Human Evolutionary Biology

Human Longevity and Senescence 541 genetic variance for LH traits, ranging from ages at studies, e.g., Washoe, and those like Cheeta, Timmy, first reproduction and intrinsic dysfunction to fecund- and Colo. Learned, shared, adaptive, and accumulated ity and life span (Arking et al., 2002). Research on CR behaviors and beliefs (culture) drive humans to create rodents shows that a nutritionally adequate but CR microenvironmental niches suiting their current per- diet slows LH, reduces age-specific fertility, and ceived needs and tastes. Most organisms must respond increases somatic maintenance. Conversely, laboratory to more immediate evolutionary pressures driving mice eating energy-rich ad libitum diets show more their behavior, form, and function. Humankind uses rapid LH, early reproduction, and decreased life spans. extrasomatic mechanisms to maintain intrinsic integ- Even among nonhuman primates, CR improves rity. Animal skins and fire reduced dependence on immune function and reduces inflammation (Ingram physiological resources. Tools and fire increased the et al., 2004, 2005; Nikolich-Zugich and Messaoudi, range of obtainable foods and relaxed selection for 2005). The laboratory environment differs from that large teeth and jaws. Each generation, NS favors indi- of wild animals. Laboratory populations have fewer viduals with phenotypes that increase their likelihood stressors than nonlaboratory. Calorie restriction gener- of producing and rearing fertile offspring in their spe- ally extends mean and maximum life spans of labora- cific environment. Modern humans constantly adapt to tory rodents, but it does not do so for the wild-born. a variety of culturally created microenvironments. Laboratory experiments show that multiple biomole- Genetic adaptations of LH to these new environments cular processes, for example telomere shortening and may be slow. Easier to detect may be developmental replicative capacity in vitro and antioxidant levels, are changes that occur without genetic alterations through related to but may not be directly responsible for in changes in hormonal release, timing, or response vivo senescence. We expect multiple cellular processes (Finch and Rose, 1995; Crews and Bogin, 2010) and to correlate with whole organism senescence because patterns of phenotypic plasticity exposed as response most are secondary processes, having evolved within to changing environments (Weiss and Buchannan, already senescing organisms. Others likely result from 2003; Hallgrimsson and Hall, 2005). antagonistic pleiotropy, mutation accumulation, and evolutionary inertia, representing ubiquitous senes- Human life history plasticity cence in living cells. At the cellular level, senescence reflects the loss of cellular integrity that results from Human developmental milestones and the timing and ROS, mutation, DNA and protein errors, loses of regu- pattern of LH events are plastic (Finch and Rose, 1995; latory, repair and housekeeping functions, immunity Barker, 1998; Bogin, 1999; Cameron and Demerath, and self-recognition systems, telomere shortening and 2002; Crews, 2003; Finch and Crimmins, 2004; Weiss lack of replacement of cells, and waste accumulation, and Buchannan, 2003; Hallgrimsson and Hall, 2005; changes that characterize all aging cells. Human sen- Kirkwood et al., 2005; Crews and Bogin, 2010). To escence begins with these same biological processes. some degree, the mid-childhood and adolescent Over evolutionary time humans developed additional growth spurts are genetically programmed. However, protections against such senescent alterations, they are still sufficiently flexible that their timing, dur- allowing them to show a unique pattern of senescence ation, and rapidity vary across populations (Bogin, and LH. Nevertheless, their underlying biology 1999; Crews and Bogin, 2010). Flexibility is the rule remains that of a large-bodied mammal and ape. The rather than exception in human LH milestones, first bioculturally constructed niche modern humans have and last menses, age-at-first birth, age at death, and the created protects them from many extrinsic stressors point of MRP (Larke and Crews, 2006). Using cultur- experienced by other species and previous hominins. ally derived adaptive strategies humans change their This allows those with intrinsic stamina and RC to environments and allow their somas to respond to new express predispositions to longevity. Phenotypes less and old stressors in different ways (Baker, 1984). prone to stress-related, environmental, and intrinsic Cultural processes lead to animal domestication, damage, biological wear and tear, and with high increasing the general availability of protein and fats immune competence and mechanical reliability may (Larsen, 2003). This may have led to increased height, now express their predispositions and live long lives. weight, and improved nutrition. Animal domestication also brought novel infectious diseases (zoonoses) to humans, increasing frequencies of alleles promoting The human constructed niche and longevity disease resistance. Animal and plant domestication Humankind currently lives in constructed niches and and, subsequently, agriculture exposed humans to built environments different from those of their ances- more than just new nutritional stresses. Population tors, nonlaboratory organisms, most nonhuman pri- density increased and permanent settlements followed mates, and nondomestic animals. Exceptions include increased availability of calories from agriculture. some hominoids raised by humans during language This created an ecological setting wherein infectious

542 Douglas E. Crews and James A. Stewart diseases and nutritional deficiencies dramatically maintenance, development of RC, and additional increased (Larsen, 2000). As population densities and reproductive effort (Crews, 2003; Bogin, 2009; Crews trading networks expanded, infectious diseases flour- and Bogin, 2010). As RS and fitness became dependent ished and spread in villages, towns, and cities that upon learned activities and social relations (culture), developed (Fenner, 1970). Skeletal remains suggest biocultural selection pressures for neurological devel- measures of health declined following the innovation opment likely increased predispositions toward pro- of agriculture until recent epidemiological transitions cesses that enhanced mental abilities. Based upon (Larsen, 2000; Howell and Pfeiffer, 2006). available data, Homo ergaster may have birthed less Human LH patterns respond to culturally derived precocial more altricial young than did earlier homi- adaptive strategies. As humans created new microen- nins. Altricial human infants require high postgesta- vironments within which NS and developmental plas- tional PI to support their brain and somatic growth ticity occurred, they exposed a reservoir of genetic and and development. Culturally constructed environ- phenotypic plasticity for LH. In the classic Livingsto- ments provide a safe haven for altricial offspring to nian model, culturally derived behaviors allow humans not only grow and develop, but to be a viable ESS to change their environment, eliminating, creating, and (Crews, 2003; Odling-Smee et al., 2003). Without a altering selection pressures on themselves (Livingston, culturally constructed environmental niche in which 1958; Baker, 1984). As cultural forces created cushy to survive, humankind’s altricial offspring may not living environments, selection relaxed for some traits, have been an ESS. Human encephalization seems to created new stressors, and allowed a fuller expression have followed cultural developments toward more of human developmental and LH plasticity (Crews, stimulating environments with fire, tools, social activ- 2007). ities, and complex social relationships. Laboratory experiments with rodents demonstrate that more com- plex (enriched) environments lead to more highly net- Culture, diet, and life history worked brains. More highly networked brains seem to Large-brained neonates and toddlers require calories work in ways considered more intelligent by humans. and nutrients beyond what is provided by diets of other Animals with more networked brains solve experimen- large-bodied apes (Aiello and Wells, 2002; Leonard, tal tasks considered relevant to humans more rapidly. 2002). One cultural development, using fire, allowed Cultural developments, technologies, and processes later Homo to consume toxic and difficult to process enriched and complicated the lives of evolving Homo foods (Wrangham et al., 1999; Wrangham and Con- species, likely leading to a more intelligent longer-lived klin-Brittain, 2003). Fire allowed intensive exploitation species of old and new food sources and influenced human Many of today’s “modern” human populations tend LH, skeletal biology, and digestive anatomy and physi- to consume only a small portion of edibles in their ology. Humankind’s shorter colon than other apes environments. In today’s “more marginal” environ- reflects bioculturally mediated selective pressures and ments, among predecessors of recently “modernized” adaptation. Compared to other mammals and large- groups, and in more densely populated settings, a bodied apes, modern human gut anatomy suggests broader array of edibles – larvae, insects, spiders, modifications toward high throughputs of calorie- amphibians, reptiles, bats, and other less desirable dense foods (Milton, 1999). Dietary changes toward animals and plants – are and were consumed. Archaeo- meat eating and related technological innovations logically and historically, the amount of time and coincided with brain expansion of the Homo species human energy devoted to food preparation in cosmo- and our modern LH. Use of fire and meat consumption politan societies decreased as production increased. At likely predisposed evolving hominins to small intes- the same time, rates of acute, infectious diseases and tines of greater length as they digested more cooked childhood death rates declined. Among humans, time and uncooked protein. Conversely, shorter colons of weaning is highly variable and related to multiple likely followed diets with less fiber content. Cultural cultural and biological, and physiological factors. This innovations improved physiological extractive effi- LH event is relatively easy to determine bioarchaeolo- ciency compared to other large-bodied apes, and also gically (Larsen, 2000). Selective pressures on age at allowed Homo species, including eventually humans, weaning apparently decreased as humans developed to consume more calorie-dense and fewer low-calorie adequate and effective weaning foods. Availability of foods (Larsen, 2003). quality weaning foods relaxed selective pressure on New technologies and richer diets, freed somatic humans, releasing a mortality bottleneck limiting the resources previously invested in food processing for proportion of children attaining adulthood. During investments elsewhere. They were available for pro- much of early hominin evolution, those who survived moting early neurological development, slow steady infancy likely faced high selective pressures after growth over an extended growth phase, somatic weaning through puberty, as is seen in marginal

Human Longevity and Senescence 543 environments yet today. Those who survived likely humans and promoted modern human patterns of possessed genetic predispositions promoting meta- LH, senescence, and longevity. Their general focus bolic efficiency, efficient cellular housekeeping, less has been to obtain data from modern human popula- inflammation, better DNA repair, and more efficient tions and extrapolate it into the past, with little immune- and stress-responses. In such settings, those reference to comparative mammalian biology. These attaining adulthood likely were hardier and better able extrapolations often are based upon selection extending to combat prevailing environmental stressors. As child- longevity; an unlikely process if selection to lengthen hood environmental assaults were reduced and less life is generally weak (Stearns, 1992; Carey and Judge, energy was expended on daily food gathering and prep- 2001; Crews and Ice, 2010). aration, resources were freed to be retained as RC Models based upon ecology observations of multiple through adulthood and into late life. As life styles extant species and populations reveal a commonality became cushier, humans produced and retained more of senescent processes across sexually reproducing total energetic capacity over their early lives (Crews, animals (Jones, 1975; Gravilov and Gravilova, 1991; 2003, 2007; Drenos et al., 2006; Bogin, 2009; Crews and Charnov, 1993; Finch and Rose, 1995; Austad, 1997; Bogin, 2010). Eventually, humans capable of retaining Arking et al., 2002; Crews, 2003; Holliday, 2004; Austad RC into later decades of life showed increased life spans and Fischer, 2005). Human longevity is not unique. (Crews, 2003; Bogin, 2009; Crews and Bogin, 2010). Whales, tortoises, sharks, and elephants are equally, Evolutionarily the majority of life span extension or more, long-lived. Among chimpanzees, bonobos, occurred over a relatively short time. It is not likely that gorillas, modern hunter-gatherers, foragers, and agri- NS, as described in traditional or neo-Darwinian culturalists females migrate from their natal groups models, greatly reshaped the distribution of senes- upon maturity. A behavior that likely characterized cence-slowing or longevity-enhancing alleles in this earlier hominins and most modern humans. In such period. Prior to historical times, evolutionary alter- social settings, grandchildren seldom see their mater- ations in human LH occurred as cultural became nal grandmother. Thus, in most species, maternal humankind’s primary adaptive response, biocultural grandmothers live in different locations and do not feedback loops began determining the pace and pat- have opportunities to invest in their daughter’s grand- tern of early LH, and altricial offspring became an children as some have proposed (Hawkes et al., 1997, ESS. Altricial offspring require more time to grow 1998; Alvarez, 2000). and develop. The need to nourish altricial offspring As parts of a species’ LH strategy, correlations resonated throughout human LH, slowing the pace of among LH traits and their timing are expected, but infancy, inserting childhood and adolescent periods correlation is not causation. Thus, ages at menarche, and a puberty growth spurt, extending the ages of menopause, first birth, MRP, and the lengths of life reproductive effort, and ultimately increasing selective span, growth span, infancy and childhood, and prere- pressures on somatic maintenance (Bogin, 2009; productive and adult mortality rates should be correl- Crews and Bogin, 2010). It is not likely that selection ated. Longer periods of growth and development acted directly to increase human life span, because influence how investments in somatic maintenance, “selection to lengthen life is generally weak” (Stearns, and the length of the reproductive phase are appor- 1992, p. 20; see also Carey and Judge, 2001; Crews and tioned. Events occurring in early life determine the Ice, 2010). Rather, NS molds somatic responses to slow MNLS, the pace of growth and development, and the and halt already existing processes of senescence. age at MRP, determining in part the reproductive span Secondly, NS acts most strongly in early life and the and how long intrinsic adult mortality must be delayed period of maximum reproductive effort. Its effects to allow sufficient reproductive effort to accomplish on late-life are neither positive nor negative because the necessary tasks of life. Mammals require growth late-life is beyond the purview of NS. and reproductive phases for a successful ESS. Over time, somatic stabilizing factors evolved to protect the developing human reproductive unit during its Models for the evolution of human life history maturation and reproduction phases in relatively Models proposing “man the hunter” and “women the harsh environments. By slowing intrinsic senescent gatherer” (e.g., Lee and DeVore, 1969; Lovejoy, 1981) processes they delayed somatic dysfunction and were replaced by models suggesting that grandmothers altered intrinsic and extrinsic mortality rates, produ- or future reproduction of relatives (Hill and Hurtado, cing correlations with other coadapted LH traits. 1991; Hawkes et al., 1997, 1998; Alvarez, 2000), adult As a population’s gene pool evolves toward a better mortality (Charnov, 1993; Stearns et al., 2000), or fit to local environmental pressures, any alleles learning and embodied capital (Kaplan, 1996; Kaplan improving survival during the growth and reproductive et al., 2000, 2003; Bird and Bird, 2002; Kaplan and phases of life should be advantaged. Alleles with Robson, 2002) altered evolutionary pressures on late-acting effects on survival, beyond the ages of

544 Douglas E. Crews and James A. Stewart reproductive effort, whether positive or negative, are settings of early and late Homo species reducing intrin- neither disadvantaged nor advantaged. Because their sic dysfunction and extrinsic mortality rates. These frequencies are unaffected by NS, multiple alleles pre- changes allowed individuals to avoid extrinsic stressors disposing to better or worse late-life survival, may be and retain RC into later life. They also provided a niche active during the senescent phase of LH. As biocultural wherein secondarily altricial offspring could survive processes continue to provide a means for older and prosper as an ESS. Secondarily altricial human persons to increase their own RS and IF, additional newborns continue growth and development well into advantages accrue to alleles predisposing to improved their second decade of life. The second decade of life is late-life survival. Considering that having a significant the first decade of reproductive effort among other number of elders in any one local population is a rela- large-bodied apes. Biocultural evolution during the tively recent phenomenon (Caspari and Lee, 2004), it is earliest phases of life altered all later aspects of LH, not likely that such alleles were greatly advantaged modulating growth and development, reproduction, until the advent of modern humans. and length of life (Bogin, 2009; Crews and Bogin, Across human populations, older surviving men 2010). have more offspring than men who die at younger ages. Human LH, senescence, and longevity are based Greater variation in male than female RS allows men upon a suite of characteristics – encephalization, non- to benefit more from long life than women. There are genetically programmed behaviors as survival strat- intrinsic constraints on completed fertility of women, egies, sociality, and group living – shared with many but not men. This may be more relevant than meno- primate species (Shea, 1998; Crews, 2003). Parental pause and grandmothers to life span and LH evolution investment, social groupings, incipient culture, group in humans (Marlowe, 2000; Crews, 2003, 2008). hunting, group protection, and sharing of meat are all Genghis Kahn and his male relatives are hypothesized seen among other large-bodied apes. As the hominin to have contributed their Y-chromosome and to be the large-bodied ape clade evolved, several uniquely homi- direct ancestors of about 8% of contemporary Chinese nin trends, beyond bipedalism and culture, emerged. men living in central Asia (about 16.7 million or 0.5% Culture and hands freed from locomotion led to add- of all living men) (Zerjel et al., 2003). Conversely, a itional uniquely human traits, extensive use of tools significant number of men fail to ever sire children. and fire, niche construction, secondarily altricial off- This may be related to why men may show lower rates spring, slow development to reproductive maturity, of senescence at extreme old age than do women mutually supporting social networks of kin, and life- (Gavrilov and Gavrilova, 1991; Carey, 1995; Graves long PI. et al., 2006). Alleles predisposing to somatically com- In modern cosmopolitan settings, most women live petent men likely were advantaged in environments to experience menopause; however, in the late nine- of evolutionary adaptation. In today’s cushy environ- teenth and early twentieth centuries only 20% of Native ments these competencies may be expressed as greater American, 30% of Black, and 60% of White US women RC at older ages and longevity. survived to age 55, respectively (see Figure 3.5 in Crews, 2003, p. 114). Even in the twenty-first century many women in Third-world settings do not survive CONCLUSIONS past menopause. It seems unlikely that many females did so among earlier Homo species. Nor are life spans Natural selection for longevity may not be the reason of over 50 years often observed among wild living non- for modern humankind’s seemingly slow senescence. It human large-bodied female apes or mammals of is unlikely that modern humans would senescence as known age. Ovarian depletion, reduced fertility in the slowly in any of our ancestral environments as they do late fourth and early fifth decades, and menopause in today’s constructed niches. That is, Cheeta would occur in all female mammals who survive sufficiently never have attained 75 years in the wild. Humans con- long, past their fourth decade of life (Austad, 1994; tinue to face high selective pressures, but today’s indi- Leidy, 1994; Rogers, 1993; Packer et al., 1998). Con- viduals are descended from ancestors who were trary to several selective models of human LH, lifeways reproductively successful in harsher environments. of modern-day traditional living populations are not a Today, these pressures are avoided by living in built window on earlier Homo and human lifeways. Nor do environments created as sociocultural adaptations to they represent the lifeways of hominins when our cur- external stressors. Most current scenarios for human rent LH developed. Every extant population is exposed senescence and longevity fail to consider these factors. to modern cultures, lifeways, and multiple outside Contrary to many evolutionary models based on selec- influences (Crews and Gerber, 2003). Societies not so tion for longevity, a biocultural model suggests that influenced prior to the arrival of missionaries and cultural developments, niche construction, and cultur- anthropologists included residents of tropical South ally derived adaptive strategies altered the ecological America and Africa and highland New Guinea at first

Human Longevity and Senescence 545 contact. Although isolated, none was struggling to feed extending well beyond those of other large-bodied apes itself, suggesting little energetic trade-off between appear to be an epiphenomena of NS acting on aspects reproduction and self-maintenance. They lived in of early LH, altricial offspring, slow growth, and an highly integrated societies. They had sufficient free extended growth phase that stretched out the period time to elaborate extensive social activities. Their tradi- for attaining MRP (Bogin, 2009; Crews and Bogin, tional lifeways do not conform to evolutionary scen- 2010). This early LH is now played out in culturally arios based upon scarcity of resources or difficult constructed environments that allow retention of RC processing to extract limited resources as are reported and lead to somatic maintenance into the ninth, tenth, among some modern-day foragers (Kaplan, 1996; and later decades of human life. Kaplan et al., 2000, 2003; Bird and Bird, 2002). It is unclear if late-life stages when both senescence DISCUSSION POINTS and mortality rates slow their increases exist among multiple species. It is certain that no currently popular 1. The disposable soma theory for the evolution of model of human LH evolution explains a mortality senescence is based upon what aspects of repro- plateau in the last decades of human life. Conversely, ductive biology? How have recent developments in biocultural evolution leading to the retention of som- understanding the living histories of single-celled atic resources over a lifetime of living in cushy environ- organisms altered this view? How would you ments is compatible with a late-life mortality plateau. reframe this model in light of these new results? Understanding human senescence and longevity What are two mechanisms by which senescence- depends as much on comparisons with short-lived promoting alleles may be retained in the genome and nonmammalian taxa, as it does on comparisons over evolutionary time? with other long-lived and mammalian organisms. 2. What methods might one use to measure pheno- Increased focus on how biocultural influences on typic aging and why should it be measured? What humans changed survival probabilities and longevity methods might one use to measure biological will be a positive development toward understanding senescence at the cellular level and why should it LH evolution across all species. be measured? What are some differences between Understanding how modern humans became rela- senescence and aging? tively long-lived compared to other apes requires com- 3. Givenwhatyouhavereadandknowofmodernhuman parisons with other primates, mammals, and life forms life history and variation, describe how because and examinations of across population human LH humans are cultural animals their life history may variation. Among humans RS, reproductive effort, evolve differently from nonculture-using animals. RC, stress resistance, life span, longevity, and senes- 4. What are some biological factors that pattern cence are highly variable individual traits. Not even life history (LH) of animals and mammals? Does identical twins show the same ages at death and famil- modern human LH show factors other than biology ial correlations for longevity often are low. Mechanistic that influence their LH? Are humans so unique in models for human LH evolution often are retrospective their LH that we need special models to explain and do not account for the influences of biocultural their LH evolution? evolution. Biological processes contribute to human 5. Austad critiqued earlier definitions of senescence senescence via mostly unknown genes and unidentified and aging for not including any mention of repro- physiological pathways. Pushed by the grand theory duction and fertility. Why are reproduction and of evolution by NS, existing models of human LH fertility important for defining senescence and evolution often lack mid-level theory, failing to identify aging? What are the meanings of “age of maximum or hypothesize genetic or physiological mechanisms, reproductive potential” (MRP) and “minimum or physiological pathways linking genes and LH. No necessary life span” (MNLS)? How does the age of system of accounting by which NS may tally the influ- MRP influence the MNLS? ences of epigenetic factors and learning or the future RS of offspring and calculate the probability of grand- offspring has been proposed. Clearly intrinsic factors ACKNOWLEDGEMENTS acting throughout the growth phase influence adult mortality and human life spans. Natural selection Sincere thanks to the editor Michael P. Muehlenbein for likely acted on early LH factors linked to RS that also his efforts in bringing this comprehensive volume improved resistance to extrinsic stressors, retention of together and inviting us to include this work. We also RC, and ultimately extended life spans in culturally acknowledge the insightful comments and suggestions created settings (Crews and Bogin, 2010). However, of two reviewers that improved this contribution. NS may never have acted directly to extend human life Finally, we wish to thank Courtney McFadden and Rhea span or postreproductive survival. Rather, life spans Alleyne for typing multiple versions of this manuscript.

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32 Evolutionary Psychiatry: Mental Disorders and Behavioral Evolution Brant Wenegrat INTRODUCTION can play a role in treatment. Concepts explaining social life seem especially suited to shed light on dis- Since W. D. Hamilton’s seminal work on kin-selection orders with social precipitants, causes, consequences, (Hamilton, 1964a, 1964b) advances in the field of and remedies. behavioral evolution have changed our view of animal In this chapter, I review some of the efforts to and human social behavior. A wide range of social understand mental disorders and possible treatments behaviors – altruistic, co-operative, aggressive, paren- for them in terms of concepts drawn from behavioral tal, and sexual – are now seen as products of past evolution, a field known as evolutionary psychiatry. selective forces, many of which were generated by Authors and researchers working in this field employ social interactions. Fifty years ago, it was possible five disparate paradigms (see Nettle, 2004). Although for Behaviorists to argue that humans are blank slates the differences between them are sometimes ignored, whose nature – if such exists – is wholly determined these paradigms have differing aims and relative by cultural/environment forces. The most basic emo- strengths and weaknesses. Many debates in the field tional attitudes – for example, sexual preferences and result from application of disparate paradigms to the parental concern for children – were said to result same disorder. This chapter will cite examples from from training and cultural expectation. That position each of the five major paradigms to illustrate their is no longer tenable, in large part due to concepts differences, logic, goals, and weaknesses. from behavioral evolution. At the same time, important advances have been made in psychiatry. Over the last 40 years, psychiatric THE ADAPTATIONIST PARADIGM researchers have identified mental disorders that can be reliably diagnosed, may affect Darwinian fitness, and are The adaptationist paradigm aims to view mental dis- partly caused by genes. A large proportion of people in orders, their milder variations, or illness-related traits as most or all societies suffer from one or another of these behavioral adaptations that confer or have conferred mental disorders. The research on diagnosis culminated inclusive fitness benefits. Widely cited models of schizo- in the 1994 publication of the Diagnostic and Statistical phrenia and schizotypal disorder, depression and mania, Manual of the American Psychiatric Association, Fourth and anorexia nervosa illustrate the goals and pitfalls of Edition, known as the DSM-IV, which lists objective this paradigm. criteria for diagnosing disorders (American Psychiatric Association, 1994). The DSM-IV criteria for specific Schizophrenia and schizotypal disorder disorders are described later in this chapter, along with pertinent prevalence, genetic, and fitness data. To give According to the DSM-IV, schizophrenics suffer from readersabettersenseofsomedisorders,caseexamples social–emotional deficits (emotional flatness, apathy, are given. loss of social interests), odd or magical thinking, and Insofar as concepts from behavioral evolution can psychotic symptoms, such as hallucinations and delu- explain human behavior, they might shed light on sions (American Psychiatric Association, 1994). Their disorders like those in the DSM-IV (Troisi, 2005). speech and behavior may be eccentric, disorganized, or These concepts deal with social life, social events, even unintelligible. The symptoms must cause social or and experiences known to trigger disorders, or cause occupational impairment, have lasted for six months them in some cases. Concomitant social deficits or longer, and not be attributable to another condition, account for the disabilities resulting from these dis- such as drug abuse. A typical case of schizophrenia is orders, and psychotherapy, which is a social process, described in Box 32.1. Human Evolutionary Biology, ed. Michael P. Muehlenbein. Published by Cambridge University Press. # Cambridge University Press 2010. 551

552 Brant Wenegrat BOX 32.1. A case of schizophrenia. LN, a 41-year-old woman, had been normal until and returned to her parents’ home. Over the next 20 years, adolescence, when she began to withdraw from friends and her delusions were generally controlled by medications, but became increasing “odd” and emotionally inexpressive. she had no interest in meeting other people and didn’t like She completed high school and was admitted to college, leaving the house. She never worked or dated. When her but during her first semester she became convinced her elderly parents needed to sell their house, LN went to live professors were trying to kill her. She thought students in with her sister, in another town. Her sister, who had two her dormitory were spying on her, and that there were children, could not manage LN’s disruptive behavior and coded messages about her in the campus paper. She had to place her in a group home for the mentally ill. LN’s thought that campus football scores somehow foretold her maternal grandmother and a maternal aunt were also future. She was admitted to the student infirmary and schizophrenic and a maternal uncle was thought to be diagnosed with schizophrenia. LN withdrew from college schizotypal. Schizophrenia runs in families (Gottesman and larger-than-family groups might be beneficial. Along Shields, 1982). For example, first-degree relatives of a a similar line, Sullivan and Allen (1999, 2004) argued schizophrenic (children or full siblings) are 10 times that individuals with schizoid personalities are some- more likely to develop this disorder than individuals times better able to balance their own needs and inter- drawn from the general population. If one identical ests against those of their social group, to which they twin is schizophrenic, the chances are 50% that the other are less committed. will also be ill. Relatives of schizophrenics are also at An advantage might also accrue from creative increased risk for personality disorders that are thought eccentricity. The notion that there is a close relation- to represent milder forms of the same trait or illness. ship between creative genius and madness goes far Schizoid personalities, for example, are emotionally back in Western culture (Burns, 2006). In fact, while flat and socially disengaged, but their thinking and schizophrenics themselves are not especially creative, speech are normal. Schizotypal personalities are socially some of their healthy relatives do have unusual gifts, disengaged, and in addition their thinking is odd or which might lead to increased fitness in some soci- magical and they have strange beliefs (American Psychi- eties (Karlsson, 1966; Anthony, 1968; Heston and atric Association, 1994). They resemble schizophrenics, Denny, 1968; Kauffman et al., 1979; Rabin et al., but lack the psychotic symptoms. A typical case of schi- 1979; Rothenberg, 1983; Ludwig, 1995; Nettle, 2001). zotypal personality disorder is described in Box 32.2. In a sample of British adults, Nettle and Clegg (2006) Schizophrenia and related personality disorders are showed that a measure of schizotypal eccentricity referred to as the “schizophrenia spectrum disorders” correlates with artistic and creative activities, which and are generally believed to be caused by multiple correlate in turn with numbers of sexual partners. illness-promoting alleles, each of small effect, acting at Studies of the fertility of relatives of schizophren- multiple loci (see Crow, 2007). Environmental insults – ics have had mixed results. Some show increased such as in utero viral exposures – interact with genetic reproductive fitness, while others do not (Kendler risks. The higher the dose of illness-promoting genes et al., 1998; Avila et al., 2001; Haukka et al., 2003). and environment insults, the more likely an individual Proving increased fitness in families of schizophren- will develop schizophrenia or schizotypal personality ics is an obvious first step in validating advantages of disorder; the lower the dose, the more likely the person illness-related traits. will be relatively normal. Stevens and Price (2000a, 2000b) hypothesized that As one might guess from the case described in schizotypal oddity and eccentricity served an adaptive Box 32.1, schizophrenics – especially males – living in function in early human groups, even if it is a handicap modern societies have fewer children than average today. According to these authors, ancestral groups (Bassett et al., 1996; Avila et al., 2001). However, if repeatedly grew to the point that they outstripped their schizophrenia impairs reproduction, how do alleles resources, leading to in-group conflict. At such times, that cause it maintain their place in the gene pool? schizotypal persons could catalyze group splitting. Why don’t they disappear? Because of their odd, other-worldly manner and One potential answer is that relatives of schizo- strange beliefs and convictions, schizotypal persons phrenics with mild to moderate traits related to schizo- may take on cultic status in times of social stress. Such phrenia might have selective advantages that offset the a person could form the nidus for an incipient new handicaps resulting from full-blown illness. Selection group emerging from an old one. against schizophrenics might be balanced by kin Although Stevens and Price (2000a, 2000b) cite stud- advantage. Kellett (1973), for example, speculated that ies showing that schizotypal traits promote formation schizoid personalities enjoy a fitness advantage in of cult-like groups, other research undermines their some societies, in which weaker emotional ties to hypothesis. Modern-day studies of hunter-gatherer tribes

Evolutionary Psychiatry: Mental Disorders and Behavioral Evolution 553 BOX 32.2. A case of schizotypal personality disorder. AH came to psychiatric attention for the first time in his late influence him, but he was able to keep a professional – if not 50s. He had been living with his elderly mother in her friendly – demeanor. After dropping off a passenger, he apartment until her sudden death from a stroke. He had would “review” his thoughts to see that they hadn’t been completed high school and two years of junior college altered by contact with other people. After AH’s mother and worked as a cab driver for the previous 25 years. He died, the apartment manager – who had tolerated AH’s had never married or had intercourse, and he had never had glaring, unpleasant manner for his mother’s sake – asked friends or socialized, other than with his mother. He didn’t him to leave. AH created a disturbance and the police were experience this as a problem. He felt uncomfortable having called. As part of the ensuing court process, AH was referred passengers in his cab and feared they would try to cheat or for a psychiatric evaluation. show that although group splitting can occur, it is an Pointing out that some depressive episodes are trig- infrequent occurrence (Chagnon, 1979). When groups gered by real or threatened loss of social standing, split, moreover, kinship – not cult beliefs – determine Stevens and Price (2000b) argue that depression is an who joins which daughter group. Studies in Western adaptive strategy in that situation. By withdrawing from societies show that people join cults because they are competition, the depressed individual avoids further socially isolated, not because they are captivated by the conflict and losses. He or she submits to the fact he or cult ideology or entranced by the leader (Galanter, 1978, she has failed, and ceases to struggle further. Depression, 1989; Wenegrat, 1989). Accepting cult ideology and the by this account, communicates submission. In a related leader’sauthority is the price paid for group membership, vein, Gardner hypothesized that depression manifests an not the motivation. Finally, in his comprehensive cross- evolutionarily ancient “PSALIC,” or “Propensity State cultural study of shamanism, I. M. Lewis found that Antedating Language in Communication;” a primitive shamans in traditional societies are distinguished from signaling system, in other words (Gardner, 1988). others by virtue of their excellent social skills, not by their Watson and Andrews (2002) suggest that depression eccentricity (Lewis, 1971). Social skills, not eccentricity, evolved as an adaptive response to intractable social are needed to establish a credible claim to cultic or problems. The mental effect of depression is to focus magical powers. the individual’s attention on his or her problems. It also sends a signal to potential helpers that more assistance is needed. Since uninterrupted depression may even end Depression and mania in death, those who have an interest in the depressed According to the DSM-IV, major depression is character- person’s survival are virtually extorted to offer increased ized by depressed mood most of the day, diminished aid. Hagen (1999) made a similar argument regarding interest and pleasure in usually enjoyable activities, postpartum depression. According to Hagen, postpartum insomnia or excessive sleeping, agitation or mental and depressionis a way that mothers signal their partnersand physical slowing, persistent feelings of worthlessness or other persons that they need assistance caring for their guilt, impaired thinking or concentration, and frequent newborns. thoughts of death (American Psychiatric Association, Individuals who have episodes of mania or hypo- 1994). Appetite may be increased or decreased, with mania – which usually alternate with periods of consequent changes in weight, and sexual interest is depression – are given the DSM-IV diagnosis bipolar diminished or lost. Depressed individuals may harm or disorder (American Psychiatric Association, 1994). kill themselves. As is the case with schizophrenia, these Mania is characterized by an increase in energy, symptoms impair social or occupational functioning and euphoria, high self-esteem and even delusions of they cannot be accounted for by other disorders or grandeur, disregard for risks and consequent reckless illnesses. Severely depressed patients may experience behavior, and initiation of projects that are patently hallucinations or delusions with depressive themes; for unrealistic. A manic patient, for instance, may believe example, they may hear voices condemning them and he or she alone has the answer to the world’s problems. believe they are already dead. Depressive episodes may He or she may plan to run for President, spend all his come and go, even without treatment, but generally money on campaign posters, attack the banker who recur. A case of severe major depression without psych- refuses to finance his television adverts, and fight with otic features is described in Box 32.3. policemen who are called to quell the disturbance. Since major depression is partly caused by genes Hypomania is a milder form of mania, which doesn’t (Sullivan et al., 2000) and leads to decreased fitness causemarkedsocialoroccupationalimpairmentor (Cuijpers and Smit, 2002), it presents the same conun- require hospitalization. Bipolar disorder is partly genet- drum as schizophrenia: how are alleles promoting it ically caused (Craddock and Forty, 2006). Adaptationist maintained in the population? models of low-level forms of mania mirror those of

554 Brant Wenegrat BOX 32.3. A case of severe depression. ME experienced his first severe depressive episode 2 years depressive symptoms returned. His ex-girlfriend – they had after graduating from college, at age 26. This episode broken up six months before – saw he was depressed again started after he failed to get a work promotion he and tried to get him back into treatment, but ME refused. He expected. He was pervasively sad, he lost 20 pounds, he again stopped going to work, neglected his hygiene, and lost interest in sports, sex, and friends, and he slept only started losing weight. He cried frequently and thought that 4 hours nightly, although he was exhausted during the day. he was worthless. His ex-girlfriend called ME’s landlord when He was consumed by feelings of shame and he saw himself as he didn’t answer his phone for a couple of days. Using his a failure and disappointment to everyone. After two months passkey, the landlord found ME lying on his bed, of illness, he stopped going to work. His girlfriend eventually malodorous, disheveled, and emaciated. ME improved got him to seek medical care. He recovered with dramatically after a month in the hospital. ME’s father and antidepressants and psychotherapy. Three years later, sister had also been treated for depressive episodes, which when he was off medications and out of therapy – the were not as severe as ME’s. depression. According to such models, mania might be held belief that it has a long history, anorexia nervosa as adaptive when social standing is rising (Gardner, 1988; it is now known first appeared in Western Europe and the Stevens and Price, 2000a), and milder manic traits United States during the late nineteenth century, and its may help individuals achieve positions of leadership subsequent prevalence has largely been determined by (Gardner, 1982; Akiskal and Akiskal, 2005). cultural dictates regarding ideal weights (reviewed in These models of mood disorders run counter to some Wenegrat, 1996). of the data. Contrary to the notion that depression is a Beyond the obvious weak points of adaptationist way of avoiding hostility, many depressed individuals models, some of which were cited above, the adaptation- are markedly irritable (Painuly et al., 2005). Contrary to ist paradigm faces some general challenges. Firstly, the notion that depression leads to assistance, depressed adaptationist models may not be needed or called for. individuals are seen in a negative light (Coyne, 1976) and Since psychiatric disorders are promoted bymany alleles, lose important relationships (Reich, 2003). Moreover, each with a small effect size, persistence of alleles leading Nettle (2004) points out that the high heritability of to mental disorders can be explained without recourse depressive disorders, the tendency of depression to occur to putative positive benefits (Keller and Miller, 2006). out of the blue – not in response to stressors, the chron- Occasional germline mutations can replenish any alleles icity of the illness once it is established, the absence of lost due to mental illness. concrete evidence that it serves a useful function, and the Secondly, even if risk alleles for psychiatric dis- plethora of evidence for adverse fitness effects are incon- orders do confer positive benefits, the adaptationist sistentwith depression being atruebiologicaladaptation. paradigm might focus too much on illness and illness- related traits: Genes leading to mental disorders might promote advantageous behaviors unrelated to illness Anorexia nervosa per se or confer advantages in other realms entirely. For example, a short allelic variant of the promoter The adaptationist paradigm has also been applied to region of the serotonin transporter gene increases anorexia nervosa, a disorder that occurs mostly in the risk of depression, especially following stressors young women and is characterized by a preoccupation (Jacobs et al., 2006; Wilhelm et al., 2006), but seroto- with thinness and a terror of becoming fat (American nergic dysfunction may lead to greater impulsiveness Psychiatric Association, 1994). By fasting and exercising, and earlier reproduction (Stein, 2006). A considerable anorexics reduce their weight to the point that they body of evidence suggests that immune system genes stop menstruating and become temporarily infertile. may contribute to schizophrenia (Strous and Shoe- Untreated anorexia may end in death from starvation. nfeld, 2006). If so, some genes that promote schizophre- A typical case of anorexia nervosa is described in nia may protect their carriers against viruses, cancer, or Box 32.4. Like schizophrenia, major depression, and autoimmune disorders. Neither of these possibilities bipolar disorder, anorexia nervosa is partly caused by are captured by adaptationist approaches to mental genes (Bulik et al., 2006). Several authors argued that disorders or illness-related traits. anorexia nervosa is an adaptive strategy for suppressing reproduction, when circumstances are such that repro- duction would be disadvantageous (Wasser and Barash, THE ETHOLOGICAL PARADIGM 1983; Surbey, 1987; Voland and Voland, 1989). As the case described in Box 32.4 illustrates, this model has Ethology is the study of species-typical animal behav- to explain how an illness so devastating can possibly ior.Humanethologyreferstothestudyofbehaviors increase fitness. Furthermore, contrary to the widely typical of Homo sapiens (Eibl-Eisbesfeldt, 1989) Being

Evolutionary Psychiatry: Mental Disorders and Behavioral Evolution 555 BOX 32.4. A case of anorexia nervosa. At age 14, SL was considered pudgy. She started dieting, on several occasions and was found to be anemic and to and by her 15th birthday she was noticeably thin. Over the have electrolyte abnormalities. Her bones were starting to subsequent six months her weight continued to drop. At lose calcium. She weighed herself numerous times each day. 15½, she was 5’4” tall and weighed only 95 pounds. Her If her weight was lower, she felt ecstatic; if it was even periods, which had started when she was thirteen, had slightly higher, she felt panic-stricken. She was afraid the stopped some months before. In spite of her weight loss, slightest gain would lead to loss of control and to her she saw herself as fat and would eat only diet food or salads becoming obese. When her weight dropped below 90 with no dressing. If allowed to, she would jog or use a pounds, SL was hospitalized and given nutrition through a stationary bicycle for two to three hours daily. She fainted naso-gastric tube. species-typical, such behaviors must result from the failure of a particular piece of the species-typical human action of human genotypes in “normal” human envir- behavioral repertoire. Individuals with these disorders onments. The ethological paradigm asks if signs and fail to fully engage in larger-than-family social groups symptoms of mental disorders can be described effi- or to adopt their worldviews. They are generally normal ciently by reference to human ethology. children, but when they reach adolescence – when For example, one typical human behavior evident normal individuals orient themselves in larger-than- in all cultures is to form close-knit social groups, family social groups – their social disengagement and members of which are considered superior to outsiders their inability to learn subtle social rules and the consen- (Tinbergen, 1976). In traditional tribes, for instance, sual worldviews of these larger groups first become outsiders may be killed, especially if they are male. apparent. They may seem odd to others. They start to The name of the tribe is frequently the term for feel uncomfortable outside their families of origin and human beings (Berger and Luckmann, 1966). In such fearful of others within the groups they might join. societies, small groups are composed of kin. Early Like some adaptationist models described in the studies of hunter-gatherer tribes, for instance, showed previous section, this ethological model locates the that members were only slightly less related on average pathology of the schizophrenia spectrum in larger- than first cousins (Chagnon, 1979). In such conditions, than-family groups, but it does not presume that the positive attitudes toward group members and invidi- deficit is or has been adaptive. The emphasis is on ous attitudes toward outsiders are consistent with kin placing deficits seen in illness in the context of the altruism. normal human behavioral repertoire. Persons in modern societies may not kill outsiders (though, sadly, they sometimes do), but they nonetheless Attachment theory cohere in small, invidious social groups. Spontaneous group formation and resultant outward hostility has John Bowlby, whose “Attachment Theory” has had a been shown in psychology laboratories, occurring major impact in psychiatry, studied relationships among total strangers (Tajfel and Billig, 1974; Tajfel, between caretakers and infants, and infants’ responses 1981, 1982). Formation of social groups is thought to to being separated (Bowlby, 1969, 1973, 1980). He dis- have protected early hominids from predation and early covered that infants separated from their principal humans from competing groups, and to reflect innate attachment figure, who don’t have other familiar psychological and behavioral factors (Alexander, 1979). attachment figures available, engage in stereotyped Human social groups, even those created in the emotional displays. In the first, or “Protest” phase, laboratory, develop consensual worldviews (reviewed in the infant cries or screams and attempts to follow or Wenegrat, 2001). Reality, in other words, is socially con- find the missing attachment figure. This phase may structed within the human group. Lumsden and Wilson last several days. If the caretaker doesn’t return, the (1981) argued that group enculturation was probably “Despair” phase will set in. Active efforts to signal or highly adaptive and led to the selection of conformity- find the caretaker cease, and the infant becomes promoting genotypes. The neurological basis of social apathetic and socially withdrawn. The third, or imitation is only now beginning to be understood “Detachment,” phase starts after separations lasting (see Meltzoff and Prinz, 2002). In real groups and in two weeks or more. The child in this phase is docile, groups created in laboratories, individuals who fail to apathetic, and detached from his or her social envir- conform may be seen as outgroup members and become onment. This phase may last a long time, even if the the object of aggression. attachment figure reappears. Many signs and symptoms of schizophrenia spec- Bowlby noted the similarities between children’s trum disorders manifest failure of normal group- attachment behaviors and separation responses and orientation (Wenegrat, 1990a). That is, they represent those shown by immature primates. He considered

556 Brant Wenegrat attachment behaviors and separation responses as evolved to solve social problems (Dunbar, 1998), evolved behavioral patterns common to humans and capacities like those listed here may depend on evolved primates. neural circuitry specialized for each purpose. According The resemblance between the phases of the separ- to researchers broadly identified as Evolutionary Psych- ation response and certain types of depression were ologists, specialized mental capacities that evolved evident to Bowlby. The Protest phase, for instance, for particular functions – or innate psychological resembles agitated depressions in adults. The Despair modules – comprise the basic structures of human and Detachment phases resemble “retarded” depres- mental life (Barkow et al., 1992; Hirschfeld and Gelman, sions, which are depressions characterized by psycho- 1994; Pinker, 1997; Cosmides and Tooby, 1997). The motor slowing, apathy, and withdrawal. This led to the innate-module paradigm asks if mental disorders can be hypothesis that adult depression is a manifestation of understood as dysfunctions of discrete evolved mental early attachment behaviors somehow reactivated, and modules. to the hypothesis that early attachment disruptions For example, studies have shown that humans more predispose to later depression. The latter hypothesis readily learn fear responses to objects and situations has found some empirical support, though depressive that posed threats to our ancestors – such as snakes, illness also occurs in people who had no attachment spiders,threatening animals,darkness,and high spaces– disruptions (Gilmer and McKinney, 2003). than to far more dangerous modern-day objects and This model of depression resembles an adaptation- situations, such as guns, knives, and high-speed driving ist model that treats depression as a response to loss of (Marks, 1987; Marks and Tobena, 1990). Also, fears of attention and interest from others, but there is no ancestral threats don’t diminish as rapidly in the supposition that depression as such is adaptive. absence of reinforcement as fears of modern-day Borderline personality disorder, pathological threats. Evidence like this suggests that common troub- mourning, and some factitious illnesses can also be ling phobias – such as phobias of snakes, spiders, understood as miscarried attachment behaviors animals, darkness, and high spaces (American Psychi- (Wenegrat, 1990a). For example, borderline personal- atric Association, 1994) – reflect evolved mental ity disorder is characterized by clinging, dependent modules that promote acquisition of fears advantageous behavior, intolerance of rejection, anxiety, depression, to human ancestors. poorly controlled aggression, and self-mutilation or Nesse (2001) compared evolved anxiety modules to injury – such as cutting or burning oneself – in human-made smoke detectors. As an occasional false response to stress. Nonhuman primates deprived of alarm is better than failure to sound an alarm in the maternal care show behavioral signs of depression event of a fire, smoke detectors are set to go off at a and increased aggression and fearfulness. When anx- very low threshold. An evolved anxiety module that ious, they bite and hit themselves. Studies of border- served to protect from a dire threat might likewise be line personality disorder patients reveal a very high tuned to sound an occasional false alarm. Individuals incidence of early abuse or neglect (Paris et al., 1994). whose experience or genes equipped them with slightly Ethological models may cast light on salient aspects more sensitive innate anxiety modules would be of serious mental disorders, but they do not account plagued by repeated false alarms, to their detriment. for all of their signs and symptoms. Schizophrenics, for The cerebral modularity of linguistic functions has instance, hear voices of people arguing; a model of been known since the nineteenth century. Psycholinguis- schizophrenia as a failure of group social strategies tic studies support the view that humans have innate cannot account for this or many other such symptoms. syntactical language processors. According to Timothy Crow, human vulnerability to psychotic disorders is a by-product of the modular organization of language THEINNATE-MODULEPARADIGM (Crow, 1995, 1997; 2002, 2007). Green and Phillips (2004) cite evidence that specialized neural networks – Evolved behavior patterns depend on innate perceptual, comprising an evolved social threat detector – rapidly cognitive, emotional, and motivational processes. For process signs of potential aggression from others.Clinical example, human males seek exclusive sexual access paranoia might result from excessive activity of this to fertile women (Trivers, 1985). To do so, they must evolved mental module, which causes ambiguous stimuli recognize signs of female fertility; experience sexual to be perceived as threatening. Schizophrenics with attraction to women in general and to fertile women in persecutory delusions have structural and functional particular; be able to understand their immediate social abnormalities in some of the neural systems described milieu – including social alliances, sexual rules, and by Green and Phillips. mores, and styles and manners of courtship; and feel High and low moods reflect changes in activity in emotions promoting stable, exclusive relationships, such specialized neural circuits (Morgane et al., 2005), which as affection and jealousy. Insofar as the human brain can be conceptualized as moodmodules. Several authors

Evolutionary Psychiatry: Mental Disorders and Behavioral Evolution 557 have analyzed potential adaptive functions served by the social deficits seen in autistic disorders. Among the normal moods (or normally functioning modules) to findings cited by Baron-Cohen, autistic children fail shed light on mood disorders (Nesse, 2000; Sloman and to demonstrate joint-attention behaviors: they do not Gilbert, 2000; Nettle, 2004; Dickinson and Eva, 2006; monitor or follow an adult’s gaze, nor do they point to Freed and Mann, 2007). To give just one example, objects or show objects to adults as a way of directing Nesse (2000) argued that normal moods serve to insure attention. To engage in such behaviors, children must productive effort allocations. In unpropitious circum- surmise an adult’s attentional focus. They fail “false stances, when goals and desires cannot be fulfilled, belief” tests. A typical false belief test involves seeing mood is normally lower. At such times, pessimism one person, say Sally, put a marble in one place, and and low motivation serve to conserve resources that later, while Sally is away, seeing Anne move the object would otherwise be wasted. In propitious circumstances, elsewhere. When asked where Sally thinks the object is mood is normally higher (see Tiger, 1979). Optimism located, very young normal children point to where and increased energy ensure that strong efforts are Anne placed it. Around the age of three or four years, made to utilize opportunities. Nesse’s view explains the however, they correctly point to where Sally had put it key role of low expectations in depressive disorders before leaving. They understand Sally’s viewpoint, and (Overmier, 2002). that Sally has a false belief. Unlike normal children, or The innate-module paradigm has been applied to mentally handicapped children without autistic fea- autism, a severe disorder appearing in early childhood tures, autistic children fail such tests at much later ages. or even infancy (American Psychiatric Association, In the early 1990s, a research group in Genoa study- 1994; Tidmarsh and Volkmar, 2003). Autism – like ing macaques discovered so-called mirror neurons in a schizophrenia – occurs in milder forms; hence psych- part of the frontal lobe corresponding to Broca’s area in iatrists now refer to autistic spectrum disorders. human beings (di Pellegrino et al., 1992). Mirror Severely disturbed children avoid physical closeness, neurons fire just before animals perform specific motor fail to make eye contact or respond to emotional ges- acts – grasping an object, for example – and also when tures, and ignore their parents’ voices. They lack inter- they see the same acts performed by others. Such est in other children or in normal childhood games, neurons seem to encode the concept of the act, whether such as hide-and-seek. They show stereotyped bodily in self or other. Related neurons in the temporal sulcus movements, such as clapping, rocking, or swaying, and even encode for intentions (Jellema et al., 2002). For are fascinated by repetitious motions, such as of fans example, such a neuron might fire when another animal or pendulums. Older children may become obsessed is observed trying to open a cylinder, regardless of the with collections or interests, such as bottle-caps or method – twisting the top or pulling it, or whether the baseball statistics, to the exclusion of other activities act is completed or not. and interests. Autistic children resist change and prefer Although the evidence is indirect, a system of mirror unvarying routines. New restaurants, stores, or routes neurons appears to exist in humans (Keysers and may meet with strong objections. Language skills are Gazzola, 2006). For example, functional brain scans limited. Higher functioning patients, with the mildest show that human brain regions corresponding to those forms of autism, generally become independent adults where mirror neurons have been found in monkeys show with deficits in social skills, but most affected children similar activations in preparation for motor acts and have a poor prognosis. When it was first described, while observing the same acts. Transcranial magnetic autism was thought to be extremely rare, but more stimulation (TMS) is a procedure for stimulating regions recent estimates show that its incidence is about 1 in of cerebral cortex with changing magnetic fields adm- 1000 children. Another 5 in 1000 may have spectrum inistered through the scalp. During TMS, observing a disorders closely related to autism. While there is a motor act triggers corresponding peripheral nerve activ- known genetic component to the disorder, environ- ity: A subject who sees someone grasping may show mental factors may also play causal roles. increased activity in nerves to his own hand. A critical step in anticipating and altering other Mirror neurons – and neurons encoding intentions, people’s behavior is to correctly infer their mental state – rather than just actions – encodesimple theories ofmind. that is, their beliefs, moods, and desires – from their In an animal study cited above, for instance, neuronal current and past behavior (Dennett, 1987). Since modern firing signified an inference that an act was intended to concepts of behavioral evolution suggest that the human open a cylinder – regardless of the method used (twisting brain was shaped by social necessities, such inferences or pulling) or the actual outcome. Hence, mirror neuron could depend on evolved neural structures specialized for systems may play key roles in social cognition, including that purpose. There might be mental modules adapted to theory of mind (Keysers and Gazzola, 2006). forming accurate theories of others’ minds. The same techniques that reveal mirror neuron Barron-Cohen (1995) and others suggested that a systems in healthy humans reveal deficits in autistic deficit in a “theory of mind module” can account for children (Fecteau et al., 2006). For example, with TMS,

558 Brant Wenegrat they fail to show peripheral nervous activation while gyrus, the frontal cortex, the nucleus accumbens, and viewing others’ actions (The ´oret et al., 2005). Mirror related regions are known to mediate reward and neuron deficits might disable a theory of mind module pleasure sensations (Baler and Volkow, 2006). In a in autistics, or the deficit might be elsewhere and drug-free environment, these ancient pathways reflected in mirror neurons. In any event, if these find- promote adaptive reward-seeking behaviors. However, ings hold up in future research, they will bolster the modern-day societies expose people to drugs that affect theory-of-mind hypothesis of autism. neurotransmitters – especially dopamine, glutamate, Like ethological models, innate-module models may and endogenous opioids – or neurotransmitter recep- fail to account for critical signs and symptoms of complex tors employed in these pleasure pathways, in effect mental disorders. Buller (2005), for instance, argued that hijacking the pathways to promote drug-seeking Baron-Cohen’s treatment of autism ignores serious def- behavior (Lu ¨ scher and Ungless, 2006). For example, icits unrelated to theory-of-mind. Also, some of these cocaine and amphetamine congeners (e.g., amphet- models may be criticized on the ground that essential amine, methamphetamine, Ecstasy) act to release mental capacities – even those dependent on localized dopamine from nerve terminals, increasing the brain circuits – may not be adaptations in a technical amount of dopamine in synapses, and opiates (e.g., sense (see Buller, 2005). For example, specific brain morphine and heroin) stimulate receptors that are regions are needed to read and write. Furthermore, we otherwise only responsive to endogenous opioids can identify children with highly specific deficits in (endorphins and enkephalins). Sedative hypnotics reading or writing abilities. Yet, reading or writing (alcohol, barbiturates, benzodiazepines) subject to “modules” cannot be adaptations, in the sense that they abusealterthebalancebetweenexcitatory(mostly evolved because of advantages accruing from written glutamatergic) and inhibitory (mostly gabaergic) neu- language. Instead, reading and writing are epiphenom- rotransmission and also stimulate dopamine and enal skills enabled by brain regions serving more primi- opioid release. In drug addicts, neural pathways that tive language and visual functions. In the absence might have promoted fitness promote self-destructive of definite evidence that capacities are adaptations, behaviors that lower inclusive fitness. Heroin addicts, modular models of illness – however instructive they for example, neglect or abuse their children while may be – are social-deficit models dressed up in Darwin- ruining their own health. Mothers addicted to ian garb. cocaine – which has especially powerful effects on pleasure pathways – may let their children die in order to stay high. THE MISMATCH PARADIGM Unlike other drugs of abuse, alcohol was present in the ancestral environment. Ripe, fermenting fruit is The mismatch paradigm starts with the fact that human especially rich in calories and nutrients and can be behavior evolved before the dawn of agriculture, some localized by the odor of alcohol it emits. In frugivores 8000–10 000 years ago, and that too little time has since (fruit eaters) – including nonhuman primates and early elapsed for large-scale evolutionary changes to have hominids – preference for the smell and taste of ethanol occurred. If this is true, human behavior evolved in the may be adaptive, since ethanol is linked with nutritional setting of small hunter-gatherer groups composed of rewards (Dudley, 2000, 2002, 2004). Opportunistic, close kin moving about in small ranges. Such groups fruit-induced drunkenness has been observed in several may have resembled extant hunter-gatherer tribes frugivorous species; most famously, elephants. which have been studied intensively by modern-day Human fermentation of fruits and grains appeared anthropologists. in Mesopotamia 6000 years ago. Alcohol distillation, to Modern society is a far cry from the small hunter- produce more potent beverages, was discovered in gatherer band. Unlike hunter-gatherers, people in seventh-century China and spread to Central Asia, the modern cities are exposed every day to strangers with Middle East, and later Europe. For the first time, a pref- whom they have little in common, may live far from kin, erence for the smell and taste of ethanol could lead to play ambiguous or conflicting roles in multiple social overconsumption. With alcohol freely available, genetic groups (such as at home, at work, or in their place of differences that were previously fitness-neutral began to worship), and lack clear authority figures or a sense of moderate the risk of becoming addicted. Research, for their social placement. If human behavior is adapted to instance, shows that genetic differences in enzymes life in small groups, then some mental disorders in the involved in degrading alcohol correlate with ethnic and DSM-IV might result from our living in settings to which racial differences in alcoholism risk, though not with we are ill adapted: a mismatch, in other words, between other health indices (Mulligan et al., 2003). According to our current setting and our evolved psychology. this model, alcoholism belongs with obesity and diabetes: The mismatch paradigm has been applied to disorders fueled by preferences that evolved in conditions drug abuse. Neural pathways in the anterior cingulate of scarcity, operating now in conditions of oversupply.

Evolutionary Psychiatry: Mental Disorders and Behavioral Evolution 559 The mismatch paradigm may explain societal differ- than those who have not been exposed. This is how ences in the outcome of schizophrenia. Schizophrenics epidemiologists established that cigarette smoking living in traditional rural societies are more likely to causes lung cancer and heart disease, and that asbestos marry and reproduce, to contribute to child-rearing, exposure produces certain malignant tumors. Cur- and to avoid isolation than schizophrenics living in rently, mismatch models suffer from lack of definite modern urban societies (Sartorius et al., 1996). As evidence that people in modern societies are actually discussed above, individuals with schizophrenia spec- mentally worse off than people who live in societies trum disorders don’t feel part of larger-than-family more akin to ancestral groups. As noted above, a tenta- social groups as healthy people do, nor do they conform tive case can be made for increased risk of psychosis in to the consensual worldviews associated with such urban societies, but much more data is needed before groups. They are loners with odd ideas. Large complex even tentative statements can be made regarding mood societies with competing and often incoherent world- and anxiety disorders. views may render schizophrenia-promoting genes much more dysfunctional than they were in the environment in which human beings evolved. In a related vein, com- THE PSYCHOTHERAPY PARADIGM plex urban environments – in contrast to rural ones – may exacerbate or even cause psychotic disorders, espe- Even with modern medicines, psychotherapy is an cially in individuals with strong genetic risks (Peen and essential component in the treatment of most mental Dekker, 2004). disorders (see, for example, Fava et al., 2005; Two mismatch models attribute anorexia nervosa to Rosenbaum et al., 2006). There are many different the novel power of media acting on evolved psychological types and schools of psychotherapy, but all of them processes. In a well-nourished society, slenderness is a aim to change feelings, beliefs, and relationship styles sign of female youthfulness and hence fertility (Singh, in a healthy direction. 1993). In such a society, same-sex competitive urges A therapist has to decide which of his or her patient’s cause women to value slimness. Mass media present feelings, beliefs, and relationship styles lead to distress in them with images of extremely thin high-status women, life, how best to talk about them, and how they can be such as models and actresses, which they try to emulate. changed. Explicitly or not, such decisions are theory- The result is self-starvation (Abed, 1998). Alternatively, driven. For example, if a patient whose mother just died some of the psychological and behavioral traits of seems upset but denies it, a therapist might suggest that patients with anorexia nervosa– such as their restlessness they’re not acknowledging how their mother’s death has and subjectively increased energy and their denial of affected him. The suggestion is based on theories of thinness – may be evolved responses to weight loss that parent–child relationships, loss and normal grief, emo- helped ancestral humans flee from local famines. In the tional control, and self-deception. Although different modern world, mass media disseminates unrealistic schools of therapy produce equivalent outcomes, therap- standards of feminine thinness, girls diet to meet ists who are most aware of the theories that guide their them, and adaptations to famine are set into motion decisions appear to be most effective in helping patients (Guisinger, 2003). change (Wampold, 2001). Therapists who cannot articu- Humans evolved in social groups composed of long- late their reasons for interventions are less likely to help term familiars. Modern humans, by contrast, may spend most patients. days surrounded by strangers with whom they can’t Although current therapies are certainly benefi- communicate. Emigrants or people living or working cial, the conceptual frameworks used by modern-day abroad are more likely than other people to develop psychotherapists share limitations or weaknesses paranoid delusions (Allodi, 1982; Kendler, 1982). In such (see, for example, Fancher, 1995). If therapists were cases, returning home may be curative. Exposure to armed with a more robust conceptual framework, strangers may also contribute to social anxiety disorder. could they offer more effective help to patients? The Many patients with social anxiety, for example, are psychotherapy paradigm asks if modern concepts of limited by anxiety when speaking in front of groups behavioral evolution can help therapists better iden- (American Psychiatric Association, 1994). If students, tify feelings, beliefs, events, and relationship styles they cannot take courses which involve giving presenta- relevant to illness and to mental health and to better tions. If working, they cannot take jobs or accept promo- understand these in particular patients. It asks if these tions requiring public speaking. Humans in ancestral concepts can offer a robust theoretical framework for groups would seldom if ever have needed to speak to informing the kinds of decisions psychotherapists groups of people who weren’t long-term familiars. make. In testing whether environmental factors cause On the face of it, the answer is likely to be positive. disease, the first step is usually to see whether individ- Patients in psychotherapy present with feelings and uals exposed to such factors have higher rates of illness thoughts, and with relationship problems, directly

560 Brant Wenegrat related to issues addressed in the overall framework of To give a simple example, the ethological attachment behavioral evolution: among many others, attachment model of depression implies that therapists should and separation, parent–child conflict and manipulation, pay special attention to patients’ concerns about lost conflict with siblings and children, conflicts with other relationships. Adaptationist and ethological social rank kin, regulation of sexual appetites, same-sex and other- models direct attention to patients’ concerns about social sex conflicts, resource competition, status competition, status. But the therapeutic enterprise is over 100 years membership in social groups or ostracism from them, old now, and much has already been learned. Therapists social reputation, reciprocity obligations and moralistic already know that depressed patients ruminate about aggression, control of aggression and fear of other lost or threatened relationships and/or their social status, peoples’ behavior, and self- and other-deception. All of and that talking about these issues is vital to their these have been treated from a Darwinian viewpoint. recovery. In fact, the plausibility of the attachment In fact, the Darwinian framework is singular in models and the social rank models rests in large part on explicitly tackling the range of issues encountered by clinical knowledge gleaned by psychotherapists. psychotherapists. Adaptationist, mismatch, and ethological models cited in previous sections may guide therapy of specific SUMMARY disorders (Glantz and Pearce, 1989; Sloman and Gilbert, 2000; Stevens and Price, 2000a). However, evolutionary Psychiatric disorders are common, occur in all societies, models of normal behavior may prove to be more and have fitness consequences. Concepts from behav- valuable in relation to psychotherapy than models of ioral evolution – so successful in accounting for human illness per se. For example, evolutionary concepts of behavior generally – may shed light on their symptoms, normal behavior have been applied in relation to clas- causes, and possible treatments. sical Freudian theory (see, for example, Slavin, 1985; Most work in the field of evolutionary psychiatry Badcock, 1986; Slavin and Kriegman, 1988, 1992), to has relied on one of five paradigms. The adaptationist the Jungian notion of archetypes (see, for example, paradigm aims to view mental disorders, their milder Wenegrat, 1990b; Stevens, 2002), and to some aspects variations, or illness-related traits as behavioral adapta- of object-relations theory, a branch of psychoanalysis tions that confer or have conferred inclusive fitness (see Wenegrat, 1990a). Evolutionary treatments of benefits. The best-known adaptationist models are of normal behavior can also shed light on aspects of schizotypal oddity and depressive episodes, but there psychotherapy generally, such as mental suggestion also adaptationist models of several other disorders, (Wenegrat, 2001) and unconsciousness, self-deception such as anorexia nervosa. As we have seen, the evidence and mental inconsistency (see, for example, Trivers, is weak that any mental disorder or a milder variant is 1985; Kurzban and Aktipis, 2007). an adaptation, in the technical sense, but research on Findings in social psychology and social cognition reproductive fitness of patients and relatives and its will prove essential to the psychotherapy paradigm. correlation with illness-related traits – exemplified by a In many cases, these findings flesh out more abstract study conducted by Nettle and Clegg (2006) – may lead to concepts from Behavioral Evolution. For example, future progress. Future research could be strengthened social cognitive research has uncovered mental processes by using life-history data to estimate inclusive fitness, that produce co-ordinated behavior in larger-than-family which is a broader measure of Darwinian fitness than groups (reviewed in Wenegrat, 2001). This research and reproductive success (see, for example, Madan, 2002). the related evolutionary ideas turn out to be highly Whether adaptationist models of mental illness are relevant to the process of psychotherapy. really needed at all – that is, whether persistence of genes Of course, evolutionary concepts cannot be used in promoting mental illness really implies some benefits – therapy except in relation to cultural factors and differ- and whether such models are focused on the right kinds ences. Evolved behavioral patterns take on particular of benefits are two major open questions. forms, depending on the culture in which they are The ethological paradigm asks if a mental disorder expressed. Some cultures, for example, favor paternal can be described economically in relation to elements investment; other cultures don’t (Kurland, 1979). The of the normal behavioral repertoire observed in all same paternal behavior – care or neglect – has a different societies. As we have seen, mental disorders can be meaning depending on whether the culture is of one type characterized as miscarriages of attachment behaviors or the other. However, the same is true for other theoret- and group-related behaviors. However, ethological ical frameworks psychotherapists now use: none can be models generally don’t encompass the full complexity applied in the absence of cultural knowledge. of DSM-IV disorders. A more serious challenge for psychotherapy The innate-module paradigm asks if mental dis- models is avoiding triviality or even circular reasoning, orders can be explained in terms of evolved mental especially when relying on models of mental disorders. modules, as these are hypothesized by Evolutionary

Evolutionary Psychiatry: Mental Disorders and Behavioral Evolution 561 Psychologists. Anxiety, mood, and autistic spectrum flaws in their current conceptions of health, behaviour, disorders have been analyzed as modular dysfunctions. and therapy processes. If strong concepts and research Like ethological models, innate-module models often findings from behavioral evolution – along with related fall short of encompassing the full range of illness ideas from social and cognitive psychology – can be phenomena, and they are also subject to the concep- broadly disseminated while avoiding the obvious pitfalls, tual problem vexing evolutionary versions of modular they should be warmly received. To paraphrase Sigmund theory: the difficulty of proving that given mental cap- Freud, who was writing of dream analysis, the psycho- acities are technically adaptations. therapy paradigm provides a royal road through which The mismatch paradigm tries to explain disorders in Darwinian concepts can enter the minds of clinicians. terms of potential mismatches between our current environment and our evolved psychology. This viewpoint is most convincingly applied to drug addiction and to DISCUSSION POINTS alcoholism. It may also shed light on some little-noticed epidemiologicalfeaturesofmentaldisorders,suchas 1. Compare and contrast adaptationist and mismatch cultural differences in the outcome of schizophrenia models of anorexia nervosa (AN). Identify some life and the high incidence of paranoia in immigrants. As events for which these models predict different discussed above, cross-cultural incidence data will be effects on the course of patients with AN. For essential in proving that features of modern society example, what would these models predict for a cause any mental disorder. mother with AN as she approaches menopause? Finally, the psychotherapy paradigm asks if modern Identify social conditions which these models pre- concepts of behavioral evolution can help therapists dict would affect prevalence rates. Do online understand feelings, beliefs, and relationship styles research to see if some of these predictions have been relevant to illness and to mental health. It asks if these studied. (Suggestion: start by searching Medline at concepts can offer an overarching framework for the www.ncbi.nlm.nih.gov/pubmed.) types of decisions psychotherapists make. The psycho- 2. Argue for and against the following proposition: therapy enterprise is over 100 years old now, and much “Evolutionary psychiatry is bedeviled by confusion is already discovered. To be successful, the psychother- between extreme mental states and their normal apy paradigm will have to do more than tell therapists counterparts.” In arguing this point, consider each what therapists already know, while avoiding circular of the major disorders described in this chapter reasoning. and each of the separate paradigms. Which para- It seems likely that all five paradigms will figure in digm(s) are best equipped to deal with normal the future of evolutionary psychiatry. Adaptationist states? Which paradigms are best equipped to deal models may explain some disorders, while ethological, with extreme states? innate-module, or mismatch models explain others. 3. The risk of schizophrenia is increased in individ- Several paradigms may apply to a single disorder: uals whose mothers had influenza in the early For example, creativity may explain the persistence of second trimester. Likewise, the risk of schizophre- certain risk genes in the families of schizophrenics, while nia in offspring of schizophrenics appears to be dysfunctionof socialcognition accounts for who actually increased by complications at birth. Which of the falls ill. Cultural variation in the outcome of schizophre- evolutionary models of schizophrenia described in nia may be due to factors explained by mismatch this chapter can most readily accommodate these models. Adaptationist models might account for mild facts? How could such findings be reconciled with depression, while ethological or innate-module models other models? better describe severe depression. The triggers for mild 4. Schizophrenics and major depressives have high depression and the causes of ethological or modular lifetime risks of suicide. How might you reconcile dysfunctions that occur in severe depression might both adaptationist models of these disorders with these be analyzed in terms of mismatch models. high suicide risks? Under what conditions might Above all the others, the psychotherapy paradigm suicide have positive effects on inclusive fitness? probably holds the key to the future of evolutionary With these conditions in mind, why should schizo- psychiatry. Although it can utilize work from each of phrenics and major depressives be more likely to the other paradigms, the psychotherapy paradigm kill themselves than anyone else? doesn’t require robust models of mental disorders. As 5. Describe several novel predictions derived from we have seen, for the most part such models are lacking. adaptationist models of mental disorders. Do Existing evolutionary accounts of normal behavior are online research using databases like Medline to equally – if not more – relevant to psychotherapy than find existing data pertaining to your predictions. models of mental disorders narrowly conceived. Further- If you can’t find such data, briefly outline studies to more, many practicing therapists are keenly aware of test your predictions.

562 Brant Wenegrat 6. Describe several novel predictions derived from Bowlby, J. (1969). Attachment and Loss, vol. 1. New York: mismatch models of mental disorders. Do online Basic Books. research using databases like Medline to find Bowlby, J. (1973). Attachment and Loss, vol. 2. New York: existing data pertaining to your predictions. If Basic Books. you can’t find such data, briefly outline studies to Bowlby, J. (1980). Attachment and Loss, vol. 3. New York: Basic Books. test your predictions that could be performed in a Bulik, C. M., Sullivan, P. F., Tozzi, F., et al. (2006). Prevalence, single country. heritability, and prospective risk factors for anorexia ner- 7. Psychotherapy often focuses on patients’ responses vosa. Archives of General Psychiatry, 63(3), 305–312. to disturbing events. From the point of view of Buller, D. J. (2005). Adapting Minds: Evolutionary Psychology behavioral evolution, describe some common events and the Persistent Quest for Human Nature. 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33 Industrial Pollutants and Human Evolution Lawrence M. Schell INTRODUCTION: THE ANTHROPOLOGICAL humans? And, given that the study of pollutants is not STUDY OF INDUSTRIAL POLLUTANTS traditional in anthropology, what is the right way to determine if industrial pollutants have any effects on Human experience with industrial pollutants is very human biology, evolution, and health? An important recent and very brief relative to the span of our species’ and related question is, how do anthropologists deter- evolution. Marked increases in pollution exposure mine successful adaptation, what are the appropriate began in the mid 1700s with the industrial revolution. measures? It seems paradoxical that Homo sapiens evolved in This chapter will address these questions but the response to features of decidedly nonindustrialized conclusions are provisional. The research necessary to environments but is now largely an urban species living address these questions is still developing across a in industrialized societies. Are we somehow prepared broad range of disciplines. Typically, reviews of by our evolutionary history to deal with industrializa- research on pollutants are organized to describe the tion, or is this an adaptive challenge confronting effects of one pollutant at a time. In contrast, this modern Homo sapiens? review is organized by endpoints that relate to chal- This large question is dissected into more scien- lenges to reproduction: human growth and aging, mor- tifically manageable ones that evolutionary human bidity and mortality which are areas anthropologists biologists can use to structure research. For example, have studied to understand human evolution and bio- using demographic measures of species success (Gage, logic variation (Stinson et al., 2000). Due to space limi- 2005), Homo sapiens appears to be flourishing. This tations this is not a comprehensive review of all conclusion is based on comparisons of populations’ pollutants, or of all effects of any one pollutant. An mortality profiles, over space and in different historical effort is made to include contrary studies in each case periods. Using other measures of adaptation however, to emphasize methodological issues that are raised by such as patterns of growth and development or mor- the diversity in results. The review is intended to intro- bidity patterns, the adjustment may appear far less duce the subject including the inherent methodological than complete. Although industrialization produces difficulties that may produce variety in the results. economic benefits and related health benefits, it also Unfortunately, the review cannot include a description produces pollutants that are detrimental to biological of global warming and its impact on human evolution systems particularly among the socioeconomically dis- although global warming is clearly related to industrial advantaged. Should we consider all the impacts pollution and may have a tremendous impact on together in a summary measure of success such as life our species. span, or should we “unpack” the urban environment by An important consideration when considering pol- determining the specific constituents of urban environ- lution’s effects on human evolution is how much of an ments, and considering the effects of each constituent impact do pollutants make? This is a difficult question on specific outcomes (Schell and Ulijaszek, 1999)? This to answer for several reasons. Most research on pollu- latter approach is taken here. By analyzing the ques- tants concerns disease outcomes rather than fertility or tion in terms of effects of specific industrial pollutants, other effects of import to evolution (changes in gene we may be able to see the direct effects of these elem- frequencies in a population). In large populations such ents, remembering that the relationship between as those in industrialized societies where pollution is industrialization and health is dynamic and could generally greatest, fertility is low and influenced change (Schell and Ulijaszek, 1999). greatly by social factors. Natural selection in response The questions are these: Are there features of to pollution and modern stressors in such populations industrialization that pose biological challenges to has not been studied and probably cannot be because Human Evolutionary Biology, ed. Michael P. Muehlenbein. Published by Cambridge University Press. # Cambridge University Press 2010. 566

Industrial Pollutants and Human Evolution 567 of the limitations of modern methods. However, evolu- biologists have left biological typology behind and tion may be affected without natural selection operat- may now leave environmental typology behind as ing as the two are not synonymous, and evidence for well. A second reason is the effect of offsetting impacts. nonadaptive genetic changes, such as mutations, in Industrial pollutants may have detrimental effects that response to pollutants are evidence of evolutionary pose challenges to adaptation yet at the same time the change too. delivery of health care may be more intense in indus- trialized areas. The two opposing forces can balance one another producing a net effect of zero in a general HOW WILL WE EVER KNOW? METHODS, health measure. However, this does not mean that the METHODS, METHODS pollutants are innocuous. The third and final reason is that the aggregate approach does not recognize the Knowing the answer to the questions of effects of many effect of social arrangements, by which I mean all the environmental features, including pollution, depends terms that are used today to indicate that power rela- on the suitability of methods. Generally we observe tions in societies structure resources, exposures and only statistical relationships between pollutants and risks that produce biological differences along lines of health effects because we would not knowingly create social difference (Schell, 1998). Health disparities an experiment by exposing persons to possibly injuri- (minority, “racial” [sic], or ethnic disparity) is the term ous pollutants. With observational studies there are used in public health to describe this. Thus, large five elements that should be present (usually requiring aggregates may seem healthy but the analysis of health more than one study) to determine if the pollutant by social gradients within these larger aggregates may actually causes the biological effect, and these are reveal the true biological challenges. known as Hill’s Criteria of causation. The criteria A better approach is to measure the amount of most often emphasized are: (1) a dose–response rela- exposure to a particular pollutant and compare that tionship between putative cause and effect; (2) a bio- to specific effect of interest to human biologists (fertil- logically plausible relationship; (3) replication of ity, menstrual cycle characteristics, sperm counts, pre- results; (4) a temporal sequence (cause precedes reproductive mortality, growth, development, etc.). effect); (5) a strong relationship; and (6) consistency Human biologists have excellent methods for measur- across tests of the relationship. When all six conditions ing effects in physiological systems, but measuring the are met we are much more certain that a relationship environmental factor is often not as rigorous. This is an observed between a pollutant and a health effect has a example of unbalanced precision. Comparisons of causal basis. urban and rural populations, the environmental typ- Sometimes there is a reason to relax at least one of ology referred to just above, involves not measuring these criteria. For example, some biologically implaus- environmental features as they are assumed to be the ible relationships between a pollutant and a health same in each type of environment. This approach pre- effect have turned out to be true, and in pursing the vents observation of effects of the specific features of implausible we learn about new biological processes. each. Measuring those features should produce more In this vein, sometimes a straight dose–response rela- accurate descriptions of their effects, and yield more tionship does not fit the data and a U- or J-shaped accurate and reliable information. relationship is evident. Today the matter of hormetic effects, that is a reversal in the direction or strength of a dose–response relationship that occurs at very low WHAT ARE INDUSTRIAL POLLUTANTS? levels of exposure, is under close investigation (Cala- brese, 2005). Pollution is usually defined as an unwanted material The old standby approach of comparing industrial- or energy that is considered a threat to well-being. Pollu- ized and nonindustrialized populations is no longer tants are produced by industrial processes, but many used to discern effects of specific pollutants for several pollutants, carbon dioxide (CO 2 ), methane, dust, etc., good reasons (Schell and Denham, 2003). Firstly, are produced by natural processes as well (Waldbott, industrialized places vary amongst themselves as do 1978). For this reason alone humans may have physio- nonindustrialized ones. Further, they do so across sev- logical mechanisms to deal with exposure to some pollu- eral dimensions and continuously. To classify settle- tants. Some of the best information on pollutants is ments into just two categories is a form of typology, available through US government websites (for example and typology steamrollers over variation. A typological http://www.atsdr.cdc.gov/toxpro2.html). approach to understand the impact of industrialization Persistent organic pollutants (POPs) are a group of ignores the diversity inherent in such populations, compounds that are toxic, are resistant to breakdown and thus it cannot use that diversity to understand in the environment (indeed many were created to the different impacts of industrialization. Human have this property for industrial or agricultural

568 Lawrence M. Schell despite widespread reductions in environmental lead TABLE 33.1. Persistent organic pollutants. The US Environmental Protection Agency’s “Dirty achieved over the past 25 years. Dozen.” Humans are exposed to lead and POPs chiefly through the diet, although airborne and dermal routes Industrial Pollutant Pesticide chemical By-product of exposure may contribute to some extent also. Humans consume POPs in commercially available Aldrin X foods, fish caught locally in contaminated waterways, Chlordane X as well as through packaging. Nonoccupational lead Dichlorodipheny- X exposure occurs largely through ingestion especially ltrichloroethane by placing nonfood items in the mouth, which is very (DDT) common among toddlers. Respiration of lead particles Dieldrin makes a far smaller contribution to the intake. Expos- Endrin ure to industrial pollutants is widespread. The US Heltachlor Centers for Disease Control and Prevention (2005) Hexachlorobenze X X X reported that evidence of tobacco smoke, lead, mer- Mirex X cury, and phthalates are detected in nearly the entire Toxaphene X US population and nearly 150 chemicals were detected Polychlorinated XX in some portion of the US population. biphenyls (PCBs) Air pollution is a heterogeneous mixture including Polychlorinated X oxides of nitrogen (NO x ), oxides of sulfur (SO x ), carbon dibenzo-p-dioxin monoxide (CO), ozone (O 3 ), and particulate matter Polychlorinated X dibenzo-p-furans (PM). Particulate matter is usually classified by par- ticle size. Particulate matter is not only a pulmonary irritant but also is a vehicle to bring specific com- pounds into the lung and then the bloodstream where it can produce systemic effects. applications). Generally POPs are lipophilic and there- Noise is the only pollutant included in this review fore are present in dietary fats and are stored in that is not a material but a form of energy (radiation adipose tissue. As a result of this biologic process, and light are others). Noise is defined as unwanted POPs typically increase in tissue concentration up the sound, and is measured in terms of duration, fre- food chain in a process termed biomagnification quency, and volume (decibels). Noise produces both (Table 33.1; http://www.epa.gov/oppfead1/international/ auditory and nonauditory effects, the former related pops.htm). Thus, animals near the top of the food chain, more to the nerve damage produced by the energy piscivores and carnivores, can have substantial concen- content, and the latter by its ability to create annoy- trations of POPs because in a lifetime they consume ance, stimulate the autonomic nervous system and to many animals that have consumed other animals that produce stress (Kryter, 1985). Thus, although noise is have consumed small quantities of POPs. Notable POPs measured as energy, its nonauditory effects are pro- are polychlorinated biphenyls (PCBs) and dioxins which duced by stress. have similar structures (Figure 33.1). It is impossible to include here detailed descriptions Phthalates are compounds used widely in con- of the routes of exposure to these pollutants, although sumer products primarily to soften plastic items such such maps provide ample interesting evidence of the as shower curtains, garden hoses, food containers, but social input to pollutant exposure of interest to anthro- also can be present in floor tiles, furniture upholstery, pologists (Schell and Czerwinski, 1998). Likewise, shoes, hairspray, and other products used in daily life details of pollutant measurement methods would (Yang et al., 2006). They are found in polyvinylchlor- require substantial additional space, although they per- ide, which is widely used and familiar to us as plastic tain to the quality of research discussed. Readers are plumbing and vinyl siding. Phthalates are also found in referred to the many excellent reviews and texts on this plastics used in medical tubing, and are found in air, subject (National Research Council, 1999). water, and food (Duty et al., 2003). Lead is a base metal that is completely unnecessary for human health. Lead dust is more concentrated POLLUTANTS AND PRENATAL GROWTH: alongside roadways as a result of deposits from vehicle OPPORTUNITY FOR FETAL PROGRAMMING exhaust, and in, on, and around older homes painted AND EFFECTS with lead-based paint. Depressed, older, inner-city neighborhoods with both features have populations Alterations in the pattern of prenatal growth are most with higher lead levels relative to other populations commonly discerned as changes in birthweight, length

Industrial Pollutants and Human Evolution 569 (a) (b) 3 2 2′ 3′ Cl O Cl Cl x Cl y 11′ OO 4 4′ Cl O Cl PCDD 56 6′ 5′ 2,3,7,8 - tetrachlorodibenzo-p-dioxin (c) 3′ 3 OH HO OCH CH C 2 5′ 5 NH O 2 3,5,3′,5′,-Tetraiodothyronine (thyroxine, T ) 4 HO O CH 2 CH C OH NH O 2 3,5,3′,-Triiodothyronine (T ) 3 (d) OH I IO 33.1. Polychlorinated biphenyl (a), dioxin (b), thyroxine (c), and estradiol (d), showing similarities in structure that are thought to underlie some of the hormonal effects of the toxicants. The numbered positions on each ring of the polychlorinated biphenyl may be substituted with a chlorine. Depending on the location and number of substitutions, the molecule will vary in persistence and toxicological properties. Unchlorinated molecules can resemble dioxin and dibenzofurans which are considered highly toxic. of gestation, and the occurrence of congenital malfor- unsuccessful changes as programming but consider mations. Alterations in prenatal growth signify adverse these changes as the result of constraint. These would circumstances for growth and development and pos- be changes in fetal growth induced by the environment sibly health generally (Schell, 1997). Alterations in that produce malformations or other clearly detrimen- growth patterns also suggest the action of fetal pro- tal effects. Distinguishing between altered fetal growth gramming with significant effects occurring far later that is a part of fetal programming from altered fetal in life (Kuzawa and Pike, 2005; Newbold et al., 2006). growth that is only detrimental, is difficult on theoret- Fetal programming refers to alterations in fetal physi- ical grounds (Ellison and Jasienska, 2007). ology through epigenetic processes, wrought by infor- The classic work on programming concerns the mation transferred from mother to fetus. Programming influence of nutrition on adult health and disease. How- can result in altered patterns of postnatal growth and ever, a recent review of research on pollutants and functioning, and much later affect adult health. Pro- reproduction emphasized the role of pollutants in modi- gramming usually refers to changes that are adaptive fying the epigenome (the biochemical reactions that in the short term in that they are thought to allow fetal influence and constitute gene expression) (Woodruff survival or anticipate conditions in postnatal life, but et al., 2008). As more studies on pollutants and gene may involve changes with a cost, and could be detrimen- expression find links of exposure to later adult health, tal to health in later life. As such they involve a classic pollutants should be considered another influence on trade-off between resources devoted to promote growth fetal programming. versus those devoted to promote reproduction. Gener- Pollutants can alter prenatal growth and or pro- ally most writers on programming do not include duce effects pertinent to reproduction later in life.

570 Lawrence M. Schell Although such effects have not been considered cognitive development even at rather low levels of programming as just described, they have all the out- blood lead, although contrary studies can be found also ward signs of it except the production of benefit (for review see Andrews et al., 1994). The case of lead is at some point in the life span. The classic case of instructive because the size of the reduction in birth- chemical modification of long-term development is weight or head circumference may be small, but the diethylstilbestrol (DES) (Newbold, 2004). This is a syn- size of the affected population is enormous. thetic sex hormone with estrogenic effects prescribed Evidence for an effect of POPs on prenatal growth to many pregnant women in the mid twentieth century is extensive but not consistent (see Schell 1991, 1999 to prevent miscarriage but was ineffective. However, it for reviews, and for some evidence of the complexity of did promote the development of vaginal cancer in the analysis also see Berkowitz et al., 1996; Longnecker young adult women who were in utero while their et al., 2001; Eskenazi et al., 2003). The strongest evi- mothers were taking the drug. Thus, we know that dence for an effect comes from studies of the offspring exogenous hormones can influence the developing of Japanese and Taiwanese mothers who consumed reproductive system and produces significant late- rice oil contaminated with a mixture of POPs including occurring effects including changes in behavior and dibenzofurans and PCBs. The contamination caused a adult-onset disease. Hormonally active agents in the disease called Yusho in Japan and Yu-cheng in Taiwan. environment are of great concern (National Research Offspring in utero at the time the rice oil was con- Council, 1999). sumed were smaller at birth in both cases (Yamaguchi There have been several reviews of studies on air et al., 1971), and offspring exposed in utero after con- pollution and prenatal growth (Schell and Hills, 2004; sumption ended were smaller also probably from POPs Lacasana et al., 2005; Sram et al., 2005) and in addition stored in mother’s adipose tissue from the earlier to the main finding of reduced prenatal growth, it is exposure (Yen et al., 1989). Studies of birth size in apparent that the strength of biological effects varies relation to fish consumption (Dar et al., 1992), a by pollutant. There are mixed findings for effects of common route of POP exposure, are complicated by nitrogen dioxide (NO 2 ), carbon monoxide (CO), and the nutrients in fish that promote prenatal growth sulfur dioxide (SO 2 ). At this time the strongest evi- (Jacobson, 2004). dence is for an effect of particulate matter including Noise is a consistent by-product of many industrial increased frequency of low birthweight and prematur- processes and transportation in industrialized soci- ity (Xu et al., 1995; Bobak, 2000; Lee et al., 2003; Leem eties. Changes in mean birthweight and the frequency et al., 2006), small for gestation age (Parker et al., of low birthweight may be influenced by noise pollu- 2005), and intrauterine growth retardation (Dejmek tion because noise is capable of producing a stress et al., 1999) as well as to reductions in mean birth- response during pregnancy (Welch and Welch, 1970; weight (Chen et al., 2002; Yang et al., 2003; Gouveia Committee on Environmental Health of the American et al., 2004; Parker et al., 2005). The validity of air Academy of Pediatrics, 1997). Many studies of popula- pollution’s role is supported by the worldwide distribu- tions living near airports find that noise stress from tion of studies in this literature: e.g., Canada, China, airplane takeoffs and landings is associated with Czech Republic, Korea, Taiwan (Xu et al., 1995; Bobak reduced prenatal growth (for review, see Schell and and Leon, 1999; Bobak, 2000; Liu et al., 2003; Lee et al., Denham (2003). Studies conducted in Japan have ana- 2003; Yang et al., 2003). When results are replicated in lyzed large numbers of births and found a clear dose– different societies it suggests that the statistical associ- response relationship between noise levels and the fre- ations are not produced by bias from uncontrolled quency of small newborns (Ando and Hattori, 1973) as variables especially socially mediated ones. Some well as temporal associations between the introduction uncontrolled variables exist in most observational of loud jet aircraft and the frequency of small new- studies, but the same configuration of socially medi- borns (Ando, 1988). Repeated associations of the same ated variables is less likely to occur when many differ- direction and magnitude, a temporal association and a ent societies are studied. dose–response curve all support the theory that noise The effect of lead on prenatal growth is now well stress affects prenatal growth. No single study is defini- established and the problem of impaired cognitive tive by itself, but when the entire body of work is development has been included in US Government considered in conjunction with laboratory and field publications on the risks of lead exposure (Centers for studies of short-term physiological responses to airport Disease Control and Prevention, 1991). Studies con- noise (Evans et al., 2001) most of the criteria for a ducted in a variety of settings, including those where causal inference are met. There are, however, studies lead exposure does not covary closely with poverty as it that have not found effects. Some have studied women has in the United States (Bornschein et al., 1987; exposed to lower levels of noise than is found around Bellinger et al., 1991a, 1991b; Gonzalez-Cossio et al., airports or noise that is expected and therefore not 1997; Schell and Stark, 1999) show that lead impairs necessarily very stressful (Wu et al., 1996).

Industrial Pollutants and Human Evolution 571 What is true for all studies of environmental influ- controlled for socioeconomic factors and body size ences is that findings pertain to a specific range of statistically. exposures, and the effects reported in any single Delay in reaching menarche in relation to blood study depend on the range of exposure present. Some lead level was observed also among Akwesasne variation in results across studies of different expos- Mohawk adolescents. Also, PCBs were associated with ures and social circumstances is therefore expected a significantly earlier age at menarche (Denham et al., and evident. 2005). In this study, not all PCBs were associated with changes in age at menarche, and the effect was found with a group of estrogenic congeners identified as such ENDOCRINE SYSTEM EFFECTS: GROWTH, through laboratory studies. Polybrominated biphenyls MATURATION, AND MENARCHE (PBBs) have been associated with earlier age at menar- che and attainment of pubic hair stages in breast-fed Many POPs are known to alter the development of girls (Blanck et al., 2002). However, Flemish adolescents some parameter of the endocrine system that suggests experienced delayed sexual maturation in relation to effects may develop later in life (Brouwer et al., 1999; polychlorinated aromatic hydrocarbons (Staessen Stein et al., 2002). Growth, sexual maturation, men- et al., 2001; Den Hond et al., 2002). Furthermore, age strual cycle characteristics, sperm quality by numerous at menarche among girls in Seveso, Italy who had been measures, fertility, and fecundability have been stud- exposed to dioxin from an industrial explosion, was not ied in one or more populations, usually retrospectively, altered (Warner et al., 2004). Interestingly, the authors following known exposure. Nevertheless, there is noted that most effects of dioxin seen in laboratory ample evidence for effects on these parameters. studies were from prenatal exposure, whereas the Effects of some pollutants on postnatal physical sample of Seveso girls had had postnatal exposure only. growth have been reviewed (Schell and Knutson, These results illustrate the variation in effects that 2002). Blood lead clearly influences postnatal growth can be found in studies of many groups of pollutants. and development even at moderate to low levels Here there is a variety of chemical substances involved (Ignasiak et al., 2006). Also, POPs can affect growth, in uncontrolled exposures at possibly different ages and the strongest evidence coming from studies of children at different doses. As these results are based on obser- exposed to rice oil contaminated with a variety of POPs vational studies of humans, the cause and effect rela- including dibenzofurans and PCBs (Rogan et al., 1988). tionship cannot be inferred. Support for a true causal Studies of other samples are supportive of 1,1-dichloro- relationship is derived from experimental studies in 2,2-bis(p-chlorophenyl)ethylene (DDE)-related effects which laboratory animals were dosed with a toxicant (Gladen et al., 2000; Longnecker et al., 2000) and PCBs and experienced delayed maturation (for example, with may play a role as well (Blanck et al., 2002; Gallo et al., lead, McGivern et al., 1991; Corpas et al., 2002; Dearth 2002). Air pollution is related to poorer physical growth et al., 2002), suggesting that the associations in humans in many studies (reviewed in Schell and Hills, 2004); for do not occur by chance and are not caused by some particularly good recent studies see Jedrychowski et al. other unmeasured factor (Goldman et al., 2000). (1999) and Jedrychowski (2000). Sexual maturation holds special interest as altera- tions in age at menarche relate to the length of the ENDOCRINE SYSTEM EFFECTS: FEMALE reproductive span and may affect fertility. Alterations REPRODUCTIVE FUNCTIONING in age at menarche also signal significant effects on the system of endocrine and central nervous system (CNS) Some of the earliest studies of PCBs found substan- control over maturation and other related endpoints tially reduced fertility and increased newborn mortal- such as ovulation, fertilization, implantation, and ity among rhesus macaques (Allen et al., 1979). Animal reproduction generally. Age at menarche is also related models continue to be important in studying repro- to adult-onset diseases. ductive effects as PCBs have been related to alterations In humans populations, lead and persistent organic of the menstrual cycle in nonhuman primates (Willes pollutants have been associated with changes in age at et al., 1980), and studies in other model species (rats, menarche. Analyses of data representing the US popu- mice, and mink) are confirmatory (http://www.atsdr. lation showed that the level of lead in the blood at the cdc.gov/DT/pcb007.html). time of interview was associated with delayed menar- Strong evidence of effects among humans comes che among girls 8–18 years of age (Selevan et al., 2003; from studies following the Yu-cheng accident. Women Wu et al., 2003). The delays varied from one to six who had consumed rice oil that had been contamin- months. Also attainment of Tanner breast and pubic ated with a combination of POPs (dioxin, dibenzofur- hair stages was associated with very small increases of ans and PCBs) had significantly more abnormal blood lead levels from 1 to 3 g/dL. The investigators menstrual bleeding (Yu et al., 2000). Girls who had

572 Lawrence M. Schell been exposed in utero had higher rates of irregular answered well by studies of human populations menstrual cycles, and serum estradiol and follicle- because of the normal variation in sperm quality, the stimulating hormone (FSH) were higher too (Yang large variety of pollutants that might be tested for et al., 2005). influence, and the presence of other influences that Premenarchael girls in Seveso, Italy exposed to may go unmeasured. Many studies focus on one or dioxin had longer menstrual cycles after they reached two pollutants leaving questions concerning the roles menarche compared to women who were postme- of other pollutants unanswered, and there are a narcheal when exposed (Eskenazi et al., 2002). How- number of measures of quality being used. The result ever, women exposed to PCBs through consumption of is a large body of literature on humans that is uneven, contaminated fish from the US Great Lakes and containing many reports of relationships and other women exposed through the consumption of Baltic reports of their absence. Studies of laboratory animals fish, had cycles of reduced length (Mendola et al., and in vitro studies provide the most control and weigh 1997; Axmon et al., 2004). heavily in favor of the ability of many pollutants to Carefully constructed studies have shown that detrimentally influence sperm or testicular develop- PCBs are associated with reduced female fecundability ment in some way (Andric et al., 2000a, 2000b; Gold- (Buck et al., 2000) and longer time to conception man et al., 2000; Faroon et al., 2001; Gray et al., 2001; (Courval et al., 1999). Higher miscarriage rates have Corpas et al., 2002; Veeramachaneni, 2008; Woodruff been reported also (Gerhard et al., 1998), and in the et al., 2008). Yu-cheng cohort, more stillbirths and preadolescent A fairly consistent finding is that some measures of deaths of offspring (Yu et al., 2000). Though PCBs were sperm quality are affected by air pollution levels. In a not related to menstrual cycle length or other cycle careful study of young men from Teplice, Czech parameters, dichlorodiphenyltrichloroethane (DDT) Republic, which is highly industrialized, clinical meas- level (measured as DDE) was significantly associated ures of sperm quality (number, motility, frequency of with shorter cycles, including the luteal phase length malformations) did not vary systematically in relation alone (Windham et al., 2005). to episodes of air pollution. However, the sperm chro- Although POPs are involved in all these studies, matin structure assay showed that the percentage of they can differ considerably in their effects, and in sperm with DNA fragmentation was significantly ele- the laboratory have been shown to produce estrogenic vated in relation to such episodes (Rubes et al., 2005). or anti-estrogenic, androgenic or anti-androgenic Such fragmentation may cause increased rates of male effects. Some are known to act through different recep- mediated reproductive effects including infertility and tors. The timing of exposure is likely to produce differ- miscarriage. Comparing Teplice men with men from ent effects as well. Seemingly contradictory results an unindustrialized area, however, showed more (delayed or accelerated sexual maturation) may be abnormal chromatin, a lower proportion of motile consistent with exposure to different types or combin- sperm, sperm with normal morphology, and normal ations of POPs, and especially to the timing of exposure sperm head shape among the Teplice men, although in the context of sexual differentiation and develop- mean and median sperm concentration and count did ment prenatal and possibly other critical periods. not differ (Selevan et al., 2000). Evidence for effects of different PCB congeners on measures of sperm quality is mixed. Follow-up of EFFECTS ON SPERM AND THE MALE Yu-cheng boys exposed in utero show that they had REPRODUCTIVE SYSTEM DEVELOPMENT increased abnormal sperm morphology, reduced motility, and reduced hamster oocyte penetration cap- This is a controversial topic (Toppari et al., 1996; acity compared to controls (Guo et al., 2000) as well as Giwercman and Bonde, 1998; Chia, 2000). Numerous reduced penile length at 11–14 years of age (Guo et al., studies have related an apparent decline in some meas- 1993). Studies of males chronically exposed to lower ures of sperm quality (number, motility, frequency of levels of POPs have produced less clear results. Sperm sperm deformations) to an increase in exposure to chromatin integrity was related to levels of PCB (CB- pollutants while others have not (Carlsen et al., 1992; 153) in a consistent dose–response relationship among Fisch et al., 1996; also see Chapter 21 of this volume). European men but not in Inuit men from Greenland, Some of the controversial elements of this body work and no relationships with DDE levels were detected include whether there has in fact been a decline in (Spano et al., 2005). Significantly less sperm motility sperm quality or a change in sampling the population was found in men with relatively high levels of marker (for example, including more older men) that mimics PCBs than in the less exposed (Rignell-Hydbom et al., such an effect, and whether there is any relation 2004) and no differences were related to levels of DDE. between concurrent pollutant exposure and sperm Studies comparing fishermen on the east coast of quality (Comhaire et al., 2007). The question is not Sweden, where PCB and other POP contamination

Industrial Pollutants and Human Evolution 573 levels are high, to those on the west coast, where they weight, was inversely related to levels of blood are lower, have found negative associations of this phthalates (Swan et al., 2005) suggesting that some exposure with sperm motility, sperm chromatin integ- phthalates are anti-androgenic. Boys with short dis- rity, and Y:X chromosome ratio but not with sperm tances for body weight also had higher frequency of concentration or semen volume; couple fertility did not undescended testicles and scrotal sacs characterized as differ (Axmon et al., 2008). Other studies have reported small or indistinct from surrounding tissues. no relationship between PCB exposure and fertility and The relationship of blood lead levels to measures of sperm counts (Emmett et al., 1988a, 1988b; Buck et al., male fertility, particularly sperm quality or function, 1997). It may be that metabolites are more potent has been well established through many studies than the parent compounds as sperm count and motil- of humans and in experimental work with animals. ity have been associated with PCB metabolite levels Generally, among workers at a lead–zinc smelter, (Dallinga et al., 2002). sperm count and concentration were related to the A set of recent studies based on a sample of drawn concentration of blood lead especially among those from men using the andrology laboratory at Massachu- men with a specific genotype of d-aminolevulinic acid setts General Hospital used a novel measure, the dehydratase (Alexander et al., 1998). Analysis of the Comet assay that measures DNA integrity, showed that fertility potential of sperm in conjunction with in vitro sperm DNA damage was associated with specific urin- fertilization efforts found that seminal plasma lead ary phthalate metabolites after statistic adjustment for levels were related to decreased human sperm function appropriate covariates (Duty et al., 2003; Hauser et al., (Benoff et al., 2003), and decreased success with in 2007). An additional study examined the effect of a vitro fertilization (IVF). These results on sperm func- combination of certain PCBs and phthalates and found tion agree to a great extent with findings from studies that the combination was strongly related to “below of laboratory animals (as reviewed in Benoff et al., reference value sperm motility” (Hauser et al., 2005). 2003) and with findings from studies of fertility and The authors used standard World Health Organization lead levels. Importantly, the findings from studies of measures of sperm motility, and the measured levels of male partners of IVF patients are relevant to the gen- phthalate metabolites in this sample were typical of eral population because the lead levels are similar to levels in US men, generally suggesting that the findings reference values and are below levels associated with may apply widely. Other studies have found elevated decreased sperm function and fertility through occu- serum estradiol levels and decreased sperm motility in pational exposure (Lancranjan et al., 1975). relation to exposure to pesticides and solvents (Oliva et al., 2001). As a conclusion to the different results from studies DIABETES AND OBESITY of humans, consider the study by Kuriyama and Cha- houd (2004) who found that low doses in utero of one Diabetes and obesity are associated with reduced fer- PCB (#118) produced smaller testes, epididymides and tility in both men and women. Factors that contribute larger seminal vesicles, decreased sperm and sperm- to increased obesity and diabetes may indirectly influ- atid numbers, and impaired daily sperm production ence fitness. In recent years independent studies from in adult male rats. Whereas other studies have shown different parts of the world, the United States, Bel- that large doses produce increased sperm production gium, and Sweden, have demonstrated that levels of and testis weight (Cooke et al., 1996; Kim, 2001). dioxins and PCBs are related to diabetes and obesity. Researchers have postulated that effects at different Using data from the US National Health Examin- doses of endocrine mimics may produce very contrary ation Survey, diabetes prevalence was strongly and effects (nonlinear, U-shaped, etc.), especially so with positively associated with lipid-adjusted serum concen- regard to endocrine mimics (Calabrese and Baldwin, trations of the six POPs found in 80% or more of the 2003; Kuriyama and Chahoud, 2004). The study of sample. The analysis included adjustment for appro- low dose effects from POPs has raised serious ques- priate control variables including age, sex, race, body tions about the nature of dose–response generally, and mass index (BMI), waist circumference, poverty level, the monotonic dose–response relationship, once con- etc. A strong dose–response relationship was evident sidered a hallmark of causal relationship between in the data. The risk of diabetes increased steadily exposure and an effect, may not be that hallmark in with increasing POP level and was several-fold greater every instance. in groups above the 75th percentile of toxicant Ano-genital distance, a measure usually much level compared to those below the 25th percentile greater in males than females, is a frequently used (Lee et al., 2006). measure of sexual differentiation in toxicological stud- In a Belgian sample, levels of POPs were between ies of rodent sexual development (Sharpe, 2001). 62% and 39% higher in diabetic patients compared to Young boys’ ano-genital distance, corrected for body controls, a highly significant difference before and

574 Lawrence M. Schell after statistical adjustment for appropriate covariates Genotoxicity (Fierens et al., 2003). The risk of diabetes was signifi- The genotoxicity of air pollution was discovered cantly greater in the top tercile of toxicant level; risk through investigations of the relationship between air ratios varied between 5.1 and 13.3 depending on the pollution and lung cancer (Pope et al., 2002). Several compound or group of compounds, In a Swedish studies have demonstrated that air pollution, particu- sample there were positive though weaker relation- larly exposure to polycyclic aromatic hydrocarbons ships between diabetes risk and chlorobiphenyl and (PAHs), is associated with increases in measures of DDE levels (Rylander et al., 2005). genotoxicity, specifically changes in carcinogen-DNA adducts and carcinogen-protein adducts using in vitro methods. These are mutations in somatic cells but the AIR POLLUTION: A SPECIAL CASE ability of air pollution to affect genes in human germ cells is a matter pertaining to human evolution and Anthropological concern with the evolutionary signifi- therefore of importance to anthropologists. cance of pollutants requires focusing on influences Air pollution can contribute to chromosomal on fitness. Evidence of an association between air abnormalities. Chromosomal abnormality frequency pollution and standard measures of fitness is not a was calculated for 60 African-American and Domin- subject of study in public health where most of the ican mother–infant pairs living in low income areas research is concentrated. Most studies of the effects of New York (Bocskay et al., 2005). Airborne PAH level of air pollution on mortality focus on adults and par- measured by air monitoring was significantly and posi- ticularly the elderly where effects are thought to be tively associated with stable chromosomal aberrations greater and of greater significance to public health. in cord blood though not with unstable ones which are Nevertheless, in the air pollution literature there is less significant as a cancer risk. work on some indirect influences on fitness such as The genotoxicity of PAHs is supported by compari- sperm quality and effects on the age of attainment of sons of levels of airborne PAHs and genotoxicity of sexual maturation, both of which influence the length particles (greater than 10 mm) collected in Antwerp, of the reproductive span. However, evidence is now from an industrial site, and a rural site (Brits et al., accumulating that indicates that some types of air pol- 2004). The most damaging particles came from the lution have more direct effects that pertain to human urban area and were highest in PAH concentration. evolution. Genetic damage could result from airborne particles or from compounds adhered to them because particles more easily enter the distal lung tissue where com- Prereproductive mortality pounds are absorbed into the bloodstream and can be Studies of air pollution have a long history and carried to the liver. There they may be metabolized into there is arguably more information on its effects chemicals more damaging to DNA and then carried to than any other pollutant. The link between air pollu- the spermatogonial stem cells in the testes (Samet tion and adult mortality is soundly established by et al., 2004). Studies of human lung cell cultures also population-based studies (Dockery et al., 1993; Pope, show dose-dependent increases in genotoxicity in 1999). Anthropological concern with the evolutionary terms of DNA breaks (Dybdahl et al., 2004; Karlsson significance of pollutants requires greater attention to et al., 2004). influences on fitness especially to prereproductive Studies with animal models allow for manipulation mortality. of exposures and stronger inferences regarding causal The first well-documented episode of pollution connections. The most informative studies to date related mortality was the London smog of 1950 formed demonstrated that heritable mutations in mammals by particulates and SO 2 from home heating fires Adult may be caused by particulate air pollution, and that mortality was increased and infant mortality was the primary contributor is the PAH compounds. increased significantly as well, although this point Laboratory mice 6–8 weeks old housed downwind was not fully appreciated against the higher death rates from steel mills for 20 weeks had 1.5–2.0 times the among the elderly. Recently studies of infant deaths in number of heritable mutations compared to an unex- Mexico City have pointed to the role of small particular posed group, and primarily inherited through the matter (PM 2.5 , e.g., particulates smaller than 2.5 mmin paternal line (Somers et al., 2002). In a follow-up study, diameter) (Loomis et al., 1999). An increase of 10 units mice caged in an industrial environment breathing in the level of particulates less than 2.5 mm in diameter unfiltered air had significantly elevated mutation rates (PM 2.5 ) was linked to a 4–7% excess mortality in compared to mice kept in rural areas with unfiltered or infants (excluding accidents and other sources of mice breathing HEPA-filtered air in either rural or mortality clearly unrelated to air pollution). industrial environments (Somers et al., 2004). As

Industrial Pollutants and Human Evolution 575 HEPA filtration reduced the expanded simple tandem metabolized, the dose or exposure, and when in devel- repeat (ESTR) mutation rates at the industrial site, the opment it occurs. They do not all produce the same airborne agents that were filtered were responsible for constellation of effects. Some groups of pollutants do the elevated rate, and these were most likely PAHs. alter parameters that pertain to reproduction and fit- Taken together, these studies demonstrate that ness. Germ-cell mutations, reduced fertility in males some component of air pollution, probably PAHs, is and females, changes in menstrual cycle characteris- able to produce heritable mutations in mammals. The tics and measures of male potency, as well as in the impact of these mutations in germ cells on human pattern or timing of sexual reproduction have been mortality, morbidity, and evolution has yet to be linked to one or more pollutants in several different investigated. studies of humans. Research ethics do not permit ran- domized control trials of humans and pollutants, which is appropriate but makes it virtually impossible GENETIC VARIATION IN SUSCEPTIBILITY to formally establish cause and effect. Yet, there is TO INDUSTRIAL POLLUTANTS plentiful supporting evidence from laboratory studies of the same pollutants among appropriate animal In the simplest terms, for natural selection to occur models that is substantial and cannot be dismissed. genetic variation in a trait must be linked causally to Certainly there are unknown factors that create vari- variation in the contribution of offspring number to ability in results. Further research will identify these the following generation. This may be due to differen- and in so doing will increase knowledge of normal and tial fertility, mortality, or by some more indirect path. disturbed reproduction. If genetic susceptibility to the effects of industrial pol- Since Silent Spring was published (Carson 1962), lutants exists, and these effects may affect fertility or scientists have known something of the power of pesti- mortality before the end of the reproductive span, then cides to alter reproduction. More recently, Our Stolen selection may occur for variations conferring protec- Future (Colborn et al. 1996) has reawakened concern tion against such effects. about the long-term effects of pesticides and pollutants Much of the evidence for genetic variation in sus- generally on human reproduction and health. The US’s ceptibility to pollutants is drawn from studies of PAHs National Research Council (1999) report, Hormonally and aromatic amines. Both are generated by combus- Active Agents in the Environment, has substantiated tion, the first from fossil fuels and the second from many concerns about chemicals and human reproduc- cigarette smoke and other sources. The genes most tion, and even a cursory examination of government often found related to variation in response to carcino- websites dealing with toxicants finds many reports of gens are the metabolic genes (P450), glutathione S- effects on reproduction. Differences in reproduction is transferase (GST) and the N-acetyltransferase (NAT) not by itself evidence of evolution, but it is a required (Perera, 1997). Common genetic polymorphisms in element. Understanding how genetic variation associ- P450s and NAT2 have an impact on cancer suscepti- ates with reproductive effects is the next step in under- bility. Increased lung cancer risk upon exposure to a standing how pollution may affect human evolutionary carcinogen, especially at low dose, is associated with trajectories. one or more of the CYP1A1 polymorphisms. DNA repair varies tremendously. The activity of 6 two DNA repair enzymes, O -alkyldeoxyguanine-DNA alkyl-transferase and uracil DNA glucosylase, differs DISCUSSION POINTS by over 100-fold within humans (Perera, 1997), which is linked to increased cancer risk. Genetic variation in 1. Which pollutant seems most likely to influence receptors involved in toxicokinetics of carcinogens human evolution? also impact risk of cancer. An important receptor for 2. What evidence is there that pollutants really are effects of many aromatic hydrocarbons such as dioxin bad for human populations, and what standard is and some PCBs, as well as PAHs, is the arylhydrocar- applied to decide this? bon (Ah) receptor. Individuals with this high-affinity 3. Is it possible that humans are adapted to any of the binding receptor upregulate CYP1A1, CYP1A2, and pollutants discussed, and if so, how could this have other genes. happened? 4. What evidence is required to prove that a pollutant influences human evolution and is it possible to SUMMARY AND CONCLUSION collect that information in less than a generation with methods currently available? Pollutants exist in a huge variety and their effects 5. Why is it so difficult to know the effects of depend on their chemical structure, how they are pollutants?

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34 Acculturation and Health Thomas W. McDade and Colleen H. Nyberg INTRODUCTION populations represent a Rousseauian vision of humans living in harmony with their environment, with incur- We currently live in an era of rapid globalization, with sions leading to losses of autonomy and disruptions in a few societies beyond its reach. In 1950, 30% of the delicate homeostasis that impair health (Wirsing, world’s population lived in urban areas; today the pro- 1985). For others, health improves when cultural and portion of urban residents is nearly 50%, and will economic trends provide reliable access to nutritional exceed 60% by 2030 (United Nations, 2001). Expansions and health care resources (Dennett and Connell, 1988; in international trade, market economies, and formal Gage, 2005). Still others recognize both the challenges systems of education provide opportunities for some and opportunities of change, and explicitly consider the and social inequality for many, while a global mass multiple, and potentially conflicting, paths through media fuels new consumer desires and expectations which cultural and economic factors may shape health (Ger and Belk, 1996; Navarro, 1999). Populations that (Berry et al., 1986; McElroy, 1990; Godoy et al., 2005c; were once relatively isolated – geographically, linguis- Steffen et al., 2006). tically, culturally – are becoming increasingly exposed Many terms have been used to describe the processes to, or interfacing with, novel environments and life- of change that affect health, including “acculturation,” styles that may differ considerably from their own. “Westernization,” “modernization,” and “market inte- What implications do these processes have for human gration.” While these terms reflect significant differences biology and health? For our understanding of processes in emphasis, they all share a common interest in linking related to human adaptation? individual well-being to surrounding social, cultural, These questions have been hotly debated by anthro- economic, and political dynamics. “Acculturation” fore- pologists, epidemiologists, and economists for over half grounds changes in local culture resulting from regular a century, and simple answers are not forthcoming. interaction between two or more autonomous cultural Most research focuses on the health impact of recent systems (Social Science Research Council Summer transitions related to globalization, but it is important Seminar, 1954). “Westernization” and “modernization” to recognize that human biology has been shaped by typically focus on the development of a cash economy, dynamic relationships with cultural, economic, and secularized government, systems of formal education, broader ecological factors since the Neolithic Revolu- and urban residential units (Levy, 1966; Spindler, tion. For example, rises in infectious disease associated 1984). “Market integration” focuses more specifically with shifts from hunting and gathering to sedentization on the emergence of market-based systems of exchange, and agricultural intensification beginning about 10 000 and the degree of participation in, and dependence on, years ago can be considered the first epidemiologic markets to meet subsistence needs (Godoy, 2001). transition (Barrett et al., 1998). Links between cul- Obviously, these are overlapping, closely related tural/economic transitions and health are fundamental processes of change, and in this review we use the more to human evolutionary biology since morbidity and general term “cultural and economic transitions” to mortality are important correlates of reproductive fit- encapsulate all of them. After introducing key concepts ness, and because cultural/economic factors define, in that serve as a foundation for research in this area, we large part, the environments to which humans adapt. review the state of current knowledge regarding the Field-based research on cultural/economic changes health impact of cultural and economic transitions in and health has provided an opportunity to explore populations around the world. We discuss the mechan- mechanisms of human adaptation, and to consider the isms through which these transitions affect human biol- local consequences of broader cultural and economic ogy and health, and highlight the models that have been processes. For some scholars, isolated indigenous used to reveal these associations. Human Evolutionary Biology, ed. Michael P. Muehlenbein. Published by Cambridge University Press. # Cambridge University Press 2010. 581

582 Thomas W. McDade and Colleen H. Nyberg DEVELOPMENT OF KEY CONCEPTS Culture, adaptation, and health History Although frequently invoked as a causal factor in shaping Despite elegant work by Boas (1911) with immigrant human behavior, biology, and health, culture is rarely populations demonstrating biological plasticity in operationalized and a consensus definition remains response to environmental change, prevailing concep- elusive. For most purposes, culture can be defined as tualizations of human populations as genetically socially transmitted systems of shared knowledge, fixed and bounded entities dominated into the 1940s beliefs, values, and/or behaviors that vary systematically (Little, 1982; Johnston and Little, 2000). The predom- across recognizable social groups (Tylor, 1924). Culture inance of such typological thinking left little room for is a primary component of the human adaptive strategy. serious consideration of cultural factors as determin- For the past 20000 years humans have inhabited a ants of human biological variation. However, in the wider ecological and geographic range than any other 1950s and 1960s, evidence for adaptive biological respon- vertebrate, and – for better and for worse – over the past siveness to climatic stressors – cold, heat, altitude – began 10000 years humans have become Earth’s dominant to accumulate in a wide range of human populations, species due to the emergence of sophisticated techno- thereby documenting considerable phenotypic plasticity logical and social systems (Alexander, 1991; Boyd and and setting the stage for an ecological approach to human Richerson, 2005). Culture reduces the costs of learning biology. and increases the breadth and accuracy of knowledge With a renewed emphasis on theory and hypothesis accumulated across generations, and it is a necessary testing, the “new physical anthropology” (Washburn, input for normal cognitive and neurological development 1951) encouraged a series of studies – many as part of (Changeux, 1997; Tomasello, 1999). Culture is thus the International Biological Programme – on biobeha- often seen as providing solutions to challenges posed to vioral mechanisms of adaptationto diverse environments reproduction and survival, but it simultaneously creates around the world (Baker and Weiner, 1966). Climate, new problems in these same domains (Schell, 1997). For disease, nutrition, and other aspects of the physical example, cultural factors may allocate risks and ecology were investigated as primary stressors with resources along lines of residence, occupation, and/or implications for human development and health. From social class. In some situations, inequality in the distribu- this perspective it was but a small step to acknowledge tion of resources may be so pronounced that reproduc- cultural factors as key organizers of exposure to, and tion and survival are compromised for significant buffers against, environmental stressors (Baker et al., numbers of individuals. Thus, culture is both a buffer to 1986; Huss-Ashmore, 2000). adversity and an unequal allocator of risk to health, pro- These historical developments set the stage for viding adaptive opportunities as well as challenges culture change and health as a major area of ongoing (Thomas, 1992; Schell, 1997). Lasker (1969) outlined research in human biology, with the field currently three levels at which organisms adapt to shifting eco- confronting two significant challenges. The first con- logical circumstances: (1) genetic modifications resulting cerns the recognition that the majority of research on from natural selection across generations; (2) ontogen- culture and health relies on relatively simplistic under- etic modifications that emerge over an individual life standings of culture, and that more sophisticated course; and (3) short-term physiological and behavioral operational definitions of cultural factors are needed in responses. Recently, Kuzawa (2005) has proposed future research (McDade, 2002; Dressler, 2005). The “phenotypic inertia” as a fourth level of adaptability, second concerns the importance of political–economic intermediate in time course between genetic and onto- factors in structuring exposure to stressors associated genetic changes, which allows for intergenerational with change, and in constraining ability to respond to transmission of information through nongenetic mech- those stressors in ways that attenuate their adverse anisms. Humans are unique among animals in the degree impact on health (Singer, 1996). An emphasis on plasti- to which we rely on behavioral responses and extra-som- city and the mechanisms through which humans are able atic adaptations to facilitate survival and reproductive survive in a wide range of environments can divert atten- success, an attribute that provides considerable flexibility tion from the quality of these environments – many of in response to environmental change. which are marginal, at best – and runs the risk of natur- Culture is thus a key mechanism of human adapt- alizing or justifying social inequality. Human biologists ability, but it also constructs in large part the settings have recognized this risk, and a number of studies have to which humans must adapt. For humans, culture attempted to consider the local effects of global pro- is the environment. Shifts in the cultural landscape cesses, the biological costs of adaptation, and the social can therefore be expected to result in phenotypic and economic relations underlying adaptive capacity changes at multiple levels by acting through genetic, and stress exposure (Leatherman and Goodman, 1997; intergenerational, ontogenetic, and/or physiological/ Goodman and Leatherman, 1998). behavioral mechanisms.

Acculturation and Health 583 There are a number of cases demonstrating the Developmental inertia is a relatively unexplored mechan- impact of cultural factors on human genetic diversity ism linking cultural and economic transitions to health, (Durham, 1991). For example, classic research in West butitislikelytobeparticularlyimportantforunder- Africa suggests that the intensification of agriculture standing secular trends in growth and chronic disease. led to changes in the population frequency of alleles Similar developmental mismatches – albeit within a protective against malaria (Livingstone, 1958). Clearing shorter time frame – have been invoked as mechanisms wide patches of tropical rainforest provided abundant to explain a wider range of associations between culture breeding grounds for the mosquito vector, which change and health. Early work on the social origins of encouraged the transmission of malaria and conferred hypertension, for example, suggested that incongruity a selective advantage upon resistant individuals. between the cultural environment an individual is social- Although cultural transitions have left their mark on ized into as a child and the one he or she functions in as the human genome – particularly in a deep evolutionary an adult, may lead to upregulation of stress pathways and time frame – it is important to emphasize that contem- poor health (Cassel, 1974). Similarly, individuals who porary human populations adjust to environmental grow up at high altitude acclimatize by developing larger changes primarily through nongenetic mechanisms. lung volumes, whereas individuals who migrate to high This is due to the slow pace of genetic change, as well altitude as adults do not show the same level of functional as the exceptional degree of phenotypic plasticity that is capacity in hypoxic environments (Frisancho, 1978). a defining trait of the human species. Behavioral and The vast majority of research on how environments developmental mechanisms provide more rapid, flexible, affect health focuses on the final mechanism of adap- and mutable options for adaptive responsiveness such tation: short-term (i.e., nondevelopmental) physio- that genetic changes come into play only as a “last logical and behavioral responses to challenge. This resort” (Slobodkin, 1968; Huss-Ashmore, 2000). reflects the importance of phenotypic plasticity to the Recent interest in the early life origins of adult dis- human adaptive strategy, and is particularly the case ease (see Chapters 2 and 30 of this volume) has provided for research on culture and health, since most investi- evidence that “intergenerational inertia” may be an gators are interested in the impact of relatively rapid important mechanism linking cultural/economic transi- cultural and economic transitions, typically occurring tions and health. For example, in the Philippines, adoles- within a single generation. This body of research is the cents have high levels of cholesterol despite low rates of primary focus of this chapter, with numerous obesity and relatively low intakes of dietary fat, and examples discussed below. unexpectedly high rates of hypertension at any given It is important to acknowledge that the relationships level of body mass (Colin Bell, et al. 2002; Kuzawa among environmental stressors, processes of adapta- et al., 2003). These results – and similar findings from tion, and health are not always straightforward. For other populations as well as research with animal example, the development of a thrifty phenotype in a models – suggest that prenatal undernutrition leads to nutritionally marginal environment may well represent permanent changes in organ structure and physiological an adaptive process, but the consequences for health in function that lower the energy needs of the individual as a nutrient-rich environment (obesity, chronic disease) an adult. In teleological terms, the developing organism are hardly positive. Similarly, even though a thrifty uses the prenatal environment to predict future resource phenotype may be beneficial in a nutritionally marginal availability such that a “thrifty phenotype” may be an environment compared to a more spendthrift pheno- adaptive response to an impoverished nutritional type, undernutrition early in life compromises work ecology. capacity, reproductive performance, cognitive function, But when calorie-dense foods are readily available and longevity (Martorell, 1989; Pelletier et al., 1995) – later in life, prenatal undernutrition may make individ- again, outcomes that are clearly suboptimal. For these uals particularly vulnerable to diseases related to energy reasons, some scholars eschew the term adaptation surplus, including obesity, cardiovascular disease, and altogether when making reference to human biological diabetes. Globally, industrial agriculture and commercial responses to social, economic, and cultural contexts, food production are increasing the availability of concen- particularly when these contexts are impoverished trated sources of calories (e.g., refined sugar, cooking (Pelto and Pelto, 1989; Frisancho, 1993; Singer, 1996). oils), and levels of physical activity are dropping Several general hypotheses follow from this discus- (Popkin, 1994, 2003). Populations experiencing rapid sion of the mechanisms of adaptation that can be used nutritional and lifestyle changes may be particularly vul- as a guide for research into the impact of cultural and nerable to the contribution of “developmental mismatch” economic transitions on human biology and health. to chronic degenerative diseases. Birthweights in India, Firstly, since changes in gene frequency in response for example, are among the lowest in the world, yet the to shifting selection pressures represent an exceedingly country is currently experiencing an epidemic of type II slow mechanism of “last resort,” few studies are likely to diabetes despite low levels of obesity (Yajnik, 2004). find genetic signatures of natural selection in response

584 Thomas W. McDade and Colleen H. Nyberg to contemporary changes in the cultural and economic features of this literature prior to discussing the path- environment. This does not deny the importance of gen- ways linking change and health. etic mechanisms of adaptation in an evolutionary time frame, nor does it discount the possibility that the Topical foci unique evolutionary history of a particular population may shape its response to contemporary environmental The major emphases of recent studies have been on changes in significant ways (Snodgrass et al., 2007). outcomes related to child growth, chronic degenerative Secondly, intergenerational and developmental pro- diseases such as obesity, cardiovascular disease, and cesses provide a degree of phenotypic plasticity for diabetes, and mental health. Changing patterns of infants and juveniles that is not available to adults. With infectious disease have also received considerable fewer mechanisms of adaptation online, adults can be attention, while other health outcomes addressed in expected to pay a higher biological toll in response to recent studies include violent deaths, and risk behav- rapid environmental change than they would have paid iors such as substance abuse. if they confronted the same changes earlier in life. Simi- larly, conditions experienced early in life – prenatally Child growth and in infancy – can be expected to have long-term as Measures of growth and nutritional status are sensitive well as intergenerational implications for health in the indicators of past, present, and future health, and have context of changing environments. therefore served as key outcomes for research on the Thirdly,thepaceofchangeshouldbeassociated impact of cultural and economic transitions. In part with its impact on health. Rapid cultural and economic due to the relative ease of anthropometric data collec- transitions pose more immediate adaptive challenges by tion, studies of child growth have been conducted in a opening up larger gaps between old and new environ- wide range of populations, with mixed results (Panter- ments, and by constraining options for phenotypic Brick et al., 1996). In some settings, cash earnings from adjustments that strive to optimize fitness. Genetic, market activities are used to purchase food and to intergenerational, and developmental mechanisms of supplement traditional diets, which may improve adaptation, for example, do not apply in situations of nutritional status and reduce growth stunting (Santos rapid change, and behavioral responses – particularly and Coimbra, 1991; Stinson, 1983; Norgan, 1995; those embedded in cultural systems handed down across Reyes et al., 2003; Godoy et al., 2005c; Foster et al., generations – may have to overcome considerable inertia 2005). In others, market participation leads to an before they can serve as effective buffers. Related to this increase in growth stunting through nutritional stress point, the adverse health impact of environmental or an increase in infectious disease that acts synergistic- change should be greatest in the short term, and should ally with undernutrition to impair growth (Fitton, attenuate over time through phenotypic responsiveness 2000). In the Andes, the impaired statural growth of on multiple levels. many high-altitude populations was revealed to be the result of poverty and disease, rather than primarily high altitude stress, underscoring the role that inequalities in CULTURAL AND ECONOMIC TRANSITIONS access to the benefits of economic development play in AND HEALTH: WHAT DO WE KNOW? shaping child growth (Leonard, 1995; Leatherman, 1998). While one in four children globally suffer from In the past 25 years, over 200 peer-reviewed studies have undernutrition (de Onis et al., 2004), in many develop- been published investigating the impact of cultural and ing nations the prevalence of childhood obesity and economic transitions on health in diverse populations associated metabolic disorders is growing rapidly 1 around the world . Few consistent patterns of association (Gracey, 2003). emerge from this literature, cautioning against any attempts to draw sweeping conclusions regarding the Chronic degenerative diseases impact of cultural and economic change on health in One of the most consistent findings of recent research is contemporary populations. Here we summarize key the positive association between market integration and the emergence of chronic degenerative diseases. 1 This estimate is based on searches in electronic databases Increases in adult body weight and the prevalence of (PubMed, PsychInfo, Google Scholar), as well as anthropo- obesity have been demonstrated in several populations, logical journals and bibliographies of past publications on the and at differing levels of articulation with market econ- topic. A variety of search terms were used to capture the most inclusive sample of articles, including acculturation, Westerniza- omies (Zimmet et al., 1980; Baker et al., 1986; Norgan, tion, modernization, market integration, urbanization, industrial- 1994; Shephard and Rode, 1996). Similarly, blood pres- ization,andculture change. Studies were included if they sure is higher for adults in affluent countries and in contained individual-level health outcomes (i.e., no regional or national level datasets) and were studies of in situ c hange (i.e., populations that have moved away from subsistence- not studies of migrants). based economies. Mortality rates from cardiovascular

Acculturation and Health 585 disease are also elevated (Scotch, 1963; Waldron et al., speculation that the encroachment of Western insti- 1982; Poulter et al., 1990; Dressler and Bindon, 1997; tutions and values, the decline of local communities, Egusa et al., 2002; Steffan et al., 2006). Often, the “mod- the disintegration of extended family networks, and a ernization” gradient in high blood pressure is more lack of economic opportunities have contributed to pronounced in men than in women, although the precise adolescent stress (Kraus and Buffler, 1976; Macpher- mechanisms underlying this difference remain unclear son and Macpherson, 1987; Rubinstein, 1992; (Schall, 1995). Accompanying changes in body compos- McDade, 2002). A model of acculturative stress pro- ition and blood pressure is the emergence of type II posed by Berry and Kim (1998) suggests that degree of diabetes in a range of populations, including Pacific distress depends largely on whether those acculturat- Islanders (Prior and Rose, 1966), Australian Aborigines ing wish to maintain their traditional identity, and the (Norgan, 1994), Pima Indians (Ravussin et al., 1994), and degree to which they want to integrate and interact among circumpolar peoples (Shephard and Rode, 1996). with those in the new culture (Berry and Kim, 1998). Although changes in diet and reductions in physical Research on response to colonial stressors among activity levels are obvious contributors to cardiovascular Inuit youth highlights the role of coping behaviors and metabolic diseases, psychosocial distress associated in buffering stress-related health outcomes (O’Neil, with culture change may also be a powerful factor 1986), while several studies in the Samoa Project (McGarvey and Schendel, 1986; Steffen et al., 2006). have documented physiological responses to the psy- In addition, mismatch between prenatal nutritional chological and behavioral changes accompanying environments and those encountered later in life may rapid social and economic transition (McGarvey and be an important, though relatively unexplored, mechan- Schendel, 1986; Baker et al., 1986; Pearson et al., ism leading to the development of chronic disease 1993). Recent research with an Amazonian horticul- (see Chapter 30 of this volume). turalist population in the early stages of transition While broad-scale epidemiological surveys indicate suggests that greater participation in the market econ- that rates of cancer are increasing dramatically through- omy is significantly linked to anger, fear, and sadness out the developing world, scant data are available directly (Godoy et al., 2005c). linking this increase to cultural and economic transi- The effects of psychological distress may also tions. As with cardiovascular and metabolic diseases, manifest through the emergence of excessive alcohol changes in diet and activity levels are thought to be major consumption and substance abuse. While these contributors: excessive bodyweight has been recognized behaviors may initially serve as coping mechanisms by the World Cancer Research Fund as an important risk in response to the experience of acculturative stress, factor for many malignancies (World Cancer Research the consequences for individual health and commu- Fund and American Institute for Cancer Research, 2007; nity well-being can be devastating (Berry, 1970; Neff, Renehan et al., 2008). However, the link between obesity 1993; Dressler et al., 2004). Sporadic episodes of binge and certain cancers may vary dramatically between sexes drinking are common among communities undergo- and populations of different geographic origin. ing rapid social and economic transitions, and may be In addition, the adoption of risky behaviors such as most problematic (Graves, 1967; Singer et al., 1992). smoking and alcohol abuse have also been hypothesized Cigarette smoking has been documented in many to contribute. For example, high rates of lung cancer transitioning populations, but precise estimates of among indigenous Siberian populations have been duration and frequency of smoking are not known. linked to smoking, while increased rates of reproductive The abuse – rather than controlled social or ritual carcinomas have been attributed to high rates of sexually use – of marijuana, stimulants, cocaine, depressants, transmitted diseases and high-risk sexual behavior in tranquilizers, and hallucinogens has also become Arctic communities (Freitag et al., 1991). China, which more common among many indigenous communities has the largest global production and consumption of (Shephard and Rode, 1996; Curtis et al., 2005). Alco- tobacco, experiences over 1 million smoking-related hol and substance abuse have also been implicated in deaths each year, most the result of lung cancer (Zhang escalating rates of accidents and violent crimes and Cai, 2003; Jiang et al., 2008). among modernizing populations (Curtis et al., 2005). Mental health and substance abuse Infectious and parasitic diseases Several studies have documented increased rates of Infectious disease persists as a major contributor to mor- depression and suicide, as well as increased levels of bidity and mortality around the world. While historical physiological indicators of stress, in populations in improvements in standard of living have reduced rates of transition (Graves and Graves, 1979; Brown, 1981; infectious disease (McKeown, 1976), contemporary asso- Dressler, 1991; Shephard and Rode, 1996). Epidemics ciations with cultural and economic transitions are of adolescent suicide among circumpolar popula- mixed. Economic development may facilitate prevention tions, in Samoa, and in Micronesia have fueled and treatment by providing access to health-care

586 Thomas W. McDade and Colleen H. Nyberg resources, yet it may also contribute to disease transmis- biological, and health data it compiled (Baker et al., sion and severity through degradation of the local ecol- 1986). The project took advantage of the recent emer- ogy (Walsh et al., 1993; Brinkman, 1994; Santos et al. gence of a “modernization gradient” across the islands 1997). Rapid urbanization may contribute to increases to reveal a general pattern of increasing obesity, hyper- in population density, erosion of basic infrastructure, tension, adverse lipid profiles, as well as adverse stress deforestation, and changing subsistence and agricultural hormone profiles in individuals residing in more West- patterns with direct implications for pathogen exposure ernized areas. Several studies have continued to track (Armelagos et al., 1996; Garruto et al., 1999). For these trends over time (McGarvey, et al., 1993; example, in Guyana the conversion of cattle-grazing Keighley et al., 2007), and to explore culture change fields to a more economically viable cash crop, rice, pro- as a source of adolescent stress (McDade et al., 2000; vided an ideal breeding ground for mosquitoes. Conse- McDade, 2002). quently, malaria rates soared (Desowitz, 1976; Brown Similar findings emerged from the Tokelau Island and Whitaker, 1994). The case of the Ache ´ of Paraguay Study, in which a cohort of central Pacific islanders were underscores the profound impact of infectious disease on surveyed before migration to New Zealand in 1967 and immunologically naı ¨ve Amerindian populations: two- then followed post-migration for over two decades. The thirds of the adult population developed tuberculosis health consequences of migration included a shift within just 20 years of sustained contact with outsiders toward a more carbohydrate- and sugar-laden diet, a (Hurtado et al., 2003). greater likelihood of developing gout, adverse lipid pro- Although macroparasites have received less attention files, an increase in the prevalence of type II diabetes, than other infectious diseases, they may play a major role and a modest increase in blood pressure (Stanhope and in malnutrition, growth stunting, and comorbidity with Prior, 1980; Prior et al., 1987; Salmond et al., 1989). other infections (Lawrence et al., 1980). In cases where A similar study in the Solomon Islands revealed more urbanization is associated with higher parasite loads, modest post-migration changes in blood pressure and increased infection is often attributed to crowding, poor body composition (Page et al., 1974; Friedlander, 1987). sanitation, and proximity to animals and fecal material In Papua New Guinea, the relative isolation of the (Confalonieri et al., 1991; Fitton, 2000). Type of water highlands has provided a baseline for comparison with source may also be a significant predictor of parasite the more rapidly transitioning settlements in coastal exposure: in the Philippines, neighborhoods which relied areas, and numerous studies have demonstrated links on rain water rather than irrigation canals had a higher between economic integration and elevated blood pres- prevalence of the water-borne parasite schistosomiasis sure, body mass index (BMI), and reduced activity levels (Payne et al., 2006). In other populations, increased (Jenkins, 1989; Schall, 1995; Yamauchi, et al., 2001; market integration and education have been linked to a Ulijaszek, 2007). Other studies based in Papua New reduction of intensity in intestinal parasites, a pattern Guinea have cautioned against the assumption that observed among the Tsimane’ of the Bolivian Amazon isolated highland populations represent idealized states (Tanner, 2005). of good health and harmony with the natural environ- ment: many of these populations have long histories of contact with outsiders, and rates of undernutrition and Regional foci infectious disease are high (Dennett and Connell, 1988). While research into the health impact of cultural and economic transitions has been conducted globally, the Arctic Pacific Islands, Latin America, and the Arctic have Circumpolar populations provide case studies in served as particularly important testing grounds for mechanisms of adaptation to extreme cold, but arctic exploring the physiological and psychological correl- research has also served as a major foundation for ates of lifestyle change. Many of the projects in these exploring the ramifications of acculturation on psy- areas represent the legacy of human adaptability chological and physical health. The Inuit of northern research initiated by the International Biological Pro- Canada, for example, are frequently cited as a classic gramme and the Man and the Biosphere Programme example of how acculturation can provoke mental (Little et al., 1997). distress and undermine health through risk behaviors such as smoking and alcoholism (Berry, 1970; Lynge, Pacific Islands 1976; O’Neil, 1986; Shephard and Rode, 1996). In Rapid economic development in the Samoan islands addition to increased rates of infectious diseases occurring post-World War II provided a compelling introduced through contact with outsiders, circumpo- backdrop for a comprehensive assessment of the lar peoples have experienced soaring rates of chronic impact of lifestyle changes on health. The Samoan diseases such as hypertension, diabetes, and cancer Studies Project – initiated in 1975 – is distinguished due to changes in diet and physical activity (Shephard by the breadth of economic, demographic, cultural, and Rode, 1996). More recent research has integrated

Acculturation and Health 587 a political–economic perspective to explore the influ- Defining “change” ence of the collapse of the former Soviet Union on the Deriving a meaningful operational definition of health of indigenous populations (Leonard et al., “change” is a major challenge associated with research 2002; Sorensen et al., 2005; Snodgrass et al., 2006). into the health consequences of cultural and economic transitions. The vast majority of studies to date (well Latin America over three-quarters of those reviewed for this chapter) Early research in Latin America focused largely on adap- employ group-level, ecological comparisons of individ- tation to high altitude, but attention soon shifted to uals sharing a common biological and cultural history, patterns of social relations and economic stratification but currently living in divergent cultural and/or eco- that shaped resource access, with implications for nomic conditions. Comparisons across urban and adaptive processes and health (Leatherman et al., 1986; rural populations are particularly common. Leatherman, 1998). For example, these investigations For obvious logistical reasons, cross-sectional revealed that factors linked to poverty – undernutrition, designs are frequent, and were used in almost 90% of infectious disease – played a stronger role than high the studies reviewed for this chapter. In these studies, altitude hypoxia in contributing to growth stunting “change” is captured by making cross-sectional com- (Leatherman et al., 1995; Leonard, 1989; Stinson, parisons across two or more environments, where it is 1996). Research in Amazonia has considered a wide assumed that the baseline environment will in the breadth of topics, including changing patterns of infec- future become similar to the environment used for com- tious and parasitic diseases, blood pressure, diversity of parison. Change is thus anticipated, but not directly dietary strategies within shifting social and ecological measured, within individuals. Only prospective studies contexts, and socioeconomic factors affecting adult can measure changes in cultural and economic environ- nutritional status and work capacity (Reed et al., 1970; ments within individuals across time. This approach Dufour, 1983; Fleming-Moran et al., 1991; Fitton and has been applied most productively to studies of Crews, 1995; Dufour et al., 1997). Ongoing research in migrants, where dramatic environmental changes can lowland Bolivia is collecting repeat observations from a be captured in relatively short lengths of time. Prospect- population at the early stages of market integration in an ive studies of in situ change are less common, but are attempt to explicitly distinguish the effects of market, important resources for assessing causal linkages cultural, and ecological factors on health (Foster et al., between cultural and economic transitions and health 2005; Godoy et al., 2005c; McDade et al., 2005). (Little and Johnson, 1987; Adair and Popkin, 1988; Godoy et al., 2005a, 2005b). Africa Despite a high level of anthropological and public health interest in Africa, relatively few studies have CULTURAL AND ECONOMIC TRANSITIONS, explicitly investigated the health effects of cultural ADAPTATION, AND HEALTH: PATHWAYS and economic transitions. Exceptions include import- ant comparative research on blood pressure, investiga- There are several pathways through which cultural and tions into changing patterns of fertility, and the economic transitions impact health (Figure 34.1). These development of demographic models of shifting popu- processes are not mutually exclusive, and they inter- lation dynamics (Scotch, 1963; Howell, 1979; Caldwell relate in complex and variable ways across different and Caldwell, 1987; Hyatt and Milne, 1993). The Turkana project has explored changing subsistence and settlement patterns among Turkana pastoralists Changes in economic, social, political, and/or cultural systems and contexts in northern Kenya, and has revealed better health among nomads with reference to child growth and maternal nutritional status (Leslie et al., 1993; Little et al., 1993; Shell-Duncan and Obiero, 2000). The recent and rapid emergence of maternal obesity represents a Behavior Environment/ Psychosocial new public health problem in urbanizing Africa, where natural resources stress child stunting and wasting remain prevalent (Garrett Health care Demographics and Ruel, 2005; Villamor et al., 2006). Despite the enor- mous importance of these studies in underscoring the complexity of the “nutrition transition” in Africa, most data have been collected at the population level and therefore cannot explore the within-household dynam- Mental and physical health ics that may contribute to the simultaneous existence of 34.1. Primary pathways through which cultural and economic malnutrition and overweight. transitions affect human health.

588 Thomas W. McDade and Colleen H. Nyberg geographic, ecological, and historical contexts to shape prevalence of disordered eating behaviors, including health through the mechanisms of adaptation outlined self-induced vomiting to lose weight, followed pro- above. longed television viewing among adolescent girls in Fiji (Becker, 2004). Becker notes that “the impact of televisions appears especially profound, given the Behavior longstanding cultural traditions that previously had Cultural and economic transitions initiate behavioral appeared protective against dieting, purging, and body changes that may have dramatic implications for pat- dissatisfaction” (Becker et al., 2002, p. 511). terns of diet and physical activity. A number of studies have documented shifts in energy balance resulting Health care from reductions in physical activity and increased con- sumption of calorie-dense foods as populations move For many populations, early stages of acculturation from a labor-intensive, subsistence-based diet to a par- and market integration provide for the first time reli- tial or complete reliance on commercially prepared able access to primary health care, vaccines and anti- foods. In places like the Samoan Islands, these behav- biotics effective against a wide range of infectious ioral changes have fueled the rapid emergence of epi- diseases, and new explanatory models for the preven- demics of obesity and chronic degenerative diseases tion of disease grounded in germ theory (Akin et al., (McGarvey et al., 1993; Keighley et al., 2007). On the 1985; Gage, 2005). The implications for child health other hand, for marginally nourished populations, the and survival may be particularly dramatic. For availability of commercial foods – and the means to example, among Venezuelan lowlanders, economic acquire them – has been associated with better nutri- changes provided households tied to the market with tional status by improving dietary diversity and the greater access to medical services, and cash from wage quantity of macronutrients (DeWalt, 1983). labor allowed them to purchase health care (Holmes, Breast-feeding is a critical determinant of infant 1985). A by-product of emerging markets is the credit health in low-income settings, and contextual factors system, which can smooth shocks by providing the that discourage breast-feeding may therefore have dra- means to borrow money to pay for medicines and matic implications for infant morbidity and mortality health services during times of need (Amin, 1997; (McDade and Worthman, 1998). The availability of Godoy, 2001). Access to a well-functioning credit infant formula may discourage breast-feeding, particu- system may also buffer vulnerable individuals from larly when there are competing demands for a mother’s nutritional shortfalls, and prevent the further deterior- time and energy (Nerlove, 1974), and when formula is ation of health from fluctuating food consumption that perceived to represent a more advanced, technological, impairs ability to work, whether at a subsistence level or “modern” option (Manderson, 1982). or for cash wages (Rose, 1995; Morduch, 1995). In addition to changes in patterns of diet and phys- In contrast, access to Western biomedical models ical activity, health may be affected by the emergence of and treatments may actually impair health, as in the risk behaviors such as smoking or excessive alcohol con- case of the global distribution and promotion of infant sumption. Alcoholism was pronounced among Native formula as a substitute for breast milk (Post and Baer, Americans undergoing forced assimilation in the United 1978). Women in rural Kenya who deliver their babies States (Graves, 1976), emerged as an adolescent in hospitals are twice as likely to feed their infants response to colonial stress in the Arctic (O’Neil, 1986), formula (Cosminsky, 1985). In rural Mexico, women and has soared in communities that are becoming enga- who seek care in a local hospital introduce supplemen- ged in the regional market economy in lowland South tal foods to their infants earlier than women not near America (Godoy et al., 2006). While social and economic the hospital since medicines used in hospitals are transitions have been associated with increased alcohol believed to enter breast milk and make breast-feeding use across a variety of populations, perhaps nowhere dangerous (Millard and Graham, 1985). In other set- have the effects of rapid change on substance abuse been tings, formula may be given to mothers in hospitals or more pronounced than in the former Soviet Union. The prescribed by physicians, thereby associating formula fall of the Soviet government led to calamitous economic with modern medicine (Manderson, 1982; Simpson, collapse, with wide-ranging ramifications for health and 1985). The rapid spread of formula can be attributed well-being. This “failed modernization” and the resulting to an aggressive global marketing campaign mounted health crisis has contributed to a declining life expect- by formula manufacturers, and it was not until grow- ancy, largely due to increased mortality from lung cancer ing concerns regarding the contribution of formula use and alcohol-related cardiovascular failure in men to rising rates of infant mortality that the campaign (McKee, 2005; Sorensen et al., 2005). was stopped. Associations with risky health behaviors may also Another level of complexity is added when tensions be more indirect. For example, an increase in the arise between mothers and public health policy makers

Acculturation and Health 589 regarding recommendations for breast-feeding prac- of Akwesasne Mohawk youth, increased blood lead tices in the context of epidemic HIV, especially in levels predicted a substantial delay in the timing of Africa. For HIV-positive mothers, breast-feeding con- menarche (Denham et al., 2005). Studies of the organic fers a 15–20% risk of mother-to-child-transmission pollutants polychlorinated biphenyls (PCBs), have (Atashili et al., 2008). However, this risk must be revealed reduced birthweight in infants born to PCB- balanced against the concerns of malnutrition and exposed mothers (Schell et al., 2006), and a negative mortality attributed to an increased susceptibility to association between adolescent PCB levels and meas- infectious disease contracted from water-based formu- ures of long-term memory (Newman et al., 2006). The las. Careful evaluation of the pros and cons led the potential for intergenerational transmission of these World Health Organization to recommend exclusive pollutants may be especially profound, as these lipo- breast-feeding for 6 months of life even for HIV- philic toxins are concentrated in human fat cells where positive mothers, as breast-feeding remains a major they can be transferred in utero to the developing fetus protector of child survival in sub-Saharan Africa and to infants via breast milk (Schell and Knutson, (Coutsoudis et al., 2008; David et al., 2008). 2002; also see Chapter 33 of this volume). Closely related to changes in the physical environ- ment is the possibility that cultural knowledge Environment and natural resources regarding the use and management of local natural Rapid alterations in the local physical environment can resources will be lost as a result of acculturation. Local have significant implications for health. Although few ecological knowledge serves as a guide for activities populations rely exclusively on local natural resources central to survival and well-being, including effective for subsistence, rapid population growth and intensifi- habitat management, subsistence and food procure- cation of agriculture put pressure on natural resources. ment, and attempts to prevent and cure disease Among slash and burn horticulturalists, market inte- (Brookfield and Padoch, 1994; Atran and Medin, gration is associated with more rapid deforestation 1997; Etkin, 2000; Pandey, 2001). Cultural and eco- and intensification of farm production (Vadez et al., nomic transitions may threaten this knowledge if 2004), while constraints on land use encourage formal schooling and integration into emerging market nomads to shift from pastoralism to farming (Little economies prioritize alternative sources of informa- and Leslie, 1999; McCabe, 2003). These changes may tion and provide access to substitute products not have implications for the sustainability of natural made from local resources (Godoy et al., 1998; Reyes- resource use, as well as for the quality and quantity of Garcia et al., 2005). Recent research in lowland Bolivia nutrients extracted from the local environment. has demonstrated the potential cost to health if this In addition, increases in population density knowledge is lost: adults with better knowledge resulting from and contributing to agricultural intensi- regarding the availability and potential uses of local fication facilitate the spread of infectious disease, as ethnobotanical resources have healthier children, as does more frequent contact with outsiders, particularly indicated by higher measures of nutritional status in the absence of improvements in sanitation and and lower levels of infection (McDade et al., 2007). hygiene (Jenkins, 1989). Initial exposure to novel infec- tious diseases has in some cases had devastating conse- Demographic processes quences for indigenous populations, leading to dramatic rates of mortality, as well as social and economic Classic demographic transition theory states that as upheaval (McNeill, 1977). Recent research in lowland living conditions improve in preindustrial populations Bolivia has documented higher concentrations of mortality rates will drop – particularly for infants and C-reactive protein (an indicator of inflammation) in chil- children – and life expectancy will increase (Caldwell, dren regularly attending school compared to children 1976). Declining fertility rates will follow, thus com- not in school, suggesting that the relatively recent intro- pleting the transition from high rates of birth and duction of formal schooling may promote pathogen death, to low rates of birth and death in industrialized transmission in this population (McDade et al., 2005). settings. Over the last 200 years, global life expectancy In urban (and urbanizing) environments, industrial in industrialized populations has more than doubled, development and rapid increases in population density from about 25 to 65 years for men and 70 years for may outpace the management of organic waste and women (Oeppen and Vaupel, 2002), and rates of total other forms of pollution, such as noise, air, mercury, fertility have dropped to about 2 children in industrial- and lead (Schell and Denham, 2003). Exposure to ized nations since World War II. In comparison, total environmental pollutants may be particularly severe fertility rates in the developing world are far higher, for children, who may experience impairments in likely due to the lack of contraceptives and less access endocrine function, physical growth, and cognitive to education in these populations (Caldwell and Cald- development as a result. In a community-based study well, 1987). This represents an idealized model of the

590 Thomas W. McDade and Colleen H. Nyberg complex relationships among socioeconomic and into life on reservations near the forest. State and mis- demographic changes that may apply to many popula- sionary interventions, changes in diet, and access to tions in transition, with important implications for Western medicines have resulted in reduced mortality health. Local processes of demographic change may rates compared to life in the forest at all ages except for also deviate substantially from this model. the first year of life, when rates of infant mortality are As standard of living improves adolescent girls and actually higher on the reservation. boys reach puberty earlier, lowering the age at which During life in the forest, the total fertility rate was successful reproduction is possible (although social, cul- 8 live births per woman, with an interbirth interval tural, and/or economic factors may encourage delayed of 37.6 months, and an average age of first birth of childbearing). Lactational amenorrhea – induced by a 19.5 years (Hill and Hurtado, 1996). On the reserva- neuroendocrine cascade initiated by frequent nipple tion, women start reproducing nearly 2 years earlier at stimulation – increases interbirth intervals in noncon- 17.7 years of age, and have more live births (8.5) tracepting populations (Konner and Worthman, 1980; at interbirth intervals that are 6 months shorter (31.5 Vitzthum, 1994). The availability and use of supplemen- months). This accelerated reproductive schedule may tal infant foods may interrupt this process and lead to have implications for women’s health, infant, and child rapid population growth, as well as increases in rates of well-being, as well as population growth for the Ache ´. infant morbidity (McDade and Worthman, 1998). Sexu- ally transmitted diseases and patterns of secondary ster- Psychosocial stress ility may also reduce fecundity (Caldwell and Caldwell, 1983; Ellison et al., 1986; Hill and Hurtado, 1996). Changes in neuroendocrine activity are an essential Cultural transitions may also encourage shifts in part of the “fight-or-flight” response in all vertebrates. the number of children desired by adults, and in pat- For most species these are critical adaptive responses terns of parental investment. Greater parental invest- to social and ecological stressors, but the metabolic ment in offspring education, a smaller desired family consequences may be more profound for humans size, and a delay in the onset of reproduction, as well as who experience the same hormonal activation in a reduction in total number of offspring can result in response to purely psychosocial stressors (Sapolsky, reduced- and below-replacement fertility (Levine, 2004). Stress has been shown to be an important deter- 1994; Leslie et al., 1994; Kaplan et al., 2002). In Kenya, minant of mental and physical health for humans for example, increased female education was associ- (McEwen and Lasley, 2002; Cohen et al., 2007), and ated with a substantial decrease in the number of may therefore be a significant mediator of the health births (Hyatt and Milne, 1993). In such situations, impact of cultural and economic transitions. Psycho- parents may perceive increased “costs” associated with social stressors initiate the activation of multiple neu- raising children that motivate shifts in patterns of fer- roendocrine pathways, including the sympathetic tility and child rearing (Caldwell and Caldwell, 1987). adrenal medullary system (SAM), and the hypothalamic- Rapid population growth following accelerations in pituitary-adrenocortical (HPA) axis, which in turn reproductive schedules and/or declines in infant mor- cause changes in cardiovascular, metabolic, and tality may increase population density, thereby facili- immune system activity (Johnson et al., 1992; tating the transmission of pathogens and increasing McEwen, 1998). Short-term responses facilitate rates of infectious diseases (Barrett et al., 1998). Popu- adaptation to a wide range of stressors, but frequent lation growth may also put strain on local natural or excessive demands contribute to poorer health resources, and serve as an impetus for outmigration outcomes. The operationalization of stress poses sig- and urbanization (Armelagos et al., 1991, 2006). nificant challenges to cross-cultural research, since Demographic data from the Ache ´ – a small indigen- self-report measures of perceived stress or symptoms ous population of eastern Paraguay – underscore many of emotional distress (e.g., depression, anxiety) com- of these points. Until relatively recently, the Ache ´ lived monly used in Western countries may not be valid in in small, mobile bands and subsisted by hunting different linguistic and cultural contexts. Physiological animals and gathering plants and insects in the forest measures provide relatively objective indicators of (Hill and Hurtado, 1996). Duringthis period, age-specific stress that are comparable and interpretable across mortality rates were high compared to contemporary different populations (despite cultural and linguistic industrial populations, but similar to other foraging differences), and that provide insight into the bio- populations. Even though rates of infant and child logical pathways that may lead to impaired health mortality were particularly elevated, approximately (Ice and James, 2007). For this reason a number of one third of all Ache ´ born lived to the age of 60. First studies have investigated the impact of cultural and contact with outsiders in the 1970s brought epidemics economic transitions on biomarkers of stress. of infectious diseases that killed nearly 40% of the The potential impact of rapid social change on population, and since that time the Ache ´ have settled stress and health has long been recognized, with early