AR254-AN34-25 ARI 25 August 2005 15:10

The Ecologies of HumanImmune FunctionThomas W. McDadeDepartment of Anthropology, Northwestern University, Evanston, Illinois 60208;email: t-mcdade@northwestern.edu

Annu. Rev. Anthropol.2005. 34:495–521

First published online as aReview in Advance onJune 28, 2005

The Annual Review ofAnthropology is online atanthro.annualreviews.org

doi: 10.1146/annurev.anthro.34.081804.120348

Copyright c© 2005 byAnnual Reviews. All rightsreserved

0084-6570/05/1021-0495$20.00

Key Words

immunology, growth and development, human biology, infectiousdisease

AbstractImmune function is notoriously complex, and current biomedicalresearch elaborates this complexity by focusing on the cellular andmolecular mechanisms that characterize immune defenses. How-ever, the human immune system is a product of natural selection thatdevelops and functions in whole organisms that are integral parts oftheir surrounding environments. A population-level, cross-cultural,adaptationist perspective is therefore a necessary complement to themicro levels of analysis currently favored by biomedical immunol-ogy. Prior field-based research on human immunity is reviewed todemonstrate the relevance of cultural ecological factors, with an em-phasis on the ecologies of nutrition, infectious disease, reproduction,and psychosocial stress. Common themes and anthropological con-tributions are identified in an attempt to promote future research inhuman ecological immunology that integrates theory and methodfor a more contextualized understanding of this important physio-logical system.

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Ecologicalimmunology: anadaptationistapproach toinvestigating thecosts and benefits ofinvestment inimmune activity andthe potential role ofpathogens in shapinglife history variation

Contents

INTRODUCTION. . . . . . . . . . . . . . . . . 496INTRODUCTION TO HUMAN

IMMUNE FUNCTION . . . . . . . . . 497Measuring Immune Function . . . . . 500

ECOLOGIES OF HUMANIMMUNE FUNCTION . . . . . . . . . 500Nutritional Ecology . . . . . . . . . . . . . . 501Ecology of Infectious Disease . . . . . 505Reproductive Ecology . . . . . . . . . . . . 507Social Ecology . . . . . . . . . . . . . . . . . . . 509Political Ecology . . . . . . . . . . . . . . . . . 511

TOWARD A HUMANECOLOGICALIMMUNOLOGY . . . . . . . . . . . . . . . . 512

CONCLUSION . . . . . . . . . . . . . . . . . . . . 514

INTRODUCTION

Immunology has recently gained the atten-tion of anthropology for at least three rea-sons. First, infectious disease has been, andcontinues to be, a major global health burden,particularly in many populations of anthropo-logical interest (Inhorn & Brown 1990). Sec-ond, the immune system is an excellent modelfor exploring developmental processes, phe-notypic plasticity, life history trade-offs, andadaptation—all central concepts for biologi-cal anthropology. Finally, the metaphors com-monly used to characterize immune functionreference biological as well as broader socialprocesses and may reflect, as well as reinforce,contemporary cultural models and social di-visions (Martin 1990, Wilce 2003). This thirdpoint—alluding to the critical perspective ofcultural and linguistic anthropology—is be-yond the scope of this review.

Biomedical immunology dominates cur-rent immunological research and focuses al-most exclusively on the proximate cellular andmolecular mechanisms that function to pro-tect us from infectious and neoplastic dis-eases and that malfunction to cause autoim-

mune and atopic diseases. The majority of thiswork relies on selectively bred strains of lab-oratory animals or on humans carefully se-lected from specific clinical populations. Thecontributions to disease prevention and treat-ment, as well as to basic biology, are difficult tooverstate.

However, current biomedical approachestell only part of the story. Human physiolog-ical systems are products of natural selection,developing and functioning in whole organ-isms that, in turn, develop and function in re-lation to surrounding physical and social en-vironments (Oyama 1985, Williams & Nesse1991). Studies relying on animal models, oron humans drawn from clinics in relativelyaffluent Western settings, do not adequatelyrepresent the diverse cultural and environ-mental circumstances around the world thatcontribute to human variation. Biological an-thropology in particular has demonstrated theimportance of this diversity in shaping hu-man biology, development, and health acrossa wide range of human populations (Little &Haas 1989, Stinson et al. 2000).

For these reasons, there is emerging schol-arly interest in field-based research on humanimmune function and its relevance to adapta-tion, ecology, and life history (Lochmiller &Deerenberg 2000, McDade 2003b, Sheldon& Verhulst 1996). Much of this work is re-viewed here, along with findings from in-ternational health, behavioral ecology, andbiomedical immunology that demonstrate therelevance of cultural and ecological factorsto the development and function of the hu-man immune system. Genetics also plays animportant role (Tishkoff & Williams 2002,Weiss 1993) but is not covered in this review.Rather, the direct contributions of nutritional,pathogenic, reproductive, and psychosocialfactors to human immune function are dis-cussed in an attempt to lay the groundworkfor an integrated human ecological immunol-ogy that incorporates theory and method fora more contextualized understanding of thisimportant physiological system.

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INTRODUCTION TO HUMANIMMUNE FUNCTION

A detailed discussion of the immune systemis well beyond the scope of this review; in-stead key terms, concepts, and componentsare highlighted and the reader is referred tointroductory and advanced texts for more de-tails (Goldsby et al. 2000, Paul 2003). Theprimary function of the immune system is toprovide protection from the myriad bacteria,viruses, and parasites that share our world.The tension between host and pathogen is notunique to humans, and all vertebrates—fromcartilaginous fish to mammals—share homol-ogous elements of immunity (Du Pasquier1992, Marchalonis & Schluter 1994). Theimmune system is also centrally involved incellular renewal and repair and thus plays acritical role in wound healing and protectionagainst cancer.

The immune system is composed of multi-ple interdependent and complementary sub-systems that establish a relatively seamlessnetwork of antipathogen defenses (Table 1).Components of innate immunity includeanatomical barriers such as skin and mucosalmembranes; antimicrobial soluble proteins inblood, saliva, and tears; phagocytic cells that

Innate immunity:also called naturalimmunity, thesedefenses arephylogeneticallyolder than specificimmune defenses, donot depend on priorantigen exposure,and represent thebody’s first line ofdefense againstinfection and injury

Specific immunity:the defining features(also called acquiredor adaptiveimmunity) includespecificity, diversity(wide range ofantigen-bindingspecificities),memory, andself/nonselfdiscrimination

Antigen: asubstance that elicitsa specific immuneresponse; mostpathogens (i.e.,bacteria, viruses,parasites) arecomposed ofmultiple distinctantigens

scavenge extracellular macromolecules; andthe inflammatory response (involving acute-phase proteins and the recruitment of phago-cytic cells to the site of injury or infection).

Cell-mediated and humoral-mediated im-mune processes define specific immunity,which, unlike innate immunity, can recognizeand target specific antigens. T and B lym-phocytes are the central mediators of specificimmunity and contain receptors that recog-nize antigens with exquisite precision, to thepoint that a single amino acid substitution mayprevent binding by a given T or B lympho-cyte receptor. Other characteristics of specificimmunity include an enormous range of di-versity in antigen-binding receptors, the abil-ity to recognize and respond more quicklyto antigens upon second exposure (memory),and the ability to distinguish self from nonself.

T lymphocytes perform a range of reg-ulatory, activational, and effector functionsthat are critical to eliminating intracellularpathogens and managing specific immuneprocesses. Subsets of T lymphocytes are iden-tified by the expression of membrane gly-coproteins, in particular CD4 (identifyinghelper T cells) and CD8 (associated with cy-totoxic/suppressor T cells). Helper T lym-phocytes have also been further differentiated

Table 1 Major components of the immune system and methods used in their measurement

Component MeasuresLymphoid organsThymus, spleen, bone marrow,lymph nodes

Organ size/histology; patterns of cell circulation; production ofthymic peptides, cytokines

Nonspecific defensesComplementAcute phase responsePhagocytosis

Assays for complement and acute-phase protein concentrations;phagocytic cell counts; functional measures of cellular chemotaxis,lytic ability

Cell-mediated immunityT lymphocytes:Helper (Th1, Th2)Suppressor/cytoxicNaıve/memory

Number, percentages of T lymphocyte subpopulations; in vitromeasurement of lymphocyte proliferation and/or cytokineproduction in response to mitogens; delayed-type hypersensitivity;assay for antibody titers to latent herpesviruses

Humoral-mediated immunityB lymphocytesImmunoglobulins(IgA, IgM, IgG, IgE, and IgD)

Number, percentage of B lymphocytes; in vitro measurement oflymphocyte proliferation; assay for Ig concentrations; assay forspecific antibody titers following vaccination

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Figure 1Development ofenumerative (top)and functional(bottom) aspects ofhuman immunefunction with age(McDade 2003b).

sIgA: secretory IgArecently into Th1 and Th2 subtypes that reg-ulate distinct patterns of immune activity.

B lymphocytes and the antibodiesthey produce are definitive components ofhumoral-mediated immunity and are involvedprimarily in protection against extracellularpathogens. Antibodies belong to one offive immunoglobulin isotypes (IgG, IgA,IgM, IgE, or IgD), each of which possessesunique structural and functional properties.IgG is the predominant immunoglobulin incirculation, whereas secretory IgA (sIgA) isabundant in external secretions, includingmucus, saliva, breastmilk, and tears. IgMis produced when a new antigen is firstencountered and accounts for less than 10%of the total serum immunoglobulin concen-tration. IgE is a potent mediator of allergicreactions and is involved in antihelminthicdefenses. IgD is present in serum in very lowconcentrations, and its function is not wellunderstood.

Figure 1 presents age-related changes inmajor aspects of immunity from infancy toyoung adulthood. Immediately apparent arethe elevated numbers of T and B lympho-cytes and the relatively high volume of thymiccortical tissue (in which T lymphocytes ma-ture prior to their release into circulation).Lymphocyte activity is also upregulated earlyin life, whereas remaining immune factorsdemonstrate the more familiar developmen-tal trend of incremental increase with age.

Prior work has interpreted the unusualdevelopmental trajectory of human immunefunction within an adaptationist, life-historyframework (McDade 2003b, McDade &Worthman 1999). From this perspective, in-creased activity in multiple parameters of spe-cific immunity early in life can be understoodas a response to the fundamental evolution-ary advantage enjoyed by pathogens relativeto their long-lived human hosts. Pathogensare present in high numbers, they have short

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intergenerational intervals, and they producelarge numbers of offspring with increased op-portunities for mutation (Zinkernagel et al.1985). Humans can never match the paceof pathogen evolution; rather, the processthrough which specific immune defenses areestablished incorporates evolutionary pro-cesses to counter this advantage.

In particular, lymphocytes circulate in highnumbers, reproduce quickly following acti-vation, and display a tremendously diverserange of antigen-binding receptors. Eventhough the human genome contains fewerthan 30,000 genes, the judicious incorpo-ration of stochastic processes during recep-tor development (random rearrangement ofmini-gene segments, imprecise joining ofnucleotide sequences, random combinationsof heavy and light peptide chains, and so-matic mutation during replication) producesfar more than 100 million different antigen-binding specificities (Paul 2003).

Once this diverse pool of lymphocytes isestablished—each lymphocyte with its ownunique antigen-binding receptor—the mat-uration of specific immune defenses is arelatively straightforward Darwinian processtermed clonal selection: Antigens select lym-phocytes with matching receptors; these lym-phocytes activate, replicate, and pass on theirreceptor genes to daughter cells; and these celllines become disproportionately representedin subsequent generations of the lymphocytepopulation. In essence, pathogens drive a de-velopmental process that closely resemblesnatural selection, leading to somatic evolutionof the lymphocyte repertoire. A major impli-cation of this design is that the development ofimmunity is context dependent: The systemis designed to incorporate information fromthe surrounding disease ecology, and the in-tensity and diversity of antigen encounters—especially early in life—can have a lasting im-pact (McDade & Worthman 1999).

Excessive or self-directed immune re-sponses can do more harm than good, andimmune processes are therefore regulated atmultiple levels. Many aspects of immunity are

self-limiting in that antigens activate an arrayof innate and specific defenses, and once theantigen is cleared these defenses downregu-late. In addition, the immune system receivesinput from the nervous and endocrine sys-tems through innervation of lymphoid organsand through receptors for major endocrineaxes expressed on lymphocytes as well as lym-phoid tissues (Figure 2). Information fromthe immune system feeds back to the ner-vous and endocrine systems, forming an in-tegrated neuro-immune-endocrine networkthat is central to the development and reg-ulation of immune function (Ader et al. 2001,Besedovsky & del Rey 1996). These reciprocalconnections provide a number of physiologi-cal pathways through which ecological factorsmay influence human immunity.

Thus, there are conceptual, developmen-tal, and physiological reasons to anticipate amajor contribution of culture and ecology tovariation in immune development and func-tion across populations. Unfortunately, veryfew investigators have addressed this issue,

Figure 2Immune function is an integral part of nervous- and endocrine-systemactivity. Immune tissues express receptors for major neuro-endocrineproducts and release a wide range of substances that modulate immune,nervous, and endocrine system processes at multiple levels (Besedovsky &del Rey 1996).

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EBV: Epstein-Barrvirus

although a handful of field-based studies indiverse populations are suggestive. For ex-ample, reference values for lymphocyte de-velopment have been established in Westernpopulations (Denny et al. 1990), but healthy,well-nourished children in West Africa (Lisseet al. 1997), as well as healthy adolescents inhighland Papua New Guinea (Witt & Alpers1991), demonstrate developmental patternsthat differ significantly from these “norms.”Investigators have also documented wide pop-ulation variation in age-related patterns of im-munoglobulin production (Lau et al. 1992,Rowe 1972), as well as the production ofnonspecific defenses such as C-reactive pro-tein (McDade 2003b). Such variation under-scores the importance of an ecological ap-proach to complement and contextualize thecellular and molecular emphasis of biomedicalimmunology.

Measuring Immune Function

The complexity of immune function poses aserious challenge to measurement, particu-larly in field-based settings with limited lab-oratory facilities. Current research uses arange of enumerative and functional measures(Table 1), but these protocols typicallyrequire large volumes of blood collectedthrough venipuncture and prompt access tolaboratory facilities for the processing andanalysis of samples. These procedures haveserved as major impediments to field-based,population-level research on human immunefunction and are a primary reason why the vastmajority of current work is based in laboratoryor clinical settings, with relatively homoge-nous, opportunistic samples. With consider-able effort (and expense), rudimentary labo-ratory facilities can be established in remoteareas that allow for limited sample process-ing and analysis (Powell et al. 2001), but thisis not likely to facilitate anthropological workin a wide range of cultural settings. Rather, agrowing number of minimally invasive meth-ods are now available that are amenable to theconstraints of field-based research.

Salivary measures such as sIgA assess mu-cosal defenses protecting the gastrointesti-nal tract, a major entry point for pathogens(Mestecky 1993, Nishanian et al. 1998). Im-mune factors in blood provide more com-prehensive information on systemic immuneactivity, and a number of methods have beendeveloped using small quantities of wholeblood collected from a simple finger stick.For example, a single drop of blood collectedon filter paper can be assayed for acute-phaseproteins and antibodies against the Epstein-Barr virus (EBV) (an indirect measure of cell-mediated immunity) (McDade et al. 2000a,2004a; Panter-Brick et al. 2004). In addi-tion, whole blood smears on glass slides al-low the quantification of white blood cellfractions and lymphocyte subsets (Lisse et al.1990). Last, delayed-type hypersensitivity—involving the intradermal application of testantigens to the forearm—has been success-fully used in a number of sites as a semiquan-titative measure of cell-mediated immuno-competence (Shell-Duncan & Wood 1997).Additional methodological development isneeded, particularly given the complexity ofimmune function and the fact that no singlemeasure can provide a comprehensive indica-tor of immunocompetence.

ECOLOGIES OF HUMANIMMUNE FUNCTION

By focusing on the proximate mechanismsunderlying the development and function ofthe immune system, biomedical immunologyhas established a solid mechanistic foundationupon which an ecological perspective can bebuilt. Expanding the level of analysis to in-clude the individual in context allows us toask new questions. What constitutes “nor-mal” immune function, and do immune pa-rameters vary across populations? Which cul-tural and ecological factors contribute to thisvariation, and through which mechanisms?What is the contribution to differential pat-terns of disease, or variation in life histories?Because physiological systems are products

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of natural selection, can an adaptationist per-spective help explain, rather than just de-scribe, the impact of ecology on immune de-velopment and function?

In protecting the body against infectiousand neoplastic diseases, the immune system iscentral to survival, and thus evolution. How-ever, immune function is costly, both in termsof the resources it consumes and in its effect onwell-being when immune processes are mis-directed. Other critical physiological and de-velopmental systems also require resources,and natural selection can be expected to fa-vor the optimal allocation of resources acrossthese systems in ways that maximize fitness.In contrast to biomedical or epidemiologicalapproaches, an adaptationist, ecological per-spective recognizes that there are costs, aswell as obvious benefits, associated with im-mune activity, and that trade-offs are there-fore inevitable (Lochmiller & Deerenberg2000, Sheldon & Verhulst 1996).

These trade-offs may be genetically en-coded, or they may be developmentally medi-ated as a result of facultative adaptation to en-vironmental circumstances during an individ-ual’s lifetime. The latter process is generallyinvoked to explain biological variation acrosshuman populations, where limited pheno-typic plasticity allows individuals to respondadaptively to a range of ecological condi-tions (Hill & Hurtado 1996, Stearns & Koella1986). Conceptually, trade-offs may occurbetween major life history functions (e.g.,investing resources in maintaining the somaversus investing in reproduction or growth),between physiological systems (e.g., investingin immune tissues at the expense of the mus-culoskeletal system), and/or between subsys-tems within one system (e.g., biasing immunefunction toward Th1- versus Th2-mediatedprocesses). Key ecological factors will deter-mine the intensity of these trade-offs andwill make investment in certain physiologi-cal systems (or subsystems) more critical thanothers.

The following sections review evidencedemonstrating the impact of nutritional,

pathogenic, reproductive, and psychosocialfactors on human immune development andfunction. This organization mirrors the stateof current research that highlights the impor-tance of these ecological domains, but tends toinvestigate their effects in isolation. But froman anthropological perspective, each of thesedomains falls under the rubric of culture. Forhumans, culture and ecology are inseparable:We actively construct our environments, andculturally mediated behaviors structure ourinteractions with these environments. In re-viewing prior research in the pages that follow,common themes and anthropological contri-butions are identified in an attempt to plot acourse for future research in human ecologicalimmunology.

Nutritional Ecology

History documents a close relationship be-tween inadequate nutrition and epidemicsof pestilence and communicable disease(Chandra 1992). Today, international healthresearch consistently associates malnutritionwith immunosuppression and infectious dis-ease risk in low-resource settings (Gershwinet al. 2000, Lunn 1991). For these reasons,nutritional inadequacy has been the most in-tensively investigated ecological factor linkedto human immunity. A large body of researchhas documented the effects of macro- and mi-cronutrient deficiencies on immune structureand function, and recent attention has beenfocused on the costs of immune function andtheir implications for child growth, as well asthe long-term immunological consequencesof undernutrition early in life.

Cell-mediated immunity is particularlysensitive to deficiencies in macronutrition:Thymic volume declines dramatically, T lym-phocytes circulate in reduced numbers, pro-liferative responsiveness is attenuated, anddelayed-type hypersensitivity is suppressed(Table 2). In contrast, humoral-mediatedimmunity is relatively buffered: B lympho-cyte numbers remain within the normalrange (except with severe undernutrition), and

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Table 2 Summary of the effects of protein-energymalnutrition on parameters of human immunity

Immune component EffectLymphoid organsThymus ↓Spleen ↓Lymph nodes ↓Nonspecific defensesAcute phase response ↓Phagocytosis ↓Complement levels/activity ↓Cell-mediated immunity# T lymphocytes ↓Lymphocyte proliferation/cytokine production ↓Delayed-type hypersensitivity ↓Thymic hormones ↓Humoral-mediated immunity# B lymphocytes ↔ or ↓Immunoglobulin concentrations ↔ or ↑sIgA ↓Vaccine responsiveness ↓

immunoglobulin concentrations are in manycases elevated, possibly reflecting higher lev-els of pathogen exposure in malnourished in-dividuals (Lunn 1991). Cases of kwashiorkoror marasmus have been associated with majorreductions in serum albumin production butnormal or slightly elevated immunoglobulinproduction, suggesting preferential allocationof protein resources to immune function un-der these circumstances (Cohen & Hansen1962, El-Gholmy et al. 1970). The acute-phase response is also impaired, although evenseverely malnourished children can mount aresponse to infection (Morlese et al. 1998).

Micronutrient deficiencies rarely ariseindependently of some degree of protein-energy deficiency, but they are also indepen-dent modulators of immune function. Defi-ciencies in vitamins A, C, E, and B complex,as well as trace elements iron, zinc, selenium,and copper, impair cell-mediated immunity,antibody production, and a wide range of non-specific immune processes (Chandra 1997,Gershwin et al. 2000). In addition, recentwork has suggested that oxidative stress re-sulting from micronutrient deficiency may ac-

tually promote the evolution of more virulentviral strains within the undernourished host(Beck 2000).

Among the micronutrients, iron has re-ceived considerable attention, both becauseiron deficiency is common globally and be-cause it has been linked to a wide range of ad-verse developmental outcomes, including im-paired immunity (Stoltzfus 2001). Althoughreductions in cell-mediated and nonspecificimmune processes may result from iron de-ficiency (Bhaskaram 1988), mild anemia hasalso been associated with increased resistanceto infectious disease (Murray et al. 1980) andmay represent an adaptive, nonspecific im-mune response to infection (Weinberg 1984).Iron is an essential nutrient for many mi-crobes, and iron-binding proteins (e.g., trans-ferrin, lactoferrin) sequester circulating ironduring infection and limit its availability topathogens. This raises the question as towhether diets that limit iron intake may rep-resent a nutritional adaptation to infectiousdisease risk in high pathogen environments(Kent et al. 1994, Murray et al. 1980).

The close association between immuno-competence and dietary factors—particularlymacronutritional adequacy—underscores thehigh resource costs of immune activity. In-fection motivates major shifts in the body’smetabolic priorities; severe infections increaseresting metabolic rates by 25%–55% and con-sume 15%–30% of body weight (Lochmiller& Deerenberg 2000). Responses to less se-vere, as well as subclinical, infections also re-quire energetic and protein resources to fuelimmune cell replication and function, as wellas the production of antibodies, cytokines,and acute-phase proteins. In addition, thethymus is a relatively large organ that con-tains an enormous number of maturing Tlymphocytes, nearly a quarter of which arecreated each day. More than 95% of theseT lymphocytes are destroyed before being re-leased from the thymus owing to stringent se-lection criteria that reduce the chances of self-reactivity (George & Ritter 1996). The costsof these immune processes are substantial,

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particularly for those on the margins of nutri-tional adequacy. Given these costs, an adapta-tionist, ecological perspective recognizes thatthere may be situations—particularly in low-resource settings—where it is necessary todownregulate investment in immunity to freeup resources for other purposes.

Such trade-offs may provide insight intothe complex associations among nutrition, in-fectious disease, and child health. The syn-ergistic effects of malnutrition and infectionon child growth and child survival are wellknown (Pelletier et al. 1995, Scrimshaw 2003),but few studies have considered immune func-tion as a potential mediator. This is particu-larly important given that infection and mal-nutrition may contribute to growth falteringand increase mortality risk through multiplepathways: (a) Undernutrition may reduce theeffectiveness of immune defenses and there-fore increase the frequency and/or severityof infection; (b) more frequent infections (ei-ther due to higher levels of pathogen exposureor compromised immunity) require a higherlevel of energetic investment in immune acti-vation, consuming resources that would oth-erwise be available for growth; (c) pathogens(and associated immune responses) can causelong-term damage to intestinal mucosa, whichimpairs nutrient absorption beyond the pointof recovery (Lunn 2000); (d) cytokines associ-ated with fighting infection may lead to lossof appetite, reducing energy intake when de-mands are high (Hart 1990, Martorell et al.1980); and (e) symptoms of infectious diseasemay motivate culture-specific caregiving be-havior, often replacing normal foods with wa-tery substitutes lacking in nutrient and caloricdensity (Mata 1992).

Recent research in biological anthropol-ogy has begun to investigate these issues.In a highland population in Papua NewGuinea with extreme burdens of infectiousand nutritional stress, measures of childgrowth have been associated with white bloodcell fractions, including numbers of circulat-ing leukocytes, lymphocytes, and neutrophils(Ulijaszek 1998). Among nomadic Turkana

ACT: alpha-1antichymotrypsin

CRP: C-reactiveprotein

children in northern Kenya, low weight-for-height has been related to increased ratesof acute respiratory infection (Shell-Duncan& Wood 1997). However, suppressed cell-mediated immune function (measured bydelayed-type hypersensitivity) was a strongerpredictor of infectious morbidity, indicatingthat immunity may be the proximate variablemediating the nutrition-morbidity relation-ship in this population.

Taking a slightly different approach, recentfield studies in Nepal and Bolivia have investi-gated the direct contribution of immune acti-vation to impaired growth. Blood concentra-tions of acute-phase proteins such as alpha-1antichymotrypsin (ACT) and C-reactive pro-tein (CRP) increase in response to a widerange of viral, bacterial, and parasitic agents,making them potentially useful nonspecificindicators of the degree of investment in an-tipathogen defenses (Calvin et al. 1988). A ma-jor advantage of this approach is that it can de-tect subclinical infectious processes that maynot manifest as observable symptoms (andwould therefore not be reported) but that maynonetheless involve the activation of energet-ically costly antipathogen defenses (Roushamet al. 1998). Accordingly, among 10- to 14-year-olds in Nepal, elevated concentrations ofACT have been associated with growth falter-ing (Panter-Brick et al. 2000). Boys residingin rural villages—who had the highest con-centrations of ACT—had the lowest level ofself-reported morbidity, further underscoringthe value of direct measurement of immuneactivation in relation to growth outcomes.

Preliminary analysis of data from ongo-ing research with a horticulturalist populationin lowland Bolivia reports similar associationsbetween immune activation (as measured byCRP) and growth faltering but also suggeststhat individual differences in nutritional re-sources may moderate the costs of immuneactivation. Height was measured at baselineand again three months later, with heightgain interpreted as investment in growth ef-fort during this period. Skinfold measuresof body fat stores at baseline were used as

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Figure 3Growth costs of immune activation in lowland Bolivia. Elevatedconcentrations of CRP at baseline are associated with reduced height gainin the subsequent 3 months in 2–4-year-old children (N = 122) who havelow body fat reserves (as indicated by skinfold measurements) (McDade2005).

indicators of energetic reserves that could bedrawn on to fuel immune function. Youngchildren with elevated CRP at baseline grewless than did children with low CRP, and thisdifference was most pronounced among chil-dren with low energetic reserves at baseline(Figure 3). These results demonstrate a po-tential cost of immune activation and suggestthat environments characterized by low nu-tritional resources may increase the severityof trade-offs between immunity and growth(McDade 2005).

Although the short-term effects of under-nutrition on the immune system are well-established, recent research suggests that nu-tritional factors early in life may conditionlong-term investment in immune function.For instance, early studies showed that un-dernourished rats gave birth to offspring withimmune deficiencies that last into adulthood,even though the offspring had unrestrictedaccess to food. Furthermore, these immunedeficits carried over into the next generationof offspring, demonstrating a long-term, in-tergenerational effect of maternal undernutri-tion (Beach et al. 1982, Chandra 1975).

Similar processes appear to be at work inhumans. Infants in an expanding urban areaof the Philippines born small-for-gestationalage—indicating a relatively impoverishedprenatal nutritional environment—are lesslikely to respond to vaccination in adoles-cence, and produce lower concentrations ofthymopoietin, a thymic hormone importantfor cell-mediated immunity (McDade et al.2001a,b). In addition, slow rates of growth ininfancy—likely indicative of inadequate post-natal nutrition—are associated with reducedvaccine responsiveness and thymopoietin pro-duction in adolescence. In this population, therelationships among early undernutrition andadolescent immunocompetence are indepen-dent of a wide range of potentially confound-ing variables and suggest that nutritional fac-tors early in life may have organizationaleffects on important immune processes.

In a mechanistic sense, because gestationand early infancy are critical periods of im-munological development, early nutritionalinsults may therefore have a disproportionalimpact on immunity later in life (Moore1998). A complementary, and by no meanscontradictory, adaptationist explanation sug-gests that environments early in life may be re-liable predictors of future resource availabilityand that individuals may set long-term invest-ment in immune defenses accordingly. Giventhe relatively high resource costs of immunefunction, limiting one’s allocation to immu-nity may serve to ensure sufficient resourcesfor other critical purposes (McDade 2005).

In sum, nutritional factors have direct im-plications for immune development and func-tion, as well as indirect effects by determin-ing the severity of trade-offs associated withinvestment in immunity versus other life his-tory functions. The quantity and quality of lo-cal food resources are therefore likely to con-tribute to variation in immune function, alongwith other cultural factors such as subsistencestrategy, food preferences and taboos, gender-and age-specific patterns of food distribu-tion, and patterns of supplemental feeding ininfancy.

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Ecology of Infectious Disease

Because protection against microbial invasionis the primary function of the immune system,one might anticipate significant developmen-tal sensitivity to the ecology of infectious dis-ease. Furthermore, as noted above, immunityis a demand-driven system that “expects” anti-genic input to guide its development and func-tion. This occurs on two levels: through spe-cific antigenic encounters that determine anindividual’s memory lymphocyte repertoire,and through broad patterns of pathogen en-counter that have more generalized effects onspecific immune subsystems.

The first and most obvious way in whichthe local disease ecology shapes immune de-velopment and function follows logically fromthe mechanics of clonal selection. Specificantigens bind only those T and B lymphocyteswith matching receptors. These lymphocytesbecome active, replicate, and differentiate intoeffector as well as long-lived memory cells thatmobilize stronger and more rapid responsesupon antigen re-exposure (Paul 2003). Differ-ent patterns of antigen exposure lead to theselection and proliferation of different lym-phocyte clones, establishing different reper-toires of specific immune defenses. Throughthis antigen-driven process of clonal selec-tion, the immune system literally embodiesknowledge about the local disease ecology inits repertoire of memory T and B lympho-cytes. Different ecologies will therefore pro-duce different immune repertoires.

In addition to specific pathogen encoun-ters, broad patterns of exposure can have last-ing developmental implications. For example,in the Philippines, a higher burden of infec-tious disease in the first year of life morethan doubles the likelihood of respondingadequately to typhoid vaccination in adoles-cence, controlling for a number of poten-tially confounding variables (McDade et al.2001a). Similar associations between early in-fection and later immunocompetence havebeen reported in other populations as well(Rook & Stanford 1998), although inconsis-

tent findings are also present (Shaheen et al.1996). Just as early nutritional environmentsmay influence long-term investment in im-munity, early pathogen exposure may serve asa predictor of future ecological pathogenicity.Investments in immune function may be setaccordingly; individuals in high pathogen en-vironments may devote more resources to thedevelopment of antipathogen defenses.

In addition, the frequency and intensity ofpathogen exposure may have lasting organi-zational effects on subsystems of defense. Forexample, two subsets of helper T lymphocytesplay complementary roles in regulating spe-cific immune activities, with Th1 cells con-tributing to cell-mediated and inflammatoryprocesses and Th2 cells promoting humoral-mediated activities and antibody production(Dong & Flavell 2001, Paul 2003). T lym-phocytes are biased toward the Th2 pheno-type at birth, and developing a proper balancebetween Th1 and Th2 responses is critical formaximizing effectiveness against a wide rangeof potential pathogens and for minimizing therisk of immunopathology. Exposure to infec-tious disease early in life plays a critical role inentraining an effective regulatory T cell net-work (Yazdanbakhsh et al. 2002).

The absence of such input may be re-sponsible for rising rates of IgE-mediatedatopic diseases such as allergy and asthmain populations where recent improvementsin sanitation and vaccination have signifi-cantly reduced pathogen exposure (Cookson& Moffatt 1997, Rook & Stanford 1998).Support for this “hygiene hypothesis” comesfrom a number of studies reporting that in-fectious morbidity early in life is associatedwith increases in Th2 cytokine production,IgE concentration, and symptoms of allergyand asthma later in life (Matricardi et al. 2000,McDade et al. 2004b, Shirakawa et al. 1997)(Figure 4). In contrast, populations charac-terized by chronic helminthic infection alsoproduce high concentrations of Th2 cytokinesand IgE but do not suffer from allergy orasthma (Hurtado et al. 1997, Yazdanbakhshet al. 2002). In these cases, chronic pathogen

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Figure 4Relationshipbetween infectiousmorbidity in thefirst 6 months oflife and total IgEconcentration atage 14–15 years inthe Philippines.Results areadjusted for sex,pathogen exposurein the first year oflife, birth weight-for-gestational age,weight gain in thefirst 6 months, andcurrent householdincome (McDadeet al. 2004).

exposure promotes the development of astrong anti-inflammatory regulatory networkthat allows Th2-mediated processes to fighthelminthic infection without invoking the im-munopathological side effects that such pro-cesses may elicit in populations with low lev-els of pathogen exposure (Yazdanbakhsh et al.2002).

Thus, the ecology of infectious disease mayshape physiological trade-offs within the im-mune system itself and contribute to the de-velopment of antipathogen defenses that areadapted to the local disease ecology. Thisplasticity may explain the divergent effects ofearly pathogen exposure on adolescent im-mune function in the Philippines: High ratesof infectious disease in infancy are associatedwith stronger vaccine responses in adoles-cence but lower concentrations of total IgE.Early pathogen exposure may have organiza-tional effects by selectively upregulating in-vestment in certain aspects of immunity, whiledownregulating others. Whether this is anadaptive process that mobilizes more effectivedefenses that are tailored to the local diseaseecology remains to be seen.

Rising rates of allergy and asthma may rep-resent a breakdown in this process. Just asthe nervous system relies on appropriate sen-sory input during critical periods of develop-ment (Changeux 1997), the immune systemmay expect antigen encounters to guide thedevelopment of regulatory networks, informinvestment in subsystems of defense, and es-tablish a mature lymphocyte repertoire. In-deed, Fessler & Abrams (2004) have arguedthat the propensity of infants to mouth objectsduring the first two to three years of life—despite considerable risk of choking and toxinexposure—may be motivated by the need tosample the pathogenic environment.

However, cultural models that constructgerms as threats to be avoided at all costs,that promote the use of antibacterial soapsand other “sanitizing” products, and that en-courage parents to believe that infections arenot a normal part of child development maylimit pathogen exposure early in life. Demo-graphic trends toward small nuclear familiesliving in relatively isolated residential unitsmay contribute further. The cultural ecologyof pathogen exposure may therefore result in

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a poorly educated immune system that is morelikely to engage in inadequately regulated orself-reactive activities, with implications forallergy and asthma later in life.

Reproductive Ecology

Reproductive ecology is a thriving area of an-thropological research that has transformedcurrent understandings of human reproduc-tion on multiple levels (Ellison 2001, Konner& Worthman 1980, Vitzthum 1994, Wood1994), but links with immunity have yet tobe elaborated. Recent work relying primar-ily on bird models has emphasized the costsof reproduction, and similar issues may affectimmune function in humans as well.

In particular, a number of studies haveevaluated whether secondary sexual traits inmale birds (e.g., size of combs, tail feath-ers) are honest signals of their ability toresist parasitic infection that serve as cuesfor sexual selection (Moller et al. 1999, Zuket al. 1995). The extent to which androgens—testosterone in particular—mediate these as-sociations has been the subject of recent de-bate, and a number of investigators have em-phasized the more general point that immuneactivity and reproductive effort must competefor limited energetic resources (Buttgereitet al. 2000, Lochmiller & Deerenberg 2000,Sheldon & Verhulst 1996). For example, ex-perimental lengthening of ornamental tailfeathers in male barn swallows decreases im-mune responsiveness to immunization (Saino& Moller 1996). And across mammals, specieswith a higher degree of sexual dimorphism inbody size have a more pronounced sex bias inparasitic infection, suggesting that sexual se-lection for increased body size comes at a costto investment in immune defenses (Moore &Wilson 2002).

Analogous processes linking sexual dimor-phism, reproductive effort, and immunity maybe operating in humans, although empiricaltests are currently lacking. The costs of re-production for humans differ dramatically bysex: For females, gestation and lactation are

demanding in terms of both time and energy,whereas cost for males can be as minimal asa single contribution of sperm. However, thedevelopment and maintenance of male sec-ondary sexual characteristics can be concep-tualized as investment in reproductive effort,and males pay relatively higher costs than dofemales in this area owing to their larger over-all body mass and higher proportion of skele-tal muscle (Bribiescas 2001, Campbell et al.2001).

The immunological consequences of dif-ferential allocations to reproductive effortwithin males have not been directly evaluated,although recent findings from the Turkanaare suggestive. Men reporting symptoms ofchest infection (likely the result of tuberculo-sis) had higher concentrations of testosterone,consistent with the interpretation that repro-ductive effort may come at a cost to invest-ment in immune defenses (Campbell et al.2001). Contrary evidence comes from a largestudy of aggression and immune function inAmerican men, in which enumerative mea-sures of immunity were positively associatedwith testosterone (Granger et al. 2000). How-ever, these associations were weak and canbe explained largely by the positive associ-ation between testosterone and risky healthbehaviors.

Alterations in immune function asso-ciated with puberty correspond to risingconcentrations of sex steroids and may pro-vide evidence in support of a trade-off be-tween reproductive effort and immunity.However, the causal role of sex steroids is notclear: Although their effects are generally im-munosuppressive (particularly testosterone),these effects are far from simple and may bebetter described as immunomodulatory (DaSilva 1999, Schuurs & Verheul 1990).

The immunological costs of reproductionfor females are more direct: Pregnancy initi-ates a number of changes, including reducedT lymphocyte proliferation, shifts in helperT activity toward the Th2 phenotype, slowedneutrophil chemotaxis, and reduced concen-trations of IgG as a result of active transfer to

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the fetus (Blackburn & Loper 1992, Iwatani &Watanabe 1998). This strategic pattern of im-munosuppression prevents rejection of the fe-tus but increases vulnerability to certain infec-tious agents during pregnancy. Recent workhas suggested that the mechanisms invokingthis immunosuppression may function mal-adaptively outside of pregnancy to contributeto the etiology of HIV (Hoff 1999).

In addition to direct immune suppres-sion, increased demands for macro- and mi-cronutrients during gestation limit their avail-ability for immune processes (Lunn 1994,Prentice & Prentice 1988). This can be par-ticularly problematic when opportunities forcompensatory increases in dietary intake arelimited, and when the cumulative demands ofmultiple, closely spaced pregnancies can leadto progressive declines in maternal nutritionalstatus (Merchant & Martorell 1988, Wood1994). The immunological costs of reproduc-tion may be particularly high for women inpronatalist settings that do not provide the so-cial and/or nutritional resources necessary tosupport this effort.

Lactation is also an important link be-tween reproduction and immune function be-cause breastmilk provides effective protectionagainst infectious disease. Infants are particu-larly vulnerable owing to the naıvete of theirspecific immune defenses, but the antigen-binding specificities of sIgA in breastmilk arethe product of prior maternal antigenic en-counters and therefore provide specific im-mune defenses that are tailored to the lo-cal disease ecology. Cultural practices thatshape the intensity and diversity of maternalantigen exposure therefore have direct im-plications for infant immunity. In addition,a range of nonspecific defenses are presentin breastmilk that inhibit pathogen coloniza-tion and growth in the infant gastrointesti-nal and respiratory tracts, and growth factorsfacilitate the maturation of mucosal tissues(Ogra & Fishaut 1990). Breastfeeding thusbolsters the infant’s developing defenses andprovides a period of buffered exposure dur-ing which pathogen encounters can educate

the infant’s immune system while posing areduced risk of infection (Fessler & Abrams2004, McDade & Worthman 1999). Breast-feeding also has long-term effects on immunedevelopment, with implications for allergylater in life (Bjorksten & Kjellman 1990).

Although there are nutritional and emo-tional, as well as immunological, benefits toprolonged breastfeeding, mothers pay signif-icant energetic, nutritional, and reproductivecosts as well. Mothers and infants must bal-ance these costs and benefits in relation to arange of social and cultural ecological factorsthat support, as well as constrain, breastfeed-ing behavior (McDade & Worthman 1998).With the antipathogen benefits of breastmilkand the high risk of infection in infancy, theintensity of pathogen exposure is likely toplay an important role in defining this trade-off. This appears to be the case in an ur-ban environment in the Philippines, wheremothers living in less sanitary households ex-clusively breastfeed their infants for signifi-cantly longer than do mothers in more sani-tary households where pathogen exposure islikely to be reduced (60.1 versus 55.9 days)(McDade 2003b). The nutritional resourcesof the mother are also likely to be an im-portant factor since undernourished moth-ers are less able to pay the costs of pro-longed breastfeeding, even in high pathogenenvironments.

Last, given the costs of reproduction andtheir relevance to immune function, increasedreproductive effort over the life course maycontribute to accelerated immunosenescenceand early aging. For example, historical de-mographic data from Germany reveal thata woman’s lifespan is negatively related tothe number of children to whom she gavebirth (Lycett et al. 2000). This associationwas significant only among poor landlesswomen, which suggests that reproductive ef-fort may exact a higher toll in ecological orcultural circumstances that limit resource ac-cess. Immune function may be an impor-tant mediator here, although it remains to beseen if increased reproductive effort early in

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life can affect immunological aging later inlife.

Social Ecology

Although aspects of the surrounding physi-cal ecology are important to immune func-tion, recent research has also demonstratedthat social and cognitive processes leadingto psychosocial stress have direct implica-tions for multiple parameters of immunity. Asnoted earlier, the immune system interdigi-tates with the nervous and endocrine systemsat multiple levels, providing the physiologi-cal infrastructure through which psychosocialexperience can have direct immunomodula-tory consequences (Ader et al. 2001, Bese-dovsky & del Rey 1996). The growing fieldof psychoneuroimmunology (PNI) has es-tablished this as an important area of re-search, and has challenged prevailing no-tions of brain/body dualism by elucidatingthe mechanisms through which psychosocialphenomena influence physiology (Ader et al.2001, Glaser & Kiecolt-Glaser 1994).

Most PNI research uses experimental an-imal models or clinic-based research designs,but a number of studies have established thathuman immunity is sensitive to a wide rangeof naturalistic stressors (Table 3). In particu-

PNI: psychoneuro-immunology

lar, social relationships are important sourcesof stress, as well as sources of support. Forexample, early work in this area has reportedconsistent impairments in immune functionfollowing the loss of a loved one (Irwin et al.1987), whereas more recent research alongthis theme has demonstrated that problem-atic personal relationships adversely affect arange of immune parameters (Kiecolt-Glaseret al. 1994). Slowed wound healing, increasedlikelihood of infection, and impaired responseto vaccination are all immune-mediatedhealth outcomes that have been convincinglyassociated with psychosocial stress (Cohenet al. 1991, Glaser et al. 1992).

The impact of stress on immune functionhas been investigated primarily in adults, butthe relatively few studies conducted with chil-dren and adolescents indicate significant ad-verse effects as well (Birmaher et al. 1994,Boyce et al. 1993). In addition, experimen-tal research with nonhuman primates suggeststhat maternal stress during pregnancy and ma-ternal separation in infancy have lasting ef-fects on offspring immune function that per-sist into adulthood (Coe et al. 2002).

Chronic psychosocial stressors have beenconsistently associated with decreased num-bers of T, B, and NK cells, suppressed lym-phocyte proliferation and cytotoxic activity,

Table 3 Previous research with healthy individuals documenting an association betweennaturalistic stressors and human immune function (Biondi 2001)

Stressor Immune outcomesNatural disasters ↓ lymphocyte proliferation; ↓ NK activity; ↓ # CD4+, CD8+Loneliness/low social support ↓ lymphocyte proliferation; ↓ NK activity; ↓ # lymphocytesBereavement ↓ lymphocyte proliferation; ↓ NK activitySeparation/divorce ↑ herpesvirus antibody titersMarital conflict ↓ lymphocyte proliferation; ↓ NK activity; ↑ herpesvirus antibody

titers; ↑ # CD4+Caring for disabled ordemented relative

↓ lymphocyte proliferation; ↓ NK activity; ↓ vaccine response;↑ herpesvirus antibody titers; ↑ # CD8+; ↓ # NK cells

Unemployment/economiccrisis

↓ lymphocyte proliferation; ↓ IL-2, ↑ IL-4 production

Starting a new school ↓ lymphocyte proliferation; ↑ #, % CD4+Academic stress ↓ NK activity; ↓ vaccine response; ↑ herpesvirus antibody titers;

↓ # CD4+

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and lower levels of sIgA and IgM. Antibodiesto latent herpesviruses are also consistentlyelevated under stress, indicating reductionin aspects of cell-mediated immune function(Biondi 2001, Herbert & Cohen 1993). Ameta-analysis of this literature supports thefollowing tentative conclusions regarding theimpact of stress on human immune function:(a) Objective events have greater effects thando self-reports of stress; (b) long-term stres-sors have more consistent negative effectsthan do acute stressors, with little evidencethat the immune system adapts to chronicstress; and (c) social and nonsocial stressorshave different immunological consequences(Herbert & Cohen 1993).

One shortcoming of PNI is that the vastmajority of studies draw from relatively ho-mogenous, affluent Western populations. Arecent review underscores this point, stat-ing “[t]he typical experimental subject in psy-choimmunology is a young, male, Caucasian,healthy, medical or psychology student, prob-ably a light or nonsmoker, consuming little orno alcohol or coffee, with no history of allergyor recent infectious disease. . .” (Biondi 2001,p. 202). This scenario reflects in part method-ological constraints associated with assessingimmune function, but it is also indicates thatsociocultural factors shaping the experienceof stress are not of central concern. Rather,stressors are conceptualized as the startingpoint for investigating the proximate phys-iological mechanisms linking behavior, neu-roendocrine activity, immune function, anddisease. The experience of stress is locally con-structed and embedded within specific cul-tural contexts (Young 1980), and the relativelynarrow focus of PNI misses an opportunity toconsider cultural and ecological diversity instressors and their impact on immunity.

Stress is a central concept in biologicalanthropology (Brown 1981, Dressler 1995,Goodman et al. 1988), but relatively few stud-ies have considered its impact on immunefunction. Flinn & England have conducted along-term, naturalistic investigation of child-hood stress and physical health in Dominica

using multiple measures of salivary cortisolto gain insight into the physiological effectsof a range of psychosocial stressors (Flinn &England 1995, 1997). Chronic stressors—inparticular stressors related to family composi-tion and stability—are associated with higheraverage cortisol, which is in turn associatedwith increased frequency of infection. Stress-induced alteration in immune function maybe an important mediator of these associ-ations: Recent analyses report that chroni-cally stressed children have lower concen-trations of sIgA and that salivary concentra-tions of neopterin and β2-microglobulin (in-terpreted as measures of cell-mediated im-mune activity) are suppressed for at leasttwo days following a stressful event (Flinn &England 2003).

In an explicit attempt to integrate PNIand biological anthropology, McDade andcolleagues have investigated culture change,stress, and immune function among childrenand adolescents in Samoa. Immunity was as-sessed in 760 4- to 20-year-olds by measur-ing EBV antibodies in dried blood spot sam-ples collected following a simple finger prick(McDade et al. 2000a). This indirect, func-tional measure of cell-mediated immune func-tion is among the strongest and most con-sistent immunological correlates of chronicstress (Herbert & Cohen 1993), and itsmeasurement in dried blood spots overcomeslogistical obstacles associated with collectingand transporting serum or plasma.

Ecological comparisons indicated thatchildren and adolescents in the capital cityand surrounding areas had higher EBV an-tibody titers than did their peers in re-mote areas, independent of a range of po-tentially confounding factors (McDade et al.2000b). Higher EBV antibody titers reflectpoorer cell-mediated immune function andsuggest an increased burden of psychosocialstress, possibly due to the emerging influ-ence of Western lifestyles in more urban ar-eas of Samoa. In addition, consistent withprevious research on stress and immunityin U.S. populations, major life events were

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Figure 5Interaction betweenthe occurrence offaalavelave in theprevious year andhouseholdsocioeconomic statusin predicting EBVantibody titers in10–20-year-olds inSamoa. Faalavelave isa system of public,formalized giftexchange in Samoa,and the financial andsocial debtsassociated withfaalavelave are asignificant source ofstress (McDade2003a).

associated with increased EBV antibodies, al-though socioeconomic status was a modera-tor of this effect (Figure 5) (McDade 2003a).An additional series of analyses has exploredmore fine-grained, individual-level models ofculture change and stress (McDade 2002,McDade & Worthman 2004). This work hasbeen significant in demonstrating the feasibil-ity of studying stress and immune function innon-Western, nonclinical settings and in un-derscoring the importance of cultural factorsin defining the experience of stress.

It is not clear why, in an evolutionarysense, psychosocial stress should suppress im-mune defenses, particularly because stressfulcircumstances may be associated with greaterrisks of infection and/or injury. Psychoneu-roimmunology has addressed this question inmechanistic terms, focusing largely on thedual role of cortisol as a central componentof the physiological response to stress and asa potent immunosuppressive agent (Munck& Guyre 1991). Given the costs of immu-nity, suppressing immune activity under timesof stress may serve the adaptive function offreeing up limited resources for more press-ing metabolic demands (Maier et al. 1994,

Sapolsky 1994, Sheldon & Verhulst 1996).Alternatively, cortisol-mediated immunosup-pression may reflect an important regula-tory mechanism that prevents immune re-sponses from getting out of control, therebyreducing the risk of self-reactivity and au-toimmunity in times of stress (Raberg et al.1998).

In sum, psychosocial factors have direct ef-fects on multiple parameters of human im-mune function. Stress is an inevitable part ofhuman experience, and current research inPNI has built a solid foundation upon which amore contextualized, cross-cultural approachcan be constructed.

Political Ecology

Just as cultural factors are defining compo-nents of the ecologies of human immunefunction, regional as well as global politi-cal and economic processes inform the localcultural ecology. Broader political-economicstructures—and individuals’ positions withinthem—limit access to nutritional and eco-nomic resources, condition probabilities ofpathogen exposure, motivate patterns of

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reproductive behavior, and impose differen-tial burdens of psychosocial stress.

There are substantial challenges associatedwith linking macro- and microlevel processes,and a political ecology of immune function hasyet to be elaborated. A recent analysis takes astep in this direction by proposing that in-creased consumption of processed foods pro-duced and distributed by the global food in-dustry may modify immune reactivity andtherefore contribute to rising rates of allergyand autoimmune disease (Cone & Martin2003). In addition, although the epidemio-logic triad of host, pathogen, and environ-ment has guided public health approaches toinfectious disease, critical medical anthropol-ogy has emphasized that economic, social, andpolitical factors are the ultimate causes of dis-ease (Farmer 1993, Turshen 1984). A politi-cal ecology of immune function can draw onthese conceptual and analytic tools and con-tribute to the new biocultural synthesis thatattempts to integrate political-economic fac-tors into the study of human biology and adap-tation (Goodman & Leatherman 1998).

TOWARD A HUMANECOLOGICAL IMMUNOLOGY

The ecologies of human immune function aremultiple: Central aspects of immune develop-ment and function are responsive to a rangeof nutritional, pathogenic, reproductive, andsocial factors. However, research in each ofthese areas has proceeded in relative isolation.A fuller understanding of the contextual fac-tors shaping human immunity requires a morecomprehensive, multidimensional approach(Figure 6). Despite significant methodologi-cal and conceptual challenges, there are sev-eral advantages to such an approach.

First, an integrated perspective mirrorsthe overlapping nature of real-world environ-ments. Although laboratory or clinic-basedresearch can isolate specific variables of in-terest, psychosocial and ecological stressorsare rarely discrete. For instance, undernutri-tion and infectious disease frequently go hand

in hand. Food insecurity may be a signifi-cant source of psychosocial stress, as well asa contributor to malnutrition. Reproductivebehavior may be associated with patterns ofpathogen exposure. Simultaneous considera-tion of these factors represents the reality ofthe environments in which we live and thatshape human immune function.

Second, simultaneous consideration ofmultiple ecological factors is consistent withthe fact that physiological systems integrateinformation across multiple sources. For ex-ample, as noted above, the hypothalamic-pituitary-adrenal axis, and its primary endproduct, cortisol, are important mediators ofthe association between psychosocial stressand immune function. However, cortisolalso plays a critical metabolic role in mo-bilizing energetic resources, and concentra-tions increase with undernutrition (Sapolsky1994). Furthermore, cortisol production isupregulated following infection (Munck &Guyre 1991). Testosterone and estradiol—primary products of the hypothalamic-pituitary-gonadal axis—may mediate trade-offs between investment in immune func-tion and reproductive effort (Bribiescas 2001,Campbell et al. 2001), but their physiologicalactivity is also affected by psychosocial stress,nutritional status, and infection (Ellison 2001,Sapolsky 1994). The point here is that mul-tiple ecological factors affect immune func-tion through shared mechanisms, and thesemechanisms are in turn sensitive to a variety ofecological factors. Although the simultaneousconsideration of the immunological impact ofnutritional, pathogenic, psychosocial, and/orreproductive factors adds considerable com-plexity, it reflects the complexity of the un-derlying physiology that transduces ecologi-cal information into physiological action.

Third, an integrated approach encouragesinvestigation of interactions across ecologicaldomains. For example, the extent to whichundernutrition exacerbates, or overwhelms,the impact of psychosocial stress on im-mune function is currently unknown. Currentresearch in psychoneuroimmunology avoids

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Figure 6A conceptual modelfor human ecologicalimmunology.Overlappingecological factors areembedded in broadercultural andpolitical-economiccontexts and havedirect effects onimmunedevelopment andfunction. Interactiveeffects are also likelybut have yet to befully investigated.

this question by conceptualizing undernutri-tion as a nuisance factor that must be con-trolled for by focusing exclusively on healthyindividuals. As with other physiological mea-sures that are responsive to multiple exoge-nous factors (e.g., blood pressure), there isno a priori reason why population-level anal-yses cannot model the simultaneous effectsof multiple physical as well as psychosocialstressors on human immune function. The na-ture of interaction across these domains thenbecomes an interesting empirical question.For example, does undernutrition obscure

the immunosuppressive effects of psychoso-cial stress, or are their joint effects additive ormultiplicative?

A foregrounding of development will beimportant to an integrated ecological per-spective since the immune system may bemore or less sensitive to various ecologi-cal inputs at different life stages (Figure 7).Current research suggests that nutritionaland pathogenic factors are particularly crit-ical early in life, whereas reproductivetrade-offs are not likely to emerge untiladolescence. Psychosocial stress is important

Figure 7The relative impactof differentecological factors onimmune function atmultipledevelopmentalstages.

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Life history theory:a branch ofevolutionary theorythat emphasizes thelife cycle and thatattempts to explainvariation inreproductive anddevelopmentalstrategies (andrelated traits), bothwithin and acrossspecies

throughout life, although organizational ef-fects may occur early in life. At this point, therelative strength of these effects must be re-garded as speculative because they have yetto be evaluated simultaneously. In addition,different factors may be more or less rele-vant to specific subsystems of immune de-fense, and circumstances early in life may con-dition sensitivity to ecological stressors laterin life. Regardless, as human ecological im-munology moves forward it will be importantto keep developmental issues in mind.

Last, human ecological immunology canproceed as a purely descriptive endeavor, orit can draw on theory to guide hypothesistesting and interpretation. Life history theoryhas provided such an adaptationist frameworkfor a growing body of avian research (Molleret al. 1999, Sheldon & Verhulst 1996, Zuket al. 1995), and human ecological immunol-ogy may profit from its application as well.With its emphasis on strategies for the opti-mal allocation of limited resources, life his-tory theory can suggest testable hypothesesregarding trade-offs in investment in immu-nity at various life stages (McDade 2003b). Itcan also help identify the culturally mediatedbehaviors and settings most likely to set theparameters for these trade-offs. A groundingin life history theory provides a basis for antic-ipating and explaining—not just describing—the associations among cultural ecological fac-tors and human immune function.

CONCLUSION

The human immune system—like other phys-iological systems—is a product of natural se-lection and is responsive to the contingenciesof the surrounding nutritional, pathogenic,reproductive, and psychosocial environmentsin which it develops and functions. Apopulation-level, cross-cultural, adaptationistapproach is therefore a necessary complementto the cellular and molecular levels of analy-sis currently favored by biomedical immunol-ogy. Just as previous research in reproductiveecology has led to conceptual and physiolog-

ical insights into the dynamics of human re-production (Ellison 2001), human ecologicalimmunology promises to make similar con-tributions to our understanding of this multi-faceted system of defense.

Research in human ecological immunol-ogy is in its earliest stages and will face con-siderable challenges as it progresses, not theleast of which is the complexity of immunefunction and its assessment. This is, however,a surmountable obstacle because a number ofrobust field methods are currently available,and the range of options will increase with fu-ture technological innovations.

An important first step will be the appli-cation of these methods across a wide rangeof populations to investigate the degree ofvariation in major parameters of immunity.Such variation may challenge current defi-nitions of “normal” immune function basedon research in overnourished, underinfectedWestern populations and will provide a foun-dation for testing hypotheses regarding therelative contributions of multiple ecologicalfactors. Conceptual and analytical tools bor-rowed from life history theory can be used toconstruct an adaptationist framework that willencourage the development of human eco-logical immunology as an explanatory, ratherthan merely descriptive, endeavor. Attentionto cultural and political-economic processeswill further increase explanatory power andacknowledge their fundamental contributionto human behavior, biology, and health.

Biological anthropology is in an excellentposition to play a major role in this effort. De-velopment, human variation, and adaptationare central concepts, with an emerging em-phasis on the underlying physiological pro-cesses that link cultural and ecological con-texts with developmental and health outcomes(Dressler 1995, Goodman & Leatherman1998, Panter-Brick & Worthman 1999). Inaddition, a longstanding tradition of field-work has encouraged the application of in-novative methods that are amenable to theconstraints of population-level, community-based research in remote settings (Ellison

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1988, Worthman & Stallings 1997). We cur-rently possess the theoretical and method-ological tools to develop human ecological

immunology as a thriving area of investiga-tion that makes important contributions toanthropology, immunology, and beyond.

SUMMARY POINTS

1. The immune system is a product of natural selection, and a population-based, adap-tationist, ecological perspective is a necessary complement to current biomedical per-spectives that emphasize clinical and molecular levels of analysis.

2. There are trade-offs associated with investment in immunity, and a consideration ofcosts as well as benefits across a range of ecological settings may help explain patternsof variation in this complex physiological system.

3. Immune function is context-dependent: There are multiple mechanisms throughwhich the immune system incorporates information from surrounding ecological fac-tors to inform its development and function.

4. Nutritional resources, patterns of pathogen exposure, reproductive behavior, and psy-chosocial stress are all critical determinants of immune development and function,and together they comprise the cultural ecology of human immunity.

5. Current research considers these ecological factors in isolation, but an integrative,developmental approach is needed to promote human ecological immunology as anactive area of research that can make important contributions to anthropology as wellas immunology.

UNRESOLVED ISSUES/FUTURE DIRECTIONS

1. The complexity of the immune system is a significant obstacle to its measurement—particularly in field settings—and additional work is needed to validate methodologicaltools for assessing and interpreting parameters of immune function.

2. The measurement of immune parameters across a wider range of populations is neededto determine the degree of variation in these parameters, and to establish a foundationfor formulating hypotheses regarding the relative contributions of ecological factorsto explaining this variation.

3. Theoretical and conceptual tools—possibly borrowed from life history theory—willbe necessary to develop human ecological immunology as an explanatory, rather thanmerely descriptive, endeavor.

ACKNOWLEDGMENTS

I am grateful to the National Science Foundation Physical Anthropology Program for financialsupport through a Presidential Early Career Award for Scientists and Engineers (PECASE;BCS-0134225).

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Annual Review ofAnthropology

Volume 34, 2005

Contents

FrontispieceSally Falk Moore � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � xvi

Prefatory Chapter

Comparisons: Possible and ImpossibleSally Falk Moore � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Archaeology

Archaeology, Ecological History, and ConservationFrances M. Hayashida � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �43

Archaeology of the BodyRosemary A. Joyce � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 139

Looting and the World’s Archaeological Heritage: The InadequateResponseNeil Brodie and Colin Renfrew � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 343

Through Wary Eyes: Indigenous Perspectives on ArchaeologyJoe Watkins � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 429

The Archaeology of Black Americans in Recent TimesMark P. Leone, Cheryl Janifer LaRoche, and Jennifer J. Babiarz � � � � � � � � � � � � � � � � � � � � � � � 575

Biological Anthropology

Early Modern HumansErik Trinkaus � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 207

Metabolic Adaptation in Indigenous Siberian PopulationsWilliam R. Leonard, J. Josh Snodgrass, and Mark V. Sorensen � � � � � � � � � � � � � � � � � � � � � � � � � � 451

The Ecologies of Human Immune FunctionThomas W. McDade � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 495

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Linguistics and Communicative Practices

New Directions in Pidgin and Creole StudiesMarlyse Baptista � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �33

Pierre Bourdieu and the Practices of LanguageWilliam F. Hanks � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �67

Areal Linguistics and Mainland Southeast AsiaN.J. Enfield � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 181

Communicability, Racial Discourse, and DiseaseCharles L. Briggs � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 269

Will Indigenous Languages Survive?Michael Walsh � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 293

Linguistic, Cultural, and Biological DiversityLuisa Maffi � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 599

International Anthropology and Regional Studies

Caste and Politics: Identity Over SystemDipankar Gupta � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 409

Indigenous Movements in AustraliaFrancesca Merlan � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 473

Indigenous Movements in Latin America, 1992–2004: Controversies,Ironies, New DirectionsJean E. Jackson and Kay B. Warren � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 549

Sociocultural Anthropology

The Cultural Politics of Body SizeHelen Gremillion � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �13

Too Much for Too Few: Problems of Indigenous Land Rights in LatinAmericaAnthony Stocks � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �85

Intellectuals and Nationalism: Anthropological EngagementsDominic Boyer and Claudio Lomnitz � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 105

The Effect of Market Economies on the Well-Being of IndigenousPeoples and on Their Use of Renewable Natural ResourcesRicardo Godoy, Victoria Reyes-Garcıa, Elizabeth Byron, William R. Leonard,

and Vincent Vadez � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 121

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An Excess of Description: Ethnography, Race, and Visual TechnologiesDeborah Poole � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 159

Race and Ethnicity in Public Health Research: Models to ExplainHealth DisparitiesWilliam W. Dressler, Kathryn S. Oths, and Clarence C. Gravlee � � � � � � � � � � � � � � � � � � � � � � � � 231

Recent Ethnographic Research on North American IndigenousPeoplesPauline Turner Strong � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 253

The Anthropology of the Beginnings and Ends of LifeSharon R. Kaufman and Lynn M. Morgan � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 317

Immigrant Racialization and the New Savage Slot: Race, Migration,and Immigration in the New EuropePaul A. Silverstein � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 363

Autochthony: Local or Global? New Modes in the Struggle overCitizenship and Belonging in Africa and EuropeBambi Ceuppens and Peter Geschiere � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 385

Caste and Politics: Identity Over SystemDipankar Gupta � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 409

The Evolution of Human Physical AttractivenessSteven W. Gangestad and Glenn J. Scheyd � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 523

Mapping Indigenous LandsMac Chapin, Zachary Lamb, and Bill Threlkeld � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 619

Human Rights, Biomedical Science, and Infectious Diseases AmongSouth American Indigenous GroupsA. Magdalena Hurtado, Carol A. Lambourne, Paul James, Kim Hill,

Karen Cheman, and Keely Baca � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 639

Interrogating Racism: Toward an Antiracist AnthropologyLeith Mullings � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 667

Enhancement Technologies and the BodyLinda F. Hogle � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 695

Social and Cultural Policies Toward Indigenous Peoples: Perspectivesfrom Latin AmericaGuillermo de la Pena � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 717

Surfacing the Body InteriorJanelle S. Taylor � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 741

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Theme 1: Race and Racism

Race and Ethnicity in Public Health Research: Models to ExplainHealth DisparitiesWilliam W. Dressler, Kathryn S. Oths, and Clarence C. Gravlee � � � � � � � � � � � � � � � � � � � � � � � � 231

Communicability, Racial Discourse, and DiseaseCharles L. Briggs � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 269

Immigrant Racialization and the New Savage Slot: Race, Migration,and Immigration in the New EuropePaul A. Silverstein � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 363

The Archaeology of Black Americans in Recent TimesMark P. Leone, Cheryl Janifer LaRoche, and Jennifer J. Babiarz � � � � � � � � � � � � � � � � � � � � � � � 575

Interrogating Racism: Toward an Antiracist AnthropologyLeith Mullings � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 667

Theme 2: Indigenous Peoples

The Effect of Market Economies on the Well-Being of IndigenousPeoples and on Their Use of Renewable Natural ResourcesRicardo Godoy, Victoria Reyes-Garcıa, Elizabeth Byron, William R. Leonard,

and Vincent Vadez � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 121

Recent Ethnographic Research on North American IndigenousPeoplesPauline Turner Strong � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 253

Will Indigenous Languages Survive?Michael Walsh � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 293

Autochthony: Local or Global? New Modes in the Struggle overCitizenship and Belonging in Africa and EuropeBambi Ceuppens and Peter Geschiere � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 385

Through Wary Eyes: Indigenous Perspectives on ArchaeologyJoe Watkins � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 429

Metabolic Adaptation in Indigenous Siberian PopulationsWilliam R. Leonard, J. Josh Snodgrass, and Mark V. Sorensen � � � � � � � � � � � � � � � � � � � � � � � � � � 451

Indigenous Movements in AustraliaFrancesca Merlan � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 473

Indigenous Movements in Latin America, 1992–2004: Controversies,Ironies, New DirectionsJean E. Jackson and Kay B. Warren � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 549

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Contents ARI 12 August 2005 20:29

Linguistic, Cultural, and Biological DiversityLuisa Maffi � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 599

Human Rights, Biomedical Science, and Infectious Diseases AmongSouth American Indigenous GroupsA. Magdalena Hurtado, Carol A. Lambourne, Paul James, Kim Hill,

Karen Cheman, and Keely Baca � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 639

Social and Cultural Policies Toward Indigenous Peoples: Perspectivesfrom Latin AmericaGuillermo de la Pena � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 717

Indexes

Subject Index � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 757

Cumulative Index of Contributing Authors, Volumes 26–34 � � � � � � � � � � � � � � � � � � � � � � � � � � � 771

Cumulative Index of Chapter Titles, Volumes 26–34 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 774

Errata

An online log of corrections to Annual Review of Anthropology chaptersmay be found at http://anthro.annualreviews.org/errata.shtml

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