Skip to main content
SpringerLink
Log in
Book cover

Adaptive and Maladaptive Aspects of Developmental Stress pp 45–64Cite as

Prenatal and Maternal Psychosocial Stress in Primates: Adaptive Plasticity or Vulnerability to Pathology?

  • Chapter
  • First Online:

Part of the book series: Current Topics in Neurotoxicity ((Current Topics Neurotoxicity,volume 3))

Abstract

In many species of vertebrates, prenatal and early postnatal stress can have long-lasting consequences for neuroanatomical, neuroendocrine, or behavioral development. In primates including humans, prenatal psychosocial stress and postnatal psychosocial stress induced by the mother’s behavior represent important sources of nongenetic maternal effects through which mothers can modify their offspring’s phenotype. Prenatal and maternal psychosocial stress are probably mediated by similar physiological mechanisms and primarily including the HPA axis. The biomedical/clinical view, the stress-inoculation model, and the adaptive calibration model make different assumptions and predictions concerning the adaptive or maladaptive developmental consequences of prenatal and maternal psychosocial stress. Studies of experimentally induced prenatal psychosocial stress in primates indicate that fetal programming occurs with characteristics similar to those observed in laboratory rodents and in humans. Studies of naturally occurring maternal psychosocial stress in primates have focused on maternal abuse and rejection of offspring. Although the developmental consequences of exposure to maternal abuse or high rates of maternal rejection are unlikely to be adaptive, exposure to moderate levels of rejection appears to result in physiological and behavioral changes that enhance resilience later in life. It is possible that some aspects of normal parenting in nonhuman primates and humans are designed to be stress inducing to prepare offspring to deal with the psychosocial stress that is an inevitable part of life in complex and competitive social environments.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Bardi M, Huffman MA (2006) Maternal behavior and maternal stress are associated with infant behavioral development. Dev Psychobiol 48:1–9

    Article  PubMed  Google Scholar 

  • Bardi M, Bode AE, Ramirez SM (2005) Maternal care and development of stress responses in baboons. Am J Primatol 66:263–278

    Article  PubMed  Google Scholar 

  • Belsky J, Pluess M (2009) Beyond diathesis-stress: differential susceptibility to environmental influences. Psychol Bull 135:885–908

    Article  PubMed  Google Scholar 

  • Berman CM (1990) Intergenerational transmission of maternal rejection rates among free-ranging rhesus monkeys. Anim Behav 39:329–337

    Article  Google Scholar 

  • Breuner C (2008) Maternal stress, glucocorticoids, and the maternal/fetal match hypothesis. Horm Behav 54:485–487

    Article  CAS  PubMed  Google Scholar 

  • Champagne FA, Curley JP (2009) The trans-generational influence of maternal care on offspring gene expression and behavior in rodents. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. The University of Chicago Press, Chicago, pp 182–202

    Google Scholar 

  • Coe CL, Lubach GR, Crispen HR, Shirtcliff EA, Schneider ML (2010) Challenges to maternal wellbeing during pregnancy impact temperament, attention, and neuromotor responses in the infant rhesus monkey. Dev Psychobiol 52:625–637

    Article  PubMed  Google Scholar 

  • Del Giudice M (2012) Fetal programming by maternal stress: insights from a conflict perspective. Psychoneuroendocrinology 37:1614–1629

    Article  PubMed  Google Scholar 

  • Del Giudice M, Ellis BJ, Shirtcliff EA (2011) The adaptive calibration model of stress responsivity. Neurosci Biobehav Rev 35:1562–1592

    Article  PubMed  Google Scholar 

  • DeVries A, Holmes MC, Heijnis A, Seier JV, Heerden J, Louw J, Wolfe-Coote S, Meaney MJ, Levitt NS, Seckl JR (2007) Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic-pituitary-adrenal axis function. J Clin Invest 117:1058–1067

    Article  CAS  Google Scholar 

  • Dodic M, Peers A, Coghlan JP, Wintour M (1999) Can excess glucocorticoid, in utero, predispose to cardiovascular and metabolic disease in middle age? Trends Endocrinol Metab 10:86–91

    Article  CAS  PubMed  Google Scholar 

  • Ellis BJ, Boyce WT, Belsky J, Bakermans-Kranenburg MJ, van Ijzendoorn MH (2011) Differential susceptibility to the environment: an evolutionary-neurodevelopmental theory. Dev Psychopathol 23:7–28

    Article  PubMed  Google Scholar 

  • Fairbanks LA (1996) Individual differences in maternal styles: causes and consequences for mothers and offspring. Adv Study Behav 25:579–611

    Article  Google Scholar 

  • Fairbanks LA, McGuire MT (1988) Long-term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. Dev Psychobiol 21:711–724

    Article  CAS  PubMed  Google Scholar 

  • Fairbanks LA, McGuire MT (1995) Maternal condition and the quality of maternal care in vervet monkeys. Behaviour 132:733–754

    Article  Google Scholar 

  • Flinn MV, Nepomnaschy PA, Muehlenbein MP, Ponzi D (2011) Evolutionary functions of early social modulation of hypothalamic-pituitary-adrenal axis development in humans. Neurosci Biobehav Rev 35:1611–1629

    Article  CAS  PubMed  Google Scholar 

  • Glover V (2011) Prenatal stress and the origins of psychopathology: an evolutionary perspective. J Child Psychol Psychiatry 52:356–367

    Article  PubMed  Google Scholar 

  • Glover V, O’Connor TG, O’Donnell K (2010) Prenatal stress and the programming of the HPA axis. Neurosci Biobehav Rev 35:17–22

    Article  CAS  PubMed  Google Scholar 

  • Gluckman PD, Hanson MA (2004) Living with the past: evolution, development, and patterns of disease. Science 305:1733–1736

    Article  CAS  PubMed  Google Scholar 

  • Groothuis TTG, Maestripieri D (2013). Parental influences on offspring personality traits in oviparous and placental vertebrates. In: Carere C, Maestripieri D (eds) Animal personalities: behavior, physiology, and evolution. The University of Chicago Press, Chicago

    Google Scholar 

  • Gunnar MR, Gonzalez C, Goodlin C, Levine S (1981) Behavioral and pituitary-adrenal responses during a prolonged separation period in infant rhesus macaques. Psychoneuroendocrinology 6:65–75

    Article  CAS  PubMed  Google Scholar 

  • Hauser MD, Fairbanks LA (1988) Mother-offspring conflict in vervet monkeys: variation in response to ecological conditions. Anim Behav 36:802–813

    Article  Google Scholar 

  • Hayward LS, Wingfield JC (2004) Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen Comp Endocrinol 135:365–371

    Article  CAS  PubMed  Google Scholar 

  • Horton TH (2005) Fetal origins of developmental plasticity: animal models of induced life history variation. Am J Hum Biol 7:34–43

    Article  Google Scholar 

  • Koch H, McCormack KM, Sanchez MM, Maestripieri D (2013) The development of the hypothalamic-pituitary-adrenal axis function in rhesus monkeys: effects of age, sex, and early experience. Dev Psychobiol, in press

    Article  Google Scholar 

  • Kofman O (2002) The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci Biobehav Rev 26:457–470

    Article  CAS  PubMed  Google Scholar 

  • Loman MM, Gunnar MR (2010) Early experience and the development of stress reactivity and regulation in children. Neurosci Biobehav Rev 34:867–876

    Article  PubMed  Google Scholar 

  • Love OP, Williams TD (2008) The adaptive value of stress-induced phenotypes: effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness. Am Nat 172:135–149

    Article  Google Scholar 

  • Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O (2003) Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev 27:119–127

    Article  CAS  PubMed  Google Scholar 

  • Macrì S, Würbel H (2006) Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm Behav 50:667–680

    Article  PubMed  Google Scholar 

  • Macrì S, Würbel H (2007) Effects of variation in postnatal maternal environment on maternal behaviour and fear and stress responses in rats. Anim Behav 73:171–184

    Article  Google Scholar 

  • Maestripieri D (1998) Parenting styles of abusive mothers in group-living rhesus macaques. Anim Behav 55:1–11

    Article  PubMed  Google Scholar 

  • Maestripieri D (2002) Parent-offspring conflict in primates. Int J Primatol 23:923–951

    Article  Google Scholar 

  • Maestripieri D (2005) Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proc Natl Acad Sci U S A 102:9726–9729

    Article  CAS  PubMed  Google Scholar 

  • Maestripieri D (2009) Maternal influences on offspring growth, reproduction, and behavior in primates. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. The University of Chicago Press, Chicago, pp 256–291

    Google Scholar 

  • Maestripieri D, Carroll KA (1998a) Risk factors for infant abuse and neglect in rhesus monkeys. Psychol Sci 9:143–145

    Article  Google Scholar 

  • Maestripieri D, Carroll KA (1998b) Behavioral and environmental correlates of infant abuse in group-living pigtail macaques. Infant Behav Dev 21:603–612

    Article  Google Scholar 

  • Maestripieri D, Mateo JM (eds) (2009) Maternal effects in mammals. The University of Chicago Press, Chicago

    Google Scholar 

  • Maestripieri D, Wallen K, Carroll KA (1997) Infant abuse runs in families of group-living pigtail macaques. Child Abuse Negl 21:465–471

    Article  CAS  PubMed  Google Scholar 

  • Maestripieri D, Tomaszycki M, Carroll KA (1999) Consistency and change in the behavior of rhesus macaque abusive mothers with successive infants. Dev Psychobiol 34:29–35

    Article  CAS  PubMed  Google Scholar 

  • Maestripieri D, Higley JD, Lindell SG, Newman TK, McCormack KM, Sanchez MM (2006a) Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques. Behav Neurosci 120:1017–1024

    Article  PubMed  Google Scholar 

  • Maestripieri D, McCormack K, Lindell SG, Higley JD, Sanchez MM (2006b) Influence of parenting style on the offspring’s behavior and CSF monoamine metabolites levels in crossfostered and noncrossfostered female rhesus macaques. Behav Brain Res 175:90–95

    Article  CAS  PubMed  Google Scholar 

  • Maestripieri D, Lindell SG, Higley JD (2007) Intergenerational transmission of maternal behavior in rhesus monkeys and its underlying mechanisms. Dev Psychobiol 49:165–171

    Article  PubMed  Google Scholar 

  • Maestripieri D, Hoffman CL, Anderson GM, Carter CS, Higley JD (2009) Mother-infant interactions in free-ranging rhesus macaques: relationships between physiological and behavioral variables. Physiol Behav 96:613–619

    Article  CAS  PubMed  Google Scholar 

  • Mateo JM (2009) Maternal influences on development, social relationships, and survival behaviors. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. The University of Chicago Press, Chicago, pp 133–158

    Google Scholar 

  • McCormack K, Newman TK, Higley JD, Maestripieri D, Sanchez MM (2009) Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants. Horm Behav 55:538–547

    Article  CAS  PubMed  Google Scholar 

  • Mousseau TA, Fox CW (eds) (1998) Maternal effects as adaptations. Oxford University Press, Oxford

    Google Scholar 

  • Oitzl MS, Champagne DL, Van der Veen R, de Kloet ER (2010) Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci Biobehav Rev 34:853–866

    Article  CAS  PubMed  Google Scholar 

  • Parker KJ, Maestripieri D (2011) Identifying key features of early stressful experiences that produce stress vulnerability and resilience in primates. Neurosci Biobehav Rev 35:1466–1483

    Article  PubMed  Google Scholar 

  • Parker KJ, Buckmaster CL, Sundlass K, Schatzberg AF, Lyons DM (2006) Maternal mediation, stress inoculation, and the development of neuroendocrine stress resistance in primates. Proc Natl Acad Sci U S A 103:3000–3005

    Article  CAS  PubMed  Google Scholar 

  • Price T (1998) Maternal and paternal effects in birds. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, Oxford, pp 202–226

    Google Scholar 

  • Sanchez MM, McCormack K, Grand AP, Fulks R, Graff A, Maestripieri D (2010) Effects of early maternal abuse and sex on ACTH and cortisol responses to the CRH challenge during the first 3 years of life in group-living rhesus monkeys. Dev Psychopathol 22:45–53

    Article  PubMed  Google Scholar 

  • Schino G, Speranza L, Troisi A (2001) Early maternal rejection and later social anxiety in juvenile and adult Japanese macaques. Dev Psychobiol 38:186–190

    Article  CAS  PubMed  Google Scholar 

  • Schneider ML, Coe CL (1993) Repeated social stress during pregnancy impairs neuromotor development of the primate infant. J Dev Behav Pediatr 14:81–87

    Article  CAS  PubMed  Google Scholar 

  • Seery MD (2011) Resilience: a silver lining to experiencing adverse life events? Curr Dir Psychol Sci 20:390–394

    Article  Google Scholar 

  • Simpson MJA (1985) Effects of early experience on the behaviour of yearling rhesus monkeys (Macaca mulatta) in the presence of a strange object: classification and correlation approaches. Primates 26:57–72

    Article  Google Scholar 

  • Simpson MJA, Datta SB (1990) Predicting infant enterprise from early relationships in rhesus macaques. Behaviour 116:42–63

    Article  Google Scholar 

  • Simpson MJA, Gore MA, Janus M, Rayment FDG (1989) Prior experience of risk and individual differences in enterprise shown by rhesus monkey infants in the second half of their first year. Primates 30:493–509

    Article  Google Scholar 

  • Talge NM, Neal C, Glover V etal (2007) Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol Psychiatry 48:245–261

    Article  PubMed  Google Scholar 

  • Uller T, Pen I (2011) A theoretical model of the evolution of maternal effects under parent-offspring conflict. Evolution 65:2075–2084

    Article  PubMed  Google Scholar 

  • Uno H, Lohmiller L, Thieme C, Kemnitz JW, Engle MJ, Roecker EB, Farrell PM (1990) Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus. Dev Brain Res 53:157–167

    Article  CAS  Google Scholar 

  • Welberg LA, Seckl JR (2001) Prenatal stress, glucocorticoids, and the programming of the brain. J Neuroendocrinol 132:113–128

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute for Mind and Biology, The University of Chicago, 5730 South Woodlawn Avenue, Chicago, IL, 60637, USA

    Dario Maestripieri & Amanda C. E. Klimczuk

Authors
  1. Dario Maestripieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amanda C. E. Klimczuk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dario Maestripieri .

Editor information

Editors and Affiliations

  1. Istituto Superiore di Sanità, 299 Viale Regina Elena, Rome, 00161, Italy

    Giovanni Laviola

  2. Istituto Superiore di Sanità, 299 Viale Regina Elena, Rome, 00161, Italy

    Simone Macrì

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Maestripieri, D., Klimczuk, A.C.E. (2013). Prenatal and Maternal Psychosocial Stress in Primates: Adaptive Plasticity or Vulnerability to Pathology?. In: Laviola, G., Macrì, S. (eds) Adaptive and Maladaptive Aspects of Developmental Stress. Current Topics in Neurotoxicity, vol 3. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5605-6_3

Download citation

Publish with us

Policies and ethics

Search

Navigation