Living organisms are flexible; they can respond to changing conditions with a variety of morphological, physiological, and behavioral mechanisms. The processes that organisms use to change and respond to environmental challenges are posited to be evolved adaptations (West-Eberhard Reference West-Eberhard2003). The development of the psychology of the human child may be viewed as a complex set of flexible adaptations (Bjorklund & Pellegrini Reference Bjorklund and Pellegrini2002). Del Giudice proposes a comprehensive model for how humans might adjust future reproductive strategies – such as timing of puberty, mate choice, and parental behavior – in response to environmental conditions during middle childhood. His ideas are exciting because they suggest new research directions, including investigation of the stimuli that affect release of adrenal androgens (DHEA/S), and the associated effects on neurobiological development.

The human child must master the dynamics of social networks and culture, supported by the extraordinary information-processing capacities of the human brain (Adolphs Reference Adolphs2003; Roth & Dicke Reference Roth and Dicke2005). We are interested in the unusual sensitivity of the fetus and child to the social environment – interpersonal relationships – and the consequent changes that occur in neuroendocrine systems. Our curiosity is piqued by both the paradoxical nature of this phenomenon – for some hormonal responses have attendant somatic costs (e.g., Flinn Reference Flinn2006; Muehlenbein & Bribiescas Reference Muehlenbein and Bribiescas2005) – and its importance for human health. For example, maternal depression and high levels of social anxiety during pregnancy are associated with low birth weight, elevated stress reactivity, and subsequent disease risk for offspring (Barker Reference Barker1998; Gluckman & Hanson Reference Gluckman and Hanson2006; Weinstock Reference Weinstock2005). The processes that underlay this biological embedding of information from the social environment in humans remain obscure.

On the basis of life history theory, the delayed reproductive maturity represented by an extended period of childhood and juvenility in humans is predicted to be important for learning cultural, social, and ecological skills that help prepare the child for the adult socio-competitive environment (Flinn et al. Reference Flinn, Geary and Ward2005; Geary & Bjorklund Reference Geary and Bjorklund2000). During this developmental period, boys and girls show behavioral sex differences in play and social interactions: boys tend to invest more time in organizing groups of peers, among which they form hierarchies, and compete with other groups. Conversely, girls usually invest more time in dyadic interactions with similar-age girls, caring for siblings, and doing domestic chores (Geary & Flinn Reference Geary and Flinn2002; Quinlan et al. Reference Quinlan, Quinlan and Flinn2003). How the onset of male coalitional and female dyadic psychobiology and life history trajectories might be influenced by family environment is yet an open question.

In the target article, Del Giudice draws our attention to the life history stage of middle childhood, which has not received much attention in comparison with infancy and early childhood on the one hand, and adolescence and the transition to early adulthood on the other. Yet it is childhood that distinguishes humans from other primates (Bogin Reference Bogin1999), and it is the period during which some of the most uniquely human socio-cognitive abilities are developed and refined (Geary Reference Geary2005b). Adrenarche appears to be a key neuroendocrine transition in middle childhood that may facilitate the ontogeny of the neural mechanisms that underpin human sociality (Campbell Reference Campbell2006). Humans (and chimpanzees), moreover, have an unusual pattern to adrenarche. A few months after birth, the fetal zone of the adrenal cortex disappears and the levels of DHEA(S) diminish to near zero. In other primates, such as macaques and baboons (Muehlenbein et al. Reference Muehlenbein, Richards, Campbell, Phillippi, Murchison, Myers and Svec2003; Nguyen & Conley Reference Nguyen, Conley, Flück and Miller2008), newborns have high levels of DHEA(S) (compared to chimpanzees and humans) that slowly and steadily decrease with age.

In humans, adrenarche typically begins around age 7 years for females and 9 years for males (Dhom Reference Dhom1973), and DHEAS levels peak earlier in females than in males (Orentreich et al. Reference Orentreich, Brind, Rizer and Vogelman1984; Sulcova et al. Reference Sulcova, Hill, Hampl and Starka1997). The zona reticularis of the adrenal gland gradually begins developing at around age 3 years, at which time the production of DHEA(S) begins (Palmert et al. Reference Palmert, Hayden, Mansfield, Crigler, Crowley, Chandler and Boepple2001; Remer et al. Reference Remer, Boye, Hartmann and Wudy2005). DHEA(S) is produced by the adrenal gland and converted to DHEA within target cells (Labrie et al. Reference Labrie, Belanger, Luu-The, Labrie, Simard, Cusan, Gomez and Candas1998). DHEA can then be converted into other androgens, such as androstenedione, as well as estrogens. DHEA acts antagonistically to cortisol (Hennebert et al. Reference Hennebert, Chalbot, Alran and Morfin2007; Kimonides et al. Reference Kimonides, Spillantini, Sofroniew, Fawcett and Herbert1999), and both are derived from the pregnenolone precursor (Rainey et al. Reference Rainey, Carr, Sasano, Suzuki and Mason2002). Timing of adrenarche also appears to be sensitive to environmental conditions; low-quality parental investment predicts earlier onset of adrenarche (Ellis & Essex Reference Ellis and Essex2007). Infants with a lower birth weight also exhibit earlier age at adrenarche (Ong et al. Reference Ong, Potau, Petry, Jones, Ness, Honour, de Zegher, Ibanez and Dunger2004).

The links between adrenarche and the socio-cognitive demands of middle childhood are uncertain. Androgens associated with adrenarche are likely important for brain maturation (Campbell Reference Campbell2006). DHEA(S) is a neurosteroid expressed in the developing brain in a region-specific fashion and involved in regulating the organization of the neocortex (Compagnone & Mellon Reference Compagnone and Mellon1998). While brain growth in humans is almost complete by age 7 years (the typical time of onset of adrenarche), cortical maturation with synaptic pruning continues (Gogtay et al. Reference Gogtay, Giedd, Lusk, Hayashi, Greenstein, Vaituzis, Nugent, Herman, Clasen, Toga, Rapoport and Thompson2004). Glucose metabolism rates in the brain also remain high until around age 10 years (Chugani et al. Reference Chugani1998). DHEA(S) promotes neurological functions in rodents (Karishma & Herbert Reference Karishma and Herbert2002), and DHEA(S) binds to various receptors in the human brain, including GABAa (Majewska et al. Reference Majewska, Demigoren, Spivak and London1990). DHEA(S) may also affect mood in humans (Arlt et al. Reference Arlt, Callies and Allolio2000; Micheal et al. Reference Micheal, Jenaway, Paykel and Herbert2000).

Functional connections between the middle childhood attachment transitions and adrenarche, however, remain speculative; the timing could be coincidental. DHEA(S) production has several physiological roles in childhood, including muscle and bone growth (Zemel & Katz Reference Zemel and Katz1986) and immuno-stimulation (Chen & Parker Reference Chen and Parker2004). Rises in DHEA(S) during adrenarche may also be important in the hypothalamic desensitization associated with the onset of puberty (Tanner Reference Tanner1978).

“Attachment” in humans appears to involve additional functions beyond security and protection; the flow of information from parents and other relatives, and recruitment into kin-based coalitions, emerge as critical challenges for the child. Predicting what one's social environment will be as an adult and modifying phenotypic trajectories of the hormonal, neurological, and psychological mechanisms that comprise “internal working models” seems extraordinarily complex, and unlikely to favor early canalization of reproductive strategy. A more flexible system that allows inclusion of input throughout childhood and adolescence would have advantages over one primarily contingent on conditions during infancy (cf. Belsky Reference Belsky2002; Draper & Harpending Reference Draper and Harpending1982; Quinlan & Flinn Reference Quinlan and Flinn2003).

To evaluate the exciting new ideas about the adjustment of reproductive strategies in middle childhood proposed by Del Giudice, it would be useful to have research designed to specifically evaluate causal relations among the key proximate mechanisms. Comparisons with other primates will help identify what aspects of human adrenarche are shared or derived. Analyses of patterns of attachment and adrenarche in apes would be most interesting. Longitudinal studies of human child development that monitor DHEA(S) levels in naturalistic context could provide detailed data on links among hormone levels, family environment, affiliative bonds, and long-term outcome measures.