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Early stress and human behavioral development: emerging evolutionary perspectives

Published online by Cambridge University Press:  16 April 2014

M. Del Giudice*
Affiliation:
Department of Psychology, University of New Mexico Logan Hall, University of New Mexico, Albuquerque, NM, USA
*
*Address for correspondence: M. Del Giudice, Department of Psychology, University of New Mexico, Logan Hall, University of New Mexico, Albuquerque, NM 87131, USA. (Email marcodg@unm.edu)

Abstract

Stress experienced early in life exerts a powerful, lasting influence on development. Converging empirical findings show that stressful experiences become deeply embedded in the child’s neurobiology, with an astonishing range of long-term effects on cognition, emotion, and behavior. In contrast with the prevailing view that such effects are the maladaptive outcomes of ‘toxic’ stress, adaptive models regard them as manifestations of evolved developmental plasticity. In this paper, I offer a brief introduction to adaptive models of early stress and human behavioral development, with emphasis on recent theoretical contributions and emerging concepts in the field. I begin by contrasting dysregulation models of early stress with their adaptive counterparts; I then introduce life history theory as a unifying framework, and review recent work on predictive adaptive responses (PARs) in human life history development. In particular, I discuss the distinction between forecasting the future state of the environment (external prediction) and forecasting the future state of the organism (internal prediction). Next, I present the adaptive calibration model, an integrative model of individual differences in stress responsivity based on life history concepts. I conclude by examining how maternal–fetal conflict may shape the physiology of prenatal stress and its adaptive and maladaptive effects on postnatal development. In total, I aim to show how theoretical work from evolutionary biology is reshaping the way we think about the role of stress in human development, and provide researchers with an up-to-date conceptual map of this fascinating and rapidly evolving field.

Type
Review
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014 

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References

1. Flinn, MV. Evolution and ontogeny of the stress response to social challenges in the human child. Dev Rev. 2006; 26, 138174.Google Scholar
2. Glover, V. Prenatal stress and the origins of psychopathology: an evolutionary perspective. J Child Psychol Psychiatry. 2011; 52, 356367.Google Scholar
3. Ganzel, BL, Morris, PA, Wethington, E. Allostasis and the human brain: integrating models of stress from the social and life sciences. Pychol Rev. 2010; 117, 134174.CrossRefGoogle ScholarPubMed
4. McEwen, BS. Brain on stress: how the social environment gets under the skin. P Natl Acad Sci USA. 2012; 109, 1718017185.CrossRefGoogle ScholarPubMed
5. Beauchaine, TP, Neuhaus, E, Zalewski, M, Crowell, SE, Potapova, N. The effects of allostatic load on neural systems subserving motivation, mood regulation, and social affiliation. Dev Psychopathol. 2011; 23, 975999.Google Scholar
6. Meaney, MJ. Environmental programming of phenotypic diversity in female reproductive strategies. Adv Genet. 2007; 59, 173215.Google Scholar
7. Pechtel, P, Pizzagalli, DA. Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology. 2011; 214, 5570.Google Scholar
8. Del Giudice, M, Ellis, BJ, Shirtcliff, EA. The adaptive calibration model of stress responsivity. Neurosci Biobehav Rev. 2011; 35, 15621592.Google Scholar
9. Ellis, BJ, Del Giudice, M. Beyond allostatic load: rethinking the role of stress in regulating human development. Dev Psychopathol. 2014; 26, 120.Google Scholar
10. Ellison, PT. Fetal programming and fetal psychology. Infant Child Dev. 2010; 19, 620.Google Scholar
11. Carr, CP, Martins, CMS, Stingel, AM, et al. The role of early life stress in adult psychiatric disorders: a systematic review according to childhood trauma subtypes. J Nerv Ment Dis. 2013; 201, 10071020.Google Scholar
12. Shonkoff, JP, Garner, AS, Siegel, BS, et al. The lifelong effects of early childhood adversity and toxic stress. Pediatrics. 2012; 129, e232e246.Google Scholar
13. Koolhaas, JM, Bartolomucci, A, Buwalda, B, et al. Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev. 2011; 35, 12911301.Google Scholar
14. Sterling, P, Eyer, J. Allostasis: a new paradigm to explain arousal pathology. In Handbook of Life Stress, Cognition, and Health (eds. Fisher S, Reason J), 1988; pp. 629650. Oxford University Press: New York.Google Scholar
15. McEwen, BS, Wingfield, JC. The concept of allostasis in biology and biomedicine. Horm Behav. 2003; 42, 215.Google Scholar
16. Ellis, BJ, Jackson, JJ, Boyce, WT. The stress response system: universality and adaptive individual differences. Dev Rev. 2006; 26, 175212.CrossRefGoogle Scholar
17. Gunnar, MR, Vazquez, D. Stress neurobiology and developmental psychopathology. In Developmental Psychopathology, vol. 2, 2nd edn (eds. Cicchetti D, Cohen DJ), 2006; pp. 533568. Wiley & Sons: Hoboken, NJ.Google Scholar
18. Adam, EK, Klimes-Dougan, B, Gunnar, MR. Social regulation of the adrenocortical response to stress in infants, children and adolescents: implications for psychopathology and education. In Human Behavior, Learning, and the Developing Brain: Atypical Development (eds. Coch D, Dawson G, Fischer KW), 2007; pp. 264304. Guilford: New York.Google Scholar
19. Habib, KE, Gold, PW, Chrousos, GP. Neuroendocrinology of stress. Neuroendocrinology. 2001; 30, 695728.Google Scholar
20. Schwabe, L, Wolf, OT. Stress and multiple memory systems: from ‘thinking’ to ‘doing’. Trends Cogn Sci. 2013; 17, 6068.Google Scholar
21. Miller, GE, Chen, E, Parker, KJ. Psychological stress in childhood and susceptibility to the chronic diseases of aging: moving toward a model of behavioral and biological mechanisms. Psychol Bull. 2011; 137, 959997.Google Scholar
22. Champagne, FA. Early adversity and developmental outcomes: interaction between genetics, epigenetics, and social experiences across the life span. Perspect Psychol Sci. 2010; 5, 564574.Google Scholar
23. Meaney, MJ. Epigenetics and the biological definition of gene×environment interactions. Child Dev. 2010; 81, 4179.CrossRefGoogle Scholar
24. Boyce, WT, Ellis, BJ. Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev Psychopathol. 2005; 17, 271301.Google Scholar
25. López, HH, Hay, AC, Conklin, PH. Attractive men induce testosterone and cortisol release in women. Horm Behav. 2009; 56, 8492.CrossRefGoogle ScholarPubMed
26. Lupien, SJ, Ouellet-Morin, I, Hupbach, A, et al. Beyond the stress concept: allostatic load – a developmental biological and cognitive perspective. In Developmental Psychopathology, vol. 2, 2nd edn (eds. Cicchetti D, Cohen DJ), 2006; pp. 578628. Wiley & Sons: Hoboken, NJ.Google Scholar
27. Van den Bergh, BRH, Mulder, EJH, Mennes, M, Glover, V. Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review. Neurosci Biobehav Rev. 2005; 29, 237258.CrossRefGoogle ScholarPubMed
28. Weinstock, M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immunity. 2005; 19, 296308.Google Scholar
29. McEwen, BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev. 2007; 87, 873904.CrossRefGoogle ScholarPubMed
30. Class, QA, Abel, KM, Khashan, AS, et al. Offspring psychopathology following preconception, prenatal and postnatal maternal bereavement stress. Psychol Med. 2014; 44, 7184.CrossRefGoogle ScholarPubMed
31. Cameron, NM, Champagne, FA, Parent, C, et al. The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci Biobehav Rev. 2005; 29, 843865.Google Scholar
32. Schwabe, L, Bohbot, VD, Wolf, OT. Prenatal stress changes learning strategies in adulthood. Hippocampus. 2012; 22, 21362143.Google Scholar
33. Glasheen, C, Richardson, GA, Kim, KH, et al. Exposure to maternal pre- and postnatal depression and anxiety symptoms: risk for major depression, anxiety disorders, and conduct disorder in adolescent offspring. Dev Psychopathol. 2013; 25, 10451063.Google Scholar
34. Del Giudice, M. Fetal programming by maternal stress: insights from a conflict perspective. Psychoneuroendocrinology. 2012; 37, 16141629.Google Scholar
35. Baibazarova, E, van de Beek, C, Cohen-Kettenis, PT, et al. Influence of prenatal maternal stress, maternal plasma cortisol and cortisol in the amniotic fluid on birth outcomes and child temperament at 3 months. Psychoneuroendocrinology. 2013; 38, 907915.Google Scholar
36. Erni, K, Shaqiri-Emini, L, Zimmermann, R, Ehlert, U. Psychobiological effects of prenatal glucocorticoid exposure in 10-year-old-children. Front Psychiatry. 2012; 3, 104.Google Scholar
37. Werner, E, Zhao, Y, Evans, L, et al. Higher maternal prenatal cortisol and younger age predict greater infant reactivity to novelty at 4 months: an observation-based study. Dev Psychobiol. 2013; 55, 707718.Google Scholar
38. O’Connor, TG, Bergman, K, Sarkar, P, Glover, V. Prenatal cortisol exposure predicts infant cortisol response to acute stress. Dev Psychobiol. 2013; 55, 145155.Google Scholar
39. Gunnar, MR, Adam, EK. The hypothalamic–pituitary–adrenocortical system and emotion: current wisdom and future directions. Monogr Soc Res Child. 2012; 77, 109119.CrossRefGoogle Scholar
40. Rutter, M. Resilience: some conceptual considerations. J Adol Health. 1993; 14, 690696.Google Scholar
41. Seery, MD, Leo, RJ, Lupien, SP, Kondrak, CL, Almonte, JL. An upside to adversity? Moderate cumulative lifetime adversity is associated with resilient responses in the face of controlled stressors. Psychol Sci. 2013; 24, 11811189.Google Scholar
42. Ellis, BJ, Boyce, WT, Belsky, J, Bakermans-Kranenburg, MJ, van Ijzendoorn, MH. Differential susceptibility to the environment: an evolutionary–neurodevelopmental theory. Dev Psychopathol. 2011; 23, 728.CrossRefGoogle Scholar
43. Ellis, BJ, Boyce, WT. Biological sensitivity to context. Curr Dir Psychol Sci. 2008; 17, 183187.Google Scholar
44. DeWitt, TJ, Scheiner, SM. Phenotypic Plasticity: Functional and Conceptual Approaches, 2004. Oxford University Press: New York.Google Scholar
45. Pigliucci, M. Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol. 2005; 20, 481486.CrossRefGoogle ScholarPubMed
46. Schlichting, CD, Pigliucci, M. Phenotypic Evolution: A Reaction Norm Perspective, 1998. Sinauer Associates: Sunderland, MA.Google Scholar
47. Belsky, J, Steinberg, L, Draper, P. Childhood experience, interpersonal development, and reproductive strategy: an evolutionary theory of socialization. Child Dev. 1991; 62, 647670.Google Scholar
48. Frankenhuis, WE, de Weerth, C. Does early-life exposure to stress shape, or impair, cognition? Curr Direct Psychol Sci. 2013; 22, 407412.CrossRefGoogle Scholar
49. Kaiser, S, Sachser, N. Effects of prenatal social stress on offspring development: pathology or adaptation? Curr Direct Psychol Sci. 2009; 18, 118121.CrossRefGoogle Scholar
50. Hamilton, WD. The genetical evolution of social behavior. J Theor Biol. 1964; 7, 152.Google Scholar
51. West, SA, Griffin, AS, Gardner, A. Evolutionary explanations for cooperation. Curr Biol. 2007; 17, R661R672.Google Scholar
52. Bourke, AFG. The validity and value of inclusive fitness theory. Proc R Soc B. 2011; 278, 33133320.Google Scholar
53. Nesse, RM. On the difficulty of defining disease: a Darwinian perspective. Med Health Care Philos. 2001; 4, 3746.Google Scholar
54. Nesse, RM, Jackson, ED. Evolution: psychiatric nosology’s missing biological foundation. Clin Neuropsychiatry. 2006; 3, 121131.Google Scholar
55. Gluckman, PD, Hanson, MA, Spencer, HG. Predictive adaptive responses and human evolution. Trends Ecol Evol. 2005; 20, 527533.CrossRefGoogle ScholarPubMed
56. Gluckman, PD, Hanson, MA, Beedle, AS. Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol. 2007; 19, 119.Google Scholar
57. Korte, SM, Koolhaas, JM, Wingfield, JC, McEwen, BS. The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neurosci Biobehav Rev. 2005; 29, 338.Google Scholar
58. Pluess, M, Belsky, J. Prenatal programming of postnatal plasticity? Dev Psychopathol. 2011; 23, 2938.Google Scholar
59. Frankenhuis, WE, Del Giudice, M. When do adaptive developmental mechanisms yield maladaptive outcomes? Dev Psychol. 2012; 48, 628642.Google Scholar
60. DeWitt, TJ, Sih, A, Wilson, DS. Costs and limits of plasticity. Trends Ecol Evol. 1998; 13, 7781.Google Scholar
61. Nesse, RM. Ten questions for evolutionary studies of disease vulnerability. Evol Appl. 2011; 4, 264277.Google Scholar
62. Crespi, BJ. The evolution of maladaptation. Heredity. 2000; 84, 623629.Google Scholar
63. Stearns, S. The Evolution of Life Histories, 1992. Oxford University Press: New York.Google Scholar
64. Ellis, BJ, Figueredo, AJ, Brumbach, BH, Schlomer, GL. Fundamental dimensions of environmental risk: the impact of harsh versus unpredictable environments on the evolution and development of life history strategies. Hum Nat. 2009; 20, 204268.CrossRefGoogle ScholarPubMed
65. Hill, K, Kaplan, H. Life history traits in humans: theory and empirical studies. Annu Rev Anthropol. 1999; 28, 397430.Google Scholar
66. Kaplan, HS, Gangestad, SW. Life history theory and evolutionary psychology. In Handbook of Evolutionary Psychology (ed. Buss DM), 2005; pp. 6895. John Wiley & Sons: Hoboken, NJ.Google Scholar
67. Réale, D, Garant, D, Humphries, MM, et al. Personality and the emergence of the pace-of-life syndrome concept at the population level. Phil Trans R Soc B. 2010; 365, 40514063.Google Scholar
68. Sæther, B-E. The influence of body weight on the covariation between reproductive traits in European birds. Oikos. 1987; 48, 7988.Google Scholar
69. Figueredo, AJ, Vásquez, G, Brumbach, B, et al. Consilience and life history theory: from genes to brain to reproductive strategy. Dev Rev. 2006; 26, 243275.Google Scholar
70. Del Giudice, M. Self-regulation in an evolutionary perspective. In Biobehavioral Foundations of Self-Regulation (eds. Gendolla GHE, Koole S, Tops M), in press; Springer: New York.Google Scholar
71. Placek, CD, Quinlan, RJ. Adolescent fertility and risky environments: a population-level perspective across the lifespan. Proc R Soc B. 2012; 279, 40034008.Google Scholar
72. Simpson, JA, Griskevicius, V, Kuo, SI, Sung, S, Collins, WA. Evolution, stress, and sensitive periods: the influence of unpredictability in early versus late childhood on sex and risky behavior. Dev Psychol. 2012; 48, 674686.Google Scholar
73. Kuzawa, CW, Bragg, JM. Plasticity in human life history strategy: implications for contemporary human variation and the evolution of genus Homo. Curr Anthropol. 2012; 53, S369S382.Google Scholar
74. Del Giudice, M, Belsky, J. The development of life history strategies: toward a multi-stage theory. In The Evolution of Personality and Individual Differences (eds. Buss DM, Hawley PH), 2011; pp. 154176. Oxford University Press: New York.Google Scholar
75. Nettle, D, Frankenhuis, WE, Rickard, IJ. The evolution of predictive adaptive responses in human life history. Proc R Soc B. 2013; 280, 20131343.Google Scholar
76. Del Giudice, M. Life history plasticity in humans: the predictive value of early cues depends on the temporal structure of the environment. Proc R Soc B. 2014; 281, 20132222.Google Scholar
77. Del Giudice, M, Hinnant, JB, Ellis, BJ, El-Sheikh, M. Adaptive patterns of stress responsivity: a preliminary investigation. Dev Psychol. 2012; 48, 775790.Google Scholar
78. Fischer, B, van Doorn, GS, Dieckmann, U, Taborsky, B. The evolution of age-dependent plasticity. Am Nat. 2014; 183, 108125.Google Scholar
79. Ellis, BJ, Del Giudice, M, Shirtcliff, EA. Beyond allostatic load: the stress response system as a mechanism of conditional adaptation. In Child and Adolescent Psychopathology, 2nd edn (eds. Beauchaine TP, Hinshaw SP), 2013; pp. 251284. Wiley: New York.Google Scholar
80. Sandman, CA, Poggi Davis, E, Glynn, LM. Prescient human fetuses thrive. Psychol Sci. 2012; 23, 93100.Google Scholar
81. Talge, NM, Neal, C, Glover, V, et al. Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol Psychiatry. 2007; 48, 245261.CrossRefGoogle ScholarPubMed
82. Kapoor, A, Dunn, E, Kostaki, A, Andrews, MH, Matthews, SG. Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids. J Physiol. 2006; 572, 3144.Google Scholar
83. Trivers, RL. Parent–offspring conflict. Am Zool. 1974; 14, 249264.Google Scholar
84. Schlomer, GL, Del Giudice, M, Ellis, BJ. Parent–offspring conflict theory: an evolutionary framework for understanding conflict within human families. Psychol Rev. 2011; 118, 496521.CrossRefGoogle ScholarPubMed
85. Haig, D. Genetic conflicts in human pregnancy. Q Rev Biol. 1993; 68, 495532.Google Scholar
86. Haig, D. Putting up resistance: maternal-fetal conflict over the control of uteroplacental blood flow. In Endothelial Biomedicine (ed. Aird WC), 2007; pp. 135141. Cambridge University Press: New York.Google Scholar
87. Gangestad, SW, Caldwell Hooper, AE, Eaton, MA. On the function of placental corticotropin-releasing hormone: a role in maternal-fetal conflicts over blood glucose concentrations. Biol Rev. 2012; 87, 856873.Google Scholar
88. Wells, JCK. Is early development in humans a predictive adaptive response anticipating the adult environment? Trends Ecol Evol. 2006; 21, 424425.Google Scholar
89. Flinn, MV, Nepomnaschy, PA, Muehlenbein, MP, Ponzi, D. Evolutionary functions of early social modulation of hypothalamic-pituitary-adrenal axis development in humans. Neurosci Biobehav Rev. 2011; 35, 16111629.Google Scholar
90. Nepomnaschy, PA, Welch, KB, McConnell, DS, et al. Cortisol levels and very early pregnancy loss in humans. Proc Natl Acad Sci USA. 2006; 103, 39383942.Google Scholar
91. Belsky, J, Pluess, M. The nature (and nurture?) of plasticity in early human development. Perspect Psychol Sci. 2009; 4, 345351.Google Scholar
92. Uller, T, Pen, I. A theoretical model of the evolution of maternal effects under parent–offspring conflict. Evolution. 2011; 65, 20752084.Google Scholar
93. Brunton, PJ, Russell, JA. Neuroendocrine control of maternal stress responses and fetal programming by stress in pregnancy. Prog Neuro-Psychoph. 2011; 35, 11781191.Google Scholar
94. Haig, D. Genomic imprinting and kinship: how good is the evidence? Annu Rev Genet. 2004; 38, 553585.Google Scholar
95. Wilkins, JF. (ed.). Genomic imprinting. Adv Exp Med Biol. 2008; 626.Google Scholar
96. Heijmans, BT, Tobi, EW, Stein, AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA. 2008; 105, 1704717049.Google Scholar
97. Crespi, B, Badcock, C. Psychosis and autism as diametrical disorders of the social brain. Behav Brain Sci. 2008; 31, 241261.CrossRefGoogle ScholarPubMed
98. Del Giudice, M, Angeleri, R, Brizio, A, Elena, MR. The evolution of autistic-like and schizotypal traits: a sexual selection hypothesis. Front Psychol. 2010; 1, 41.CrossRefGoogle ScholarPubMed
99. Úbeda, F, Gardner, A. A model for genomic imprinting in the social brain: juveniles. Evolution. 2010; 64, 25872600.Google Scholar
100. Jones, JH. Fetal programming: adaptive life-history tactics or making the best of a bad start? Am J Hum Biol. 2005; 17, 2233.Google Scholar
101. Jones, JH. The force of selection on the human life cycle. Evol Hum Behav. 2009; 30, 305314.Google Scholar
102. Howerton, CL, Bale, TL. Prenatal programming: at the intersection of maternal stress and immune activation. Horm Behav. 2012; 62, 237242.Google Scholar
103. Miller, GE, Chen, E, Parker, KJ. Psychological stress in childhood and susceptibility to the chronic diseases of aging: moving toward a model of behavioral and biological mechanisms. Psychol Bull. 2011; 137, 959997.Google Scholar
104. Cole, SW. Social regulation of gene expression in the immune system. In The Oxford Handbook of Psychoneuroimmunology (ed. Segerstrom SC), 2012; pp. 254275. Oxford University Press: New York.Google Scholar
105. Murphy, MLM, Slavich, GM, Rohleder, N, Miller, GE. Targeted rejection triggers differential pro- and anti-inflammatory gene expression in adolescents as a function of social status. Clin Psychol Sci. 2013; 1, 3040.Google Scholar
106. McDade, TW. Life history theory and the immune system: steps toward a human ecological immunology. Yearb Phys Anthropol. 2003; 46, 100125.Google Scholar
107. Raison, CL, Miller, AH. The evolutionary significance of depression in pathogen host defense (PATHOS-D). Mol Psychiatry. 2012; 18, 1537.Google Scholar
108. Benros, ME, Mortensen, PB, Eaton, WW. Autoimmune diseases and infections as risk factors for schizophrenia. Annals NY Acad Sci. 2012; 1262, 5666.Google Scholar
109. Patterson, PH. Infectious Behavior: Brain-Immune Connections in Autism, Schizophrenia, and Depression. 2011. MIT Press: Cambridge, MA.Google Scholar