, and stable pair bonds in paired voles in a behavior-specific manner. As social behavior is important for survival, reproduction, and population fluctuations, we believe that our study makes a significant contribution to the literature and provides a reference for monitoring the population dynamics of social rodents, especially Brandt's voles.