Evolution and ontogeny of stress response to social challenges in the human child
Introduction
Social challenges reliably stimulate release of the stress hormone cortisol (Dickerson and Kemeny, 2004, Flinn and England, 1997, Gunnar et al., 2000, Kirschbaum and Hellhammer, 1994). Given the evident short- and long-term costs to physical health (Ader et al., 2001, McEwen, 1998, Sapolsky, 2005), this presents an evolutionary paradox: Why do social interactions have such potent effects on physiological stress response in the human child? We do not have good explanations for why natural selection favored links between the neuropsychological mechanisms involved with assessment of the social environment and the neuroendocrine mechanisms that regulate stress hormones, such as cortisol and norepinephrine. Furthermore, we do not understand why these links are modifiable during ontogeny, such that early experiences may permanently alter neuroendocrine response to social challenges (Bartolomucci et al., 2005, Buwalda et al., 2005, Francis et al., 2002, Maestripieri et al., 2005, Mirescu et al., 2004, Weaver et al., 2004).
I approach this paradox from the integrative evolutionary paradigm of Nobel laureate Niko Tinbergen (1963), who emphasized the importance of linking proximate physiological explanations with ontogeny, phylogeny, and adaptive function. Here I first briefly review the idea that humans evolved large brains and an extended childhood as adaptations for coping with an increasingly complex and dynamic social and cultural environment. I then explore relations between physiological stress response and the ontogeny of social competencies. Two complementary theoretical models of hormonal stress response are considered: (a) maladaptation to the novelty of chronic stress in social environments (Hamburg, 1952, McEwen, 1995, Sapolsky, 1994), and (b) adaptive neural reorganization (Ademec et al., 2005, Flinn et al., 2005, Huether, 1998, Kaiser and Sachser, 2005, Meaney, 2001, Rodriguez Manzanares et al., 2005). I posit that one of the important functions of the stress response system, in connection with emotional states, such as fear or anxiety, is to manage the direction of mental processes to solving specific problems. In the relatively simple case of a rabbit seeing a fox, a “freeze” response may be enabled. The human child may face more cognitively challenging problems, including especially social interactions. For example, when dealing with the threat of an approaching bully, a child needs to reallocate her cognitive efforts to the task at hand: prepare for immediate contingencies by recalling salient information, enhancing relevant sensory input, and activating circuits for appropriate actions. Stress hormones may enable not only the acute responses to such challenges, but facilitate their modification during development as well.
Hypotheses are evaluated with analyses of data from an 18-year study of child stress in a rural community on the island of Dominica. The longitudinal depth, large sample size (30,122 salivary cortisol measures from 282 children and their families), and naturalistic paradigm provide a unique research design for investigating relations between social environment and ontogeny of stress response. Empirical analysis is complicated by the pleiotropic (i.e., multiple effects) nature of the key stress hormone cortisol. Moreover, the Dominica study does not have neurological data, hence direct or strong tests of hypotheses relating stress response, neural plasticity, and ontogeny of social competencies are not possible.
My objective here is to provide a plausible model and some new data pieces for the puzzle linking stress response to the neural plasticity that enables adaptation to the dynamic human social environment. Resolution of this paradox may have significant consequences for public health (Dressler and Bindon, 2000, Dressler et al., 2005, Flinn and England, 2003, Marmot, 2004), because it could provide new insights into associations among stress response, social disparities, and perinatal programming, among other outcomes (Barker, 1998, Heim and Nemeroff, 2001, Maccari et al., 2003, Worthman, 1999).
Wayonne’s dirt bomb struck the bright yellow dress hanging on the clothesline, making an impressive star-shaped smudge. His older cousin Jenny turned angrily from sweeping the house yard to chase him with her broom. Granny Deedee’s yell halted their squabble. Jenny’s face morphed from stifled argument to guilt, head bowed. She later confided to me that she felt upset because granny did not understand; her frustration was compounded by the rule that she must accept granny’s authority without disagreement (MVF field notes, July 17, 1994). Jenny’s cortisol level, measured from her saliva that I collected from all children in the community several times a day, rose from 1.4 to 4.2 μg/dl. The next day her secretory immunoglobulin-A levels dropped from 6.04 to 3.6 mg/dl. Four days later she had common cold symptoms: runny nose, headache, and low-grade fever (Fig. 1).
This anecdotal case example contributes to a common pattern. Children in this rural Dominican community are more than twice as likely to become ill during the week following a stressful event than during a week when they had not recently experienced any significant stressors (Flinn & England, 2003). This relation between social stress and illness is not confined to Dominican children. Humans respond to challenges in their social environments by elevating cortisol levels (Dickerson et al., 2004, Kemeny, 2003), often with negative consequences for their health (Cohen et al., 2003, Maier et al., 1994, Marmot et al., 1991, Mason et al., 1979). Morbidity and mortality rates for children in the stressful environments of orphanages and hospitals in early 20th century America, lacking the evolutionarily normal intimacy and social contact of the family, were appalling (e.g., Chapin, 1922, p. 214). It is not lack of food or hygienic care, nor just the occurrence of traumatic events that affect child health, but the lack of social support, including parental warmth and other factors that influence emotional states (Belsky, 1997, Belsky, 2005, Davidson et al., 2001, Field et al., 2003, Wismer Fries et al., 2005). Why should this be so? Why do social interactions, and a child’s perceptions of them, affect stress physiology and morbidity? And, more generally, why is the social environment of such paramount importance in a child’s world? From the Tinbergen perspective, these “why?” questions ultimately involve understanding the evolutionary design of the ontogeny of the mind and brain of the human child (e.g., Bjorklund and Pellegrini, 2002, Frith and Frith, 1999, Frith and Frith, 2001).
In Jenny’s village, located on the east coast of the island of Dominica where I have lived and studied over the past 18 years, most of a child’s mental efforts seem focused on negotiating social relationships with parents, siblings, grandparents, cousins and other kin, friends, teachers, bus drivers, neighbors, shop owners, and so forth. Foraging for mangos and guavas, hunting birds, or even fishing in the sea from rock cliffs, are relatively simple cognitive enterprises, complicated by conflicts with property owners, and decisions about which companions to garner and share calories with. The mind of the child seems more concerned with solving social puzzles than with utilitarian concerns of collecting food. Other populations may have more difficult subsistence practices that require more extensive learning (e.g., Bock, 2005), but the social chess game nonetheless appears ubiquitous and cognitively demanding in all cultures (Blurton-Jones and Marlowe, 2002, Hewlett and Lamb, 2005), as it likely was during human evolutionary history (Alexander, 1989, Baumeister and Leary, 1995, Bowlby, 1969, Bowlby, 1973, Hinde, 1974, Hinde and Stevenson-Hinde, 1987).
In the following two sections I review current theories of human life history and evolution of the human family (see also Figueredo et al., 2006). I suggest that conspecific social competition was the primary selective pressure shaping the uniquely human combination of physically altricial (i.e., immature and helpless) but mentally and linguistically precocial infancy, extended childhood, and extended adolescence, enabled by extensive bi-parental and kin care. I then turn to the role that the links between psychosocial stimuli and physiological stress response may play in guiding both the acute and long-term neurological plasticity necessary for adapting to the dynamic aspects of human sociality.
Section snippets
Evolution of the social child
“Most of us see a picture of innocence and helplessness: a clean slate. But, in fact, what we see in the crib is the greatest mind that has ever existed, the most powerful learning machine in the universe.” (Gopnik, Meltzoff, & Kuhl, 1999, p. 1)
The human child is a most extraordinary organism, possessed of ‘the greatest mind’ and yet ‘innocent and helpless’—in effect, a larva equipped with an enormous brain. Even relative to other primates the human infant is unusually altricial, and highly
Evolution of the human family as a nest for the child’s social mind
The human family is extraordinary and unique in many respects (Alexander, 1989, Alexander, 2005; Flinn et al., 2005, Geary and Flinn, 2001, Lancaster and Lancaster, 1987). Humans are the only species to live in large multi-male groups with complex coalitions and extensive paternal care. Humans have concealed ovulation, altricial infants, lengthy child development, female orgasm, and menopause. These traits may be causally linked and provide important clues towards reconstructing the evolution
Stress response mechanisms
Changing, unpredictable environments require adjustment of priorities. Growth, immunity, digestion, and sex are irrelevant while being chased by a predator (Sapolsky, 1994), or coping with a traumatic social event. Emergencies—large and small, good and bad—perceived by the brain stimulate a variety of neuroendocrine systems (Ellis, Jackson, and Boyce, this issue). Hundreds of different endogenous chemicals—steroid and peptide hormones, neurotransmitters, cytokines, and so forth—are released
Physiological stress response and the ontogeny of social competencies
Early theoretical models of stress response did not attempt to directly explain the apparent evolutionary paradox of sensitivity to the social environment. For Seyle (1976), “stress” was a general syndrome, and emphasis was placed on understanding the underlying physiological mechanisms. Subsequent analysis of variation in response to different potential “stressors” suggested that stress theory needed to explain more specific connections (Mason, 1968). Munck et al. (1984) proposed that some
Ontogeny of stress response to psychosocial stimuli: The Dominica study
“What is missing are long-term prospective studies that track the nature and timing of early stress exposure and the linkages to children’s later stress exposure, HPA functioning, and behaviors.” (Essex, Klein, Cho, & Kalin, 2002, 777)
Assessment of relations among psychosocial stressors, hormonal stress response, and health is complex, requiring (a) longitudinal monitoring of social environment, emotional states, hormone levels, immune measures, and health, (b) control of extraneous effects
Conclusion
Returning to the paradox of why natural selection favored sensitivity of stress response to social stimuli in the human child, several points emerge. Mastering the social environment presents special challenges for the human child. Social competence is difficult because the target is constantly changing and similarly equipped with theory of mind and other cognitive abilities. Results from the Dominica study indicate that family environment is a primary source and mediator of stressful events in
Acknowledgments
For help with field and laboratory work I wish to especially thank my colleagues Barry England, Steve Gangestad, Bob Noone, and Randy Thornhill; former students Seamus Decker, Dave Leone, Robert Quinlan, and Mark Turner; and research assistants Edith Coipel and Eugenia Durand. Dave Geary, Pablo Nepomnaschy, and two anonymous reviewers provided superb advice on the ms. Primary funding for this research was provided by the National Science Foundation (BNS-8920569, SBR-9205373, and SBR-0136023).
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