Middle childhood: An evolutionary-developmental synthesis

Middle childhood is a crucial phase of human development characterized by a global shift in cognition, motivation, and social behavior. In this article I review recent work on middle childhood from an evolutionary-developmental perspective, and show how contributions from a broad range of disciplines can be synthesized into an integrated model of this life stage. I begin by reviewing the main evolved functions of middle childhood and the underlying hormonal mechanism of adrenarche. I then introduce the idea that the transition to middle childhood works as a “switch point” in the development of life history strategies. Finally, I discuss three important insights in the nature of middle childhood that arise from an integrated approach.

Middle childhood-conventionally going from about 6 to 11 years of age-is a crucial yet underappreciated phase of human development.On the surface, middle childhood may appear like a slow-motion interlude between the spectacular transformations of infancy and early childhood and those of adolescence.In reality, this life stage is anything but static: the transition from early to middle childhood heralds a global shift in cognition, motivation, and social behavior, with profound and wide-ranging implications for the development of personality, sex differences, and even psychopathology (Table 1).
In the last two decades, our understanding of middle childhood has been revolutionized by converging theories and findings from anthropology, primatology, evolutionary psychology, endocrinology, and behavior genetics.Here I show how these diverse contributions can be synthesized into an integrated evolutionary-developmental model of middle childhood.I begin by reviewing the main evolved functions of middle childhood and the cognitive, behavioral, and hormonal processes that characterize this life stage.I then introduce the idea that the transition to middle childhood works as a "switch point" in the development of life history strategies (Del Giudice, Angeleri, & Manera, 2009, 2012;Del Giudice & Belsky, 2011).Finally, I discuss three important insights in the nature of middle childhood that arise from an integrated approach.

WHAT IS MIDDLE CHILDHOOD?
Middle childhood is one of the main stages of human development, marked by the eruption of the first permanent molars around age 6 and the onset of androgen secretion by the adrenal glands at about 6-8 years (Bogin, 1997).In middle childhood body growth slows down to a minimum, usually following a small "mid-growth spurt."At the same time, muscularity increases and the body starts accumulating fat (the adiposity rebound; Hochberg, 2008), while sex differences in body composition become more pronounced (Del Giudice et al., 2009;Wells, 2007).Figure 1 places middle childhood in the broader context of human growth from conception to adolescence.
In biological terms, middle childhood corresponds to human juvenility-a stage in which the individual is still sexually immature, but no longer dependent on parents for survival.In social mammals and primates, juvenility is a phase of intense learning-often accomplished through play-in which youngsters practice adult behavioral patterns and acquire essential social and foraging skills.Indeed, the duration of juvenility in primates is strongly correlated with the size and complexity of social groups, as well as with cortical brain volume (Joffe, 1997).Social learning in juvenility can be usefully understood as investment in embodied capital-skills and knowledge that cost time and effort to acquire, but increase the future performance and reproductive success of an individual (Kaplan, Hill, Lancaster, & Hurtado, 2000).Increased heritability of general intelligence and language skills New genetic influences on general intelligence, language, aggression, prosociality Human children are no exception to this pattern.Social learning is universally recognized as a key evolved function of middle childhood, and is enabled by a global reorganization of cognitive functioning known as the "5-to-7 shift" (Weisner, 1996).By age 6, the brain has almost reached its maximum size, and is receiving a decreasing share of the body's glucose after the consumption peak of early childhood (Figure 1; Giedd & Rapoport, 2010;Kuzawa et al., in press).However, brain development proceeds at a sustained pace, with intensive synaptogenesis in cortical areas (gray matter) and rapid maturation of axonal connections (white matter; Lebel, Walker, Leemans, Phillips, & Beaulieu, 2008).The transition to middle childhood is marked by a simultaneous increase in perceptual abilities (including a transition from local to global visual processing), motor control (including the emergence of adult-like walking), and complex reasoning skills (Bjorklund, 2011;Poirel et al., 2011;Weisner, 1996).The most dramatic changes probably occur in the domain of self-regulation and executive functions: children become much more capable of inhibiting unwanted behavior, maintaining sustained attention, making and following plans, and so forth (Best, Miller, & Jones, 2009;Weisner, 1996).Parallel improvements take place in mentalizing (the ability to understand and represent mental states) and moral reasoning, as children become able to consider multiple perspectives and conflicting goals (Jambon & Smetana, 2014;Lagattuta, Sayfan, & Blattman, 2009).
In traditional societies, older relatives-especially parents and grandparents-are the main sources of knowledge for juveniles, supplemented by peers and-where availableprofessional teachers.Storytelling-both fictional and based in real events-is a powerful technology for transmitting knowledge about foraging and social skills, avoidance of dangers, topography, wayfinding, and social roles and norms (Scalise Sugiyama, 2011).Storytelling mimics the format of episodic memories, providing the child with a rich source of indirect experience (Scalise Sugiyama, 2011).Intriguingly, episodic memory shows dramatic and sustained improvements across middle childhood (Ghetti & Bunge, 2012).
Children, however, are not just learning and playing.Cross-culturally, middle childhood is the time when children are expected to start providing active help in domestic tasks-such as taking care of younger siblings, collecting food and water, tending animals, helping adults with food preparation, and so forth (Bogin, 1997;Lancy & Grove, 2011;Scalise Sugiyama, 2011;Weisner, 1996).In favorable ecologies, juveniles can make a substantial contribution to family subsistence (Kramer, 2011).Thanks to marked increases in spatial cognition (reflected in the emerging ability to understand maps) and navigational skills, children become able to memorize complex routes and find their way without adult supervision (Bjorklund, 2011;Piccardi, Leonzi, D'Amico, Marano, & Guariglia, 2014).The important role of juveniles in collecting and preparing food may explain why the emotion of disgust does not fully develop until middle childhood (Rozin, 1990a).
The transition to middle childhood is typically associated with a strong separation in gender roles; even in societies where tasks are not rigidly assigned by sex, middle childhood is marked by a peak in spontaneous sex segregation and in the frequency of sexually differentiated play (Del Giudice et al., 2009).At a broader social level, cross-cultural evidence shows that juveniles start "getting noticed" by adults-that is, they begin to be viewed as persons with their own individuality, personality, and social responsibility (Lancy & Grove, 2011).
In summary, the life stage of juvenility/middle childhood has two major interlocking functions: social learning and social integration in a system of roles, norms, activities, and shared knowledge.While children are still receiving sustained investment from parents and other relatives-in the form of food, protection, knowledge, and so forth-they also start to actively contribute to their family economy.By providing resources and sharing the burden of childcare, juveniles may significantly increase their parents' reproductive potential.The dual nature of juveniles as both receivers and providers explains many psychological features of middle childhood, and has likely played a major role in the evolution of human life history (Kramer, 2011).

Adrenarche
The transition to middle childhood is coordinated by a remarkable endocrinological event: the awakening of the adrenal glands, or adrenarche (Auchus & Rainey, 2004;Hochberg, 2008).Starting at about 6-8 years-with much individual variation and only minor differences between males and females-adrenal glands begin to secrete increasing amounts of androgens (Figure 1), mainly dehydroepiandrosterone (DHEA) and its sulfate form (DHEAS).While adrenal androgens have only minor effects on physical development, they have powerful effects on brain functioning.DHEAS promotes neurogenesis and modulates GABA and glutamate receptors; moreover, DHEA can directly act on androgen and estrogen receptors.Even more importantly, adrenal androgens can be converted to estrogen and/or testosterone in the brain (Campbell, 2006;Del Giudice et al., 2009).As sex hormones, adrenal androgens play a twofold role.On the one hand, they activate sexually differentiated brain pathways that had been previously organized by the hormonal surges of prenatal development and infancy (Figure 1).On the other hand, they further organize brain development along sexually differentiated trajectories (Del Giudice et al., 2009).
Adrenal androgens likely provide a major impulse for many of the psychological changes of middle childhood (Campbell, 2006(Campbell, , 2011;;Del Giudice et al., 2009), including the emergence and intensification of sex differences across domains (Table 1).Since the age of adrenarche is strongly correlated with that of gonadarche (the awakening of the testes/ovaries that marks the beginning of puberty; Hochberg, 2008), human development shows a peculiar pattern in which sexually differentiated brain pathways are activated several years before the development of secondary sexual characters.This developmental pattern (shared by chimpanzees and, to a lesser extent, gorillas; Bernstein, Sterner, & Wildman, 2012) results in a temporary decoupling between physical and behavioral development, consistent with the idea of middle childhood as a sexually differentiated phase of social learning and experimentation (Geary, 2010).Moreover, adrenal androgens promote extended brain plasticity through synaptogenesis, and may play an important role in shifting the allocation of the body's energetic resources away from brain development and toward the accumulation of muscle and fat in preparation for puberty (Campbell, 2006(Campbell, , 2011; see also Kuzawa et al., in press).

THE TRANSITION TO MIDDLE CHILDHOOD AS A DEVELOPMENTAL SWITCH POINT
The evolutionary model of middle childhood sketched in the previous section can be enriched and extended by considering the role of adrenarche as a developmental switch (Del Giudice et al., 2009).A developmental switch (West-Eberhard, 2003) is a regulatory mechanism that activates at a specific point in development, collects input from the external environment and/or the state of the organism, and shifts the individual along alternative pathways-ultimately resulting in the development of alternative phenotypes (morphological, physiological, and/or behavioral traits of an organism).For example, a switch may regulate the development of aggressive behavior so that safe conditions entrain the development or low aggression levels, whereas threatening environments trigger high aggression levels.Developmental switches enable adaptive plasticity-the ability of an organism to adjust its phenotype to match the local environment in a way that promotes biological fitness (West-Eberhard, 2003).In other words, plastic organisms track the state of the environment-usually through indirect cues-and use this information to develop alternative phenotypes that tend to promote survival and/or reproduction under different conditions.
Figure 2. The concept of a developmental switch.A regulatory mechanism (which may operate through hormonal signals) integrates current and past information from the environment with the individual's genotype.As a result, the individual's developmental trajectory is shifted along alternative pathways-here, A and B-depending on whether a threshold is reached within the mechanism.The location of the threshold, the intensity of the signal, and the timing of the switch point all depend on the joint action of the current state of the environment, the embodied effect of past environmental conditions, and individual variation in the genes involved in the regulatory mechanism.Each alternative pathway involves the modular expression of a set of specific genes, in addition to the shared genes expressed in the new developmental stage.Note that a developmental switch may integrate multiple sources of input from the environment, and/or produce graded phenotypes rather than discrete alternatives such as A and B.
The logic of developmental switches is illustrated in Figure 2.An important feature of developmental switches is that they work in a modular fashion.Activation of a switch leads to the coordinated expression of a number of different genes-both those involved in the regulatory mechanism itself and those involved in the production of the new phenotype.Moreover, alternative phenotypes (A and B in Figure 2) involve the expression of modular "packages" of genes specific to each phenotype.Another key aspect of developmental switches is that they integrate variation in the environment with individual differences in the genes that regulate the switch.For example, different individuals may have genetically different thresholds for switching between aggressive and non-aggressive phenotypes.Finally, the embodied effects of past experiences and conditions (e.g., an individual's previous exposure to stress or nutritional conditions early in life) may also modulate the functioning of the switch, allowing the organism to integrate information over time and across different life stages (Ellis, 2013).The effects of past experience on developmental switches may often be mediated by epigenetic mechanisms (see Meaney, 2010).
The concept of a developmental switch point resembles that of a sensitive period, in that the organism is maximally responsive to some environmental input.But there is a crucial difference: since genetic and environmental inputs converge in the regulatory mechanism, a developmental switch amplifies both environmental and genetic effects on the phenotype (West-Eberhard, 2003).Indeed, the activation of a developmental switch exposes many new potential sources of genetic variation, including the genes involved in the regulatory mechanism and in the expression of the new phenotypes (Figure 2).

A Switch Point in Life History Development
The role of adrenarche as a developmental switch is not limited to a single trait; in fact, the transition to middle childhood (or juvenile transition; Del Giudice et al., 2009) encompasses all the major domains of behavior-from learning and self-regulation to attachment and sexuality (Table 1).In a series of papers (Del Giudice et al., 2009, 2012;Del Giudice & Belsky, 2011) my colleagues and I argued that the transition to middle childhood is a switch point in the development of life history strategies.Life history strategies are coordinate suites of morphological, physiological, and behavioral traits that determine how organisms allocate their resources to key biological activities such as growth, reproduction, mating, and parenting.At level of behavior, individual differences in life history strategy are reflected in patterns of selfregulation, aggression, cooperation and prosociality, attachment, sexuality, and so forth (Del Giudice et al., 2009;Del Giudice & Belsky, 2011;Del Giudice, Ellis, & Shirtcliff, 2011;Ellis, Figueredo, Brumbach, & Schlomer, 2009;Kaplan & Gangestad, 2005).While life history strategies are partly heritable, they also show a degree of plasticity in response to the quality of the environment, including the level of danger and unpredictability (embodied in the experience of early stress) and the availability of adequate nutritional resources.In a nutshell, dangerous and unpredictable environments tend to favor "fast" strategies characterized by early reproduction, sexual promiscuity, relationship instability, impulsivity, risk-taking, aggression, and exploitative tendencies, whereas safe and predictable environment tend to entrain "slow" strategies characterized by late reproduction, stable relationships, high self-control, risk aversion, and prosociality.Slow strategies are also favored by nutritional scarcity in absence of high levels of danger (Ellis et al., 2009).
Our argument is that adrenarche coordinates the expression of individual differences in life history strategy, by integrating individual genetic variation with information about the child's social and physical environment collected throughout infancy and early childhood (Belsky, Steinberg, & Draper, 1991).The stress response system plays a major role in gathering and storing information about environmental safety, predictability, and resource availability; adrenarche contributes to translate that information into adaptive, sexually differentiated patterns of behavior (Del Giudice et al., 2011).Consistent with this view, both early relational stress and early nutrition modulate the timing of adrenarche (Ellis & Essex, 2007;Hochberg, 2008).It is no coincidence that the first sexual and romantic attractions typically develop in middle childhood, in tandem with the intensification of sexual play (Bancroft, 2003;Herdt & McClintock, 2000).By interacting with peers and adults, juveniles receive considerable feedback about the effectiveness of their nascent behavioral strategies.The information collected during middle childhood feeds into the next developmental switch point, that of gonadarche (Ellis, 2013); the transition to adolescence offers a major opportunity to adjust or revise one's initial strategy before attaining sexual and reproductive maturity (Del Giudice & Belsky, 2011).
The role of adrenarche as a switch point in life history development adds another level of complexity to the biological profile of juvenility.Figure 3 outlines an integrated evolutionarydevelopmental model that brings together the various strands of theory and evidence reviewed in this paper.

Insight #1: Social Integration and Social Competition are Complementary Functions of Middle Childhood
Evolutionary accounts of middle childhood typically focus on learning, helping, and other forms of social integration.A life history approach emphasizes the need to consider social competition as a crucial, complementary function of human juvenility.In the peer group, children compete for vital social resources-status, reputation, allies, and friends.While learning and play are relatively risk-free, they are not without consequences.The social position achieved in middle childhood is a springboard for adolescence and adulthood; popularity and centrality within the peer network put a child at a considerable advantage, with potentially long-term effects on his/her reproductive success (Del Giudice et al., 2009).
Physical and relational aggression are obvious tactics for gaining influence, but social competition also occurs through prosocial behaviors such as forming alliances, doing favors, displaying valuable skills, and so forth.Indeed, managing the balance between prosocial and coercive tactics is an important aspect of social skills development (Hawley, 2014).More broadly, competition shapes many aspects of cognitive and behavioral development in middle childhood; for example, increased pragmatic abilities allow children to engage in gossiping, joking, teasing, and verbal duels-all forms of social competition mediated by language (Locke & Bogin, 2006).Intensifying social competition also contributes to explain the early peak of psychopathology onset observed in middle childhood, characterized by increasing rates of externalizing disorders (e.g., conduct disorder), anxiety disorders (including social phobia), and attention deficit-hyperactivity disorder (ADHD; Del Giudice et al., 2009).

Insight #2: Sexual Selection Contributes to the Emergence and Intensification of Sex Differences in Middle Childhood
By determining children's initial place in social networks and hierarchies, competition in middle childhood indirectly affects their future ability to attract sexual and romantic partners.In other words, middle childhood is a likely target for sexual selection-that is, natural selection arising from the processes of mate choice and mating competition.My colleagues and I (Del Giudice et al., 2009) argued that sexual selection is an important reason for the emergence and intensification of sex differences in middle childhood.In particular, sex differences in physical aggression show a marked increase, in tandem with sex differences in muscularity and play fighting.At the same time, attachment styles begin to diverge between males and females, with insecurely attached boys becoming higher in avoidance and insecure girls becoming higher in preoccupation/ambivalence (Del Giudice, 2009;Del Giudice & Belsky, 2010).Different attachment styles are conducive to different social strategies, and may be adaptive in regulating children's nascent relationships with peers (Del Giudice, 2009).Sexual selection also has indirect implications for the development of psychopathology; for example, marked sex differences in the prevalence of conduct disorders become apparent at the beginning of middle childhood (Del Giudice et al., 2009).

Insight #3: In Middle Childhood, Heightened Sensitivity to the Environment Goes Hand in Hand with the Expression of New Genetic Factors
When an organism goes through a developmental switch point, inputs from the environment combine with the individual's genotype to determine the resulting phenotype.For example, when adrenal androgens begin to rise during the transition to middle childhood, they activate a multiplicity of hormone-sensitive brain pathways that have remained dormant since infancy.In doing so, they release a certain amount of previously "hidden" genetic variation (Del Giudice et al., 2009).Thus, middle childhood should be characterized by a mixture of heightened sensitivity to the environment (possibly mediated by newly activated epigenetic mechanisms; Meaney, 2010) and expression of new genetic factors.
Evidence of increased sensitivity to the environment in middle childhood is not hard to find.Two intriguing and little known examples concern the development of food preferences and erotic fetishes.In cultures where chili pepper is an essential part of the diet, children tend to dislike spicy food until middle childhood, then show a rapid increase in preference for the flavor of chili as a result of social learning (Rozin, 1990b).Fetishistic attractions also tend to form in middle childhood, with the onset of pleasurable sensations toward the fetish object (e.g., rubber, shoes) that later become fully eroticized (Lawrence, 2009).The onset of fetishistic attractions is part of a generalized awakening of sexuality in middle childhood (Table 1), and illustrates the potential for rapid plasticity with very long-lasting outcomes.Enhanced sensitivity to the environment extends beyond individual learning to the acquisition of social norms: for example, cross-cultural differences in prosocial behavior are absent in young children but emerge with clarity during middle childhood (House et al., 2013).
On the genetic side of the equation, general intelligence and language skills show a marked increase in heritability from early to middle childhood.In both cases, there is evidence that new genetic factors come into play around age 7 (Davis, Haworth, & Plomin, 2009;Hayiou-Thomas, Dale, & Plomin, 2012).Studies of prosociality and aggression show the same pattern, with new genetic influences on behavior emerging during the transition to middle childhood (Knafo & Plomin, 2006;van Beijsterveldt, Bartels, Hudziak, & Boomsma, 2003).These genetic findings dovetail with converging evidence that individual changes in aggression levels are especially frequent during the transition to juvenility (Del Giudice et al., 2009).

CONCLUSION
We cannot make sense of human development without a deep understanding of middle childhood and its many apparent paradoxes.An evolutionary-developmental approach illuminates the complexity of this life stage, and shows how different levels of analysis-from genes to society-can be tied together in a coherent synthesis.This emerging view of middle childhood should help developmental scientists appreciate its centrality in the human life history, and stimulate a novel ideas for research and intervention.The study of middle childhood may be finally ready to come of age.

Figure 3 .
Figure 3.An integrated evolutionary-developmental model of middle childhood.

Table 1 .
Development in middle childhood.See the main text for supporting references.