Human Evolutionary Biology

Evolution of Human Growth 391 takes years to complete. Even when marriage takes development, and economic productivity, the 13-year-old place before or near the time of menarche it may take boy is still more a juvenile than an adult. Anthropologists years until the bride makes a complete transference from working in many diverse cultural settings report that her natal family to live with her husband. A detailed few women (and more important from a cross-cultural description of the variety and significance of human rites perspective, few prospective in-laws) view the teenage of passage is beyond the scope of this chapter. Interested boy as a biologically, economically, and socially viable readers may consult the extensive ethnographic litera- husband and father. ture (e.g., Schlegel and Barry, 1991; Schlegel, 1995). The delay between sperm production and repro- The physiological, anatomical, growth, developmen- ductive maturity is not wasted time in either a biological tal, maturational, and behavioral differences between or social sense. The obvious and the subtle psycho- people and chimpanzees lead to the conclusion that physiological effects of testosterone and other androgen chimpanzees do not have adolescence. Some time after hormones that are released after gonadal maturation the divergence from their common ancestor, chimpan- may “prime” boys to be receptive to their future roles zees and humans evolved different life history patterns as men. Alternatively, it is possible that physical for sexual development. Physiologically, chimpanzee changes provoked by the endocrines, such as deepening femalesseemtohaveevolvedestrusswellingassomething of the voice and appearance of pubic hair, provide a new, because gibbons and orangutans do not have them social stimulus toward adult behaviors. The following (de Waal, 2001). Human females evolved permanent is an example of the interaction between biology and breasts, the adolescent growth spurt, and menarche behavior. In 2001, a research team measured and inter- followed by hidden ovulation as a unique set of traits. viewed Portuguese and Cape Verde boys, ages 10–15 years old, living near Lisbon, Portugal (Bogin and Varela Silva, 2003). We assessed pubic hair development WHY DO BOYS HAVE ADOLESCENCE? and voice “breaking.” The older, more mature boys told us that in school they “speak and act like men” because Natural and sexual selection for adolescence applies they have pubic hair, but at home they speak like boys to to both girls and boys. The forces of natural selection show respect for their parents and older siblings. Such are the same for both sexes but the particulars of sexual are the social pressures of male adolescence! selection are different. The adolescent development of Whether the influences are primarily physical or boys is quite distinct from that of girls. Boys become social, early in adolescence, sociosexual feelings fertile well before they assume the size and the physical including guilt, anxiety, pleasure, and pride intensify. characteristics of men. Analysis of urine samples from At the same time, adolescent boys become more inter- boys 11–16 years old show that they begin producing ested in adult activities, adjust their attitude to paren- sperm at a median age of 13.4 years (Muller et al., 1989). tal figures, and think and act more independently. In Yet cross-cultural evidence indicates that few boys short, they begin to behave like men. successfully father children until they are into their However – and this is where the survival advantage third decade of life. In the United States, for example, may lie – they still look like boys. One might say that a only 3.09% of live-born infants in 1990 were fathered by healthy, well-nourished 13.5-year-old human male, at a men under 20 years of age. In Portugal, for years 1990, median height of 160 cm (62 inches) “pretends” to be 1994, and 1999, the percentage of fathers under 20 years more childlike than he really is. Because their adolescent of age was always below 3% (Instituto Nacional de growth spurt occurs late in sexual development, young Estatı ´stica, 1999). In 2001, Portugal stopped presenting males can practice behaving like adults before they are results concerning the percentage of fathers below actually perceived as adults. The sociosexual antics of 20 because there were too few of them (Instituto Nacio- young adolescent boys are often considered to be more nal de Estatı ´stica, 2001). Among the traditional Kikuyu humorous than serious. Yet, they provide the experience of East Africa, men do not marry and become fathers to fine-tune their sexual and social roles before their until about age 25 years, although they become sexually lives or those of their offspring depend on them. For active after their circumcision rite at around age 18 example, competition between men for women favors (Worthman, 1993). the older, more experienced man. Because such compe- The explanation for the lag between sperm produc- tition may be fatal, the childlike appearance of the tion and fatherhood is not likely to be a simple one of immature but hormonally and socially primed adoles- sperm performance, such as not having the endurance to cent male may be life-saving as well as educational. swim to an egg cell in the woman’s fallopian tubes. More Adolescent boys do not begin to look like men until likely is the fact that the average boy of 13.4 years is only their spurt in muscle development, which takes place beginning his adolescent growth spurt (Figure 22.5). at about age 17 years. Prior to this, adolescent boys are Growth researchers have documented that in terms of fertile but still look like juveniles. This is a type of physical appearance, physiological status, psychosocial reverse sexual selection when compared with girls.

392 Barry Bogin Adolescent girls learn and practice adult behaviors dated at between 42 000 and 37 000 years BP. Using when they are infertile but look like women. modern human development reference data, Thompson Language development in adolescent boys is another and Nelson (1997) estimate that Le Moustier 1 has a influence on social and sexual success. Indeed, vocal and dental age of 15.5 years and a stature age of 11–12 years verbal performance is an essential aspect of sexual/ based on the length of his femur. The dental age and the mating behavior in human beings. Adolescent speech stature age are in poor agreement, and indicate that becomes more complex in vocabulary, including slang, Le Moustier 1 may not have followed a human pattern more rapid in speaking rate, and assumes more rhyth- of adolescent growth (Bogin, 1999). Alternatively, Nelson mic fluency (Locke and Bogin, 2006). Boys and men in and Thompson (2002) suggest that Neanderthals, both many societies engage in vocal and verbal duels, use the young and adults, may have reduced limb growth of riddles, and other complex patterns of language. due to cold adaptation (Allen’s rule). There is also the These duels develop sequentially during adolescence. suggestion that Neanderthals of Western Europe Those who can handle this complex vocal and verbal suffered iodine deficiency (Dobson, 1998; Bogin and material are considered intelligent by members of the Rios, 2003). Cold adaptation and/or nutrient deficiency social group. Anthropologists find that most oral soci- may obscure evidence for an adolescent spurt in limb- eties, and many literate societies, promote verbal skill for length growth. attention, power, prestige, and success (Locke and Given the uncertainties of the evidence derived Bogin, 2006). Vocal and verbal dueling is almost always from H. antecessor and the Neanderthals, it is quite performed in front of an audience and is often used to likely adolescence is no older than the appearance of attract mating opportunities. archaic H. sapiens in Africa at about 125 000 years ago – Girls and women also engage in vocal and verbal possibly even more recently at about 60 000 years ago. contests, but less often in highly public displays. Girls With the evolution of adolescence the modern pattern and younger women focus relatively more on social of human life history was established. With the add- talking, including gossip, deceiving, mollifying, negotiat- ition of adolescence to human life history sociocultural ing, and persuading (Locke and Bogin, 2006). As for boys, behaviors and forms, such as marriage and the family, this use of language for girls does not reach adult levels of could come into being. When all of these came to exist complexity and effectiveness until the later teenage years. is not known. From the ancient roots for the evolution Human language, in this sense, conforms closely to of childhood to the more recent emergence of adoles- Darwin’sexamplesofsexualselectionfor“...organs cence our hominin ancestors were transformed. Only for producing vocal or instrumental music . . .” which with a life history including both childhood and adoles- influence opportunities for mating. cence could the human species, in most essential bio- cultural aspects, have evolved. WHEN DID ADOLESCENCE EVOLVE? DISCUSSION POINTS In contrast to the relatively ancient evolution of homi- nin childhood, an adolescent life stage may be relatively 29. How does the pattern of human brain growth recent. Based on skeletal and dental development there during infancy and childhood help to understand is little or no evidence of human adolescence in Homo the biological and behavioral development of erectus or any earlier hominin (Dean et al., 2001; Anto ´n, human beings? 2003). Moreover, the fossil evidence indicates that the 30. In what ways does human parental investment adolescent growth stage, and the adolescent growth in offspring differ from that of other primates, spurt, evolved only in the lineage leading directly to especially the great apes? What value does human modern Homo sapiens. co-operative care of infants and children have for There is a possibility that adolescence may first human reproduction and infant-child survival? appear in Homo antesesor, a hominin from Spain that 31. Boys and girls proceed through puberty and ado- is about 800 000 years old (Bermudez de Castro et al., lescence in different ways regarding the develop- 1999). The evidence for this is based on patterns of ment of sexual characters and adult behaviors. tooth formation, which while not directly linked to What may be the biological and social value of the the presence of an adolescent growth spurt is suggest- two distinct paths of development? ive. Possible descendants of H. antecessor are the Nean- 32. Bogin proposes that human childhood is funda- derthals. There is one fossil of a Neanderthal youth in mentally a feeding and reproductive adaptation to which the associated dental and skeletal remains needed assist the mother’s reproductive success. Find other to assess adolescent growth are preserved. It is called explanations for the value of human childhood and Le Moustier 1, most likely the remains of a male, and it discuss the evidence in favor and against Bogin’s was found in 1908 in Western France. The specimen is hypothesis.

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23 Variation in Human Growth Patterns due to Environmental Factors Stanley J. Ulijaszek INTRODUCTION low socioeconomic status include single parenthood, overcrowding, low disposable income, paternal ill health, The human growth pattern is characterized by rapid dependence on social welfare, and parental abuse of growth in infancy, followed by an extensive period of alcohol and drugs (Schell, 1991b). childhood, and a relatively intense adolescent spurt In both developed and developing worlds there are (see Chapter 22 of this volume). The extended period of similar associations between stature and socioeco- biological immaturity relative to other mammalian nomic status, height correlating positively with wealth species is associated with high environmental sensitivity (Bogin, 1999). Weight, however, does not always relate and growth plasticity (Johnston, 1998), illustrated by the positively with wealth, overweight and obesity being processes of stunting and wasting in response to poor the provenance of low socioeconomic status in most nutrition and infection (Waterlow, 1988) and of catch-up industrialized nations (Sobal, 1991), and becoming growth during environmental improvements following increasingly so among emerging nations undergoing episodes of environmental stress (Prader et al., 1963). the health transition (Xu et al., 2005). Growth stunting Known environmental factors that influence in association with overweight was first identified in growth, body size, and body composition of children Peruvian children (Trowbridge et al., 1987) and more postnatally include nutrition (Barclay and Weaver, 2006), recently in children aged between three and nine years infection (Bhanet al., 2001), interactions between the two in four nations viewed to be undergoing nutrition tran- (Ruel, 2001), psychosocial stress (Powell et al., 1967), sition: Russia, Brazil, Republic of South Africa, and food contaminants (Gong et al., 2004), pollution (Schell, China (Popkin et al., 1996). 1991a), and hypoxia (Frisancho, 1977). Most of these Early life experiences involving environmental stress, factors are conditioned by poverty and socioeconomic intrauterine growth retardation, poor growth in early status (Martorell et al., 1988). They are also conditioned childhood, and subsequent catch-up growth can impact historically, culturally, and politically (Ulijaszek, 2006), on growth, body composition, and health outcomes later interacting with each other, but also with individual in life (Henry and Ulijaszek, 1996). Catch-up growth is genotypes in the production of growth, body size, and an acceleration of child growth-rate following either body composition. medical or environmental intervention or environmental Diet,nutrition,disease,hypoxia,pollution,contamin- improvement, such that body size approaches or reaches ation,behavioraltoxicants,deprivation,andpsychosocial normality, as defined by appropriate growth references stress can be clustered as proximate environmental (Prader et al., 1963). It can take place at all stages of child agents that can influence growth (Figure 23.1). They vary growth, including adolescence (Golden, 1994). However, in importance according to circumstance and the age and when the factors responsible for growth faltering or stage in infancy, childhood, and adolescence. Culture, failure are ubiquitous, this process is constrained and society, behavior, socioeconomic status, poverty, and individuals fail to reach their potential for maximal political economy can also be clustered as structurally growth and optimal body size (Martorell et al., 1988). powerful but distal agents in the production of Human growth and body size responds with sensi- growth and body size outcomes, at all ages and stages tivity to environmental quality. The term “secular of childhood and adolescence. This latter cluster is trend” is used to describe marked changes in growth conditioned historically. In the developing world, the and development of successive generations of human risks associated with poverty include low income, poor populations living in the same territories. Positive food security, inadequate health infrastructure, and secular trends in increased stature and weight, and environmental hazards. In the industrialized world, the earlier timing of the adolescent growth spurt, have risks for impaired child growth that are associated with been documented among European, European-origin, Human Evolutionary Biology, ed. Michael P. Muehlenbein. Published by Cambridge University Press. # Cambridge University Press 2010. 396

Variation in Human Growth Patterns due to Environmental Factors 397 Biological 23.1. Proximate and distal agents influencing child inheritance Genetics growth. Adapted from Ulijaszek (2006). Genotype GROWTH STATUS, GROWTH BODY COMPOSITION INCREMENT Diet, nutrition Disease BOX 1 Physical environment Hypoxia, pollution, Deprivation, contaminants, psychosocial toxicants stress BOX 2 Culture Behavior Socioeconomic status, poverty Political economy Environment History and Asian populations (Ulijaszek, 2001). Negative secu- While adolescent growth may be under stronger genetic lar trends have been identified among populations in control than growth in childhood (Hauspie and Susanne, Africa (Henneberg and van den Berg, 1990), Papua 1998), environment can influence both of these meas- New Guinea (Ulijaszek, 1993), and Central and Latin ures of adolescent growth and maturation, but to a America (Bogin, 1999). Positive secular trends have lesser extent than genetics (Bogin, 1999). This chapter largely been attributed to improved social, political, describes important environmental influences on the nutritional, and health conditions, while negative secu- growth of children from birth to adulthood, focusing lar trends are often seen as outcomes of environmen- primarily on measures of height and weight, the primary tal, social, or political deterioration (Bogin, 1999). The anthropometric measures used in child health surveil- best example of a positive secular trend is that of lance, screening, and monitoring. the Netherlands (Van Wieringen, 1986), where mean stature has increased from 165cm in 1860 to 181cm in 1990, and 184cm in 1997 (Cole, 2000). In largest INFANCY AND EARLY CHILDHOOD part, this has been attributed to improved nutrition (in terms of both quantity and quality) that came with Human infancy is the period when the mother provides economic improvements across the twentieth century, all or some nourishment to her offspring by way of as well as the control of, and decline in, infectious lactation (Bogin, 1998). Human infancy ends when the disease morbidity (Van Wieringen, 1986). However, child is weaned from the breast, which in preindustria- although most populations in Europe have experi- lized societies usually continues to beyond two years of enced a positive secular trend across the twentieth age (Sellen, 2001). Exclusive breast-feeding usually century, there is evidence that some experienced a provides adequate nutrition to support good child negative secular trend in the late eighteenth century, growth until 6 months of age (Butte et al., 2002), and due largely to poor harvests, high grain prices, and the dietary supplementation of the infant often begins poor infant and child nutrition that followed (Komlos, around or before that time (Sellen, 2001). Of the various 1985; Floud et al., 1990). environmental factors influencing growth of children The vast majority of research on environmental in developing countries, diet, nutrition, and infection influences on human growth has focussed on birth- are particularly powerful in infancy and childhood. weight (Wharton, 1989), infancy and infant feeding While infants are breast-fed, they are usually protected (Frongillo, 2001), and early childhood, up to the age from the broad disease environment nutritionally, of five years (Waterlow, 1988). Later childhood is taken immunologically (Ulijaszek, 1990), and behaviorally. to be from five years of age until onset of puberty. In Where on-demand breast-feeding is usual, infants are contrast, the environmental influences on preadoles- often kept close to their mother and are buffered from cent growth have attracted relatively little attention contact with objects or foods contaminated with patho- (Stoltzfus, 2001). Growth and body composition in gens. In developing countries, interactions between adolescence has been researched to a greater extent than undernutrition and infection usually lead to growth in preadolescence, but to a much smaller extent than faltering from about six months of age (Waterlow, 1988; among in children of preschool age (Stoltzfus, 2001). Lunn 2000).

398 Stanley J. Ulijaszek Interactions between undernutrition Inadequate dietary intake and infection Undernutrition-infection interactions can be initiated in two ways (Figure 23.2). The first involves poor nutri- tional status leading to impaired immunocompetence Anorexia Weight loss and reduced resistance to infection, while the second Malabsorption Growth faltering Metabolic change Immune function involves an exposure to infectious disease which can lead Mucosal damage to appetite loss and anorexia, malabsorption, elevated basal metabolic rate, as well as gut mucosal damage, and protein catabolism in order to fuel acute phase Disease: incidence, protein production. Delayed supplementation may lead duration, severity to growth faltering and undernutrition, leaving the 23.2. Nutrition–infection interactions in early childhood. infant more suspectible to infectious diseases, while earlier dietary supplementation may provide adequate tions fall into categories (1) and (2), as do the more nutrient intake, but concomitantly introduce the child specific diseases pneumonia, measles, malaria, and typa- to diarrheal agents. nosomiasis (Ulijaszek, 2006). The nutritional deficiencies Once started, the interactions between these two that inhibit immune system include energy, protein, major environmental stressors become increasingly vitamin A, pyridoxine, iron, and zinc (Tomkins, 2002). complex, with the nature of the disease ecology influ- However, in the absence of overt infection, deficiencies encing the duration and severity of infection, and of zinc and iron have only a small effect on linear adaptive immunity, its effect on subsequent disease growth, while vitamin A is unlikely to have any important experience, and the extent, if any, of anorexia, fever, effect (Bhandari et al., 2001). Diseases known to inhibit and malabsorption during infectious episodes, which immune system function include AIDS, measles, leprosy, impact on nutritional status. Specific nutritional defi- and malaria. The ways in which growth faltering is asso- ciencies can subsequently influence immune status and ciated with the interaction between undernutrition and responsiveness, as well as adaptive immunity. In add- infection are thus manifold, and varies with specific local ition, cultural factors and poverty can influence patterns disease and nutritional ecologies. Gut damage due to of disease management and sickness behavior, which infection also varies across ecologies (Lunn, 2000). While can in turn affect the incidence, severity and duration the growth outcomes of undernutrition – infection inter- of infection, and their effects on nutritional status. actions may look similar across the developing world, Infections that influence nutritional status and they are in fact different in specific causation. linear growth are either acute and invasive, provoking a Growth faltering due to undernutrition and infection systemic response (such asdysentery and pneumonia), or may continue for months or years, depending on the chronic,affectingthehostoverasustainedperiod(includ- severity of the disease environment, and the abundance ing gut helminth infections). Infections can diminish and quality of the nutritional environment. In most linear growth by affecting nutritional status, by way populations, the process of growth faltering is complete of decreased food intake, impaired nutrient absorption, by the age of two years, after which the shorter, stunted direct nutrient losses, increased metabolic requirements, child may follow a parallel trajectory to the Western catabolic losses of nutrients, and/or impaired transport growth references (Eveleth and Tanner, 1990). This of nutrients to target tissues. In addition, induction period of departure from the growth references derived ofthe acute phase response and host elaboration ofproin- from measures of Western populations can be regarded flammatory cytokines (Friedman et al., 2003) may con- in one sense as an accommodation to the disease and tribute to growth faltering because they directly inhibit nutritional environment. However, this accommodation the process of bone remodeling that is needed for long is usually associated with high rates of mortality and bone growth (Stephensen, 1999). morbidity, reduced energy for play, and compromised In Table 23.1, the nutrition – infection processes asso- intellectual development, and cannot therefore be ciated with growth faltering of children are reduced to regarded as desirable. four types of effect. These are: (1) the diseases and disease categories that are known to affect nutritional status; (2) Poverty the diseases and disease categories known to be influ- enced by nutritional status; (3) the nutritional deficien- Childhood undernutrition and infection are associated cies that inhibit immune system function; and (4) the with poverty. Farmer (2004) has described the exten- diseases known to inhibit immune system function. sive ways in which poverty and social inequality are The general disease categories of diarrhea, intestinal embodied as differential risks for infection with HIV parasitic infestation, and upper respiratory tract infec- and tuberculosis in developing countries, while Walls

Variation in Human Growth Patterns due to Environmental Factors 399 TABLE 23.1. Nutrition–infection processes associated with growth faltering of children. Diseases and disease categories known to affect nutritional status: Diarrhea; upper respiratory tract infections; pneumonia; measles; malaria; intestinal parasites; AIDS Diseases and disease categories known to be influenced by nutritional status: Diarrhea; cholera; leprosy; pertussis; upper respiratory tract infections; pneumonia; measles; malaria; intestinal parasites; trypanosomiasis Nutritional deficiencies that inhibit immune system function: Energy; protein; vitamin A; pyridoxine; iron; zinc Diseases known to inhibit immune system function: AIDS; measles; leprosy; malaria and Shingadia (2004) identified overcrowding, pov- Mexico (Mendez-Albores et al., 2004), high levels of afla- erty, and the HIV epidemic as contributing to the toxin often remain in the food (Plasencia, 2004). resurgence of tuberculosis globally. Bates et al. (2004) Levels of pollutants that human populations are identified poverty as a key factor operating at individ- exposed to vary markedly, depending partly on the degree ual, household, and community levels in increasing of, and proximity to, industrialization (Schell, 1991b). vulnerability to malaria, tuberculosis, and HIV infec- Generalized air pollution has been identified as an envir- tion. Poverty also underpins the nutrition and infection onmental risk factor for poor growth of children in com- interactions that impact on child growth. Tuberculosis, munities in Silesia and Belgium (Schell, 1991b), pollution associated with household crowding and poverty, may from hazardous waste sites having similar effects (Paigen not be directly associated with growth faltering, but etal.,1987).Exposuretopolychlorinatedbiphenyls(PCB) it is associated with nutritional status. Vitamin A can at very high doses can affect child growth, while exposure cause growth delay when combined with infection. to lead can affect growth at moderate to low levels. The Children born to HIV-infected women who are vitamin risk of environmental pollutant exposure to child growth A deficient during pregnancy are more likely to experi- is increasing as developing countries industrialize. China ence growth failure (Semba et al., 1997). Furthe- has seen pronounced increases in anthropogenic lead rmore, HIV infection, malaria, and diarrheal disease level during the past two decades (Huh and Chen, 1999), adversely affect growth of preschool-age children, and while in Taiwan, high serum lead levels are associated are associated with increased prevalence of vitamin with lead exposure from drinking water sources and A deficiency (Villamor et al., 2002). residential proximity to factories, as well as occupational lead exposure (Chu et al., 1998). Environmental contamination Psychological stress Exposure to aflatoxin contamination, particularly at the time of weaning, has been shown to inhibit early child- The idea that psychological stress causes growth faltering hood growth in West Africa (Gong et al., 2003). Aflatoxins in some children was first put forward by Widdowson are mold metabolites produced by toxigenic strains of (1951), who published evidence that the presence of a Aspergillus species, a number of which are hepatotoxic sadistic schoolteacher caused child growth in an orphan- and immunotoxic. Primary commodities susceptible to age to falter, despite a concurrent increase in the amount aflatoxin contamination include corn, peanuts, cotton- of food eaten. Furthermore, family conflict has been seed, and animal-derived foods such as milk when the shown to be associated with short stature in childhood animal is fed aflatoxin-contaminated feed. Although as well as short adult height in the British 1958 cohort excessive aflatoxin contamination is not global, signifi- study (Montgomery et al., 1997). The dominant mechan- cant dietary contamination has been demonstrated in ism by which short stature emerges is nutritional, by way manypartsofWestAfrica,Asia,andSouthAmerica of appetite loss and anorexia (Skuse, 1998). (Ulijaszek, 2006). Risks associated with aflatoxin- contaminated foods can be reduced through the use of Altitude multiple processing and decontamination procedures, including physical cleaning and separation procedures Relative to lowland populations, humans living at high (Park, 2002), but not with simple cooking procedures altitude are more likely to be born at low birthweight and available to poor mothers. Although aflatoxins are par- undergo postnatal growth which is slow and prolonged tially destroyed during nixtamalization, the alkaline (Frisancho, 1993). The poor growth in infancy and early cooking procedure employed to prepare tortillas in childhood among some high altitude populations is

400 Stanley J. Ulijaszek associated with poverty, poor food security and exposure adiposity rebound by Rolland-Cachera et al. (1984). Early to infectious disease, in addition to hypoxia. Ethiopians adiposity rebound has been associated with earlier age at living at high altitude have better nutrition, growth, and menarche (Barker et al., 2001) and increased relative socioeconomic conditions than low altitude populations, weight and obesity later in life, including during adoles- and this is reflected in their better growth rates cence (Cameron and Demerath, 2002). Early growth (Clegg et al., 1972), illustrating the importance of nonhy- restriction followed by catch-up growth is also associated poxic factors influencing the growth of high altitude with the development of abdominal obesity (Dulloo, populations. 2006), while higher growth velocity in early childhood, prior to adiposity rebound, has been shown to be associ- ated with greater fatness and obesity in subsequent years GROWTH IN THE LATER CHILDHOOD, (Monteiro et al., 2003). The combination of small size at JUVENILE AND ADOLESCENCE STAGES birth and during infancy, followed by accelerated weight gain from age 3 to 11 years, predicts large differences in Most of the environmental factors associated with the cumulative incidence of coronary heart disease, non- growth in adolescence are common to growth in prea- insulin dependent diabetes, and hypertension in later life dolescence, the most important of which are nutrition, (Barker et al., 2001). In the United States, low levels of infection, and the interactions between the two. Add- vigorous physical activity and high levels of television itionally, birthweight, catch-up growth, breast-feeding, viewing have been associated with fatness in children and early adiposity rebound have impacts on growth during the adiposity rebound period (Janz et al., 2002), and/or body composition into puberty. Growth in later and expose American children to an increased risk of childhood and adolescence continues to show great obesity and chronic disease in adult life. biological plasticity. Across populations, Stoltzfus (2001) In addition to undernutrition and infection, child characterizedpatternsofgrowththatdeviategreatlyfrom neglect and abuse, exposure to industrial pollutants, food normative patterns, as represented by growth references. contaminants, behavioral toxicants, single parenthood, These include populations that display: (1) prepubertal overcrowding, and parental ill health are often important catch-up growth; (2) prepubertal stunting combined with contributors to growth outcomes, according to circum- catch-up growth in puberty; and (3) prepubertal stunting stance (Schell, 1991a). Seasonality of growth is found with no catch-up growth in puberty. She concludes that among populations of both developed and developing between-population variation in growth among school- countries. In the former, effects are quite subtle climatic age children and adolescents is as great as among ones, while in the latter, they are largely due to seasonal children in early childhood. Pattern three is the most variation in food availability and infectious disease common across the developing world (Waterlow, 1988), exposure (Cole, 1993). If infants are breast-fed, they are and is usually associated with poverty and low socioeco- usually shielded from most of the stresses associated with nomic status (Martorell et al., 1988). It is also associated seasonality of infection and nutrition. However, such with infant failure to thrive in industrialized nations, seasonal factors can become significant after weaning, where growth-retarded children in infancy have been and persist across childhood and adolescence. shown to remain height and weight deficit at the age The relationships between proximate and distal of six years (Tomkins, 1994). Patterns one and two can influences on child growth (Figure 23.1) have been occur as a result of: (1) different types of infant feeding examined at macro-level. Blakely et al. (2005) identified and weaning behavior (Frongillo, 2001); (2) varying strong relationships between poverty and childhood illnessmanagement practices (Tomkins 1986); (3) dietary malnutrition, access to unsafe water and sanitation, manipulation (Steckel, 1987); and (4) changing environ- and exposure to indoor air pollution, while Frongillo ments during childhood (Golden, 1994). The latter pat- et al. (1997) found the most important determinants of tern has been observed to take place across secular stunting in children below the age of five years to be trends (Proos, 1993), and during nutrition transition dietary energy availability, female literacy, and gross (Sawaya et al., 2003). national product. In the developed world, relationships The first two of Stoltzfus’s (2001) growth patterns, between poverty and child growth persist but perhaps representing prepubertal catch-up growth, catch-up to a lesser extent than prior to positive secular trends growth in puberty, and prepubertal stunting combined that took place from the late nineteenth and across the with catch-up growth in puberty, respectively, are twentieth century (Ulijaszek, 2001). associated with critical periods of development which can have long-term implications for health, and body Diet composition in later childhood (Barker et al., 2001). Body fatness reaches a postinfancy low level typically Both dietary quantity and quality can influence growth between the ages of five and seven years, followed and body composition in later childhood, as can infant by increased body fatness, a phenomenon termed feeding patterns. While there appears to be no difference

Variation in Human Growth Patterns due to Environmental Factors 401 in weight and height between breast-fed and formula-fed Pollution children by the time they reach school-age, breast-fed Exposure of adolescents to environmental pollutants is infantsarelesslikelytobecomeobeseasadults(Frongillo, different from earlier life, as the likelihood of occupa- 2001). Deficiencies of energy, protein, and zinc have tional exposure increases, at least in the developing been implicated in growth faltering, while diets high in world. Perinatal exposure to polybrominated biphenyl fat have been associated with obesity (Ulijaszek. 2006). (PBB) has been shown to be associated with earlier age Vegetarian and vegan diets in both developed and at menarche (Blanck et al., 2000), while early exposure developing countries have been shown to be deficient to PCB is associated with delayed sexual maturation in in micronutrients. In a study from the Netherlands, both males and females (den Hond et al., 2002). In the children aged 0–10 years consuming macrobiotic diets one study in which the concurrent effects of most with adequate protein and energy intakes and protected common pollutants to which children might be from bacterial contamination were shown to have exposed was examined, Denham et al. (2005) found growth patterns similar to those of poor children in attainment of menarche to be sensitive to relatively developing countries (Dagnelie et al., 1994). low levels of lead and certain PCB congeners. Dichlor- While broad descriptive studies of adolescent growth odiphenyltrichloroethan (DDT) is a chemical once are plentiful, there are few that have critically evaluated used widely in agriculture but which is now limited the relative importance of specific environmental factors largely to public health use, especially in malarial in this process. This is because of the great variation both vector control programs in nations where equally within- and between-populations in the maturation rate effective and affordable alternatives are not locally and the timing and magnitude of peak weight and height available. The one study in the United States which velocities. In general, adolescent growth is sensitive to rigorously examined the possible effects of prenatal nutritional deficit and surfeit (Eveleth and Tanner, DDT exposure on pubertal growth and development, 1990). For many industrialized nations, there have been found no effect (Gladen et al., 2004). secular trends in the timing and size of the pubertal growth spurt which have been taken as evidence for nutritional improvement (Eveleth and Tanner, 1990). Altitude Furthermore, many of the socioeconomic differences betweengroupsingrowthinadolescencehavebeen Adolescent growth and development among populations attributed to nutritional differences (Eveleth and Tanner, living at high altitude is often characterized by slow 1990). Despite this, there appears to be only one longitu- growth and delayed puberty, resulting in smaller dinal study that demonstrates direct nutritional effects adult body size (Weitz and Garruto, 2004). Slower growth on growth in adolescence (Berkey et al., 2000), among at high altitude is a consequence of hypoxia (Frisancho, girls in Boston, in the United States. Those who con- 1993), poor economic conditions, and nutritional inad- sumed more dietary energy and animal protein than equacy (Weitz and Garruto, 2004). A study of European average two years before peak growth were shown to children of higher socioeconomic status migrating to experience both earlier age at peak growth velocity, and high altitude in the Andes has shown them to be slightly higher peak height velocity than average. The latter is shorter and lighter than their peers of same socioeco- likely to be conditional upon the former. nomic status living at sea-level, indicating that high alti- tude hypoxia has a small but independent impact on growth (Stinson, 1982). There is delayed sexual matur- ation among many, but not all, high latitude populations Infection relative to lower altitude populations, as well as a late and The impacts of infection on adolescent growth are of poorly defined adolescent growth spurt, at least among much lesser importance than nutrition. This is because Andean populations (Frisancho and Baker, 1970). the immune system has matured and adaptive immunity is largely in place by adolescence (Ulijaszek, 1998), and as a consequence of this, contraction of most common CONCLUSIONS infections of early childhood is much reduced. However, perinatal HIV-1 infection has been shown to interfere This chapter reviews the range of environmental agents with sexual maturation in children surviving this infec- know to influence growth in weight and stature across tion into adolescence (Buchacz et al., 2003). Other infec- infancy, childhood, and adolescence. Diet, nutrition, dis- tions that persist in their effects on physical growth and ease,hypoxia,pollution,contamination,behavioraltoxi- development into adolescence are tuberculosis and Heli- cants, deprivation, and psychosocial stress are clustered cobacter pylori. Furthermore, a number of chronic dis- as proximate environmental agents that can influence eases can delay onset of puberty and reduce the size of growth, which vary in importance according to circum- the pubertal growth spurt (Simon, 2002). stance and the age and stage in infancy, childhood, and

402 Stanley J. Ulijaszek adolescence. Culture, society, behavior, socioeconomic Bhandari, N., Bahl, R. and Taneja, S. (2001). Effect of micro- status, social status, poverty, and political economy are nutrient supplementation on linear growth of children. clustered as structurally powerful but distal agents in the British Journal of Nutrition, 85(suppl. 2), S131–S137. production of growth and body size outcomes, at all ages Blakely, T., Hales, S., Kieft, C., et al. (2005). The global and stages of childhood and adolescence. Early life distribution of risk factors by poverty level. Bulletin of the World Health Organization, 83, 118–126. experiences involving environmental stress, intrauterine Blanck, H. M., Marcus, M., Tolbert, P. E., et al. (2000). Age growth retardation, poor growth in early childhood, and at menarche and Tanner stage in girls exposed in utero and subsequent catch-up growth can impact on growth, body postnatally to polybrominated biphenyl. Epidemiology, composition, and health outcomes later in life. 11, 641–647. The extent to which human growth and body size Bogin, B. (1998). Patterns of human growth. In Encyclopedia responds with sensitivity to environmental quality is of Human Growth and Development,S.J.Ulijaszek, demonstrated in the secular trends in growth and body F. E. Johnston and M. A. Preece (eds). Cambridge: size that have taken place across successive gener- Cambridge University Press, pp. 91–95. ations of human populations living in the same terri- Bogin, B. (1999). Patterns of Human Growth, 2nd edn. tories. These have been mostly positive, resulting from Cambridge: Cambridge University Press. environmental improvements, but negative trends Buchacz, K., Rogol, A. D., Lindsey, J. C., et al. (2003). Delayed have also been demonstrated. Developmental plasticity onset of pubertal development in children and adolescents is an adaptive property of humans that allows them with perinatally acquired HIV infection. 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24 Evolutionary Biology of Hormonal Responses to Social Challenges in the Human Child Mark V. Flinn The human child is remarkably tuned-in to his or United States indicate that chronic stress is similarly her social environment. He or she is an informational associated with a long-term three-fold increase in sponge, absorbing bits of knowledge from others at adverse health conditions (Cohen et al., 1993, 2007). a phenomenal pace, equipped with life’s most sophisti- Exposure to stressful events early in development, cated and creative communication system (human moreover, appears to have lifelong effects (Heim et al., language). This sensitivity to social interactions is inter- 2002; Fox et al., 2007; Kolassa and Elbert, 2007; Meaney woven with the ontogeny of flexible cognitive skills – et al., 2007; Champagne, 2008; Seckl, 2008). Stress including empathy, self awareness, social-scenario endocrinology is suspected to have an important role building, and theory of mind (ToM) – that are the foun- in the links between social environment and health. dation of human relationships. In this chapter Chronic release of stress hormones such as cortisol in I examine the neuroendocrine systems that facilitate response to psychosocial challenges is posited to have the development of these distinctively human sociocog- incidental deleterious effects on immune and metabolic nitive adaptations. regulatory functions (Ader et al., 2001; Sapolsky, 2005). Neuroendocrine systems may be viewed as com- Release of androgens such as testosterone, dehydroe- plex sets of mechanisms designed by natural selection piandrosterone (DHEA), and dehydroepiandrosterone to communicate information among cells and tissues. sulfate (DHEAS) are also influenced by social condi- Steroid and peptide hormones, associated neurotrans- tions (see Chapter 16 of this volume), and can affect mitters, and other chemical messengers guide behav- immunocompetence (Muehlenbein and Bribiescas, iors of mammals in many important ways (Ellison, 2005; Muehlenbein, 2008). 2001; Lee et al., 2009; Panksepp, 2009). Analysis of This importance of the social environment for patterns of hormone levels in naturalistic contexts a child’s physical and mental health presents an evolu- can provide important insights into the evolutionary tionary puzzle. Why, given the apparent high cost functions of the neuroendocrine mechanisms that to human health of psychosocial stress, would natural guide human behaviors. Here I focus on the apparent selection have favored links between the psycho- evolutionary paradox of neuroendocrine response to logical mechanisms that assess social challenges, psychosocial stressors. and the neuroendocrine mechanisms that regulate Acute and chronic stressful experiences are associ- stress and reproductive physiology and downstream ated with a variety of negative health outcomes in immune functions? I approach this question from humans, including susceptibility to upper respiratory the integrative evolutionary paradigm of Niko infections (Cohen et al., 2003), anxiety and depression Tinbergen (1963), who emphasized the importance of (Heim and Nemeroff, 2001), and coronary heart dis- linking proximate physiological explanations with ease (McEwen, 1998). The effects of psychosocial ontogeny (development), phylogeny (ancestry), and stress can be substantial: in the rural community of adaptive function (natural selection). My basic argu- Bwa Mawego, Dominica, where I have studied child ment is that hormonal stress response to psychosocial health for the past 22 years, overall morbidity among challenges facilitates the neural remodeling and poten- children for the 3–6 days following an acute stress tiation that is necessary to adapt to the dynamic infor- event is more than double the normal rate (Flinn and mational arms race of the human sociocultural England, 2003). Studies of populations within the environment. Human Evolutionary Biology, ed. Michael P. Muehlenbein. Published by Cambridge University Press. # Cambridge University Press 2010. 405

406 Mark V. Flinn WHY IS THE HUMAN CHILD SO SENSITIVE the paradox of hormonal response to social challenge, TO THE SOCIAL ENVIRONMENT? hypothesizing that glucocorticoids and androgens help facilitate neural remodeling and long-term potentia- The human child is a social creature, motivated by and tion necessary for dynamic social cognition. highly sensitive to interpersonal relationships (Gopnik et al., 1999). The life history stage of human childhood Paternal care in multimale groups enables the development of necessary social skills (Alexander, 1987; Joffe, 1997; Bogin, 1999; Geary and Mammals that live in groups with multiple males – Bjorklund, 2000; Flinn, 2004), including emotional such as chimpanzees (Pan troglodytes) – usually have regulation. Learning, practice, and experience are little or no paternal care, because the nonexclusivity of imperative for social success. The information process- mating relationships obscures paternity (Alexander, ing capacity used for human social interactions is con- 1974; Clutton-Brock, 1991). Chimpanzee males appear siderable, and perhaps significantly greater than that to lack reliable cues for identifying their offspring. involved with foraging skills (Roth and Dicke, 2005). In contrast, it is common for human fathers to provide The child needs to master complex dynamic protection, information, food, and social status for tasks such as learning the personalities, social biases, their children. Paternal care in humans appears to relationships, and so forth of peers and adults in the be facilitated by relatively stable pair bonds, which local community, and developing appropriate cogni- not only involves co-operation between mates that tive and emotional responses to these challenges often endures over the life span, but which requires (Bugental, 2000). The learning environments that an unusual type of co-operation among coresiding facilitate and channel these astonishing aspects of males – respect for each other’s mating relationships. human mental phenotypic plasticity appear to take on The relatively exclusive mating relationships that a special importance. Much of the data required for the are characteristic of humans generate natural factions social behavior necessary to be successful as a human within the group. Mating relationships also can create cannot be “preprogrammed” into specific, detailed, alliances in human groups, linking two families or fixed responses. Social cleverness in a fast-paced, clans together. By way of comparison, in chimpanzee cumulative cultural environment must contend with communities it is difficult for even the most dominant dynamic, constantly shifting strategies of friends and male to monopolize an estrous female; most of the enemies, and hence needs information from experien- males in a community mate with most of the females tial social learning (Flinn, 1997, 2006a). The links (Goodall, 1986). Although dominant males sire a among psychosocial stimuli, emotions, and physio- higher proportion, chimpanzee males in effect “share” logical stress response may guide both the acute and a common interest in the community’s females and long-term neurological plasticity necessary for their offspring. Human groups, in contrast, are com- adapting to the dynamic aspects of human sociality. posed of family units, each with distinct reproductive interests. Human males do not typically share mating access to all the group’s females; consequently, there HUMAN SOCIALITY: KEY EVOLUTIONARY are usually reliable cues identifying which children are PUZZLES their genetic offspring, and which are those of other males (for variations see Flinn, 1981; Beckerman and Humans are characterized by a distinctive set of traits, Valentine, 2002). Because humans live in multimale including: (1) large brains; (2) long periods of juvenile groups, yet typically maintain fairly stable mating rela- dependence; (3) extensive biparental care including tionships, the potential for fission along family lines is large transfers of information; (4) multigenerational high. Still, human groups overcome this inherent con- bilateral kin networks; (5) habitual bipedal locomo- flict between family units to form large, stable coali- tion; (6) use of the upper limbs for tool use including tions (Chapais, 2008). projectile weapons; (7) concealed or “cryptic” ovula- This unusual tolerance among coresidential males tion; (8) menopause; (9) culture including language; and females stands in contrast to the norm of polyg- and (10) lethal competition among kin-based coali- amous mate competition in nonhuman primates. tions. A few other species exhibit several of these traits; Selection pressures favoring such tolerance are uncer- only humans, however, are characterized by the entire tain, but likely involve the importance of both male combination (Alexander, 2005). This suite of traits pre- parental investment (Alexander, 1990b; Geary and sents several questions or puzzles that are key to Bjorklund, 2000) and male coalitions for intraspecific understanding human evolutionary biology. Here conflict (Alexander, 1989, 2006; Wrangham, 1999; I first briefly describe these puzzles, and suggest a Geary and Flinn, 2001; Bernhard et al., 2006). The common resolution based on the importance of social hormonal mechanisms that enable these unusual competition during human evolution. I then return to aspects of human male relationships are uncertain.

Evolutionary Biology of Hormonal Responses to Social Challenges in the Human Child 407 Analysis of patterns of levels of candidate hormones – and enhanced integration of the cerebellum also such as vasopressin, testosterone, DHEA/S and appear significant (Allman, 1999; Amodio and cortisol – in natural social conditions may provide Frith, 2006). In comparison with most other parts of useful clues as to the evolved functions of male the human genome, selection on genes involved with coalitions and pair bonding among humans. brain development was especially intense (Gilbert et al., 2005). The human brain has high metabolic costs: about An extended period of juvenile dependence 50% of an infant’s, and 20% of an adult’s, energetic and child development resources are used to support this neurological activity The human baby is unusually altricial (helpless). (Aiello and Wheeler, 1995). Although the increase in Infants must be carried, fed, and protected for a energetic resources allocated to the brain was accom- long period in comparison with other primates. panied by a corresponding decrease in digestive tissue, Human childhood and adolescence are also lengthy this does not explain what the selective pressures (Smith, 1994; Bogin, 1999; Leigh, 2004). This extension were for enhanced information processing, or why of the juvenile period that delays reproduction the resources were not reallocated to direct reproduct- for much longer than the other hominoids appears ive function. The obstetric difficulties associated with costly in evolutionary terms. Parental and other birthing a large-headed infant generate additional kin investment continues for an unusually long time, problems (Rosenberg and Trevathan, 2002). The select- often well into adulthood and perhaps even after ive advantages of increased intelligence must have the death of the parents (Alexander, 1987; Coe, 2003; been high to overcome these costs. Hrdy, 2009). The human brain, in short, is a big evolutionary The selective pressures responsible for this unique puzzle. It is developmentally and metabolically expen- suite of life history characteristics appear central to sive, evolved rapidly, enables uniquely human cogni- understanding human evolution (Alexander, tive abilities such as language, empathy, foresight, 1990a, 1990b; Kaplan et al., 2000; Bjorklund and consciousness, and ToM, and generates unusual Pellegrini, 2002; Rosenberg, 2004). The normal delay levels of novelty. Advantages of a larger brain may of reproduction until at least 15 years of age involves include enhanced information processing capacities prolonged exposure to extrinsic causes of mortality to contend with ecological pressures that involve sexu- and longer generation intervals. What advantages of ally dimorphic activities such as hunting and complex an extended childhood could have outweighed the foraging (Kaplan and Robson, 2002). There is little heavy costs of reduced fecundity and late reproduction evidence, however, of sufficient domain-specific (Williams, 1966; Stearns, 1990) for our hominin enlargement of those parts of the brain associated ancestors? with selective pressures from the physical environ- ment (Geary and Huffman, 2002; Adolphs, 2003). Indeed, human cognition has little to distinguish itself Intelligence, information, and social power in the way of specialized ecological talents. A large The human brain is an astonishing organ. Its cortex brain may have been sexually selected because it was comprises about 30 billion neurons of 200 different an attractive trait for mate choice (Miller, 2000; Gavri- types, each of which are interlinked by about a thou- lets and Vose, 2006). However, there is little sexual sand synapses, resulting in a million billion connec- dimorphism in encephalization quotient or intelli- tions working at rates of up to ten billion interactions gence psychometrics (Jensen, 1998), nor is there a per second (Williams and Herrup, 1988; Koch, 1999; clear reason why brains would have been a target for Edelman, 2006). Quantifying the transduction of sexual selection driven by mate choice uniquely these biophysical actions into specific cognitive among hominins. activities – e.g., thoughts and emotions – is difficult, One area in which humans are truly extraordinary but it is likely that humans have more information is sociality. Humans are able to mentally represent processing capacity than any other species (Roth and the feelings and thoughts of others. Humans have Dicke, 2005). unusually well-developed mechanisms for ToM (Leslie The human brain evolved at a rapid pace: hominin et al., 2004; Amodio and Frith, 2006), and associated cranial capacity tripled (from an average of about specific pathologies in this domain (Baron-Cohen, 450 to 1350 cc) in less than 2 million years 1995; Gilbert, 2001). We have exceptional linguistic (Lee and Wolpoff, 2003) – roughly 100 000 neurons abilities for transferring information from one brain and supportive cells per generation. Structural changes to another (Pinker, 1994), enabling complex social such as increased convolutions, thickly myelinated learning. Social and linguistic competencies are cortical neurons, lateral asymmetries, increased roughly equivalent in both males and females, von Economo neurons, expansion of the neo-cortex, although human mothers appear to have especially

408 Mark V. Flinn important roles in the development of their offspring’s THE SOCIAL ENVIRONMENT AS A KEY sociocognitive development (Simons et al., 2001; SELECTIVE PRESSURE Deater-Deckard et al., 2004). Information processing is a core human adaptation Human coalitionary dynamics appear to have become increasingly based on information and social Children are especially tuned to their social worlds skills. Intense intergroup competition created pressure and the information that it provides. The social world is for within-group social cohesion (Alexander, 1990a; a rich source of useful information for cognitive develop- Flinn et al., 2005a) that required not only fighting ment. The human brain appears designed by natural abilities, but complex social strategies. selection to take advantage of this bonanza of data (Tooby and Cosmides, 1992; Bjorklund and Pellegrini, 2002; Belsky, 2005). “Culture” may be viewed as a highly Kin networks and multiple caretakers dynamic information pool that coevolved with the exten- All human societies recognize kinship as a key organi- sive information processing abilities associated with our zational principle (Brown, 1991). All languages have flexible communicative and sociocognitive competen- kinship terminologies and concomitant expectations cies (Alexander, 1979). With the increasing importance of nepotism (Murdock, 1949; Fortes, 1969). Human and power of information in hominin social interaction, kinship systems appear unique in the consistency of culture and traditionmay have becomean arena ofsocial both bilateral (maternal and paternal) and multige- co-operation and competition (Coe, 2003; Flinn, 2004, nerational structure, with a general trend for coresi- 2006a; Baumeister, 2005). dence of male kin. These aspects of human kinship The key issue is novelty. One of the most difficult link families into broader co-operative systems, and challenges to understanding human cognitive evolu- provide additional opportunities for alloparental care tion, and its handmaiden culture, is the unique during the long social childhood. Human grandparents informational arms race that underlies human behav- stand out as unusually important in this regard (Hrdy, ior. The reaction norms posited by evolutionary psych- 2005; Flinn and Leone, 2006, 2009). ology to guide evoked culture within specific domains Grandparents and grand-offspring share 25% of may be necessary but insufficient (Chiappe and their genes identical by descent, a significant oppor- MacDonald, 2005). The mind does not appear limited tunity for kin selection. Few species, however, live in to a predetermined Pleistocene set of options – such groups with multiple overlapping generations of kin. as choosing mate A if in environment X, but choose Fewer still have significant social relationships among mate B if in environment Y – analogous to examples individuals two or more generations apart. Humans of simple phenotypic plasticity (MacDonald and appear rather exceptional in this regard. Grandparent- Hershberger, 2005). ing is cross-culturally ubiquitous and pervasive Keeping up in the hominin social chess game (Murdock, 1967; Sear et al., 2000). Our life histories requires imitation. Getting ahead favors creativity to allow for significant generational overlaps, including produce new solutions to beat the current winning an apparent extended postreproductive stage facili- strategies. Random changes, however, are risky and tated by the unique human physiological adaptation ineffective. Hence the importance of cognitive abilities of menopause (Alexander, 1974, 1987; Hawkes, 2003). to hone choices among imagined innovations in ever The significance of emotional bonding between more complex social scenarios. The theater of the mind grandparents and grandchildren is beyond doubt. The that allows humans to “understand other persons as evolved functions are uncertain, but likely involve intentional agents” (Tomasello, 1999, p. 526) provides the exceptional importance of long-term extensive the basis for the evaluation and refinement of creative and intensive investment for the human child. solutions to the never-ending novelty of the social The emotional and cognitive processes that guide arms race. This process of filtering the riot of novel grand-relationships must have evolved because they information generated by the creative mind favored enhanced survival and eventual reproductive success the cognitive mechanisms for recursive pattern recog- of grandchildren. In addition to the physical basics of nition in the “open” domains of both language (Pinker, food, protection, and hygienic care, development of the 1994, 1997; Nowak et al., 2001) and social dynamics human child is strongly influenced by the dynamics of (Geary, 2005; Flinn, 1997, 2006a). Cultural “traditions” the social environment (Konner, 1991; Hetherington, passed down through the generations also help con- 2003a, 2003b; Dunn, 2004). Grandparents may have strain the creative mind (Coe, 2003; Flinn and Coe, knowledge and experience that are important and 2007). The evolutionary basis for these psychological useful for helping grandchildren and other relatives mechanisms underlying the importance of social succeed in social competition (Coe, 2003). Humans learning and culture appears rooted in a process of are unusual in the role of kin in alloparental care and “runaway social selection” (Alexander, 2005; Flinn group coalitions (Hrdy, 2009). and Alexander, 2007).

Evolutionary Biology of Hormonal Responses to Social Challenges in the Human Child 409 Runaway social selection selective pressure via social competition involving coalitions (Alexander, 1989; Geary and Flinn, 2002), Darwin (1871) recognized that there could be import- and dominance of their ecologies involving niche con- ant differences between: (1) selection occurring as a struction (Laland et al., 2000). The primary functions consequence of interaction with ecological factors of the most extraordinary and distinctive human such as predators, climate, and food; and (2) selection mental abilities – language, imagination, self-awareness, occurring as a consequence of interactions among con- ToM, foresight, and consciousness – involve the nego- specifics, i.e., members of the same species competing tiation of social relationships (Siegal and Varley, 2002; with each other over resources such as nest sites, Tulving, 2002; Flinn et al., 2005a). The multiple-party food, and mates. The former is termed “natural selec- reciprocity and shifting nested subcoalitions charac- tion” and the latter “social selection” of which sexual teristic of human sociality generate especially difficult selection may be considered a special subtype (West- information processing demands for these cognitive Eberhard, 1983). The pace and directions of evolution- facilities that underlie social competency. Hominin ary changes in behavior and morphology produced social competition involved increasing amounts of by these two types of selection – natural and social – novel information and creative strategies. Culture can be significantly different (Fisher, 1930; West- emerged as an intensive selective pressure on the Eberhard, 2003). evolving brain. Selection that occurs as a consequence of inter- actions between species can be intense and unending – for example with parasite-host red queen evolution Evolution of the cultural brain (Hamilton et al., 1990) and other biotic arms races. Intraspecific social competition may generate selective As noted above, the human brain is a big evolutionary pressures that cause even more rapid and dramatic paradox. It has high metabolic costs, takes a long time evolutionary changes. Relative to natural selection, to develop, evolved rapidly, enables behavior to social selection has the following characteristics (West- change quickly, has unique linguistic and social apti- Eberhard, 1983): (1) The intensity of social selection tudes, and generates unusual levels of informational (and consequent genetic changes) can be very high novelty. Its primary functions include dealing with because competition among conspecifics can have other human brains (Adolphs, 2003; Alexander, 2005; especially strong effects on differential reproduction. Amodio and Frith, 2006). The currency is not foot- (2) Because the salient selective pressures involve com- speed or antibody production, but the generation petition among members of the same species, the normal and processing of data in the social worlds of the ecological constraints are often relaxed for social selec- human brains’ own collective and historical informa- tion. Hence traits can evolve in seemingly extreme and tion pools. Some of the standout features of the bizarre directions before counter-balancing natural human brain that distinguish us from our primate selection slows the process. (3) Because social competi- relatives are asymmetrically localized in the prefrontal tion involves relative superiority among conspecifics, cortex, including especially the dorsolateral prefrontal the bar can be constantly raised in a consistent direction cortex and frontal pole (Ghazanfar and Santos, 2004; generation after generation in an unending arms race. for review see Geary, 2005). These areas appear to be (4) Because social competition can involve multiple iter- involved with “social scenario building” or the ability ations of linked strategy and counter-strategy among to “see ourselves as others see us so that we may interacting individuals, the process of social selection cause competitive others to see us as we wish them to” can become autocatalytic, its pace and directions partly (Alexander, 1990b, p. 7), and are linked to specific social determined from within, generating what might be abilities such as understanding sarcasm (Shamay- termed “secondary red queens.” For example, reoccur- Tsoory et al., 2005) and morality (Moll et al., 2005). rence of social competition over lifetimes and gener- An extended childhood seems to enable the develop- ations can favor flexible phenotypic responses such as ment of these necessary social skills (Joffe, 1997). social learning that enable constantly changing strat- egies. Phenotypic flexibility of learned behavior to con- Evolution of the human family as a nest for the tend with a dynamic target may benefit from enhanced child’s social mind information processing capacities, especially in regard to foresight and scenario-building. To summarize, the human family is the nexus for the Human evolution appears characterized by these suite of extraordinary and unique human traits. Humans circumstances generating a process of runaway social are the only species to live in large multimale groups selection (Alexander, 2005; Flinn and Alexander, with complex coalitions and extensive paternal and allo- 2007). Humans, more so than any other species, parental care, and the altricial infant is indicative of a appear to have become their own most potent protective environment provided by intense parenting

410 Mark V. Flinn and alloparental care in the context of kin groups Humans exhibit a unique “nested family” social struc- (Chisholm, 1999). The human baby does not need to ture, involving complex reciprocity among males and be physically precocial, instead the brain continues females to restrict direct competition for mates among rapid growth, and the corresponding cognitive compe- group members. tencies largely direct attention toward the social environ- It is difficult to imagine how this system of pair ment. Plastic neural systems adapt to the nuances of the bonds and male coalitions could be maintained in the local community, such as its language (Alexander, absence of another unusual human trait: concealed or 1990a; Geary and Bjorklund, 2000; Bjorklund and ‘cryptic’ ovulation (Alexander and Noonan, 1979). Pellegrini, 2002; Fisher, 2005). In contrast to the slow Human groups tend to be male philopatric (males development of ecological skills of movement, fighting, tending to remain in their natal groups), resulting in and feeding, the human infant rapidly acquires skill extensive male kin alliances, useful for competing with the complex communication system of human against other groups of male kin (Wrangham and language (Pinker, 1994; Sakai, 2005). The extraordinary Peterson, 1996; LeBlanc, 2003). However, unlike chim- information-transfer abilities enabled by linguistic com- panzees, human groups and communities are often petency provide a conduit to the knowledge available composed of several bilateral kin factions, interwoven in other human minds. This emergent capability for by pair bond relationships among them. Human intensive and extensive communication potentiates the females also have complex alliances, but usually are social dynamics characteristic of human groups not involved directly in the overt physical aggression (Deacon, 1997; Dunbar, 1998) and provides a new mech- characteristic of intergroup relations (Campbell, 2002; anism for social learning and culture. Geary and Flinn, 2002). Parents and other kin may be An extended childhood appears useful for acquir- especially important for the child’s mental develop- ing the knowledge and practice to hone social ment of social and cultural maps because they can be skills and to build coalitional relationships necessary relied upon as landmarks who provide relatively honest for successful negotiation of the increasingly intense information. From this perspective, the evolutionary social competition of adolescence and adulthood. significance of the human family in regard to child Ecologically related play and activities (e.g., explor- development is viewed more as a nest from which ation of the physical environment) are also important social skills may be acquired than just as an economic (e.g., Geary et al., 2003), but appear similar to that of unit centered on the sexual division of labor (Flinn other primates. The unusual scheduling of human et al., 2005b). reproductive maturity, including an “adrenarche” To summarize my argument to this point, human (patterned increases in adrenal activities preceding childhood is viewed as a life history stage that puberty) and a delay in direct mate competition among appears necessary and useful for acquiring the infor- males appears to extend the period of practicing social mation and practice to build and refine the mental roles and extends social ontogeny (Campbell, 2006; algorithms critical for negotiating the social coalitions Del Giudice 2009; Flinn et al., 2009). that are key to success in our species. Mastering The advantages of intensive parenting, including the social environment presents special challenges paternal protection and other care, require a most for the human child. Social competence is difficult unusual pattern of mating relationships: moderately because the target is constantly changing and exclusive pair bonding in multiple-male groups. similarly equipped with ToM and other cognitive abil- No other primate (or mammal) that lives in large, ities. The family environment, including care from co-operative multiple-reproductive-male groups has fathers and grandparents, is a primary source and extensive male parental care, although some protec- mediator of the ontogeny of social competencies. tion by males is evident in baboons (Buchan et al., Human biology has been profoundly affected by our 2003). Competition for females in multiple-male evolutionary history as unusually social creatures, groups usually results in low confidence of paternity including, perhaps, a special reliance upon smart (e.g., chimpanzees). Males forming exclusive mothers, co-operative fathers, and helpful grandpar- “pair bonds” in multiple-male groups would provide ents. Indeed, the mind of the human child may cues of nonpaternity to other males, and hence have design features that enable its development as a place their offspring in great danger of infanticide group project, guided by the multitudinous informa- (Hrdy, 1999). Paternal care is most likely to be favored tional contributions of its ancestors and codescen- by natural selection in conditions where males can dants (Coe, 2003; Hrdy, 2009). Studies of the identify their offspring with sufficient probability to patterns of hormonal responses to these complex offset the costs of investment, although reciprocity components of human sociality may provide import- with mates is also likely to be involved (Smuts and ant clues about the selective pressures that guided Smuts, 1993; Geary and Flinn, 2001; Chapais, 2008). human evolution.

Evolutionary Biology of Hormonal Responses to Social Challenges in the Human Child 411 NEUROENDOCRINE RESPONSE TO THE SOCIAL unique designs, such as romantic love (Fisher et al., ENVIRONMENT 2002), that involve shared endogenous messengers from our phylogenetic heritage. The constellation of behaviors associated with the Attachments or bonding are central in the lives of human family and the dynamics of social competition the social mammals. Basic to survival and reproduc- described in previous sections are enabled by complex tion, these interdependent relationships are the fabric regulatory systems. In this section, I first briefly review of the social networks that permit individuals to main- the potential mechanisms for human pair bonding, tain co-operative relationships over time. Although maternal and paternal attachment to offspring, kin attachments can provide security and relief from attachment, and male coalitions. Much of the research stress, close relationships also exert pressures on indi- on the basic mechanisms has been done with nonhu- viduals to which they continuously respond. It should man models and is not easily applied directly to some not be surprising, therefore, that the neuroendocrine aspects of human psychology. I then turn to a more mechanisms underlying attachment and stress are detailed analysis of how the neuroendocrine stress intimately related to one another. And although at the response system functions to enable acquisition of present time a good deal more is known about the social competencies during childhood in the context stress response systems than the affiliative systems, of the human family environment. some of the pieces of the puzzle are beginning to fall The chemical messenger systems that orchestrate into place (Panksepp, 2004). the ontogeny and regulation of sexual differentiation, The mother–offspring relationship is at the core of metabolism, neurogenesis, immune function, growth, mammalian life, and it appears that some of the bio- and other complex somatic processes, tend to be evo- chemistry at play in the regulation of this intimate lutionarily conservative among primates and more bond was also selected to serve in primary mechanisms generally among mammals. Hence rodent and nonhu- regulating bonds between mates, paternal care, the man primate models provide important comparative family group, and even larger social networks information about the functions of specific human (Hrdy, 1999; Fisher et al., 2002). Although a number neuroendocrine systems, for which we often have little of hormones and neurotransmitters are involved in direct empirical research. It is the particular balance of attachment and other components of relationships, human mechanisms and abilities that is unique and the two peptide hormones, oxytocin (OT) and arginine- reflects the history of selection for complex social vasopressin (AVP), appear to be primary (Carter, 2002; interactions that shaped the human lineage. Young and Insel, 2002; Curtis and Wang, 2003; Lim et al., 2004; Heinrichs and Domes, 2008; Lee et al., 2009), with dopamine, cortisol, and other hormones and neurotransmitters having mediating effects. The chemistry of affection The hypothalamus is the major brain site where OT Some of the most precious of all our human feelings and AVP (closely related chains of nine amino acids) are stimulated by close social relationships: a mother are produced. From there they are released into the holding her newborn infant for the first time, brothers central nervous system (CNS) as well as transported reunited after a long absence, or lovers entangled in to the pituitary where they are stored until secreted each other’s arms. Natural selection has designed into the bloodstream. Oxytocin and AVP act on a wide our neurobiological mechanisms, in concert with our range of neurological systems, and their influence endocrine systems, to generate potent sensations in varies among mammalian species and stage of devel- our interactions with these most evolutionarily signifi- opment. The neurological effects of OT and AVP cant individuals. We share with our primate relatives appear to be key mechanisms (e.g., Bartels and Zeki, the same basic hormones and neurotransmitters that 2004) involved in the evolution of human family behav- underlie these mental gifts. But our unique evolution- iors. The effects of OT and AVP in humans are likely to ary history has modified us to respond to different be especially context dependent, because of the vari- circumstances and situations; we are rewarded and able and complex nature of family relationships. punished for somewhat different stimuli than our phylogenetic cousins. Chimpanzees and humans share the delight – the sensational reward – when biting into Parental care a ripe, juicy mango. But the endocrine, neurological, and associated emotional responses of a human father Along with OT and AVP, prolactin, estrogen, and pro- to the birth of his child (e.g., Storey et al., 2000) are gesterone are involved in parental care among likely to be quite different from those of a chimpanzee mammals (Insel and Young, 2001). The roles of these male. Happiness for a human (Buss, 2000) has many hormones vary across species and between males and

412 Mark V. Flinn females. The effects of these hormones are influenced Fisher et al., 2006). These studies also demonstrate by experience and context. Among rats, for example, that the neural regions involved in attachment acti- estrogen and progesterone appear to prime the brain vated in humans are similar to those activated in non- during pregnancy for parental behavior. Estrogen has human animals. Among humans, however, neural been found to activate the expression of genes that regions associated with social judgment and assess- increase the receptor density for OT and prolactin, ment of the intentions and emotions of others thus increasing their postnatal influence (Young and exhibited some deactivation during attachment activ- Insel, 2002). ities, suggesting possible links between psychological Oxytocin is most well known for its role in regulat- mechanisms for attachment and management of social ing birth and lactation, but along with AVP, it has also relationships. Falling in love with a mate and affective been found to play a central role in maternal care and bonds with offspring may involve temporary deactiva- attachment (Fleming et al., 1999). Just prior to birth, tion of psychological mechanisms for maintaining an an increase in OT occurs, which is seen as priming individual’s social “guard” in the complex reciprocity maternal care. An injection of OT to virgin rats has of human social networks. Dopamine levels are likely been found to induce maternal care, while an OT to be important for both types of relationship but may antagonist administered to pregnant rats interferes involve some distinct neural sites. It will be interesting with the development of maternal care (Carter, 2002). to see what fMRI studies of attachment in human The new rat mother requires hormonal activation males indicate because that is where the to initially stimulate maternal behavior. Once she has most substantial differences from other mammals begun to care for her pups, however, hormones are not would be expected. Similarly, fMRI studies of attach- required for maternal behavior to continue. Olfactory ment to mothers, fathers, and alloparental-care pro- and somatosensory stimulation from interactions viders in human children may provide important between pups and mother are, however, required for insights into the other side of parent–offspring the parental care to continue (Fleming et al., 1999). bonding. The stimulation from suckling raises OT levels in rodents and breast-feeding women, which then results Paternal care in not only milk letdown but also a decrease in limbic hypothalamic-anterior pituitary-adrenal cortex system Paternal care is not common among mammals. For (HPA) activity and a shift in the autonomic nervous evolutionary reasons noted earlier, it is found among system (ANS) from a sympathetic tone to a parasympa- some rodent and primate species, including humans. thetic tone. This results in a calmness seen as condu- The extent and types of paternal care vary among cive to remaining in contact with the infant. It also species. The hormonal influence in parental care results in a shift from external-directed energy toward among males appears to differ somewhat from that the internal activity of nutrient storage and growth found among females. Vasopressin (AVP) appears to (Uvnas-Moberg, 1998). function as the male addition to OT (Young and Experience also affects the neuroendocrine Insel, 2002). Along with prolactin and OT, AVP pre- systems involved in the expression of maternal care. pares the male to be receptive to and care for infants The HPA system of offspring during development is (Bales et al., 2004). influenced by variation in maternal care, which then Paternal care is more common in monogamous influences their maternal behavior as adults. Such than polygamous mammals and is often related to changes involve the production of, and receptor dens- hormonal and behavioral stimuli from the female. ity for, stress hormones and OT (Champagne and In the monogamous California mouse, disruption of Meaney, 2001; Fleming et al., 1999). the pair bond does not affect maternal care but does The HPA-modulated hormones and maternal diminish paternal care (Gubernick, 1996). In other behavior are related in humans during the postpartum species with biparental care, however, paternal care is period (Fleming et al., 1997). During this time, cortisol not as dependent on the presence of the female (Young appears to have an arousal effect, focusing attention on and Insel, 2002). Experience also plays a role in influ- infant bonding. Mothers with higher cortisol levels encing hormonal activation and paternal behavior. were found to be more affectionate, more attracted to Among tamarins, experienced fathers have higher their infant’s odor, and better at recognizing their levels of prolactin than first-time fathers (Ziegler and infant’s cry during the postpartum period. Snowdon, 1997). Functional magnetic resonance imaging (fMRI) Androgens including testosterone also appear to be studies of brain activity involved in maternal attach- involved in the regulation of paternal behavior. For ment in humans indicate that the activated regions are example, human fathers tend to have lower testoster- part of the reward system and contain a high density of one levels when they are involved in childcare activities receptors for OT and AVP (Bartels and Zeki, 2004; (Berg and Wynne-Edwards, 2002; Fleming et al., 2002;

Evolutionary Biology of Hormonal Responses to Social Challenges in the Human Child 413 Gray and Campbell, 2009; also see Chapter 16 of this pair and larger family network, it is not surprising that volume), although the relation with the key paternal similar neurohormonal mechanisms active in the role of offspring protection is uncertain. Human males maternal–offspring bond would also be selected to stand out as very different from our closest relatives underlie these other attachments. Though there is the chimpanzees in the areas of paternal attachment some variation among species and between males and and investment in offspring. Investigation of the neu- females, the same general neurohormonal systems roendocrine mechanisms that underpin male parental active in pair bonding in other species are found in behavior may provide important insights into these the human (Wynne-Edwards, 2003; Panksepp, 2004; critical evolutionary changes. Lee et al., 2009). Androgen response to pair bonding appears complex (e.g. van der Meij et al., 2008), but similar to parent–offspring attachment in that pair Pair bonding bonded males tend to have lower testosterone levels Like male parental care, bonding between mates is also in nonchallenging conditions (Alvergne et al., 2009; uncommon among mammals but has been selected for Gray and Campbell, 2009). Moreover, males actively when it has reproductive advantages for both parents involved in caretaking behavior appear to have tempor- (Clutton-Brock, 1991; Carter, 2002; Young et al., 2002). arily diminished testosterone levels (Gray et al., 2007). Monogamy is found across many mammalian taxa, The challenge before human evolutionary biolo- but most of the current knowledge related to the neu- gists and psychologists is to understand how these roendocrine basis of this phenomenon has been general neuroendocrine systems have been modified obtained from the comparative study of two closely and linked with other special human cognitive systems related rodent species. The prairie vole (Microtus (e.g., Allman et al., 2001; Blakemore et al., 2004) to ochrogaster) mating pair nest together and provide pro- produce the unique suite of human family behaviors. longed biparental care, while their close relatives, the Analysis of hormonal responses to social stimuli may meadow vole (Microtus pennsylvanicus), do not exhibit provide important insights into the selective pressures these behaviors (Young et al., 2002). As with other that guided the evolution of these key aspects of the social behaviors in rodents, OT and AVP have been human mind. found to be central in the differences these related species exhibit with respect to pair bonding. The chemistry of stress, family, and the social mind Pair bonding occurs for the prairie vole following mating. Vagino-cervical stimulation results in a release The evolutionary scenario proposed in previous of OT and the development of a partner preference for sections posits that the family is of paramount import- the female (Carter, 2002). For the male, it is an increase ance in a child’s world. Throughout human evolution- in AVP following mating and not just OT that results in ary history, parents and close relatives provided partner preference. Exogenous OT injected in the calories, protection, and information necessary for sur- female and exogenous AVP in the male prairie vole vival, growth, health, social success, and eventual result in mate preference even without mating. This reproduction. The human mind, therefore, is likely to does not occur with meadow voles (Young et al., 2002). have evolved special sensitivity to interactions with The receptor density for OT and AVP in specific family care providers, particularly during infancy and brain regions might provide the basis for mechanisms early childhood (Bowlby, 1969; Baumeister and Leary, underlying other social behaviors. Other neurotrans- 1995; Daly and Wilson, 1995; Belsky, 1997, 1999; Geary mitters, hormones, and social cues also are likely to and Flinn, 2001; Flinn et al. 2009). be involved, but slight changes in gene expression for The family and other kin provide important cogni- receptor density, such as those found between the tive “landmarks” for the development of a child’s meadow and prairie voles in the ventral palladium understanding of the social environment. The repro- (located near the nucleus accumbens, an important ductive interests of a child overlap with those of its component of the brain’s reward system), might dem- parents more than with any other individuals. Infor- onstrate how such mechanisms could be modified mation (including advice, training, and incidental by selection (Lim et al., 2004). The dopamine D2 recep- observation) provided by parents is important for situ- tors in the nucleus accumbens appear to link the ating oneself in the social milieu and developing a affiliative OT and AVP pair bonding mechanisms with mental model of its operations. A child’s family envir- positive rewarding mental states (Aragona et al., 2003; onment may be an especially important source and Curtis and Wang, 2003). The combination results in mediator of stress, with consequent effects on health. the powerful addiction that parents have for their Psychosocial stressors are associated with offspring. increased risk of infectious disease (Cohen et al., Given the adaptive value of extensive biparental 2003) and a variety of other illnesses (Ader et al., care and prolonged attachment found in the mating 2001). Physiological stress responses regulate the

414 Mark V. Flinn allocation of energetic and other somatic resources functions. The demands of energy regulation must to different bodily functions via a complex assortment orchestrate with those of immune function, attach- of neuroendocrine mechanisms. Changing, unpredict- ment bonding, and so forth. Mechanisms for localized able environments require adjustment of priorities. targeting (e.g., glucose uptake by active versus inactive Digestion, growth, immunity, and sex are irrelevant muscle tissues and neuropeptide-directed immune while being chased by a predator (Sapolsky, 1994). response) provide fine-tuning of the preceding general Stress hormones help shunt blood, glucose, and so physiological effects. Cortisol regulation allows the on to tissues necessary for the task at hand. Chronic body to respond to changing environmental conditions and traumatic stress can diminish health, evidently by preparing for specific short-term demands (Mason, because resources are diverted away from important 1971; Munck et al., 1984; Weiner, 1992). health functions. These costs can be referred to as These temporary beneficial effects of glucocorti- “allostatic load” (McEwen, 1995). Such diversions of coid stress response, however, are not without costs. resources may have special significance during child- Persistent activation of the HPA system is associated hood because of the additional demands of physical with immune deficiency, cognitive impairment, and mental growth and development and possible inhibited growth, delayed sexual maturity, damage to long-term ontogenetic consequences. the hippocampus, and psychological maladjustment (Glaser and Kiecolt-Glaser, 1994; Dunn, 1995; McEwen, 1995; Ader et al., 2001). Chronic stress may Stress response mechanisms and theory diminish metabolic energy (Ivanovici and Wiebe, 1981; Physiological response to environmental stimuli per- Sapolsky, 1991) and produce complications from ceived as stressful is modulated by the limbic system autoimmune protection (Munck and Guyre, 1991). (amygdala and hippocampus) and basal ganglia. These Stressful life events – such as divorce, death of a components of the CNS interact with the sympathetic family member, change of residence, or loss of a job – and parasympathetic nervous systems and two neu- are associated with infectious disease and other roendocrine axes, the sympathetic-adrenal medullary health problems (Herbert and Cohen, 1993; Maier system (SAM) and the HPA. The SAM and HPA systems et al., 1994). affect a wide range of physiological functions in con- Current psychosocial stress research suggests that cert with other neuroendocrine mechanisms and cortisol response is stimulated by uncertainty that is involve complex feedback regulation. The SAM system perceived as significant and for which behavioral controls the catecholamines norepinephrine and epi- responses will have unknown effects (Weiner, 1992; nephrine (adrenalin). The HPA system regulates gluco- Kirschbaum and Hellhammer, 1994). That is, import- corticoids, primarily cortisol (for reviews, see Weiner, ant events are going to happen; the child does not 1992; McEwen, 1995; Sapolsky et al., 2000). know how to react but is highly motivated to figure Cortisol is a key hormone produced in response to out what should be done. Cortisol release is associated physical and psychosocial stressors (Mason, 1968; with unpredictable, uncontrollable events that require Selye, 1976). It is produced and stored in the adrenal full alert readiness and mental anticipation. In appro- cortex. Release into the plasma is primarily under the priate circumstances, temporary moderate increases in control of pituitary adrenocorticotropic hormone stress hormones (and associated neuropeptides) may (ACTH). The free or unbound portion of the circulating enhance mental activity for short periods in localized cortisol may pass through the cell membrane and bind areas, potentially improving cognitive processes for to a specific cytosolic glucocorticoid receptor. This responding to social challenges (Beylin and Shors, complex may induce genes coding for at least 26 differ- 2003; Lupien, 2009). Other mental processes may be ent enzymes involved with carbohydrate, fat, and inhibited, perhaps to reduce external and internal amino acid metabolism in brain, liver, muscle, and “noise” (Servan-Schreiber et al., 1990; cf. Newcomer adipose tissue (Yuwiler, 1982). et al., 1994). Cortisol modulates a wide range of somatic func- Relations between cortisol production and emo- tions, including: (1) energy release (e.g., stimulation of tional distress, however, are difficult to assess hepatic gluconeogenesis in concert with glucagon and because of temporal and interindividual variation in inhibition of the effects of insulin); (2) immune activity HPA response (Kagan, 1992; Nachmias et al., 1996). (e.g., regulation of inflammatory response and the Habituation may occur to repeated events for cytokine cascade); (3) mental activity (e.g., alertness, which a child acquires an effective mental model. memory, and learning); (4) growth (e.g., inhibition of Attenuation and below-normal levels of cortisol may growth hormone and somatomedins); and (5) repro- follow a day or more after emotionally charged events. ductive function (e.g., inhibition of gonadal steroids, Chronically stressed children may develop abnormal including testosterone). These complex multiple effects cortisol response, possibly via changes in binding of cortisol muddle understanding of its adaptive globulin levels and/or reduced affinity or density of

Evolutionary Biology of Hormonal Responses to Social Challenges in the Human Child 415 glucocorticoid or corticotrophin-releasing hormone (CRH)/vasopressin receptors in the brain (Fuchs and Flugge, 1995). Early experience – such as perinatal stimulation of rats (Meaney et al., 1991), prenatal stress of rhesus macaques (Schneider et al., 1992; 0.5 Clarke, 1993), and sexual abuse among humans (de Bellis et al., 1994) – may permanently alter HPA Cortisol (standardized) 0 response. Personality may also affect HPA response (and vice versa) because children with inhibited tem- peraments tend to have higher cortisol levels than –0.5 extroverted children (Kagan et al., 1988; cf. Gunnar Mom Single Grand- Single Distant Step- et al., 1995; Hertsgaard et al., 1995; Nachmias et al., and dad mom parents mom relatives family 1996). and kin Further complications arise from interaction Household compoistion between the HPA stress response and a wide variety 24.1. Cortisol levels and household composition of children of other neuroendocrine activities, including modula- living in Bwa Mawego, Dominica. Box and whisker plots are for tion of catecholamines, melatonin, testosterone, children’s mean values of cortisol standardized for time since serotonin, b-endorphins, cytokines, and enkephalins awakening (for descriptions of methods see Flinn 2006b). (de Kloet, 1991; Sapolsky, 1992; Saphier et al., 1994). Double lines represent average cortisol levels when an absence of stressful events were observed or reported. Stars indicate Changes in cortisol for energy allocation and modula- average cortisol levels during holidays (day before Christmas tion of immune function may be confused with and August holiday weekends). Data include 21 673 salivary effects of psychosocial stress. As reviewed in the previ- cortisol samples from 268 children collected from 1989–2001. ous section, OT and vasopressin intracerebral binding sites are associated with familial attachment in mammals and may influence distress involving effects of naturally occurring psychosocial events in caretaker–child relationships. Other components of the family environment. the HPA axis such as CRH and melanocyte-stimulating Associations between average cortisol levels of hormone have effects that are distinct from cortisol. children and household composition indicate that children living with nonrelatives, stepfathers, and half-siblings (stepfather has children by the stepchild’s Stress response and family environment mother), or single parents without kin support had Composition of the family or caretaking household higher average levels of cortisol than children living may have important effects on child development with both parents, single mothers with kin support, (Kagan, 1984; Whiting and Edwards, 1988). For or grandparents (Figure 24.1). Note, however, that example, in Western cultures, children with divorced these differences in cortisol levels are diminished when parents may experience more emotional tension or comparisons are made during nonstressed conditions “stress” than children living in a stable two-parent (double line bars in Figure 24.1). Moreover, the pattern family (Wallerstein, 1983; Pearlin and Turner, 1987; is reversed during the excitement of holidays and other Gottman and Katz, 1989). apparently hedonic emotional circumstances (stars in Investigation of physiological stress responses in Figure 24.1). Hence cortisol appears to be elevated the human family environment has been hampered during “positive” as well as “negative” social by the lack of noninvasive techniques for measurement challenges. of stress hormones. Frequent collection of plasma A further test of the hypothesis that difficult family samples to assess temporal changes in endocrine func- environments are stressful is provided by comparison tion is not feasible in nonclinical settings. The develop- of step- and genetic children residing in the same ment of saliva immunoassay techniques, however, households. Stepchildren had higher average cortisol presents new opportunities for stress research. Saliva levels than their half-siblings residing in the same is relatively easy to collect and store, especially household who were genetic offspring of both parents under adverse field conditions faced by anthropolo- (Figure 24.2). gists (Ellison, 1988). In this section I review results Several caveats need emphasis. Firstly, not all chil- from a longitudinal, 20-year study of child stress and dren in difficult family environments have elevated health in a rural community on the island of Dominica cortisol levels. Secondly, household composition is (for reviews see Flinn and England, 1995, 1997, 2003; not a uniform indicator of family environment. Flinn, 1999, 2006b). The research design uses concomi- Some single-mother households, for example, appear tant monitoring of a child’s daily activities, stress hor- more stable, affectionate, and supportive than some mones, and psychological conditions to investigate the two-parent households. Thirdly, children appear

416 Mark V. Flinn 1 whereas calm, affectionate contact was associated with diminished (–10% to –50%) cortisol levels. Of all cortisol values that were more than two standard Cortisol (standardized) 0 of substantial stress), 19.2% were temporally associ- deviations (2 SD) above mean levels (i.e., indicative ated with traumatic family events (residence change of child or parent/caretaker, punishment, “shame,” serious quarreling, and/or fighting) within a 24-hour period. In addition, 42.1% of traumatic family events were temporally associated with substantially elevated Genetic Step- –1 offspiring offspring cortisol (i.e., at least one of the saliva samples collected (N =25) (N = 27) within 24 hours was > 2 SD above mean levels). Chronic elevations of cortisol levels sometimes 24.2. Comparison of cortisol levels (standardized for time since awakening) of children (maternal half-siblings) living in the same occurred among children in difficult family environ- household that were either genetic offspring or step-offspring of ments, but this was difficult to assess quantitatively the resident adult male. (Flinn, 2009). There was considerable variability among children differentially sensitive to different aspects of their car- in cortisol response to family disturbances. Not all etaking environments, reflecting temperamental and individuals had detectable changes in cortisol levels other individual differences. associated with family trauma. Some children had These caveats, however, do not invalidate the significantly elevated cortisol levels during some epi- general association between household composition sodes of family trauma but not during others. Cortisol and childhood stress. There are several possible response is not a simple or uniform phenomenon. reasons underlying this result. Children in difficult Numerous factors, including preceding events, habitu- caretaking environments may experience chronic ation, specific individual histories, context, and tem- stress resulting in moderate-high levels of cortisol perament, might affect how children respond to (i.e., a child has cortisol levels that are above average particular situations. day after day). They may experience more acute stres- Nonetheless, traumatic family events were associ- sors that substantially raise cortisol for short periods ated with elevated cortisol levels for all ages of of time. They may experience more frequent stressful children more than any other factor that we exam- events (e.g., parental chastisement or marital quarrel- ined. These results suggest that family interactions ling – see Wilson et al., 1980; Flinn, 1988; Finkelhor were a critical psychosocial stressor in most children’s and Dzuiba-Leatherman, 1994) that temporarily raise lives, although the sample collection during periods cortisol. There may be a lack of reconciliation between of intense family interaction (early morning parent and child. And they may have inadequate and late afternoon) may have exaggerated this coping abilities, perhaps resulting from difficult association. experiences in early development. Although elevated cortisol levels are associated The events in children’s lives that are associated with traumatic events such as family conflict, long- with elevated cortisol are not always traumatic or term stress may result in diminished cortisol response. even “negative.” Activities such as eating meals, hard In some cases, chronically stressed children had physical work, routine competitive play (e.g., cricket, blunted response to physical activities that normally basketball, and “king of the mountain” on ocean evoked cortisol elevation. Comparison of cortisol rocks), return of a family member that was temporarily levels during “nonstressful” periods (no reported or absent (e.g., father returning from a job in town for observed crying, punishment, anxiety, residence the weekend), and holiday excitement (stars in change, family conflict, or health problem during Figure 24.1) were associated with temporary moderate 24-hour period before saliva collection) indicates a increases (from about 10% to 100%) in cortisol among striking reduction and, in some cases, reversal of the healthy children. These moderate stressors usually had family environment–stress association (see double bars rapid attenuation (<1 hour) of cortisol levels (some in Figure 24.1). Chronically stressed children some- stressors had characteristic temporal “signatures” of times had subnormal cortisol levels when they were cortisol level and duration). not in stressful situations. For example, cortisol levels High-stress events (cortisol increases from 100% to immediately after school (walking home from school) 2000%), however, most commonly involved trauma and during noncompetitive play were lower among from family conflict or change (Flinn et al., 1996; Flinn some chronically stressed children (cf. Long et al., and England, 2003). Punishment, quarreling, and resi- 1993). Some chronically stressed children appeared dence change substantially increased cortisol levels, socially “tough” or withdrawn and exhibited little

Evolutionary Biology of Hormonal Responses to Social Challenges in the Human Child 417 or no arousal to the novelty of the first few days of the critical selective pressure. In Bwa Mawego, and saliva collection procedure. perhaps in most human societies, children elevate their Relations between family environment and cortisol stress hormone (cortisol) levels more frequently and stress response appear to result from a combination extensively in response to psychosocial stimuli than of factors including frequency of traumatic events, to challenges associated with the physical environ- frequency of positive “affectionate” interactions, fre- ment. The adaptive effects of the major stress hor- quency of negative interactions such as irrational pun- mones (Huether, 1996, 1998; Koolhaas et al., 2006; ishment, frequency of residence change, security of Fox et al., 2007) and affiliative neurotransmitters on “attachment,” development of coping abilities, and neural reorganization appear consistent with observa- availability or intensity of caretaking attention. tions of sensitivity to the social world (Flinn, 2006b). Probably the most important correlate of household Social competence is extraordinarily difficult composition that affects childhood stress is maternal because the competition is constantly changing care. Mothers in socially “secure” households (i.e., per- and similarly equipped with ToM and other cognitive manent amiable coresidence with mate and/or abilities. The sensitivity of the stress-response and other kin) appeared more able and more motivated affiliative systems to the social environment may to provide physical, social, and psychological care for enable adaptive neural reorganization to this most their children. Mothers without mate or kin support salient and dynamic puzzle. Childhood appears neces- were likely to exert effort attracting potential mates sary and useful for acquiring the information and and may have viewed dependent children as impedi- practice to build and refine the mental algorithms ments to this. Hence coresidence of father may provide critical for negotiating the social coalitions that not only direct benefits from paternal care but also are the key to success in our species. The human may affect maternal care (Lamb et al., 1987; Belsky family provides critical support for the child to develop et al., 1991; Flinn, 1992; Hurtado and Hill, 1992). sociocognitive skills. Traumatic early environments Young mothers without mate support usually relied may result in diminished abilities to acquire social extensively on their parents or other kin for help with competencies as a consequence of glucocorticoid child care. hypersensitivity disrupting neurogenesis, particularly Children born and raised in household environ- in the hippocampus and other components of the ments in which mothers have little or no mate or limbic system (Mirescu et al., 2004; Weaver et al., kin support were at greatest risk for abnormal cortisol 2004). An improved understanding of the hormonal profiles and associated health problems. Because and neurological mechanisms that facilitate the inten- socioeconomic conditions influence family environ- sive and extensive relationships involved with ment, they have consequences for child health that human families and broader kin coalitions, including extend beyond direct material effects. Also, because comparisons between humans and our close primate health in turn may affect an individual’s social and relatives, may provide important insights into the economic opportunities, a cycle of poor health and selective pressures that shaped key features of human poverty may be perpetuated generation after biology. generation. DISCUSSION POINTS CONCLUDING REMARKS 1. What happened to our hominin ancestors? People in difficult or inequitable social environments Why are we the only species left? If humans sud- tend to be less healthy in comparison with their more denly went extinct, would another life form even- fortunate peers (e.g., Flinn, 1999; Hertzman, 1999; tually evolve high intelligence? How? Dressler and Bindon, 2000; Wilkinson, 2001; Cohen 2. Do you think chimpanzee fathers love their off- et al., 2003;). Social support can have reproductive spring? Why or why not? And chimpanzee consequences in group-living species (e.g., Silk et al., grandparents? 2003; Cheney and Seyfarth, 2007). If the brain evolved 3. Do school exams make you sick? Collect data from as a social tool, then the expenditure of somatic your classmates to test your hypotheses. resources (e.g., glucose) to resolve psychosocial prob- 4. What events cause you to become “stressed”? Why lems makes sense. Relationships, especially family do you think natural selection produced psycho- relationships, are of paramount importance. They are logical mechanisms that result in this sensitivity? likely to have been a key factor affecting human repro- 5. How are the events that cause stress for you similar ductive success at least for over half a million years, and/or different from the events that were stressful and selection may have shaped our hormonal, neural, for your parents, your grandparents, and your dis- and psychological mechanisms to respond to this tant hominin ancestors?

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25 Human Biology, Energetics, and the Human Brain Benjamin C. Campbell INTRODUCTION of behavior, the brain seems to have an almost infin- itely flexible phenotypic expression. In contrast, the Human biology has made great progress in applying standard methods of human biology focus on the modern techniques to the understanding of human measurement of relatively simple phenotypes such as biological variation at the genetic, physiological, devel- the size and shape of anatomical features and variation opmental, and phenotypic levels. For instance, rather in their developmental timing. These can be easily than only asking about disease symptoms, human quantified using methods suitable for the field and biologists measure immune makers which represent compared across populations. an underlying element of health (McDade et al., 2005; However, in terms of the brain, simple and robust Muehlenbein et al., 2005; Snodgrass et al., 2007); phenotypes are hard to come by. Measures of brain rather than simply measuring body fat, they determine size and shape are not accessible in the samples of leptin levels as a signal of energy stores (Bribiescas, living human beings favored by human biologists, even 2005). In addition to collecting self-reports of stress, if we knew how to interpret them. On the other hand, they assay for salivary cortisol (Pike and Williams, proxy measures such as skull size and shape are emi- 2006; Nepomnaschy et al., 2006). Along with collecting nently measurable, but variation across human popu- reproductive histories, they measure gonadal steroids lations reflect climatic variation, not brain function including estrogen, progesterone (Lipson and Ellison, (Beals et al., 1984). 1996), and testosterone (Campbell et al., 2006). Thus some other simple and robust metric for At the same time, human biologists have also measuring brain function is necessary. An energetic become more evolutionarily sophisticated as they have approach has at least two advantages. Firstly, the brain adopted a life history perspective (Hill, 1993; Kuzawa, is energetically expensive with 2% of body mass using 2007). There is a growing understanding that much of 20% of energy among humans (Elia, 1992), increasing the variation in the phases of the life cycle, starting in the probability of selection based on energetic con- utero, and moving through childhood, adolescence, straints. These include trade-offs within the brain itself adulthood, and aging represents an inter-related as well as somatic maintenance and growth as outlined response to energetic availability. The impact of nutri- by life history theory. Secondly, an energetic perspec- tion during fetal development, in particular may have tive is consistent with an emerging focus on energetics important implications for the rest of the life cycle in human evolution more generally (Ailleo and (Jasienska et al., 2006; Kuzawa, 2007). Furthermore, Wheeler, 1995; Leonard and Ulijaszek, 2002; Leonard the understanding that growth and development, et al., 2007). immune function, and reproductive function are In what follows I attempt to provide a sufficient responsive to energetics means that human biologists outline of human brain metabolism, including energy can use energy as a currency through which the basic utilization, storage, and substrate availability, and its functions of growth, maintenance, and reproduction association with brain development to be able to con- can be traded off (Hill, 1993). sider its implications for human evolution. In the first Yet human biologists have tended to avoid studying part of the paper, I set the stage with a brief review of the brain (see Leonard et al., 2003, 2007 for an excep- earlier work on brain metabolism and evolution. I then tion). Such shyness surely reflects the Cartesian review recent advances in assessing energy utilization dichotomy, in which the mind and body are fundamen- in the brain which highlight the intrinsic and intimate tally different spheres and hence must be studied using interplay between energetic utilization and neuronal different techniques. At the same time, it may also function. I argue that the elevated energetic costs of reflect the shear complexity of the brain. As the organ the human brain are balanced against the benefit Human Evolutionary Biology, ed. Michael P. Muehlenbein. Published by Cambridge University Press. # Cambridge University Press 2010. 425

426 Benjamin C. Campbell of increased neuroplasticity. I suggest that glucose OVERVIEW OF ENERGETICS utilization in the human brain is directly tied to synap- AND THE BRAIN tic plasticity through a process referred to as glutamate cycling, and that a high glutamate flux is important in It is well known to human biologists that the brain is to human neuroplasticity. an energetically expensive organ, consuming 20% of In the second part of the paper I review the recent the body’s energy, despite being only 2% of the body’s literature showing changes in the energetic utilization weight (Elia, 1992). But this figure only superficially of the human brain during development. I argue that reflects how pervasive the effects of energetic factors changes in energy utilization in the developing brain are in brain function. The brain depends almost are closely tied to on-going processes of brain develop- entirely on glucose as a metabolic fuel (Van Itallie ment. More specifically, I suggest that age-related and Nufert, 2003) and accounts for 50% of total body changes in glucose utilization (Chugani, 1998) are con- glucose utilization (Fehm et al., 2006). Furthermore, sistent with development patterns of neuroplasticity, brain structures such as the hippocampus and amyg- social context, and behavioral development in humans. dala known for their role in basic functions of memory I hope to show that rather than representing a release and emotional regulation are also important in regula- from energetic constraints, the development of the tion of somatic energy use and food intake (Fehm et al., human brain becomes a focal point for the selective 2006). Thus, brain activity is only tied to energy con- power of energetic constraints during evolution. sumption, but with regulating its own energy status (Peters et al., 2004). In order to understand the role of metabolism in HISTORICAL BACKGROUND brain function, it is useful to first characterize the brain on a more global level. Neurobiologists list Early interest in human brain metabolism and evolu- several qualities of the brain that may be important. tion grew out of attempts to understand the basis for These include: (1) the brain is very plastic, i.e., the allometric relationship between brain and body capable of changing; (2) it has little storage, i.e., across mammals (Martin, 1981; Armstrong, 1983, there is little evidence for glycogen storage in 1985). When the scaling coefficient of brain to body neurons; (3) is substrate specific, i.e., it will only size was thought to be around 0.67, it was suggested to metabolize glucose; (4) is separated from the body reflect the relationship between neural sensory input/ by the blood–brain barrier reducing its exposure to output function and body surface area. However, Arm- the general circulation (Peters et al., 2004). To these strong (1983) demonstrated that variation in brain size I would add: (5) the brain is energetically demanding across mammals is related to the relative amount of (Armstrong, 1985; Fehm et al., 2006), i.e., it is always energy utilized by the brain, i.e., its scales with the active and can not survive long if its energy supply amount of energy reserves (Armstrong, 1985), clearly is interrupted. suggesting the important of metabolism in brain evo- Brain function is a metabolically dynamic process, lution. Interestingly Crile (1941) had anticipated the with specific brain activity dependent on increased importance of metabolism in brain evolution and energy utilization (Shulman et al., 2004). Neural plas- argued that the importance of basal metabolism to ticity, the alteration of neural connections based on brain size must have coevolved with the thyroid experience, enhances the ability of the brain to adapt function. to the environmental by directing that energy toward When other analyses indicated that the scaling the most commonly used neuronal pathways and coefficient was closer to 0.75, than 0.67, arguments neural circuits. In contrast, the other four qualities about body surface area no longer made sense. Instead, listed above; energetically demanding, little storage, Martin (1981) suggested that the underlying relation- substrate specificity, and the blood–brain barrier, all ship might reflect constraints on maternal metabolic act to limit the physiological range in which the brain investment in fetal brain development. More specific- can operate. Thus the trade-off between energy and ally, in terms of human evolution, Martin (1989) has brain function in humans can been seen as a basic argued that australopithecines demonstrate increased function of energy utilization and the maintenance of brain to body size ratios relative to the great apes. He neural plasticity. then suggests that a reduction in gut along with an The cellular basis of both energy utilization increase in high quality food would have been neces- and neural plasticity has come into clearer focus sary to allow for the increased the energetic demands in recent years. Though still controversial (Pellerin of the brain. It is this idea that was taken up by Aiello et al., 2007), recent findings have been taken to and Wheeler (1995) and dubbed the “expensive tissue suggest a metabolic cycle between astrocytes and hypothesis.” In what follows I explore in more detail neurons in which glucose is used by astrocytes why the brain is expensive tissue. to convert glutamate to glutamine. In the process

Human Biology, Energetics, and the Human Brain 427 glucose is transformed into lactate which is ENERGY CONSUMPTION AND consumed by neurons (Magistretti, 2006). This tight BRAIN ACTIVITY metabolic coupling of neurons and astrocytes, referred to as the astrocyte-lactate neuronal shuttle Before considering the implications of specific appears central to understanding brain plasticity. aspects of energy metabolism for brain function, it Glutamate is critical to neuronal plasticity and its is important to outline the processes that contribute association with glucose directly links energetic pro- to the total energetic costs of the brain. The develop- cesses and neural plasticity throughout the lifecycle ment of functional magnetic resonance imaging (Magistretti, 2006). In fact, Ulian et al. (2004) have (fMRI) has focused attention on energy utilization suggested that astrocytes should be understood as during the activation of particular brain regions regulators of synaptic plasticity. (Shulman et al., 2004). However, such functional Furthermore, it is now clear on the basis of both activation appears to represent a remarkably small animal models (Gruetter, 2003; Brown, 2004) and fraction of the total energy consumed by the adult human studies (Oz et al., 2007) that the brain does in human brain (Raichle and Mintun, 2006). Based fact have important glycogen stores, albeit at much on both glucose and blood utilization studies it is lower levels than found in other tissues such as muscle. estimated that activation of neuronal processes Such stores appear to vary across regions of the brain accounts for some 1% of energy utilization in the and are most abundant in more metabolically active brain (Raichle and Mintum, 2006), the other 99% parts of the brain such as the hippocampus (Dalsgaard of the brain energy consumption is related to base- et al., 2007). Thus glycogen is more likely to represent a line or “resting” activity levels. Only 15% of total local energy buffer during normal use (Brown, 2004; brain energy consumption is thought to be related Brown and Ransom, 2007) than storage against patho- to the maintenance of resting action potentials logical conditions such as global ischemia, as previ- and glial cell activity (Attwell and Laughlin, 2001), ously assumed. leaving approximately 80% of brain energy consu- While the blood–brain barrier remains an mption devoted to something else (Raichle and important reality and glucose is the major energy Gusnard, 2002). source transported across the blood–brain barrier That something else has been referred to as (Peters et al., 2004), other substrates such as intrinsic brain activity (Raichle and Mintum, 2006). ketones and lactate can cross the blood–brain Intrinsic brain activity is not well defined, but is barrier (Emery, 2005), and may serve physiologically thought to represent a default brain system (Raichle important functions in addition to their role as et al., 2001) that is attenuated but not deactivated energy substrates. For instance, ketones appear to during a conscious task. Furthermore, this brain be important during early development when they system appears to show spontaneous cycles of energy are an important substrate in the production of usage suggesting it is dynamically active (Fox et al., lipids by oligodendrocytes (Edmond, 1992; Nehlig, 2005; Mantini et al., 2007). The function of such a 2004), including lipids associated with myeliniza- brain system may reflect stimulus independent tion, so important to early brain development. In thought (Mason et al., 2007 and may involve somatic another example, transport of lactate into the brain self-monitoring (Raichle et al., 2001) and the process- is particularly important during exercise (Dalsgaard, ing of episodic memory (Greicius et al., 2003; Greicius 2006), suggesting that the brain does not always and Menon, 2004). Similar brain activity appears have total priority for glucose utilization and physio- to occur during sleep, making intrinsic brain activity logical mechanisms other than glucose metabolism on-going and independent of wakefulness (Horovitz may play a role in adjusting the allocation of energy et al., 2007). between the brain and body. High levels of on-going brain activity suggest that Finally, there is growing evidence that the brain the energetic demands of the brain are both constant has cells that sense glucose (Rao et al., 2006) and and dynamic. I argue that such high energy utiliza- react accordingly, allocating energy to the brain tion and glucose dependence is directly related to depending on its needs. Peters et al. (2004) have synaptic plasticity at the cellular level, through the argued that because the brain has priority of alloca- process of glutamate cycling (Shulman et al., 2004; tion and controls other parts of the body, it is in Magistretti, 2006). Glutamate cycling appears to run control of its own energetic requirements. From a at a higher rate in the brain of humans and great life history perspective, such a “selfish brain” should apes relative to other primate relatives (Burki and include potential mechanisms for shifting allocation Kaessmann, 2004), thus allowing for higher local of energy to brain versus the body as the importance energy utilization and potentially greater neural plas- of the brain relative to reproduction shifts over the ticity. I elaborate the physiological details of this life course. argument below.

428 Benjamin C. Campbell The astrocycte-neuron-lactate shuttle The basis for the development of new synapses is not fully understood. However, N-methyl-D-aspartate Recent work has suggested that most neurons do not (NMDA) receptors appear to be involved. In the case of metabolize glucose directly, but obtain their energy dopaminergic neurons, NMDA receptors are important through an interaction with surrounding glial cells, a in trapping D 1 dopamine receptors into synapses process referred to as the astrocyte-neuron-lactate (Scott et al., 2002), thus creating a dopaminergic syn- shuttle (Bittar et al., 1996; Pellerin et al., 1998). As part apse. Since NMDA is a glutamate receptor, increased of this cycle, glutamate released into the synapse is glutamate flux may act to promote the stabilization of taken up by a glutamate transporter (EAAT2) and dendritic dopaminergic synapses. In addition, NMDA brought into astrocytes surrounding the synapse. receptors are thought to be particularly important There glucose is used to convert glutamate to glutam- in the growth of dendritic spine during long-term ine through the act of glutamine synthetase (Daikhan potentiation (LTP) (Park et al., 2006), a basic neural and Yudkoff, 2000). The glutamine produced in the mechanism underlying learning. astrocyte is then taken up by the neuron. In the Regardless of the exact cellular mechanisms invol- process, lactate is created within the astrocyte which ved in neural plasticity, it is clear that glutamate is later taken up by the neuron and used to reconvert cycling is very important in terms of brain energetics. the glutamine to glutamate for release in the synapse Ninety percent of synapses release glutamate (Abeles, (Magistretti, 2006). In addition to glutamate, a small 1991; Braitenberg and Schuz, 1998), a figure that fraction of the glutamine is converted into gamma- reflects the corelease of neurotransmitters by individ- butyric acid (GABA) the major inhibitory transmitter ual neurons (Trudeau and Gutie ´rrez, 2007). Eighty in the brain (Patel et al., 2005). percent of the utilization of glucose is linearly related As mentioned previously, the function of glutamate to glutamate cycling (Sibson et al., 1998; Shen et al., cycling has not been fully established, though it is been 1999). In addition, it has been estimated that about suggested as the basis for neural plasticity (Magistretti, 20% of the energy consumed by glutamate cycling is 2006). It is generally thought that a build up of glutam- used in the production of GABA (Patel et al., 2005), ate from the synapse into the extracellular space giving this neurotransmitter a smaller, but still poten- decreases the signal-to-noise ratio in the synapse and tially important, role in the relationship between at extreme levels can lead to axonal depolarization and energy consumption and brain function. the death of neurons. By removing glutamate from the The importance of glutamate in human brain synapse and metabolizing it within the astrocyte metabolism is illustrated by the recent discovery of a neurons are less susceptible to glutamate excitotoxicity, hominoid specific version of the glutamate dehydro- allowing for increased strengthening of synaptic con- genase gene (GLUD). GLUD2 is a variant of GLUD nections on the basis of neuronal firing and experience. found only in humans and the great apes (Burki and Rocher et al. (2003) show that levels of snyap- Kaessman, 2004) resulting in an increased capacity to tophysin, a marker of synaptic density, are related to oxidize glutamate under low oxygen conditions (Plai- regional glucose utilization in baboons, supporting the takis et al., 2003), indicative of increased glutamate idea that glucose metabolism is associated with neural turnover. Since neural plasticity is based on the connectivity. Thus the high rate of glucose utilization maintenance of synaptic connections, increased glu- of the human brain may translate directly into the tamate cycling among both humans and the great apes benefits of synaptic plasticity. may be associated with a greater capacity for neural At the cellular level, synaptic plasticity is known to plasticity than other primates. be associated with the growth and development of dendrites and dendritic spines (Calabrese et al., 2006). A greater proliferation of dendrites allows more Energetics in specific parts of the brain room for dendritic spines. Since many synapses form on dendrite spines, more dendrites spines allow for Given that 90% of all neurons express glutamate, more synapses as well. However, it is only recently that glutamate cycling can be expected to play a role in the dynamic nature of dendritic spine development has maintaining neural plasticity throughout the brain. become clear. Small filaments on the dendrites emerge However, given its association with glucose utilization, and start to grow to larger filaments (Ziv and Smith, the impact of glutamate cycling may particularly 1996). Some of these larger filaments appear to persist apparent in more metabolically active parts of the and take the form of dendritic spines (Goda and Davis, brain, such as the hippocampus. 2003). If stabilized these spines then become synapses The existence of high levels of glycogen stores (Calabrese et al., 2006). Small filaments that do not (Pellegri et al., 1996) in the hippocampus is consistent become large filaments presumably die off, forming with a high local energy flux. Furthermore, in humans, an ongoing cycle of production, growth, and loss. there is a substantial literature demonstrating that

Human Biology, Energetics, and the Human Brain 429 glucose ingestion improves performance on memory- hypoglycemia within local areas of the brain is a dependent, but not other, cognitive tasks (Meikle et al., potential outcome of reduced glucose availability. 2004; Riby et al., 2006), a finding that is thought to Given the high demand for glucose throughout the reflect the effects of glucose on hippocampal function. brain hypoglycemia could occur on a very short time In terms of neuroplasticity, Segovia et al. (2006) scale. Thus the intensity of short-term activity of report that environmental enrichment has an impact specific regions of the brain may be directly related to on the hippocampus through elevated levels of glutam- local glycogen availability. ate. In a sample of rats, environmental enrichment In the only human study to date, Oz et al., (2007) promoted both neurogenesis and increased levels of report that total glycogen stores represent three to four glutamate and GABA in the CA3 area of the hippocam- times the energy equivalents from glucose in brain pus. While this finding is intriguing more research circulation, suggesting that in terms of normal func- is needed to confirm a role for glutamate cycling in tion glycogen stores are in fact rather substantial, and hippocampal function. may play a key role in brain metabolism. On the other In addition to the hippocampus, the anterior hand, Oz et al. (2007) also report negligible consump- cingulate cortex may also be particularly metabolically tion of glycogen from neurons in the visual cortex active as part of its role in executive function (Posner during a 20 minute visual task, suggesting that glyco- and Rothbart, 1998), the default brain network gen stores may not be important in the course of (Margulies et al., 2007) and as a way station between normal brain activation and or function. emotion and cognition (Allman et al., 2001). Even In contrast, animal models indicate that glycogen is when the brain is not engaged in a focused task, the depleted under hypoglycemic conditions (Gruetter, anterior cingulate cortex may be active in maintaining 2003; Brown, 2004). Furthermore, during brain acti- generalized attention to both external and internal vation oxygen consumption does not initially increase, signals. Recent work in humans has linked glutamate which has been taken to indicate that other sources of levels in the anterior cingulate cortex and hippocam- energy, i.e., glycogen are being utilized rather than pus to sensation-seeking (Gallinat et al., 2007), consist- direct oxidation of glucose (Raichle and Mintun, ent with an important role for glutamate cycling in 2006). It is estimated that during brain activation in these two brain structures. Again more research is the rat glycogen stores are depleted by about 15%, needed to determine if glutamate cycling is associated suggesting that glycogen stores within astrocytes are with higher glucose consumption in the anterior used to support the initial costs of brain activation cingulate cortex. (Schurr et al., 1999; Shulman et al., 2001). Furthermore, the more metabolically active parts of the brain have higher levels of glycogen storage and ENERGY STORAGE deplete those stores faster than less metabolically active regions (Brown, 2004). For instance, mouse It was once thought that the brain had practically no cerebral cortex has a higher glycogen content than do energy storage leaving it critically and globally depend- deeper layers (Folbergrova ´ et al., 1970) and the dentate ent on an immediate supply of blood glucose. However, gyrus of the hippocampus, the only area with active recent research has emphasized the existence of neurogenesis, has twice the glycogen content of the glycogen stores throughout the brain (Gruetter 2003; rest of the hippocampus (Lipton, 1989). These findings Brown, 2004). The primary storage of glycogen is in clearly suggest that glycogen stores act as an active astrocytes (Phelps, 1972), though some may be stored buffer against glucose utilization during regional brain in neurons (Brown, 2004). Glycogen stores in the brain metabolism. had been previously overlooked largely because of their low levels. At 0.1% of total brain weight (Brown, 2004) Energy storage and sleep they are much lower than those of other tissues, for instance 20 times lower than that found in muscle Sleep, with its drastic behavioral inhibition, provides (Oz et al., 2007). one way of considering the role of energy metabolism, It is widely thought that glycogen stores are suffi- including that of glycogen, in brain function (Brown, cient to support brain function for only a few minutes 2004). Among humans, overall brain energy consump- (Clarke and Sokoloff, 1999). More recent work has tion as measured by oxygen uptake has been estimated extended that estimate to 100 minutes (Gruetter, to a decrease by 3–11% during light sleep, and by 2003). This is rather surprising given the sensitivity of 25–44% during slow wave sleep, but very little during the brain to hypoxia and suggests that ultimately the REM sleep (Madsen and Virstrup, 1991; Madsen et al., limiting factor in brain function is not energy but 1991). The lack of decline during REM sleep empha- oxygen. Global brain oxygen depletion, however, sizes that the brain is in fact metabolically active, is not a normal condition. On the other hand, rather than quiescent, during dreaming.

430 Benjamin C. Campbell Detailed studies in rats suggest that glycogen the brain can not run on lactate by itself, the utilization synthesis is dramatically increased during slow wave of lactate by neurons suggests that lactate can be sub- sleep relative to waking (Karnovsky et al., 1983). stituted for glucose to sustain neurons in the short Furthermore, sleep deprivation leads to a decrease in term. Such substitution is potentially important since glycogen in the frontal cortex of rats (Djuricic et al., lactate is a by-product of other energy processes in the 1977; Kong et al., 2002; though see Gip et al., 2002). body. This has lead to the suggestion that the function In fact, during vigorous exercise global brain of sleep may be the replenishment of glycogen glucose uptake declines, while the uptake of lactate by (Bennington and Heller, 1995). the brain increases, in inverse proportion (Kemppai- More recent work demonstrating variation in nen et al., 2005). At the same time lactate levels in the glycogen content in response to sleep deprivation in brain do not increase, suggesting utilization of lactate different strains of mice have been taken to suggest in neurons (Dalsgaard et al., 2004). The brain appears that accumulation of glycogen is not the primary func- to utilize lactate produced by somatic effort to directly tion of sleep (Franken et al., 2003). However, to the fuel the metabolism of neurons, by-passing the conver- extent that glycogen represents a short-term buffer sion of glucose or glycogen within astrocyctes. Further- against increased energy demands of neuronal activity, more, glycogen stores increase during recovery from interference with glycogen metabolism may be an exercise (Dalsgaard, 2006), leading to the conclusion important intermediate in explaining the impact of that they are depleted with the onset of neural activity sleep disruption on brain function (McEwen, 2006), associated with exercise, but not afterwards. Thus it and ultimately the function of sleep. appears that during strenuous exercise, glucose may be preferentially allocated to somatic energy uses over those of the brain, which is forced to deplete glycogen SUBSTRATE SPECIFICITY stores and utilize somatic metabolic wastes for its energetic requirements. As noted earlier, the brain was long considered to be Such reallocation of energy substrates may have entirely dependent on glucose as a fuel. From an evolu- important implications human brain evolution. Based tionary perspective, such dependence suggests that on anatomical features, humans have been argued to glucose metabolism may have been an important have adopted endurance running as basic strategy for limiting factor in the evolution of the large human hunting (Bramble and Lieberman, 2005; Lieberman brain. While glucose can be produced from protein in and Bramble, 2007) and hence energy acquisition. If the liver by the process of gluconeogenesis, the process so, running in the tropical heat would have placed is rather slow and glucose is most easily derived from additional energy demands on both the brain and the the consumption of carbohydrates. As has been argued body. Increased use of lactate from muscle would for polyunsaturated fatty acids (PUFAs) (Broadhurst decrease the need for the immediate metabolism of et al., 2002, though see Carlson and Kingston, 2007 glucose, increasing the duration of exercise possible for an opposing perspective) or protein (Kennedy, without endangering brain function, and linking the 2005) the availability of carbohydrates could have been potential for increased brain size with the success of an important constraint in the evolution of the human endurance running as part of a subsistence strategy. brain. Thus consumption of underground storage organs, with relatively high starch composition, might have played a role in the evolution of the human brain BRAIN DEVELOPMENT (Yeakel et al., 2007). However, in addition to glucose, the brain can also In the first part of this paper I argued that the energet- utilize ketones for fuel, and ketones have long been ics of the human brain could be seen as a trade-off considered a back-up supply in the case of starvation between the constraints of energetic cost, demand, when glucose is in short supply (Emery, 2005). While substrate specificity, and blood–brain barrier versus peripheral fat produces fatty acids which can be util- the benefits of neuroplasticity. Such trade-offs will be ized by muscle, ketones are produced from abdominal present at all times, but may be particularly evident fat suggesting that the development of a substantial during conditions of high energy demand such as high abdominal fat depot in human may be an important activity levels. Brain development is another, more buffer for the human brain (Peters et al., 2004). This extended, period of elevated brain energy utilization. may be particularly important in infants (Kuzawa, Thus the trade-off between energy and neuroplasticity 1998; Cunnane and Crawford, 2003). should be evident during the development of the The discovery of the neuronal-lactate shuttle sug- human brain as well. gests the possibility of a more finely tuned facultative At the broadest level, the overall energetic cost of use of alternative substrates by the human brain. While brain development may be subsidized by additional

Human Biology, Energetics, and the Human Brain 431 somatic energy stores or traded-off against somatic low from one to two months to two years (Lauriat growth and development by temporally offsetting et al., 2007). Together reduced glucose availability periods of elevated brain and somatic energy utiliza- and low levels of EAAT2 may leave the infant brain tion. For instance, the high level of adiposity seen in particularly susceptible to glutamate excitoxicity, as human infants has been argued to represent energy suggested by the relatively high rate of seizures during stores put on in utero to support continued brain this period (Lauriat et al., 2007). growth for the first year postnatally (Kuzawa, 1998; During infancy it is thought that experience plays Cunnane and Crawford, 2003). Similarly, very slow a key role in the development of fundamental emotional growth during human childhood (Bogin, 1999) may circuits in the brain. Alan Schore (1994, 1997, 2002) has be a reduction of somatic energy costs in favor of suggested that negative affect associated with trauma brain development and neuroplasticity during a period and neglect during the first two years of life results in a of high brain metabolism from 4 to 10 years of age hypermetabolic state of arousal, including elevated (Chugani, 1998). cortisol levels and the activation of the sympathetic In addition to overall energy consumption, the nervous system. Schore suggests that if sufficiently specific substrates which the brain uses to meet its prolonged, such arousal may lead to elevated levels of energy requirements change during development. For glutamate and resulting excitoxicity, particularly in instance, despite the importance of glucose to brain the orbitofrontal cortex, anterior cingulate cortex, function, it is well known that infants utilize ketones and amygdale, which are developing during this period. and lactate as fuel, thus potentially sparing glucose for Glutamate exotoxic shaping of emotional circuits other functions (Nehlig, 2004). However, the capacity appears to reflect a close association of nutrition and of the brain to metabolize ketones declines as the child emotional conditions during infancy. Schore’s argu- grows, leading to an increasing demand for glucose. In ment is focused early childhood trauma and neglect what follows we consider brain development and its and its effects on the development of psychopathology. implications for the allocation of energy to the brain But such an argument is applicable to infant brain and body starting with infancy. development under conditions of nutritional as well as emotional stress. Given the potentially low levels of glucose availability during infancy, as well as the risk Infant brain development of infectious disease in traditional societies, many Brain metabolism is estimated to represent some infants may exist in a state of metabolic brain arousal, 50–80% of the energy budget of the human infant leading to glutamate excitoxicity during periods of (Holliday, 1986). This reflects the large size of the acute undernutrition. In support of this, acute under- brain relative to the body, as well as rapid brain nutrition during infancy has been associated with cere- growth during the first two years of life (Leigh, bral atrophy (Hazin et al., 2007) and disruption of 2004), a period of extensive synaptogenesis and high dendrite development (Benitez-Bribiesca et al., 1999). levels of synaptic density, as well as the myelinization Thus it has been suggested that the rather remark- of major nerve tracts (Carmondy et al., 2004). In add- able degree of adiposity exhibited by human infants ition, the hippocampus and amgydala are developing may represent a metabolic buffer for brain develop- during this period. ment (Kuzawa, 1998; Cunnane and Crawford, 2003). It is important to note that breast milk, the primary Adipose tissue itself can not be metabolized by the food in early infancy is rich in lipids, but a relatively brain. However, the visceral component of adiposity poor source of glucose. However, lactate and ketone can be metabolized to produce ketones for the brain, bodies, not glucose appear to be important energy sub- which are an important source of energy and myleni- strates for the brain during this period (Edmond, 1992; zation for the infant brain as outlined above. On the Nehlig, 2004; Medina and Tabernero, 2005). In particu- other hand, subcutaneous fat stores may be used to lar, ketones can be used by oligodendryctes to make support the energetic requirements of the immune the lipids that are part of myelin, sparing glucose for system during infancy, which would free up glucose other pathways (Nehlig 2004). In addition, ketones to be used by the brain (Kuzawa, 1998). appear to shunt glutamine toward the production of GABA rather than glutamate (Melø et al., 2006), thus Childhood brain development potentially reducing the risk of glutamate excitoxicity. In fact, glucose may be in relatively short supply in Important changes in human brain metabolism are the infant brain. Glucose utilization rates during evident around the age of three to four years, when infancy start relatively low, reaching adult levels by glucose utilization rates reach their peak, at about around the age of two years (Chugani, 1998). Further- twice the level observed in adults (Chugani, 1998). more, levels of EAAT2, the transporter that removes The executive attention system, which integrates atten- glutamate from the synapse to astrocytes are relatively tion and executive function, is undergoing rapid

432 Benjamin C. Campbell development between three and seven years of age In fact, the energetic demands of brain develop- (Posner, 2005), including the development of the thal- ment may be quite a bit higher than usually calculated, amus, the parietal lobe, the orbitofrontal cortex, and since they include the costs of physical activity critical the anterior cingulate cortex. Thus the early increase in to brain development as well as the metabolic costs of glucose utilization may be directly related to the brain tissue. For instance, it has been calculated that growth and development to these parts of the brain. 17% of the total energy budget for children six years of Glucose utilization rates, however, remain elevated age is consumed by physical activity (Dufour, 1997). until around the age of 11 when they begin to decline to Much of the physical activity during childhood clearly adult rates (Chugani, 1998). Brain growth is 95% com- serves multiple purposes and can not be attributed plete by the age of 7 (Caviness et al., 1996), suggesting solely to a specific function. However, the costs of that the high rate of glucose utilization after the age of physical activity, which helps shape brain development 7 is not a function of increasing brain size. Instead, the and promotes learning through the release of brain- high glucose demand of the brain during this period is derived neurotrophic factor (BDNF) (Winter et al., presumably related to enhanced synaptic plasticity 2007), must be taken into account in calculating the (Chugani, 1998), which I have argued is maintained full energetic cost of brain development. by the energetic costs of glutamate cycling. In fact, the juvenile period is associated with Adolescence synaptic pruning, i.e., the loss of established neuronal connections, a process known to continue in adoles- Compared to childhood, during which elevated glucose cence (Huttenlocker, 1984; Huttenlocker and Dab- utilization rates suggest a dynamic process of synaptic holkar, 1997). Such pruning is based on experience; formation and pruning, adolescence is thought to be neuronal connections that are used are strengthened associated with the pruning of synaptic connections and those that are not are lost. Recent studies indicat- (Huttenlocker and Dabholkar, 1997, Gogtay et al., ing cortical maturation associated with declines in 2004). If I am correct, such synaptic pruning is associ- gray matter starting around the age of six (Gogtay ated with reduction of glucose-fueled glutamate et al., 2004) are consistent with the decreased number cycling and reflected in declining rates of cerebral glu- of synaptic connections during this period. cose utilization throughout the brain. In fact, there Thus, the age pattern of glucose utilization rates is does appear to a loss of generalized neuroplasticity, suggestive of an important shift in brain function as indicated by declining language acquisition ability, during childhood linking social context, nutrition, around the age of 12 (Sakai, 2005), roughly the same and behavior. The onset of peak levels at three to four time that that glucose utilization rates start to decline. years of age is roughly coincident with the natural end However, localized synaptic plasticity may be main- of lactation (Martin, 2007). Weaning represents a tained, particularly in the prefrontal cortex, still matur- switch away from breast milk to other sources of food ing through out adolescence (Sowell et al., 1999; that are generally higher in carbohydrate content and Gogtay et al., 2004). may provide a greater source of glucose for the brain. In addition to declining brain plasticity, the puber- In addition, weaning marks a change in the child’s tal drop in glucose utilization by the brain appears to social environment as well, as children start to spend reflect an increased allocation of energy to somatic increasing time in play with sibling and other children, growth associated with the pubertal growth spurt. The and less time in such close proximity with their onset of puberty has been linked to abdominal fat stores mother. In other words, children between the ages of in both boys and girls (Vizmanos and Marti-Henneberg, approximately 4–11 years of age soak up an increasing 2000), the same fat stores that are thought to serve as a variety of environmental influences, all of which may reserve source of ketones for the brain (Peters et al., promote the development of synaptic connections 2004), potentially placing reproductive maturation with relatively little additional reinforcement. and brain development in direct energetic competition. The period from 4–11 years of age, roughly the Boys appear to utilize prepubertal adipose storage period between weaning and puberty, is also a period as the basis for increased size and muscularity in asso- of very slow and decreasing somatic growth (Bogin, ciation with increased testosterone production (Camp- 1999). It has been argued that somatic growth is sup- bell and Mbzivo, 2006). Behaviorally these changes are pressed during this stage to allow for the increased presumably associated with male–male competition energetic costs of growing a large brain. However, for mates (Hilton et al., 2000). For girls, puberty is given that growth in brain volume is almost entirely associated with increased estrogen production and completed by the age of seven, it seems more accurate the deposition of fat stores that play an important role to say that the slow rate of somatic growth during in the modulation of reproductive function, including the juvenile period represents a priority in the use of ovarian cycling, and potential pregnancy and lactation glucose for brain development over somatic growth. (Ellison, 2001).

Human Biology, Energetics, and the Human Brain 433 The same gonadal steroids that promote second- (see Campbell et al., 2005, for an example). Thus in ary sexual characteristics and fuel somatic growth the natural human life course, rather than being a also act on the brain to change behavior during distinct postpubertal period, young adulthood may adolescence (Sisk and Zehr, 2005). The continued represent a final stage of development in which repro- maturation of the prefrontal cortex involves the ductive, somatic, and brain maturation all converge to experience-dependent maturation of the cortico- produce a fully functioning reproductive adult. thalamic-striatal circuit (Chambers et al., 2003; Crews et al., 2007). Testosterone may play a role in this process by modulating the dopaminergic reward SUMMARY system (Wood, 2004; Frye, 2007) while estrogen may have a role through its effects on the serotonergic Recent advances in neuroscience and brain imaging system (Lasiuk and Hegadoren, 2007), thus linking have greatly enlarged our understanding of human reproductive hormones and the reinforcement of brain metabolism and made the brain much more behavioral predispositions. amenable to an energetic and evolutionary analysis. From an energetic point of view, the timing of In addition to the well-known overall energetic cost of hormonal changes and their behavioral consequences the brain and its dependence on glucose as a substrate, during adolescence is a function of energy availability. more recent work has emphasized the fact that brain is Greater energy availability promotes faster childhood energetically demanding and in a position to regulate growth with earlier pubertal onset, including reproduct- its own energy supply. The human brain is also highly ive hormones (Ellison, 2001). Reproductive hormones plastic, and can utilize more than one substrate, both promote secondary characteristics which attract the during development and adulthood. It is this plasticity attention of others (see Waylen and Wolke, 2004, for (in addition to the large size) that gives the human a recent review), while at the same time acting on the brain its amazing flexibility and may play a central developing circuits in the brain to organize behavior, role in the cognitive powers that we hold so crucial including libido (Sisk and Foster 2004; Sisk and Zehr, to the nature of our species. 2005). Thus earlier maturers not only stand out phys- I argue that much of the energetic cost of the human ically from their peers, but their brains are being brain can be linked to the use of glucose in glutamate shaped by the experience of being more advanced sexu- cycling and its role in maintaining synaptic plasticity. ally than their peers, which may reinforce sexual Glutamate cycling involves the neuron-lactate-astrocyte behavior during adulthood as well as well (Ostovich shuttle, an on-going process, which may underlie intrin- and Sabini, 2005). sic brain activity, thus accounting for the energetically expensive and demanding properties of the human brain. Furthermore, though glucose remains the pre- Young adulthood ferred fuel for brain activity, the capacity of neurons Even after puberty is complete, and the production of to metabolism lactate and ketones appears to provide reproductive hormones has leveled off, the brain con- additional mechanisms for trade-offs between brain tinues to develop finishing with the maturation of the and somatic energy utilization. Such mechanisms are prefrontal cortex some time in the early 20s (Gogtay important in physical exercise and may have provided a et al., 2004). Glucose utilization rates in the anterior means to circumvent energetic constraints on physical cingulate cortex, a central structure in monitoring activity associated with subsistence strategies under- emotional impulses from the amygdala (Pezawas writing the evolution of a large human brain. et al., 2005; Etkin et al. 2006) have been shown to Developmentally, changes in the energetic costs of increase until the middle of the 20s (Van Bogaert the brain appear to map onto important neurological et al., 1998). The anterior cingulate cortex appears and behavioral stages of human development. The particularly affected by the adrenal hormone dehy- infant brain appears to be buffered from the effects of droepiandrosterone (DHEA) (Alhaj et al., 2006), which potential low energy availability during its rapid continues to increase into the 20s as well (Orentreich growth by a store of adipose tissue. On the other hand, et al., 1984; Sulcova et al., 1997). Together, these find- elevated brain glucose utilization between the ages of ings suggest a young-adult period characterized by 4 and 11 years appears to coincide with the onset of continued brain maturation in the absence of further adrenarche, suggesting that the neuroprotective effects somatic and reproductive maturation. of dehydroepiandrosterone sulfate (DHEAS) may be However, such a characterization may be mislead- important in maintaining synaptic plasticity, thus pro- ing given that favorable energetic conditions in indus- moting learning and socialization in prepubescent trialized populations has lead to early reproductive children. maturation. In many societies with low food availa- During adolescence the timing of puberty and bility somatic growth continues into the early 20s the rise of reproductive hormones reflects energy

434 Benjamin C. Campbell availability. Thus those who physically mature early two years, including Peter Ellison, Dan Eisenberg, will not only show earlier brain maturation, but such Peter Gray, and the Tea and Hormones group. maturation will tend to develop in social circumstances I would also like to thank Robert Campbell for his favoring sexual behavior and thus shape their brain continued encouragement to purse this topic. All errors to expect similar circumstances during adulthood. are my own. Though it appears that this integrative developmental process is centered on adolescence in our society, in subsistence societies where somatic growth is often slower it may also include young adulthood. REFERENCES Finally, the understanding of the dynamic nature Abeles, M. (1991). Corticonics: Neural Circuits of the Cerebral of brain energetics has fundamental philosophical Cortex. 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26 Embodied Capital and Extra-somatic Wealth in Human Evolution and Human History Jane B. Lancaster and Hillard S. Kaplan INTRODUCTION capital in the form of skills, education, and training. In past civilizations, going back to Babylonia in the third This chapter presents a theory of brain and life span millennia BC, literacy and numeracy were known but evolution and applies it to both primates in general, exceedingly rare skills. This pattern continued world- and to the hominid line, in particular. To address the wide until 1800 in Western Europe, including England, simultaneous effects of natural selection on the brain where these skills went from rarity to the norm in and on the life span, it extends the standard life history under a century (Clark, 2007). Labor markets with a theory in biology which organizes research into the particular demand for embodied capital in their evolutionary forces shaping age-schedules of fertility workers place new demands on human life history and mortality. This extension, the embodied capital and reproductive strategies in terms of mate choice, theory, integrates existing models with an economic fertility, investment in children, and the timing of analysis of capital investments and the value of life. reproduction in the life course. Once again, human life The chapter begins with a brief introduction to history radically changed in shape to a new emphasis embodied capital theory, and then applies it to under- on the acquisition of skills through training and educa- standing major trends in primate evolution and the spe- tion, postponement of reproduction to the late 20s, cific characteristics of humans. The evolution of brain and radically reduced completed family size with the size, intelligence, and life histories in the primate order reproductive part of the life course compressed into are addressed first. The evolution of the human life less than a decade. course is then considered, with a specific focus on the relationship between cognitive development, economic productivity, and longevity. It will be argued that the EMBODIED CAPITAL AND THE COEVOLUTION evolution of the human brain entailed a series of coevolu- OF INTELLIGENCE, DIET, AND LONGEVITY tionary responses in human development and aging. The second section on embodied capital and extra- According to the theory of evolution by natural selection, somatic wealth discusses humans in a comparative organic evolution is the result of a process in which context, beginning with the hunting and gathering variant forms compete to harvest energy from the envir- lifestyle because of its relevance to the vast majority onment and convert that energy into replicates of those of human evolutionary history. However, in the past forms. Forms that can capture more energy and convert 10 000 years human history traced a series of beha- that energy more efficiently into replicates of themselves vioral adaptations based on ecology and individual become more prevalent through time. This simple issue condition. The introduction of extra-somatic capital, of harvesting energy and converting energy into off- first in the form of livestock and later in land and spring generates many complex problems that are other types of wealth and power, radically changed time-dependent (Gadgil and Bossert, 1970). the shape of human life history parameters and pro- Two fundamental trade-offs determine the action duced new patterns of fertility, parental investment, of natural selection on life history strategies. The first and reproductive regimes as access to extra-somatic trade-off is between current and future reproduction. capital became a focus of life history strategies. By growing, an organism can increase its energy Finally, modern skills-based, competitive labor capture capacities in the future and thus increase its markets, combined with reduced fertility during the future fertility. For this reason, organisms typically nineteenth century, mark a returning focus on embodied have a juvenile phase in which fertility is zero until Human Evolutionary Biology, ed. Michael P. Muehlenbein. Published by Cambridge University Press. # Cambridge University Press 2010. 439

440 Jane B. Lancaster and Hillard S. Kaplan they reach a size at which some allocation to reproduc- expansion among higher primates, along with enhanced tion increases lifetime fitness more than does growth. learning abilities, reflects increased investment in trans- Similarly, among organisms that engage in repeated forming present experience into future performance bouts of reproduction (humans included), some energy (Armstrong and Falk, 1982; Fleagle, 1999). during the reproductive phase is diverted away from The action of natural selection on neural tissue reproduction and allocated to maintenance so that involved in learning and memory should depend on they can live to reproduce again. Natural selection is costs and benefits realized over the organism’s lifetime. expected to optimize the allocation of energy to current Three kinds of costs are likely to be of particular reproduction and to future reproduction (via invest- importance. Firstly, there are the initial energetic costs ments in growth and maintenance) at each point in of growing the brain. Among mammals, those costs the life course so that genetic descendents are maxi- are largely born by the mother during pregnancy and mized (Gadgil and Bossert, 1970). Variation across lactation. Secondly, there are the energetic costs of taxa and across conditions in optimal energy allo- maintaining neural tissue. Among infant humans, cations is shaped by ecological factors, such as food about 65% of all resting energetic expenditure supports supply, disease, access to mates, and predation rates. maintenance and growth of the brain (Holliday, 1978). A second fundamental life history trade-off is Thirdly, certain brain abilities may actually decrease between offspring number (quantity) and offspring performance early in life. Specifically, the capacity to fitness (quality). This trade-off occurs because parents learn and increased behavioral flexibility may entail have limited resources to invest in offspring and each reductions in “preprogrammed” behavioral routines. additional offspring produced necessarily reduces ave- The incompetence with which human infants and rage investment per offspring. Most biological models children perform many motor tasks is an example. operationalize this trade-off as number versus survival Some allocations to investments in brain tissue may of offspring (Lack, 1954; Smith and Fretwell, 1974; Lloyd, provide immediate benefits (e.g., perceptual abilities, 1987). However, parental investment may not only affect motor co-ordination). Other benefits of brain tissue survival to adulthood, but also the adult productivity and are only realized as the organism ages. The acquisition fertility of offspring. This is especially true of humans. of knowledge and skills has benefits that, at least in Thus, natural selection is expected to shape investment part, depend on their impact on future productivity. per offspring and offspring number so as to maximize Consider two alternative cases, using as an example, offspring number times their average lifetime fitness. the difficulty and learning-intensiveness of the orga- The embodied capital theory generalizes existing nism’s foraging niche. In the easy-feeding niche where life history theory by treating the processes of growth, there is little to learn and information to process, net development, and maintenance as investments in productivity (excess energy above and beyond mainte- stocks of somatic, or embodied, capital. In a physical nance costs of brain and body) reaches its asymptote sense, embodied capital is organized somatic tissue – early in life. There is a relatively small impact of the muscles, digestive organs, immune competence, brains, brain on productivity late in life (because there has been etc. In a functional sense, embodied capital includes little to learn), but there are higher costs of the brain strength, speed, immune function, skill, knowledge, early in life. Unless the life span is exceptionally long, and other qualities such as social networks and status. natural selection will favor the smaller brain. Since such stocks tend to depreciate with time, alloca- In the difficult-feeding niche, the large-brain crea- tions to maintenance can also be seen as investments ture is slightly worse off than the small-brain one early in embodied capital. Thus, the present-future repro- in life (because the brain is costly and learning is taking ductive trade-off can be understood in terms of optimal place), but much better off later in life. The effect of investments in own embodied capital versus reproduc- natural selection will depend upon the probabilities tion, and the quantity–quality trade-off can be under- of reaching the older ages. If those probabilities are stood in terms of investments in the embodied capital sufficiently low, the small brain will be favored, and if of offspring versus their number. they are sufficiently high, the large brain will be favored. Thus, selection on learning-based neural capi- tal depends not only on its immediate costs and The brain as embodied capital benefits, but also upon mortality schedules which The brain is a special form of embodied capital. Neural affect the expected gains in the future. tissue is involved in monitoring the organism’s internal and external environments and organizing physio- The human adaptive complex logical and behavioral adjustments to those stimuli (Jerison, 1976). Portions (particularly the cerebral The human adaptive complex is a coadapted complex cortex) are also involved in transforming past and of traits, including: (1) the life history of development, present experience into future performance. Cortical aging and longevity; (2) diet and dietary physiology;