Effects Of Paternal Predation Stress On Offspring’s Growth And Development And Behavior Via A Sperm Mediated Pathway In Brandt’s Voles

There have been many reports on the maternal effect and its mechanism,while the paternal effect has received little attention in recent years.Paternal health and environmental stress play an important role in regulating the phenotype of offspring.It is well known that male only provides sperm during mating,so the paternal effect may be mediated by sperm.Many studies have shown that sperm-mediated paternal stress negatively affects offspring at different developmental stages,including fetal development and behavioral and physiological health in adulthood.In the wild,animals are prone to ecological stress,especially predation.It is of great ecological value to study whether paternal predation stress affects the phenotype of offspring in a sperm-mediated way.In this study,adult male Brandt’s voles were used as animal models.Cat odor(CO)was used as the predator odor,rabbit odor(RO)as the non-predator odor,and distilled water(DW)as the control,to explore the effects of predation stress exposure on paternal behavior and reproductive traits,reproductive output,and maternal behavior of their mates,as well as the development,behavior and serum CORT level of offspring.The results are as follows:1)The mates of CO and RO voles showed less nest-building behavior than DW groups during the postpartum period.In the late postpartum period,the mates of CO and RO voles had shortened latency of pup retrieval.The behavior of pup licking decreased on PP3,and increased with the development of the pup.2)The results of offspring growth and development showed that paternal experience of CO exposure resulted in lower body weight after weaning,while RO exposure only reduced the body weight of female offspring.The index of testicular and epididymis in the male offspring CO group were significantly lower than those of the control and RO group.Paternal exposure to different odors did not affect the development of the reproductive organ in female offspring or sperm quality in male offspring.3)The offspring’s behavioral and neuroendocrine results showed that with exposure to distilled water,the offspring from the CO group showed increased avoidance and head-out behavior,whereas the offspring from the RO group showed increased contact and head-out behavior,and decreased concealing behavior,as well as the female offspring showed less jumping.Being exposed to rabbit odor,the immobility time of male offspring from the CO group was significantly higher than those of the control group and the RO group.Being exposed to CO,the grooming behavior increased and the vigilance rearing decreased in the offspring of the CO group.In addition,the total distance and average speed in the open field increased,the duration of inactivity decreased,the percentage time of the central area decreased,and visits in the dark box of rabbit odor exposure increased.These treatments did not affect these behaviors of adult offspring.Serum CORT levels were increased in adult offspring from the CO and RO groups.4)The results of reproductive traits in male Brandt’s voles showed that predator odor exposure reduced the inner diameter of the seminiferous tube and-the-rate of sperm deformity and mortality.5)The results of paternal behavioral traits showed that repeated exposure to rabbit odor reduced contact and jumping behavior,while repeated cat odor exposure did not affect antipredation behavior in male voles.In addition,exposure to different odors did not affect voluntary and anxiety-like behavior in male Brandt’s voles.These results consistent with our previous results that repeated predator odor exposure produced adaptation or habituation.6)Correlation analysis showed that there was a significant positive correlation between the paternal testicular index and male offspring’s testicular index,indicating that the influence of predation risk on paternal reproductive potential may be transmitted to male offspring.There was a significant negative correlation between the vigilance-rearing behavior of the father and the grooming behavior of offspring exposed to distilled water.The head-out behavior of father to rabbit odor was negatively correlated with jumping behavior of offspring exposed to rabbit odor.There was a significant positive correlation between paternal vigilance rearing behavior exposed to cat odor and concealing and jumping behavior of offspring exposed to cat odor,and paternal jumping behavior was significantly positively correlated with the avoidance behavior of offspring.In addition,there was a significant negative correlation between visits to the dark box during puberty and paternal immobility time in the open field,and a significant positive correlation between the immobility of offspring in the open field and paternal percentage time in the central area.These results suggest that the effect of predation risk on the paternal body may influence the antipredation response and autonomic activity of progeny through sperm-mediated means.In conclusion,paternal exposure to predator odor before mating affects paternal reproductive potential,especially sperm quality,as well as reproductive potential,behavior,and endocrine levels of offspring.Growth development,anti-predation,and anxiety-like behavior of offspring were correlated with that of the father,suggesting that paternal influence on the offspring may play a role by sperm mediated,which induces offspring to make an adaptive change in phenotypic traits and improving the fitness in predator-rich environments.