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

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Abstract

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.

Significance

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.

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Data availability

All data generated or analyzed during this study are included in this article (supplementary materials). Further inquiries can be directed to the corresponding authors.

References

  • Akatsu S, Ishikawa C, Takemura K, Ohtani A, Shiga T (2015) Effects of prenatal stress and neonatal handling on anxiety, spatial learning and serotonergic system of male offspring mice. Neurosci Res 101:15–23

    Article  CAS  PubMed  Google Scholar 

  • Alcalay Y, Tsurim I, Ovadia O (2018) Female mosquitoes disperse further when they develop under predation risk. Behav Ecol 29:1402–1408

    Google Scholar 

  • Barfield RJ, Sachs BD (1968) Sexual behavior: stimulation by painful electrical shock to skin in male rats. Science 161:392–393

    Article  CAS  PubMed  Google Scholar 

  • Bestion E, Teyssier A, Aubret F, Clobert J, Cote J (2014) Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal. Proc R Soc B 281:20140701

    Article  PubMed  PubMed Central  Google Scholar 

  • Bourin M, Hascoet M (2003) The mouse light/dark box test. Eur J Pharmacol 463:55–65

    Article  CAS  PubMed  Google Scholar 

  • Brachetta V, Schleich CE, Cutrera AP, Merlo JL, Kittlein MJ, Zenuto RR (2018) Prenatal predatory stress in a wild species of subterranean rodent: do ecological stressors always have a negative effect on the offspring? Dev Psychobiol 60:567–581

    Article  CAS  PubMed  Google Scholar 

  • Cacioppo JT, Hawkley LC (2009) Perceived social isolation and cognition. Trends Cogn Sci 13:447–454

    Article  PubMed  PubMed Central  Google Scholar 

  • Carter CS, DeVries AC, Getz LL (1995) Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci Biobehav Rev 19:303–314

    Article  CAS  PubMed  Google Scholar 

  • Chen BB (2020) The relationship between Chinese mothers’ parenting stress and sibling relationships: a moderated mediation model of maternal warmth and co-parenting. Early Child Dev Care 190:1350–1358

    Article  Google Scholar 

  • Chen G, Shi D (2003) Study on reproductive behavior of different social hierarchy of Brandt’s vole (Lasiopodomys brandtii). Acta Theriol Sin 23:220–224

    Google Scholar 

  • Clarke AS, Wittwer DJ, Abbott DH, Schneider ML (1994) Long-term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys. Dev Psychobiol 27:257–269

    Article  CAS  PubMed  Google Scholar 

  • Coslovsky M, Richner H (2011) Predation risk affects offspring growth via maternal effects. Funct Ecol 25:878–888

    Article  Google Scholar 

  • Deng K, Liu W, Wang DH (2016) A review on social behavior-kinship linkage mechanisms in population regulation of small mammals. Chin J Ecol 35:825–833

    Google Scholar 

  • Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116

    Article  PubMed  Google Scholar 

  • Dong E, Dzitoyeva SG, Matrisciano F, Tueting P, Grayson DR, Guidotti A (2015) Brain-derived neurotrophic factor epigenetic modifications associated with schizophrenia-like phenotype induced by prenatal stress in mice. Biol Psychiatry 77:589–596

    Article  CAS  PubMed  Google Scholar 

  • Ehrlich DE, Rainnie DG (2015) Prenatal stress alters the development of socioemotional behavior and amygdala neuron excitability in rats. Neuropsychopharmacology 40:2135–2145

    Article  PubMed  PubMed Central  Google Scholar 

  • Fride E, Dan Y, Feldon J, Halevy G, Weinstock M (1986) Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol Behav 37:681–687

    Article  CAS  PubMed  Google Scholar 

  • Gemmel M, Hazlett M, Bogi E, De Lacalle S, Hill LA, Kokras N, Hammond GL, Dalla C, Charlier TD, Pawluski JL (2017) Perinatal fluoxetine effects on social play, the HPA system, and hippocampal plasticity in pre-adolescent male and female rats: interactions with pre-gestational maternal stress. Psychoneuroendocrinology 84:159–171

    Article  CAS  PubMed  Google Scholar 

  • Gerardin DC, Pereira OC, Kempinas WG, Florio JC, Moreira EG, Bernardi MM (2005) Sexual behavior, neuroendocrine, and neurochemical aspects in male rats exposed prenatally to stress. Physiol Behav 84:97–104

    Article  CAS  PubMed  Google Scholar 

  • Giesing ER, Suski CD, Warner RE, Bell AM (2011) Female sticklebacks transfer information via eggs: effects of maternal experience with predators on offspring. Proc R Soc B 278:1753–1759

    Article  PubMed  Google Scholar 

  • Glombik K, Stachowicz A, Slusarczyk J et al (2015) Maternal stress predicts altered biogenesis and the profile of mitochondrial proteins in the frontal cortex and hippocampus of adult offspring rats. Psychoneuroendocrinology 60:151–162

    Article  CAS  PubMed  Google Scholar 

  • Gu C, Wang W, Ding X, Yang S, Wang A, Yin B, Wei W (2018) Effects of maternal stress induced by predator odors during gestation on behavioral and physiological responses of offspring in Brandt’s vole (Lasiopodomys brandtii). Integr Zool 13:723–734

    Article  PubMed  Google Scholar 

  • Gu C, Liu Y, Huang Y, Yang S, Wang A, Yin B, Wei W (2020) Effects of predator-induced stress during pregnancy on reproductive output and offspring quality in Brandt’s voles (Lasiopodomys brandtii). Eur J Wildlife Res 66:14

    Article  Google Scholar 

  • Gu C, Xu Z, Chen L, Gu M, Yang S, Wang A, Yin B, Wei W (2023) Effects of maternal stress on the behavioral and HPA responses of offspring exposed to the predator or non-predator odor in Brandt’s voles. Pakistan J Zool 55:2151–2162

    Article  CAS  Google Scholar 

  • Gutleb DR, Roos C, Noll A, Ostner J, Schulke O (2018) COMT Val158 Met moderates the link between rank and aggression in a non-human primate. Genes Brain Behav 17:e12443

    Article  CAS  PubMed  Google Scholar 

  • Hegab IM, Shang G, Ye M, Jin Y, Wang A, Yin B, Yang S, Wei W (2014a) Defensive responses of Brandt’s voles (Lasiopodomys brandtii) to chronic predatory stress. Physiol Behav 126:1–7

    Article  CAS  PubMed  Google Scholar 

  • Hegab IM, Wang A, Yin B, Yang S, Wei W (2014b) Behavioral and neuroendocrine response of Brandt’s voles, Lasiopodomys brandtii, to odors of different species. Eur J Wildlife Res 60:331–340

    Article  Google Scholar 

  • Hernandez-Arteaga E, Hernandez-Gonzalez M, Ramirez-Renteria ML, Almanza-Sepulveda ML, Guevara MA, Silva MA, Jaime HB (2016) Prenatal stress alters the developmental pattern of behavioral indices of sexual maturation and copulation in male rats. Physiol Behav 163:251–257

    Article  CAS  PubMed  Google Scholar 

  • Hernandez-Gonzalez M, Hernandez-Arteaga E, Guevara MA, Almanza-Sepulveda ML, Ramirez-Renteria ML, Arteaga-Silva M, Bonilla-Jaime H (2017) Prenatal stress suppresses the prefrontal and amygdaline EEG changes associated with a sexually-motivated state in male rats. Physiol Behav 182:86–92

    Article  CAS  PubMed  Google Scholar 

  • Holson RR, Gough B, Sullivan P, Badger T, Sheehan DM (1995) Prenatal dexamethasone or stress but not ACTH or corticosterone alter sexual behavior in male rats. Neurotoxicol Teratol 17:393–401

    Article  CAS  PubMed  Google Scholar 

  • Hunter LTB, Skinner JD (1998) Vigilance behaviour in African ungulates: the role of predation pressure. Behaviour 135:195–211

    Article  Google Scholar 

  • Huo Y, Wan X, Wolff JO, Wang G, Thomas S, Iglay RB, Leopold BD, Liu W (2010) Multiple paternities increase genetic diversity of offspring in Brandt’s voles. Behav Process 84:745–749

    Article  Google Scholar 

  • Jia N, Li Q, Sun H, Song Q, Tang G, Sun Q, Wang W, Chen R, Li H, Zhu Z (2015) Alterations of group I mGluRs and BDNF associated with behavioral abnormity in prenatally stressed offspring rats. Neurochem Res 40:1074–1082

    Article  CAS  PubMed  Google Scholar 

  • Klein ZA, Padow VA, Romeo RD (2010) The effects of stress on play and home cage behaviors in adolescent male rats. Dev Psychobiol 52:62–70

    Article  PubMed  Google Scholar 

  • Kowalczyk AS, Davila RF, Trainor BC (2018) Effects of social defeat on paternal behavior and pair bonding behavior in male California mice (Peromyscus californicus). Horm Behav 98:88–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langerhans RB (2007) Evolutional consequences of predation: avoidance, escape, reproduction, and diversification. In: Elewa AMT (ed) Predation in organisms. Springer, Berlin, Germany, pp 177–220

    Chapter  Google Scholar 

  • Larsson K (1963) Non-specific stimulation and sexual behavior in the male rat. Behav Genet 20:110–114

    Google Scholar 

  • Lee PR, Brady DL, Shapiro RA, Dorsa DM, Koenig JI (2007) Prenatal stress generates deficits in rat social behavior: reversal by oxytocin. Brain Res 1156:152–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. In: Moller AP, Milinski M, Slater PJB (eds) Advances in the study of behavior. Academic Press, 27:215–290

    Google Scholar 

  • Liu XH, Yue LF, Wang D, Li N, Cong L (2013) Inbreeding avoidance drives consistent variation of fine-scale genetic structure caused by dispersal in the seasonal mating system of Brandt’s voles. PLoS One 8:e58101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matrisciano F, Tueting P, Dalal I, Kadriu B, Grayson DR, Davis JM, Nicoletti F, Guidotti A (2013) Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice. Neuropharmacology 68:184–194

    Article  CAS  PubMed  Google Scholar 

  • McCauley SJ, Rowe L (2010) Notonecta exhibit threat-sensitive, predator-induced dispersal. Biol Lett 6:449–452

    Article  PubMed  PubMed Central  Google Scholar 

  • Morley-Fletcher S, Rea M, Maccari S, Laviola G (2003) Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci 18:3367–3374

    Article  PubMed  Google Scholar 

  • Neumann ID, Veenema AH, Beiderbeck DI (2010) Aggression and anxiety: social context and neurobiological links. Front Behav Neurosci 4:12

    PubMed  PubMed Central  Google Scholar 

  • Olivier JD, Valles A, van Heesch F, Afrasiab-Middelman A et al (2011) Fluoxetine administration to pregnant rats increases anxiety-related behavior in the offspring. Psychopharmacology (Berl) 217:419–432

    Article  CAS  PubMed  Google Scholar 

  • Pang J, Li S, Liu Y, Yang S, Wu R, Wei W (2022) Adolescent predatory risk alters the antipredator behavior and basal HPA axis activity of future offspring in Brandt’s voles. Acta Theriol Sin 42:177–188

    Google Scholar 

  • Patin V, Lordi B, Vincent A, Caston J (2005) Effects of prenatal stress on anxiety and social interactions in adult rats. Brain Res Dev Brain Res 160:265–274

    Article  CAS  PubMed  Google Scholar 

  • Peng Y, Wu Y, Gu C, Yang S, Yin B, Wei W (2021) Effects of repeated exposure to cat odor on anti-predator and anxiety-like behaviors of juvenile Brandt’s voles (Lasiopodomys brandtii). Acta Theriol Sin 41:451–458

    Google Scholar 

  • Pereira OC, Arena AC, Yasuhara F, Kempinas WG (2003) Effects of prenatal hydrocortisone acetate exposure on fertility and sexual behavior in male rats. Regul Toxicol Pharmacol 38:36–42

    Article  CAS  PubMed  Google Scholar 

  • Peters DA (1982) Prenatal stress: effects on brain biogenic amine and plasma corticosterone levels. Pharmacol Biochem Behav 17:721–725

    Article  CAS  PubMed  Google Scholar 

  • Qiao X, Yan Y, Wu R, Tai F, Hao P, Cao Y, Wang J (2014) Sociality and oxytocin and vasopressin in the brain of male and female dominant and subordinate mandarin voles. J Comp Physiol A 200:149–159

    Article  CAS  Google Scholar 

  • Rhees RW, Fleming DE (1981) Effects of malnutrition, maternal stress, or ACTH injections during pregnancy on sexual behavior of male offspring. Physiol Behav 27:879–882

    Article  CAS  PubMed  Google Scholar 

  • Rhees RW, Al-Saleh HN, Kinghorn EW, Fleming DE, Lephart ED (1999) Relationship between sexual behavior and sexually dimorphic structures in the anterior hypothalamus in control and prenatally stressed male rats. Brain Res Bull 50:193–199

    Article  CAS  PubMed  Google Scholar 

  • Rojo M, Marin B, Menendez-Patterson A (1985) Effects of low stress during pregnancy on certain parameters of the offspring. Physiol Behav 34:895–899

    Article  CAS  PubMed  Google Scholar 

  • Samjaa R, Zophel U, Peterson J (2000) The impact of the vole Microtus brandti on Mongolian steppe ecosystems. Marb Geogr Schr 135:346–360

    Google Scholar 

  • Sandi C, Haller J (2015) Stress and the social brain: behavioural effects and neurobiological mechanisms. Nat Rev Neurosci 16:290–304

    Article  CAS  PubMed  Google Scholar 

  • Sheriff MJ, Love OP (2013) Determining the adaptive potential of maternal stress. Ecol Lett 16:271–280

    Article  CAS  PubMed  Google Scholar 

  • Sheriff MJ, Bell A, Boonstra R, Dantzer B, Lavergne SG, McGhee KE, MacLeod KJ, Winandy L, Zimmer C, Love OP (2017) Integrating ecological and evolutionary context in the study of maternal stress. Integr Comp Biol 57:437–449

    Article  PubMed  PubMed Central  Google Scholar 

  • Song Z, Tai F, Yu C, Wu R, Zhang X, Broders H, He F, Guo R (2010) Sexual or paternal experiences alter alloparental behavior and the central expression of ERα and OT in male mandarin voles (Microtus mandarinus). Behav Brain Res 214:290–300

    Article  CAS  PubMed  Google Scholar 

  • Spear LP (2004) Adolescent brain development and animal models. Ann NY Acad Sci 1021:23–26

    Article  PubMed  Google Scholar 

  • St-Cyr S, McGowan PO (2015) Programming of stress-related behavior and epigenetic neural gene regulation in mice offspring through maternal exposure to predator odor. Front Behav Neurosci 9:145

    Article  PubMed  PubMed Central  Google Scholar 

  • St-Cyr S, Abuaish S, Sivanathan S, McGowan PO (2017) Maternal programming of sex-specific responses to predator odor stress in adult rats. Horm Behav 94:1–12

    Article  PubMed  Google Scholar 

  • St-Cyr S, Abuaish S, Spinieli RL, McGowan PO (2018) Maternal predator odor exposure in mice programs adult offspring social behavior and increases stress-induced behaviors in semi-naturalistic and commonly-used laboratory tasks. Front Behav Neurosci 12:136

    Article  PubMed  PubMed Central  Google Scholar 

  • Storm JJ, Lima SL (2010) Mothers forewarn offspring about predators: a transgenerational maternal effect on behavior. Am Nat 175:382–390

    Article  PubMed  Google Scholar 

  • Vallee M, Mayo W, Dellu F, Le Moal M, Simon H, Maccari S (1997) Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 17:2626–2636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanderschuren LJ, Niesink RJ, Spruijt BM, Van Ree JM (1995a) Influence of environmental factors on social play behavior of juvenile rats. Physiol Behav 58:119–123

    Article  CAS  PubMed  Google Scholar 

  • Vanderschuren LJ, Spruijt BM, Hol T, Niesink RJ, Van Ree JM (1995b) Sequential analysis of social play behavior in juvenile rats: effects of morphine. Behav Brain Res 72:89–95

    Article  CAS  PubMed  Google Scholar 

  • Velazquez-Moctezuma J, Dominguez Salazar E, Cruz Rueda ML (1993) The effect of prenatal stress on adult sexual behavior in rats depends on the nature of the stressor. Physiol Behav 53:443–448

    Article  CAS  PubMed  Google Scholar 

  • Verdolin JL (2006) Meta-analysis of foraging and predation risk trade-offs in terrestrial system. Behav Ecol Sociobiol 60:457–464

    Article  Google Scholar 

  • Wang J, Tai F, Yan X, Yu P (2012) Paternal deprivation alters play-fighting, serum corticosterone and the expression of hypothalamic vasopressin and oxytocin in juvenile male mandarin voles. J Comp Physiol A 198:787–796

    Article  CAS  Google Scholar 

  • Ward IL (1972) Prenatal stress feminizes and demasculinizes the behavior of males. Science 175:82–84

    Article  CAS  PubMed  Google Scholar 

  • Ward HE, Johnson EA, Salm AK, Birkle DL (2000) Effects of prenatal stress on defensive withdrawal behavior and corticotropin releasing factor systems in rat brain. Physiol Behav 70:359–366

    Article  CAS  PubMed  Google Scholar 

  • Weinstock M (2001) Effects of maternal stress on development and behaviour in rat offspring. Stress 4:157–167

    Article  CAS  PubMed  Google Scholar 

  • Weinstock M (2008) The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev 32:1073–1086

    Article  CAS  PubMed  Google Scholar 

  • Weinstock M (2017) Prenatal stressors in rodents: effects on behavior. Neurobiol Stress 6:3–13

    Article  PubMed  Google Scholar 

  • Williams JR, Carter CS, Insel T (1992) Partner preference development in female prairie voles is facilitated by mating or the central infusion of oxytocin. Ann NY Acad Sci 652:487–489

    Article  CAS  PubMed  Google Scholar 

  • Wilson CA, Terry Jr AV (2013) Variable maternal stress in rats alters locomotor activity, social behavior, and recognition memory in the adult offspring. Pharmacol Biochem Behav 104:47–61

    Article  CAS  PubMed  Google Scholar 

  • Wright LD, Hebert KE, Perrot-Sinal TS (2008) Periadolescent stress exposure exerts long-term effects on adult stress responding and expression of prefrontal dopamine receptors in male and female rats. Psychoneuroendocrinology 33:130–142

    Article  CAS  PubMed  Google Scholar 

  • Wright LD, Muir KE, Perrot TS (2012) Enhanced stress responses in adolescent versus adult rats exposed to cues of predation threat, and peer interaction as a predictor of adult defensiveness. Dev Psychobiol 54:47–69

    Article  CAS  PubMed  Google Scholar 

  • Wu R, Huang Y, Liu Y, Shen Q, Han Y, Yang S, Wei W (2020) Repeated predator odor exposure alters maternal behavior of postpartum Brandt’s voles and offspring’s locomotor activity. Behav Process 177:104143

    Article  Google Scholar 

  • Wu R, Wu X, Li S, Li G, Jiang Z, Zhong H, Wang B, Yang S, Wei W (2021) Predator odor exposure increases social contact in adolescents and parental behavior in adulthood in Brandt’s voles. Behav Process 186:104372

    Article  Google Scholar 

  • Wu R, Li S, Huang Y, Pang J, Cai Y, Zhang X, Jiang T, Yang S, Wei W (2022) Postpartum maternal exposure to predator odor alters offspring antipredator behavior, basal HPA axis activity and immunoglobulin levels in adult Brandt’s voles. Behav Brain Res 416:113532

    Article  CAS  PubMed  Google Scholar 

  • Wu R, Pang J, Xu Z, Wu X, Wang W, Zheng Y, Yang S, Wei W (2023) Adolescence predatory risk alters social behaviors and cognitive ability and central oxytocin and vasopressin expression in adult Brandt’s voles. Neuroendocrinology 113:519–534

    Article  CAS  PubMed  Google Scholar 

  • Yee JR, Cavigelli SA, Delgado B, McClintock MK (2008) Reciprocal affiliation among adolescent rats during a mild group Stressor predicts mammary tumors and lifespan. Psychosom Med 70:1050–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin F, Fang J (1998) Research advances in population ecology and behavioral ecology of Brandt’s vole. Chin J Ecol 17:65–69

    Google Scholar 

  • Young LJ, Wang Z (2004) The neurobiology of pair bonding. Nat Neurosci 7:1048–1054

    Article  CAS  PubMed  Google Scholar 

  • Yu X, Fang J, Sun R (2002) Kinship and social behavior of rodents. Chin J Ecol 6:51–56

    CAS  Google Scholar 

  • Yu X, Sun R, Fang J (2004) Effect of kinship on social behaviors in Brandt’s voles (Microtus brandti). J Ethol 22:17–22

    Article  Google Scholar 

  • Zeifman DM (2019) Attachment theory grows up: a developmental approach to pair bonds. Curr Opin Psychol 25:139–143

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Xueyan Wu for assistance with the experiments and animal care. We would also like to thank two anonymous reviewers for their helpful and constructive comments on this manuscript.

Funding

This work was supported by grants from the National Natural Science Foundation of China (31770422, 31370415, and 31900334), Natural Science Foundation of Jiangsu Province (BK20190910), Postdoctoral Science Foundation of China (2018M630610 and 2019T120468), Students’ Project for Innovation and Entrepreneurship Training Program of Yangzhou University (c202211117011Y), and Priority Academic Program Development of Jiangsu Higher Education Institutions.

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  1. Department of Animal Behavior, College of Bioscience and Biotechnology, Yangzhou University, Yangzhou, 225009, Jiangsu, China

    Ruiyong Wu, Wei Wang, Yujie Zheng, Shan Li, Lanlan Zhang, Jinyue Pang, Wanhong Wei & Shengmei Yang

  2. Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, 225009, Jiangsu, China

    Wanhong Wei

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All animal experiments were performed in accordance with the Guide for the Care and Use of Laboratory Animals of China and were approved by the Animal Care and Use Committee of the Faculty of Veterinary Medicine at Yangzhou University (IACUC No. SJXY-1).

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Wu, R., Wang, W., Zheng, Y. et al. Maternal predation risk during pregnancy alters various social behaviors in the offspring of Brandt’s voles. Behav Ecol Sociobiol 77, 121 (2023). https://doi.org/10.1007/s00265-023-03400-z

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