Effects Of Paternal Predation Stress On Offspring’s Behavior And Physiology Via A Nonsperm Mediated Pathway In Brandt’s Voles

Predator-prey coevolution has been a hot topic in zoology and ecology.In addition to directly predation,predators can also indirectly affect the fitness of the prey offspring through the intergenerational transmission effect.A large number of studies have shown that the intergeneration transmission effect of sperm-mediated paternal stress can have many effects on offspring,but there are relatively few studies on the effects of non-sperm-mediated paternal intergeneration effects on offspring and fewer studies on the effect of predation stress through this effect.Some male animals are directly involved in the care of their offspring and can therefore influence the growth and development of offspring directly by interacting with their offspring or indirectly through pregnant females.In this study,Brandt’s voles(Lasiopodomys brandtii)were used as animal models to explore the effects of paternal predation stress on offspring behavior and physiology through non-sperm-mediated paternal effect.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 different odor exposure after mating in male Brandt’s voles on social interaction and anxiety-like behavior of male and female voles,reproductive output and parental investment of mated males and females,as well as the development,behavior,neuroendocrine level of their offspring.The results are as follows:(1)In the social interaction test,the retreating behavior of CO males increased,indicating that predation stress caused social avoidance;the licking behavior of their partners was increased,showing a consolation behavior toward males,which may play a role in relieving stress.In the open field and light/dark box tests,the time spent in the central area of open field was increased,indicating a decreased anxiety-like behavior in the CO and RO males;the time in central area was decreased,and anxiety-like behavior was increased in the partners of CO and RO males,suggesting that social contagion may have occurred during the interaction between males and their partners.(2)In the parental behavior test,the percentage of pup retrieval was decreased in the males of CO and RO groups,males may reduce the frequency of pup retrieval to avoid predation;no effect was found in their partners’ maternal behavior.The litter size of CO group was increased,and the offspring of CO and RO groups was lighter,suggesting that their partners may increase their reproductive output at the cost of reducing the quality of their offspring,which has a negative impact on the growth and development of offspring.(3)The results of the offspring behavior showed that,the percentage of time spent in the open filed and light box decreased,indicating the anxiety-like behavior increased in adolescent CO offspring;the total distance and average speed were increased in the CO group of adult offspring,but the immobility time was decreased,reflecting that the anxiety level of adult offspring recovered to normal and locomotor activity increased.In the anti-predator behavior test,there was no significant difference between these groups when exposed to distilled water.Being exposed to rabbit odor,the self-grooming behavior was increased in the CO and RO groups of offspring.Being exposed to cat odor,the concealing and self-grooming behavior was increased in the CO group of offspring,the avoidance and vigilance behavior of male offspring were significantly increased compared with that of female offspring.These results suggest that paternal predation stress was transmitted to offspring through non-sperm-mediated paternal effect,which makes their offspring adopt passive avoidance to copy with predation risk.(4)Regarding the neuroendocrine level of offspring,the results showed that the levels of serum CORT and hypothalamic CRH expression was increased,but hippocampal GR expression was decreased in the offspring of CO group.Non-sperm-mediated paternal predation stress can affect the levels of HPA axis and the negative feedback regulation of hippocampal GR in offspring.In conclusion,paternal predation stress after mating affects the social behaviors,anxiety-like behavior,reproductive output and parental behavior of themselves and their partners.The non-sperm-mediated paternal effects may indirectly affect the development,behavior,and neuroendocrine level of offspring through these behavioral changes,which may be mediated by changes in the HPA axis.This study revealed the mechanism by which non-sperm-mediated paternal predation stress affects offspring phenotypes,enriched the theory of predator-prey coevolution,and provide theoretical support for the prevention and control of damage of rodents in the grassland.