Omohundro Institute of Early American History and Culture

Virgin Soils Revisited Author(s): David S. Jones Source: The William and Mary Quarterly, Vol. 60, No. 4 (Oct., 2003), pp. 703-742 Published by: Omohundro Institute of Early American History and Culture Stable URL: http://www.jstor.org/stable/3491697 Accessed: 09-10-2015 14:47 UTC

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This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VirginSoils Revisited

David S. Jones

HE decimationof AmericanIndian populations that followed European arrivalin the Americaswas one of the most shocking demographicevents of the last millennium.Indian populations declinedby as much as 95 percentin the firstcentury after the arrivalof ChristopherColumbus, promptingone historianto conclude that"early Americawas a catastrophe-a horrorstory, not an epic."' This collapse establishedthe foundationfor the subsequentsocial and politicaldevel- opmentsof Americanhistory. Since the earliestencounters of colonization, colonistsand theirdescendants have struggledto explainhow and whydepopulation occurred. They have debated the role of race,politics, and even genocide. All have concluded that infectiousdiseases, introduced by Europeans and Africans,played a decisive role. American Indians sufferedterrible mortality from smallpox, measles, tuberculosis, and many other diseases. Their susceptibilityled to American Indian declineeven as Europeanpopulations thrived. Discussions of the epidemiological vulnerability of American Indians rose to prominence with the work of William McNeill and AlfredW. Crosbyin the 1970s. Both arguedthat the depopulationof the Americaswas the inevitableresult of contact between disease-experienced Old World populations and the "virgin" populations of the Americas.As Crosby definedthem in 1976, "Virginsoil epidemicsare thosein whichthe populationsat riskhave had no previouscontact with the diseases that strikethem and are thereforeimmunologically almost

David Jonesis a memberof the Departmentof Psychiatry,McLean Hospital and the MassachusettsGeneral Hospital. This articleevolved out of conversations withAllan Brandt,Arthur Kleinman, and JohnCoatsworth. The authoralso bene- fited fromadvice fromWarwick Anderson,David Barnes, Conevery Bolton, ElizabethCaronna, Joyce Chaplin, Ward Churchill,Alfred Crosby, Ray Fisman, JeremyGreene, Nick King, Marc Lipsitch,Christopher Sellers, Keith Wailoo, Deborah Weinstein,members of the Historyof Medicine WorkingGroup at Harvard University,fellows and facultyof the Divisions of Immunologyand InfectiousDisease at Children'sHospital, Boston, and manyinsightful anonymous reviewers.The researchwas supportedin partby a grantfrom the Medical Scientist TrainingProgram, National Institutes of Health. 1 JohnM. Murrin,"Beneficiaries of Catastrophe:The EnglishColonies in America,"in Eric Foner, ed., The New AmericanHistory, rev. ed. (Philadelphia, 1997),4.

Williamand MaryQuarterly, 3d Series,Volume LX, Number4, October2003

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 704 WILLIAM AND MARY QUARTERLY defenseless."His theoryprovided a powerfulexplanation for the outcomes of encounterbetween Europeans and indigenousgroups, not just in theAmericas but throughoutthe world. Since Crosby'sanalysis of virgin soil epidemicsappeared in the Williamand Mary Quarterly,countless writershave cited his definition and attributed the devastation of American Indian populations to their immunologic inadequacy. As argued in Jared Diamond's Pulitzer Prize-winningGuns, Germs,and Steel,"The main killerswere Old World germsto which Indians had never been exposed, and against which they thereforehad neither immunenor geneticresistance." Such assertions,which apply the intu- itive appeal of natural selection to the demographic historyof the Americas,dominate academic and populardiscussions of depopulation.2 Even as Crosby'smodel of virginsoil epidemics remainsa central themeof the historiographyof the Americas,it has been misunderstood and misrepresented.Crosby actuallydownplayed the "geneticweakness hypothesis"and instead emphasized the many environmentalfactors that mighthave contributedto AmericanIndian susceptibilityto Old World diseases,including lack of childhoodexposure, malnutrition, and the social chaos generatedby Europeancolonization.3 Subsequent historians,however, have oftenreduced the complexityof Crosby'smodel to vague claims thatAmerican Indians had "no immunity"to the new epidemics. These claims obscure crucial distinctionsbetween different mechanisms that might have left American Indians vulnerable. Did AmericanIndians lack specificgenes thatmade Europeansand Africans, aftergenerations of natural selection, more resistantto smallpox and tuberculosis?Did theylack antibodiesthat theirEurasian counterparts acquired duringchildhood exposureto endemic infections?Were their immune systemscompromised by the malnutrition,exhaustion, and stresscreated by European colonization?These differentexplanations, blurredwithin simple claims of no immunity,have verydifferent impli- cations for our understandingof what was responsiblefor this demographiccatastrophe. It is now possible to revisitthe theoryof virginsoil epidemicsand reassessthe many possible causes of AmericanIndian susceptibilityto Europeanpathogens.4 The confusioncan be untangledby surveyingand

2 Crosby,"Virgin Soil Epidemicsas a Factorin theAboriginal Depopulation in America,"William and Mary Quarterly,3d Ser., 33 (1976), 289; Diamond, Guns, Germs,and Steel:The Fates of Human Societies (New York,1997), 211-12. 3 Crosby,"Virgin Soil Epidemics,"292. 4 For a challengeof anotheraspect of virginsoil theory,the assumptionthat new epidemicscaused Indian culturesand religionsto witheras quicklyas Indian bodies,see Paul Kelton,"Avoiding the SmallpoxSpirits: Colonial Epidemicsand SoutheasternIndian Survival," Ethnohistory, 50o(Fall 2oo3).

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 705 resynthesizingdiverse research about Indian depopulation.A reviewof the literatureof colonization shows the prevalenceof simplisticasser- tions of no immunityand their possible ideological appeals. It also demonstratesthe importanceof definingthe specificclaims contained withinthe theoryof virginsoil epidemicsand evaluatingeach of them separately.Recent immunological researchhas clarifiedthe different mechanismsthat can compromisehuman immunity.Parallel work by biological anthropologists,archaeologists, and historianshas elucidated the details of the mortalityof specific Indian populations. Taken together,this work suggests that although Indians' lack of priorexposure might have left them vulnerableto European pathogens,the specific contribution of such genetic or developmental factors is probably unknowable.In contrast,the analysesclearly show thatthe fatesof individual populations depended on contingentfactors of theirphysical, economic, social, and political environments.It could well be that the epidemicsamong AmericanIndians, despitetheir unusual severity,were caused by the same forcesof poverty,social stress,and environmental vulnerabilitythat cause epidemicsin all other times and places. These new understandingsof the mechanismsof depopulationrequire historians to be extremelycareful in theirwriting about AmericanIndian epidemics. If they attribute depopulation to irresistible genetic and microbialforces, they risk being interpretedas supportingracial theories of historicaldevelopment. Instead, theymust acknowledgethe ways in which multiple factors,especially social forces and human agency, shaped the epidemicsof encounterand colonization. Even a cursorysurvey of the literatureon encounterand colonization revealscountless claims that AmericanIndians died because they lacked immunityto Old World pathogens.The "epidemiologicallypris- tine" Indianswere "immunologicallyna'ive.'"5 With "no immunity,"they were "biologically defenseless."6As a result,they fell victim to "the

5 WilliamA. Starna,"The BiologicalEncounter: Disease and the Ideological Domain," AmericanIndian Quarterly,16 (1992), 513; ArthurE. Spiess and Bruce D. Spiess, "New England Pandemic of 1616-1622: Cause and Archaeological Implication,"Man in theNortheast, 34 (1987),77. 6 David E. Stannard,"Disease and Infertility:A New Look at theDemographic Collapse of Native Populations in the Wake of WesternContact," Journalof AmericanStudies, 24 (1990), 329, 346. Scores of similar accounts exist. Here is a par- tial listingsince 1990: Colin G. Calloway,New Worldsfor All: Indians,Europeans, and theRemaking of Early America (Baltimore, i997), 33; Paul H. Carlson,The Plains Indians(College Station,Tex., 1998), 8; JamesH. Cassedy,Medicine in America:A ShortHistory (Baltimore, I991), 5; A. D. Cliff,P. Haggett,and M. R. Smallman- Raynor, "Island Populations: The Virgin Soil Question," in Island Epidemics (Oxford,2000), I2o; LawrenceI. Conradet al., The WesternMedical Tradition:8oo B.C.-A.D. I8oo (Cambridge, 1995), 225-26, 474, 486; Noble David Cook and W. GeorgeLovell, eds., "SecretJudgments of God"-Old WorldDisease in ColonialSpanish

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 706 WILLIAM AND MARY QUARTERLY greatestknown demographic catastrophe in thehistory of theworld."7 Spaniardsand otherEuropeans, meanwhile, had "almostuniversal immunity"to thediseases that devastated American populations.8 Such assertionsof AmericanIndian immunologicalinadequacy appear in booksand articlesdevoted to Indianpopulation history, in historiesthat discussdepopulation in passing,and in surveysor otherworks intended forgeneral audiences. These assertions of no immunityleave readers to guesswhether the susceptibility arose from genetic handicaps, from lack of exposureto diseasesas children,or fromdetrimental effects of colonization.Writers who ignorethese crucial distinctions dodge the ques- tionof historical responsibility. Somewriters distinguish between inherited and acquiredimmunity, onlyto suggestthat Indians lacked both.9 Other writers discount the

America(Norman, Okla., 1991),xv; FrancisJennings, The Founders ofAmerica: How IndiansDiscovered the Land, Pioneered in It, and CreatedGreat Classical Civilizations; How TheyWere Plunged into a DarkAge by Invasion and Conquest,and How TheyAre Reviving (New York, I993), 383; Charles C. Mann, "1491," Atlantic Monthly (Mar. 2002), 43; AdrienneMayor, "The Nessus Shirt in the New World: Smallpox Blanketsin Historyand Legend,"Journal of American Folklore, io8 (Winter1995), 58; Murrin,"Beneficiaries of Catastrophe,"7; Linda A. Newson, "Old World Epidemicsin EarlyColonial Ecuador," in Cook and Lovell,eds., "SecretJudgments of God," 88; Gregory H. Nobles, AmericanFrontiers: Cultural Encountersand ContinentalConquest (New York, 1997), 41; Mary Beth Norton et al., A People and a Nation:A Historyof the UnitedStates, brief ed., vol. A: To 1877, 4th ed. (Boston, 1996),18; John Steckley, "Developing a Theoryof Smallpox:Huron Perceptions of a New Disease," Arch Notes, 90 (Jan.-Feb. 1990), 17; Ian K. Steele, Warpaths:Invasions of North America (New York, 1994), 22; Rebecca Storey, Life and Death in the AncientCity of Teotihuacan:A ModernPaleodemographic Synthesis (Tuscaloosa, Ala., 1992), 43; Ronald Takaki, "The Tempestin the Wilderness:The Racializationof Savagery," Journal of American History, 79 (1992), 907; Alan Taylor, American Colonies (New York, 2001), 42; Patrick Tierney, Darkness in El Dorado: How Scientistsand JournalistsDevastated the Amazon (New York,2000), 56; Daniel H. Usner,Jr., Indians, Settlers, and Slavesin a FrontierExchange Economy: The Lower MississippiValley before 178? (Chapel Hill, 1992), 16; RichardWhite, "Western History,"in Foner,ed., NewAmerican History, 2zo8; Edwin Williamson, The Penguin Historyof Latin America (New York, 1992), 13, 84-85; and Ronald Wright, Stolen Continents:The Americas ThroughIndian EyesSince 1492 (Boston, 1992), 13-14. 7 Murrin,"Beneficiaries of Catastrophe,"7. 8 Crosby,The ColumbianExchange: Biological and CulturalConsequences of 492 (Westport,Conn., 1972),57. See also WilliamH. McNeill,Plagues and Peoples(New York,1977), 184; Neal Salisbury,"The Indians' Old World: NativeAmericans and theComing of Europeans,"WMQ, 3d Ser.,53 (1996), 458; and David S. Landes,The Wealthand Povertyof Nations: Why Some Are So Richand SomeSo Poor (New York, 1998), 169. 9 JerryH. Bentley,Old WorldEncounters: Cross-Cultural Contacts and Exchanges in Pre-ModernTimes (New York,1993), 183;Robert Boyd, The Coming of the Spirit of Pestilence:Introduced Infectious Diseases and PopulationDecline amongNorthwest Coast Indians, 1774-i874 (Seattle, 1999), 17; White, The Middle Ground: Indians, Empires,and Republicsin the GreatLakes Region,165o-8175 (Cambridge, 1991), 41.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 707 contributionof geneticfactors and insteademphasize the vulnerability thatresulted from lack of prior exposure. William Cronon, for instance, notesthat "what the Indians lacked was notso muchgenetic protection fromEurasian disease-though this may have been a partialfactor-as the historicalexperience as a populationto maintainacquired immunities fromgeneration to generation."'0Many historians also acknowledgethat the social chaos of encounter(such as famine,overcrowding, warfare, stress)left American Indians vulnerable. Colin Callowaydescribes how epidemics"cut down economicproductivity, generating hunger and famine,which rendered those who survivedone diseasemore vulnerable to afflictionby the next. New diseasescombined with falling birth rates, escalatingwarfare, alcoholism, and generalsocial upheaval to turnIndian Americainto a graveyard.""Amid this jumbled mix of explanationsof AmericanIndian demise, few provide substantial evidence to back up whatare essentiallyintuitive assertions about Indianimmunity. Even fewerattempt to evaluatethe relative contributions ofdifferent factors. All too oftenthis ambiguity produces stark emphasis on powerful and inevitableforces of naturalselection. In such explanations,the absenceof naturalselection by serious pathogens in precontactAmerica leftthe "genetically-virgin"American Indians vulnerable to Old World pathogens.Crosby, after emphasizing environmental causes of Indian depopulation,later described how thousands of years of disease exposure in Eurasiahad createdan Old World"superman" with "an impressive assortmentof geneticand acquiredadaptations to diseasesanciently endemicto Old Worldcivilizations." According to FrancisJennings, AmericanIndians never had a chance:"If there is anytruth to biological distinctionsbetween the great racial stocks of mankind,the Europeans' capacityto resistcertain diseases made themsuperior, in the pure Darwiniansense, to the Indians who succumbed."Richard White

10 Cronon, Changesin theLand: Indians, Colonists,and theEcology of New England(New York, 1983), 85. See also JamesAxtell, Beyond 1492: Encountersin Colonial North America (New York, 1992), 105; Elizabeth A. Fenn, Pox Americana: The Great Smallpox Epidemic of 1775-82 (New York, 2001), 23, 27; Karen Ordahl Kupperman,Indians and English:Facing Offin EarlyAmerica (Ithaca, 2000), 34; McNeill,Plagues and Peoples,3-4, 8, 184-85;and RussellThornton, American Indian Holocaustand Survival:A PopulationHistory Since 1492 (Norman,Okla., 1987),47. 11 Calloway,New Worldsfor All, 37. See also Cook, Bornto Die: Diseaseand New World Conquest,1492-i650 (Cambridge, 1998), 166-67; Cronon, Changes in the Land, 88; Newson, "Highland-LowlandContrasts in the Impact of Old World Diseases in Colonial Social Scienceand Early Ecuador," Medicine,36 (I993), 1194; Stannard,"Disease and Infertility,"341, 346-47, 349; Taylor,American Colonies, 38-39; Michael K. Trimble, "The 1837-1838Smallpox Epidemic on the Upper Missouri,"in Douglas W. Owsleyand RichardL. Jantz,eds., SkeletalBiology in the GreatPlains: Migration, Warfare, Health, and Subsistence,(Washington, D. C., 1994), 82-87; and White,Middle Ground, 41.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 708 WILLIAM AND MARY QUARTERLY agrees: New World populations "had not been selected over time for resistance to such diseases."12 Similar claims of inevitabilityappear throughout the historical literature. Diseases "careened unchecked throughthe 'virginsoil' populations."13European and Africanmicrobes "acquired an inevitablemomentum that quicklymade human motiva- tion all but irrelevant."14American Indians were "doomed to die."'15 One finalcase demonstratesthe pervasivenature of such immunological determinism:Jared Diamond's Guns,Germs, and Steel.Diamond sought to answer a deceptively simple question: "Why did history unfolddifferently on differentcontinents?" How did Europeanscome to assert dominion over the rest of the world? Diamond knew that this quest would take him across treacherousground: "In case this question immediatelymakes you shudderat the thoughtthat you are about to read a racisttreatise, you aren't:as you will see, the answersto the question don't involvehuman racial differencesat all."16This turnsout not to be the case. Diamond asks his readersto join him in turningback the clock to 11,oo000 B. C. Nothing then could have predicted European success. However,"different rates of developmenton differentcontinents" produced "technologicaland politicalinequalities" by A. D. 1500. Diamond attributesthese differentrates to one simple fact: while the dominant geographicaxes of Africaand the Americasrun north-south,the dominant axis of Eurasia runs east-west."Around those axes turnedthe for- tunes of history."The east-west orientation of Eurasia allowed the disseminationof crops, animals, and technologiesof food production. The whole continentbecame one giant pool of genetic and cultural sharing. Latitudinal gradientsand geographicobstacles blocked such exchangein the Americas.The more rapid developmentof surplusfood productionin Eurasia fueled craftspecialists, technologies, bureaucra- cies, standingarmies, fleets, exploration, and conquest.The dense settle- ments and domesticatedanimals of Eurasian agriculturealso exposed people to animal microbesand facilitatedthe emergenceof epidemic diseases. The initialcost of those infectionsproduced a lastingbenefit:

12 J. S. Cummins, "Pox and Paranoia in Renaissance Europe," HistoryToday, 38 (Aug. 1988), 28; Crosby,Ecological Imperialism: The BiologicalExpansion of Europe, 9oo-9roo (Cambridge, 1986), 34; Jennings, The Invasion of America: Indians, Colonialism, and the Cant of Conquest (Chapel Hill, I975), 22; White, Middle Ground,41. 13Axtell, The Invasion Within: The Contest of Cultures in ColonialNorth America (New York, 1985), 96. See also Mayor, "Nessus Shirt," 74-75ni9, and Steele, Warpaths,84. 14 Murrin, "Beneficiariesof Catastrophe," 5. 15 In both Calloway, New Worldsfor All, 33, and White, Middle Ground,41. 16Diamond, Guns, Germs,and Steel,9.

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"Those humansthen evolvedsubstantial resistance to the new diseases." Americans, who never became "one huge breeding ground for microbes,"did not. The resultof European arrivalin the Americaswas predestined:"When such partlyimmune people came into contactwith others who had had no previous exposures to the germs,epidemics resultedin which up to 99 percentof the previouslyunexposed population was killed."17 Accordingto Diamond, all of historythus followed from geography. Time and timeagain he emphasizesthat race had nothingto do withit: "Historyfollowed different courses for different peoples because of dif- ferencesamong peoples' environments,not because of biological differences among peoples themselves."18The many blurbs that adorn editionsof Guns,Germs, and Steelsimilarly highlight the antiracistcon- tribution of Diamond's work. Paul Ehrlich believes that "the book demolishes the grounds for racist theoriesof history."Crosby agrees: Diamond "has done us all a greatfavor by supplyinga rock-solidalter- nativeto the racistanswer." Published reviews of Guns,Germs, and Steel follow these leads.19Yet despite this praise, the book asserteda theory grounded in supposed racial differencesbetween Americans and Europeans.20Though Diamond acknowledgesthat all groupsof humans mighthave been immunologicallysimilar in II,000 B. c., he arguedthat they were very differentby A. D. 1500. When Spanish conquistador 17 Ibid.,16, 92, 191, 212. See also Taylor, AmericanColonies, 30-31, 41-42. 18 Diamond, Guns, Germs,and Steel, 25. 19 Ibid., back cover of 1997 edition (Ehrlich), leading page of 1999 edition (Crosby). Of more than 4o reviews of Guns, Germs,and Steel examined, nearly all praised Diamond for providing an alternativeto racist theories of world history.For representativeexamples, see Sharon Begley, "Location, Location . . . A Real-Estate View of History's Winners and Losers," Newsweek,129 (June I6, 1997), 47; Thomas M. Disch, "A Crescendo of Inductive Logic," New Leader, 80 (Mar. 10, 1997), 19-20; "Geographical Determinism," The Economist, 344 (July 19, 1997), R4-R5; review of Guns, Germs,and Steel, in New Yorker,73 (Mar. 31, 1997), Ioi; and Colin Renfrew, "Human Destinies and Ultimate Causes," Nature, 386 (Mar. 27, 1997), 339-40. 20 Other critical reviewshave not addressed this point. For examples, see James M. Blaut, "Environmentalismand Eurocentrism,"Geographical Review, 89 (July1999), 391-408 (focused on geographicdeterminism); Brian Ferguson,review of Guns, Germs, and Steel,American Anthropologist, IoI (Dec. 1999), 900-or (Diamond ignoresculture, society,politics); and McNeill, "HistoryUpside Down," New YorkReview ofBooks, 44 (May 15, 1997), 48-50. Three reviewersactually criticize Diamond fordownplaying the importance of racial differences: Laurence Hurst, "Sex, War and the Pox," New Scientist,155 (Aug. 30, 1997), 40-41; Mark Ridley, "The Uselessness of Zebras," TLS: The TimesLiterary Supplement, Nov. 14, 1997, 6; and J. Philippe Rushton, review of Guns, Germsand Steel in Population and Environment,21 (Sept. 1999), 99-107. Only two reviewscomment on Diamond's implicitlyracial arguments,and neither recognizes their pervasivepresence: Bruce Mazlish, "Big Questions? Big History?" History and Theory,38 (May 1999), 232-48, and Steve Sailer, "Why Nations Conquer," National Review,49 (May 19, 1997), 51-52.

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FranciscoPizarro met Inca emperorAtahuallpa at Cajamarcain 1532,the peoplewhom each represented had genetically different immune systems withdifferent susceptibilities. One had immunityto certaindiseases, the otherdid not.What had beencontingent facts of geography in II,000 B. c. had becomeinternalized facts of biology by A. D. 1500.The different historiesof Eurasiansand Americans,environmental in origin,had becomeembedded in theirimmune systems.21 Diamond,like so manyothers who have ignored the complexities of depopulationin favorof the eleganceof immunologicaldeterminism, provokedscarce outcry from critics. The abilityof a racialtheory of disease susceptibilityto slip unnoticedinto Diamond's explicitly antiracist theoryof history hints at howdeeply embedded such theories are in the storieswe tellabout post-Columbian America.22 Why have assertions of no immunitybeen propagated so uncritically?They have many possible sourcesof appeal. One explanationmay be thatscientific arguments have an unassail- able cachetin historicalwriting that forces historians to downplayor ignoreother factors. The theoryof immunologicalvulnerability applies the intuitiveauthority of naturalselection to a challenginghistorical problemand efficientlyexplains a decisiveepisode in humanhistory.23 Its explanatorypower seems like just anotherof themany accomplishmentsof twentieth-centurybiomedicine. After all, nearlyevery week anotherteam of scientistsannounces that theyhave identifiedyet

21 Jenningsmade a similar argumentin Invasion ofAmerica,22. 22 The term "race" requires clarification. Careful writers,including McNeill, Diamond, and (but not always) Crosby, avoid the politically charged term by discussing specific historically and geographically defined populations. American Indians at the time of contact, for instance, were a distinct group compared to Europeans and Africans. It is possible to discuss virgin soil epidemics without ever mentioning race. However, many authors (especially in popular forums) discuss race and racial differenceas though they were real and self-evidentcategories. This position has gained support from genetic analyses of human populations that show a "general agreement" between popularly and genetically defined human subpopula- tions: Noah A. Rosenberg et al., "Genetic Structure of Human Populations," Science, 298 (Dec. 20o,2002), 2381-85. Such work has re-energized controversies about the relevance of race as a salient category in medical science: Richard S. Cooper, Jay S. Kaufman, and Ryk Ward, "Race and Genomics," New England JournalofMedicine, 348 (Mar. 20o,2003), 1166-70; Esteban Gonzilez Burchard et al., "The Importance of Race and Ethnic Background in Biomedical Research and Clinical Practice," ibid., 1170-75. Casual use of race, however, introduces unneeded political baggage into debates about human health and disease, confusingan already complicated picture. I avoid race, racial, or racist as much as possible except where those termsare introduced by my sources. 23 For a similar argument, see Francis J. Brooks, "Revising the Conquest of Mexico: Smallpox, Sources, and Populations," Journalof InterdisciplinaryHistory, 24 (Summer 1993), 9-10.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 7II anothergene thatincreases a person'srisk for a specificdisease. But cachetcannot explain everything. Crosby's 1976 article, as wellas subse- quentresearch in the anthropologyof depopulation,all describethe diversityof factors,biological and social,that contributed to depopulation. Moreover,many historians are suspiciousof scientificclaims of authority,and most are enamoredof complexityand contingency. Deferenceto scientificexplanations does not accountfor the appeal of "noimmunity" in historicalwriting. No immunitycould have appealed to historiansfor historiographi- cal reasons:it undermineddominant theories of academichistory in the I96os. Accordingto theanalyses of FernandBraudel, Eric Hobsbawm, and manyothers, economic determinismruled human affairs.In response,historians in the 1970s soughtalternative historical forces. Some foundthe environment, others found disease, especially the ravagesof epidemicsamong nonimmune populations. Epidemics appealed to McNeillfor exactly the same reason that they repelled earlier historians: diseases,"independent of humanintention," "spoiled the web of interpretationand explanationthrough which their art sought to make humanexperience intelligible." Following this lead, recenthistorians have turnedto epidemichistory as an alternativeto traditionalworld historiesdominated by Euroamericans.Disease, seeming to act "inde- pendentof humanagency," not onlyscoured indigenous populations, butalso providedpowerful resistance to colonizingarmies and exacteda hightoll from colonizers.24 At thesame time, McNeill, Crosby, and otherhistorians utilized virgin soil theoryto turnthis appeal on its head. If,at firstglimpse, epi- demicsseemed to defyhistorical causation, then no immunityrestored causationand meaning.The depopulationof theAmericas was no random event.Instead, the epidemicsoccurred because of specificand understandablehistorical forces: different diseases and resistanceshad evolvedin long-isolatedpopulations. When Europeans and Americans cametogether, in a contingentbut inevitable encounter, widespread epi- demicswere the logicaloutcome. Theories of no immunityallowed Diamondand theothers to fitepidemics into grand narratives of historical evolution. Perhapsthe idea thatIndian depopulation can be explainedby the Indians'lack of immunitytook hold becauseit servedan ideological 24 McNeill, Plagues and Peoples, 196. For epidemics as an alternative to Euroamerican agency, see Terence Ranger, "To Fiji with Measles," London Review of Books, 21 (Feb. 4, 1999), 30. For similar argumentsby environmentalhistorians, see Donald Worster, "Transformations of the Earth: Toward an Agroecological Perspective in History," JAH, 76 (1990), Io88, oo90. For political debates within environmental history, see the discussions by Worster, Crosby, White, Carolyn and in Merchant, Cronon, Stephen J. Pyne JAH, 76 (1990), IO87-II47.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 712 WILLIAM AND MARY QUARTERLY purpose.White physiciansin South Africa,for instance, used virginsoil theoryto explain the prevalenceof tuberculosisamong Africanmine workers.Randall Packardhas argued that "virginsoil theoryappears to have been acceptedmore forits instrumentalitythan forits basis in historical fact." By blaming the disease on biological inadequacies of Africans,the theory"provided defendersof the status quo in South Africawith a means of deflectingattention from the appalling condi- tionsunder which Africans lived and worked."25Historians do not share the politicsof the South Africanphysicians or use virginsoil theoriesas a justificationfor eitherEuroamerican hegemony or currentdisparities in healthstatus between American Indians and the generalpopulation. Instead, the theoriesare used to explain an event long since past. But since this historicevent, the depopulation of the Americas,had such profoundimplications and retainspolitical currency,it should not be surprisingthat theoriesof immunologicaldeterminism in the American context also have "instrumentality,"deflecting attention away from moraland politicalquestions. For example, many authorswho promote claims of no immunity castigateEuropeans for their treatment of AmericanIndians. Yet despite the broader critiquesin which these claims are embedded, theoriesof immunologicaldeterminism can still assuage Euroamericanguilt over AmericanIndian depopulation,whether in the consciousmotives of his- toriansor in the semiconsciousdesires of theirreaders. Despite the five hundredyears that separate us fromColumbus, many still feel the shock of the Columbian encounter.The power of this guilt transformedthe potentialcelebration of the Columbian Quincentenaryinto a moment of mourning and self-doubt.26No immunityhelps by representing depopulation as the inescapable product of historical-immunological forcesthat had been brewingfor millennia. Contact betweenthe populations was inevitable, if not by Columbus then by someone else. Epidemicscould not have been prevented.No one should be blamed.As Thomas Sowell describesit, "the unwittingspread of diseasesis morally neutral."Such effortsto turndepopulation into a blamelessevent have provokedfierce outcries from critics. David Stannardargues that "by focusingalmost entirelyon disease, by displacingresponsibility for the mass killingonto an armyof invadingmicrobes, contemporary authors increasinglyhave created the impressionthat the eradicationof those tensof millionsof people was inadvertent."27

25 Packard, WhitePlague, Black Labor: Tuberculosisand the Political Economyof Health and Disease in SouthAfrica (Berkeley, 1989), 32. 26 Rozanne Dunbar Ortiz, "Aboriginal People and Imperialism in the Western Hemisphere," MonthlyReview, 44 (Sept. 1992), 1-2. 27 Sowell, Conquest and Cultures:An InternationalHistory (New York, 1998), 327; Stannard, American Holocaust: Columbus and the Conquest of the New World

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Virginsoil theory,again showing remarkable flexibility, can also be used to mitigateguilt by shiftingresponsibility for depopulation either onto, or awayfrom, the American Indians. Some historians,such as Crosby,list behavioral factors that increased the Indians' vulnerability to Europeanpathogens, citing everything from ignorance of contagionto sweatbaths, fatalism, and suicide.If themortality caused by virgin soil epidemicscan be tracedto unwiseIndian behaviors,then Europeans (and theirdescendants) are less culpable. But thetheory also has appeal foran oppositereason. Immunological determinism has beenused as an argumentagainst supposed failuresof AmericanIndian culture. Historianshad longcredited the easy conquests by HernainCortes and Pizarroto superiorEuropean military technology, strategy, and leader- ship.In suchtraditional histories, ignorant and gullibleAztecs and Incas neverstood a chance.But by emphasizing the power of epidemics, histo- rianscan makean oppositeclaim. The Aztecsand Incas,both powerful and sophisticatedsocieties, would have been formidable adversaries had theynot been devastated by the irresistible power of smallpox. As Karen Kuppermanargues, "It was reallyEuropean diseases and not superior Europeantechnology which defeated the Indians in theearly years." But byemphasizing no immunityto divertblame from American Indian culturesand institutions,these well-meaning theorists transfer responsibilityto AmericanIndian bodies.28 Theoriesof immunologicaldeterminism also resonatewith familiar narratives.While historical writers do notexplicitly endorse these older myths,the virgin soil storiesthey tell unintentionally perpetuate powerful narrativepatterns. First, they tell a storyof purityinfiltrated and destroyedby corruption.They portray American Indians as a pristine populationruined by diseasedEuropeans. Indians' ancestors, so the storygoes, survived the arcticwastes of the BeringSea and Canadian tundra.They were purified, not by fire,but by ice. Whenthey settled theAmericas, they were a disease-freepopulation moving into an Edenic paradise.This purity,which allowed the nondevelopmentof their immune systems,left them vulnerable to the diseases of urban Europeansand tropicalAfricans. Although they were doomed, they were at leastdoomed by purity. Meanwhile, the fact that Europeans had been so diseasedfor so longbecame their greatest source of strength.29

(New York, 1992), xii. However, Stannard himselfcited Hawaiians' nonimmunityas a contributingfactor to theirdecline in the I9th century.Stannard, "Disease and Infertility,"3z5-5o. 28 Crosby,"Virgin Soil Epidemics,"296-99; Kupperman,Settling With the Indians:The Meeting of English and Indian Culturesin America,z58o-r64o (Totowa, N. J., I980), 5. See also Crosby, Columbian Exchange,48-53, and Diamond, Guns, Germs,and Steel, 210-11. 29 For an example, see Taylor, AmericanColonies, 41-42.

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Second, the narrativeof a purifyingjourney presents American Indianvulnerability as the product of theirprior triumph over adversity. Theirmigration from Asia throughoutthe Americas was a remarkable accomplishment,though with an eventuallycostly consequence. Similar narrativesof susceptibilityafter surviving adversity are common. Africans,who survived the dangerous environment of themalarial trop- ics, wereleft with sickle cell anemia.Descendants of slaves,who survived the rigorsof the Middle Passage, were leftvulnerable to hypertension.30 Third, the theoryutilizes narrativesof virginity.Some early colonistsand historiansportrayed America as a "virginland, or wilderness,inhabited by nonpeoplecalled savages,"ripe forsettlement by Europeans.Recognition that America had been full of people, the AmericanIndians, forced the abandonment of thismyth. Others, ini- tiallyimpressed by the health and skillsof the Indians, only came to see theIndians as weakand vulnerable after observing their susceptibility to Europeandiseases. Virgin soil theorycombines these older narratives, replacinga virgin,vacant land with a landfilled with virgin, vulnerable people.It presentsAmerican Indians as weak,defenseless, susceptible, female.It presentsEuropeans as aggressive,strong, resilient, male. VirginIndians were helpless before the thrust of Europeanpathogens. Their bodiesprovided fertile soils forthe growthof Europeanseeds. These genderedarguments parallel arguments that American soils pro- videdfertile fields for European crops and animalsand thatAmerican environmentsserved as fertilelands for transplantedEuropean societies.31 Finally,despite the explicit moral and politicalsympathies of most historians,modern theories of immunological determinism have striking similaritiesto Puritantheories of providence.Colonial records contain abundantevidence for providential interpretation ofAmerican Indian 30For a discussionof how AfricanAmericans in the I96os and 1970s reformu- lated sicklecell anemiaas proofof theirfitness to theirancestral environment, see KeithWailoo, Dyingin theCity of theBlues: Sickle Cell Anemiaand thePolitics of Raceand Health(Chapel Hill, zooi), ro6,114-18, 144-47, 182-89. For hypertension and the slave trade,see Thomas W. Wilson and ClarenceE. Grim,"Biohistory of Slavery and Blood Pressure Differences in Blacks Today: A Hypothesis," Hypertension,17 (Jan. 1991,supplement), 1-122. For a refutation,see Philip D. Curtin,"The SlaveryHypothesis for Hypertension among African Americans: The HistoricalEvidence," American Journal ofPublic Health, 82 (1992), I681-86. 31Jennings, Invasion of America, 15. For changingEuropean attitudes toward Indians,see JoyceE. Chaplin,Subject Matter: Technology, the Body, and Scienceon theAnglo- American Frontier, i5oo-I676 (Cambridge,Mass., zooi). For the fertile receptionof Europeanplants and animals,see Crosby,Ecological Imperialism, and ElinorG. K. Melville,A Plagueof Sheep: Environmental Consequences of theConquest ofMexico(Cambridge, 1994).

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 715 epidemics, from John Smith ("it seemes God hath provided this Country for our Nation, destroyingthe natives by the plague") to Cotton Mather ("the woods were almost cleared of those pernicious creatures,to make room fora bettergrowth"). Historians often emphasize this one aspect of Puritan responses,portraying theological reac- tions as perverseindifference to Indian suffering.32The implicationis that we would have respondedwith less judgmentand more compas- sion. But assertionsthat Indians had no immunityto European disease resemble Puritan providentialism,replacing theology with molecular biology. Puritansargued that Indian corruption(paganism) leftthem vulnerableto the wrathof God, manifestedthrough epidemics. Virgin soil theoristsargue that Indian purity(immunological naivetd) left them vulnerableto contact with Europeans, again manifestedthrough epidemics. The implicationsare similar.Both assertthat the outcome was inevitableand unstoppable.Both emphasizethe inherentinferiority of victims,absolving observers of responsibilityfor the mortalityand of responsibilityto intervene. Althoughmost of the mortalityoccurred hundreds of yearsago, it remains a relevantevent: Euroamericansare the beneficiariesof the deaths of tens of millionsof AmericanIndians; Africanswere enslaved and broughtto the Americasto providelabor as Indians died. Virgin soil theoryattempts to isolate the presentfrom the horrorsof the past by describingAmerican Indian depopulationas the productof a unique immuno-historicalmoment. But by ignoringthe social factorsthat created disease duringthe Columbian encounter,the theorymakes it easier to ignorethose same factorswhere they operate today.33

The theoryof virginsoil epidemics,with its multifacetedappeal, emergedgradually over centuries of observationof AmericanIndian epi-

32 Smith,Advertisements forthe UnexperiencedPlanters of New England,or Any Where(1631), in PhilipL. Barbour,ed., The CompleteWorks of CaptainJohn Smith Christi (1580-163I), 3 vols. (Chapel Hill, 1986), 3:275; Mather, Magnalia Americana; or, The EcclesiasticalHistory ofNew-England (1732), 2 vols. (Hartford, 1853), 1:51. For historians'fetish for Puritans' providential responses, see Calloway,ed., Dawnland Encounters:Indians and Europeansin NorthernNew England(Hanover, N. H., 1991), 12; Cronon,Changes in theLand, 126; Kupperman,Settling with the Indians, 6; and AldenT. Vaughan,New EnglandFrontier: Puritans and Indians,I62o0-675 (Norman, Okla., 1995; orig. pub. 1965),104. I discussthe role of such providentialexplana- tionsin Puritansociety in RationalizingEpidemics: Meanings and Usesof American IndianMortality since i6oo (Cambridge,Mass., forthcoming). 33 This is truefor all cases in whichsocial factorsgenerate disparities in health status,as well as thespecific case of thefew remaining "virgin soil" populations.As late as 1998,experts estimated that 55 groupsof isolatedSouth AmericanIndians had yetto encounterEuropeans, Africans, and theirpathogens; Magdalena Hurtado et al., "The Epidemiologyof InfectiousDiseases among South American Indians: A Call for Guidelines for Ethical Research," CurrentAnthropology, 42 (2001), 425-32.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 716 WILLIAM AND MARY QUARTERLY demics.Recognition of the demographiccatastrophe always generated attemptsat explanation.Bartolome de Las Casas blamedSpanish mur- der and mayhem:the Spaniardsbehaved "like ravening beasts, killing, terrorizing,afflicting, torturing, and destroyingthe nativepeoples."34 ThomasMorton credited divine intervention: "The handof God fell heavilyupon them .... theplace is madeso muchthe more fitt, for the EnglishNation to inhabitin, and erectin it Templesto the Gloryof God." Frenchand Spanishobservers, less brazen in theirunderstanding of God's providence,attributed the mortalityto "secret,but ever adorable,judgments of God." Disease,such a powerfulpresence during colonization,dominated their explanations. Morton, for instance, believedthat the hand of God did itswork by meansof "thePlague." Some earlycolonists suspected that Europeans were the source of these diseases.Hierosme Lalemant observed that where Jesuit missionaries "weremost welcome, where we baptizedmost people, there it was in factwhere they died themost."35 But most blamed the mortality on its victims.Edward Winslow traced "manifolddiseases" among the Massachusetto their"living in swampsand otherdesert places."36 Moravianmissionary John Heckewelder emphasized the "viciousand dissolutelife" produced by alcohol.37Physician O. M. Chapmancited disregardof the lawsof hygiene:Sioux mortalitywas "themeasure of theirtransgressions."38 Behavioralexplanations became increasingly implausible in the nineteenthand twentiethcenturies. As the demographiccollapse con- tinuedand AmericanIndians seemed destined for extinction, observers beganto questionthe idea thatmisbehavior could havebeen so fatal.

34 Las Casas, The Devastation of the Indies: A BriefAccount(1552), trans. Herma Briffault(Baltimore, 1992), 29. 35 Morton,New EnglishCanaan (1632), in PeterForce, ed., Tractsand Other Papers,Relating Principally to theOrigin, Settlement, and Progressof the Coloniesof North America ... (1836-1847), 4 vols. (New York, 1947), 2:18-19; Lalemant, "Relationof What Occurredin theMission of theHurons" (1640), in ReubenGold Thwaites,ed., TheJesuit Relations and AlliedDocuments: Travels and Explorationsof the Jesuit Missionaries in New France, 610o-I79p, 73 vols. (Cleveland, 1896-1901), 19:93. Both Lalement and Pedro de Lidvano (c. 1577), dean of the Cathedral of Guatemala,used the phrase"secret, but ever adorable,judgements of God." De Lilvano, quoted in Lovell, "Disease and Depopulation in Early Colonial Guatemala,"in Cook and Lovell,eds., "SecretJudgments ofGod, "77. 36 Winslow,Good Newes from New England(1624), in AlexanderYoung, ed., Chroniclesof the Pilgrim Fathersof the Colony of Plymouth,from 1602 to 1625, zd ed. (Boston, 1844), 346. 37Heckewelder, History, Manners, and Customsof the Indian Nations Who Once Inhabited Pennsylvaniaand theNeighbouring States (1819), (Philadelphia, 1876), 221. 38 Chapman,physician report, in "Reportof Agentfor Yankton Agency," in Annual Reportsof the Department of the Interiorfor ... . 4. Indian Affairs.. (Washington, D. C., 1905), 342.

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Seeking a new mechanismto explain the magnitudeof the depopulation, historians,physicians, and anthropologistsfound theirsolution in theoriesof racial susceptibilityto disease. Observersof public healthin the late nineteenthcentury turned to racial differencesto explain patternsof disease, such as whyJews resisted tuberculosis, Chinese immi- grants sufferedfrom plague, and AfricanAmericans had syphilis.39 AmericanIndians providedabundant material for such theorizing.A. B. Holder observedof the Crow: "Their resistanceto disease is much less than that of the civilizedraces, I have seen the evidenceat the bedside, in watchingthem yield and die fromdiseases that I feltsure any stout whiteman had easilythrown off." Commissioner of Indian AffairsW. A. Jones noted that since the Indians had only recentlybeen exposed to measles and pneumonia, they had "not yet acquired any immunity." Woods Hutchinsonfound that they provided "a highlysusceptible host" fortuberculosis.40 Throughout the twentiethcentury, historians increasingly recognized thatindigenous populations in theAmericas and around the globe suffereddramatic susceptibility to European diseases. In 1909, Herbert Williamsdescribed how "manytimes new epidemicdiseases from Europe have spread over America and have been very fatal to the Indians." PhysicianGeorge Bushnellfound strikingparallels between the fatesof Indiansand other"races nearly 'virgin' so faras tuberculosisis concerned." By 1937,Sherburne Cook could assertthat the vulnerabilityof aboriginal populationsworldwide was "a matterof generalknowledge."41 Postwar

39Allan M. Brandt,"Racism and Research:The Case of theTuskegee Syphilis Study,"Hastings Center Report, 8 (Dec. 1978),21-29; Alan M. Kraut,Silent Travelers: Germs,Genes, and the"Immigrant Menace" (Baltimore, 1994), 78-96, 136-65;Nancy Krieger, "Shades of Difference: Theoretical Underpinnings of the Medical Controversyon Black/WhiteDifferences in the United States, 1830-1870," InternationalJournal of Health Services,17 (1987), 259-78; Charles E. Rosenberg, "The BitterFruit: Heredity, Disease, and Social Thoughtin Nineteenth-Century America,"Perspectives in American History, 8 (1974),189-235. 40 Holder, "Paperson Diseases amongIndians," Medical Record, 42 (Aug. 13, 1892), 178; Jones,"Report of theCommissioner of IndianAffairs," in AnnualReports of the Departmentof the Interiorfor ... 1904, 36; Hutchinson, "Varieties of TuberculosisAccording to Race and Social Condition,"National Association for the and Prevention Tuberculosis:Transactions theAnnual Study of of Meeting,3 (I907), 199. 41 Williams,"The Epidemicof the Indiansof New England,1616-1620, with Remarkson NativeAmerican Infections," Johns Hopkins Hospital Bulletin, 20 (1909), 340; Bushnell,A Studyin theEpidemiology of Tuberculosis,With Especial Reference to Tuberculosisof the Tropicsand of theNegro Race (New York,1920), 35; Cook, The Extentand Significanceof Disease amongthe Indians of Baja California,1697-1773 (Berkeley,1937), 1. At about this time,medical authorities in South Africawere identifyingthe local Africansas virginpopulations; Packard, White Plague, Black Labor,4, 22-23.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 718 WILLIAM AND MARY QUARTERLY authors followed this lead. Henry Dobyns, for instance, described AmericanIndians as "a virginpopulation of susceptibleindividuals lack- ing immunities."42Aidan Cockburngave historians'theories the authority of evolutionarybiology, arguing that AmericanIndian decimation was "thetypical reaction of a 'herd' to a pathogennot previouslyexperi- enced."43 The assumption that natural selection had left Europeans with inheritedresistance to manydiseases, and AmericanIndians withoutit, was eminentlyplausible. In the 195os and I96os, evolutionarybiologists and populationgeneticists modeled the differentialsurvival of individuals whose genes conferred benefits in specific environments. As Cockburn described,"Infection with a pathogen reduces the survival capacityof the host, and all otherfactors being equal, the host withthe most resistanceis the one most likely to survive.If this resistanceis inherited,then naturalselection can be expectedto produce a population moreand more resistantto the prevalentpathogens."44 The protective benefitof sickle cell traitagainst malaria became a centerpieceof the burgeoningfield of evolutionarygenetics.45 Such theories found logical application in the fate of American Indians. Centuriesof smallpox,measles, and plague seemed certainto have selected European populations that carried resistance genes. American Indians, who lived without epidemics, would have lacked these protections. Their unprecedented mortality,from Aztecs to Alaskans, seemed to prove the theory.Bruce Triggercould describe AmericanIndian depopulationas a "crueland fantasticexample of natural selection."However, initial studies of virginsoil populationsfound that theirimmune systemsworked normally. In 1968, geneticistJames Neel studied the firstoutbreak of measles among isolated Yanomami populations in Venezuela and Brazil. Although mortalityrates were high,he foundno evidenceof innateIndian susceptibilityto measles.46 42 Dobyns, "An Outline of Andean Epidemic History to 1720," Bulletin of the HistoryofMedicine, 37 (1963), 494. For similar claims, see C. H. Haring, The Spanish Empire in America (New York, 1947), 43, and John Duffy, "Smallpox and the Indians in the American Colonies," Bulletin of the HistoryofMedicine, 25 (July-Aug. 1951), 327. 43 Cockburn, "The Evolution of Infectious Diseases," in Cockburn, ed., InfectiousDiseases: TheirEvolution and Eradication (Springfield,Ill., 1967), 90. 44 Ibid., 1o4. McNeill echoed this: see Plagues and Peoples,272n3. 45 This connection served many agendas, fromthe desire of molecular biologists and population geneticiststo make contributions to medicine, to the needs of the growing black identitymovement; Wailoo, Dying in the Cityof theBlues, Io6, 114-18, 144-47, 182-89. 46 Trigger, "Comments," on Dobyns, "Estimating Aboriginal American Population: An Appraisal of Techniques with a New Hemispheric Estimate," CurrentAnthropology, 7 (Oct. 1966), 440; Neel et al., "Notes on the Effects of

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The discrepancybetween the intuitiveappeal of naturalselection and the preliminarystudies of virginpopulations left historians in a difficult position. These tensions appear clearlyin Crosby's1976 article,which articulated the modern form of the theory of virgin soil epidemics. Crosby's opening assertion that lack of prior exposure left American Indians "immunologicallyalmost defenseless" and the Darwinian tone of his otherwork jarred with the article'sconcluding emphasis on environmental causes of Indian susceptibility: "The scientific community inclinestowards the view thatNative Americans have no special susceptibilityto Old World diseases that cannot be attributedto environmental influences, and probably never did have."47 Furthermore,although Crosbycould list a wide rangeof factorsthat might have contributedto no immunity,he could not substantiatehis intuitiveclaims or evaluate the relativecontribution of differentfactors. As a result,Crosby's work has been cited as both proofof immunologicalweakness and as evidence againstit.48 Since 1976, however,historians, archaeologists, biological anthropologists,and medical scientistshave generateda vast amount of relevant new data. It is now possible forhistorians to update the popular,if con- fused,virgin soil theoryand produce a moreprecise and powerfulmodel of AmericanIndian depopulation. This effortmust begin by disentan- glingthe theory'sdifferent components. As definedby Crosby,virgin soil theorymakes four basic claims. The firstthree are descriptive:many AmericanIndians died, theydied of Europeandiseases, and theyhad not been previouslyexposed to those diseases. The last is an argumentof cause and effect:virginity left them vulnerable. Each claim must be assessedindividually. Much of the difficultythat historians have had with explanationsof depopulationarises from the unprecedentedmagnitude of the event.The earliestrecords of colonizationshow thatmassive mortality began quickly

Measlesand MeaslesVaccine in a Virgin-SoilPopulation of SouthAmerican Indians," AmericanJournal of Epidemiology,91 (1970), 418-29. For debates about Neel's role in these epidemics,see Tierney,Darkness in El Dorado, 53-82, and "Perspectiveson Tierney'sDarkness in El Dorado," CurrentAnthropology, 42 (Apr. 2001), 265-76. 47Crosby, "Virgin Soil Epidemics,"291. In otherwritings on depopulation, Crosbyemphasized the lack of immunity without discussing contributing social factors:Columbian Exchange, 39, 52,57; "'God . . . WouldDestroy Them, and Give Their Country to Another People ... ,"' AmericanHeritage, 29 (Oct./Nov. 1978), 39. 48Crosby as theauthority on immunologicaldeterminism: Fenn, Pox Americana, 25-26; Kupperman,Indians and English,34; Salisbury,"Indians' Old World,"458; White,"Western History," 208. Crosby as theauthority on socialdisruption: Axtell, Beyond1492, 237; Chaplin, Subject Matter, 158; Calvin Martin, Keepers of the Game: Indian-AnimalRelationships and theFur Trade(Berkeley, 1978), 49-50.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 720 WILLIAM AND MARY QUARTERLY amongAmerican Indians. The Arawakof SantoDomingo bore the first assault,with their population falling from as manyas 3,770,000in 1496 to 125 in 1570.49 Everynew encounter brought new epidemics. Disease spreadalong existing Indian trade routes and movedeven more quickly thanthe conquistadors.Smallpox, introduced to Mexico by Cortes, reachedthe Incan empirebefore Pizarro. This processcontinued for centuries.In the seventeenthcentury, epidemics followed the French intoNew Franceand theEnglish into New England.As settlersmoved acrossNorth America in theeighteenth and nineteenthcenturies, tribe aftertribe experienced outbreaks. Hawaiians, spared extensive contact untilthe nineteenth century, saw their population decline from possibly 8oo,ooo in 1778to 40,000 in I885.As recentlyas the1940s and I96os, newhighways and newmissionaries brought new diseases to previously isolatedtribes from Alaska to Amazonia.50 Colonists,stunned by thedecimation they observed, attempted to estimatethe magnitudeof the mortality.Daniel Gookininterviewed survivingMassachuset and estimatedthat 90 percenthad died. Cotton Matherasserted that the "prodigious pestilence . . . carriedaway not a tenth,but nineparts of ten,(yea, 'tis said, nineteenof twenty)among them."51Systematic efforts to measureIndian populations began in the nineteenthcentury. An 1877 reportto the Commissionerof Indian Affairsstruggled to determinewhether or not AmericanIndians were doomedto extinction.52In the193os, A. L. Kroebercompiled estimates of Indianpopulations at thetime of firstcontact with Europeans. He calculateda totalpopulation of 8.4 millionfor the western hemisphere, with only 900,000 livingin NorthAmerica. After World War II, WoodrowBorah, Sherburne Cook, and HenryDobyns revisited this estimate.They argued that Kroeber ignored the disease-induced decline thatoccurred between European arrival in theAmericas and theircon- tactwith each tribe. Estimating this loss at over95 percent,Dobyns pro-

49 Cook, Bornto Die, 22-23; Newson,"Indian Population Patterns in Colonial SpanishAmerica," Latin American Research Review, 20 (1985),46. Taylorprovides a lower,but still severe,estimate of initial population and subsequentmortality, 3oo,ooo; Taylor, American Colonies,38. 50 Stannard,"Disease and Infertility,"325-50 (Hawaii); McNeill, Plaguesand Peoples,171 (Alaska); Neel et al., "Notes on the Effectsof Measles," 418-29 (Amazonia). 51Gookin, Historical Collections of the Indians in New England;of TheirSeveral Nations,Numbers, Customs, Manners, Religion and Government,before the English Planted There (c. 168o) (Leicester, Mass., 1970; orig. pub. 1792), 9-12; Mather, MagnaliaChristi Americana, 1:51. 52S. N. Clark,"Are the Indians Dying Out? PreliminaryObservations Relating to Indian Civilizationand Education," in Annual Reportof the Commissionerof IndianAffairs to theSecretary of theInterior for the Year1877 (Washington,D. C., 1877), 487-520.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 721 poseda precontactpopulation of 112million for the hemisphere and 18 millionfor North America.53 Efforts by archaeologists and paleopatholo- giststo resolvethis debatehave only narrowedthe rangefor North Americato between2 and 12 million,and enormousproblems exist with all of the estimates.With estimates of hemisphericpopulation ranging between8 and 112million, estimates of totalmortality range between 7 and ioo million.Die-off ratios (pre- vs. postcontactpopulation) range between2:i and 5o:I.54Whatever the exact numbers, the mortality was unprecedentedand overwhelming. Ambiguitiesabout the pace of mortality,the role of epidemics,and theidentity of epidemics further cloud the issue. The bulkof themortal- ityoccurred in the firstcentury after sustained contact (the sixteenth centuryin Centraland SouthAmerica; the seventeenthto nineteenth centuriesin NorthAmerica and the Pacificislands). Though cata- strophic,90 or even95 percentmortality could have resulted from a sub- tle imbalancein birthsand deathsthat led to a 2-3 percentannual decline.55While thismight have happened in some areas,other areas clearlysuffered dramatic collapse. Las Casas describedhow thepopula- tion of Santo Domingoplummeted precipitously after Spanish arrival. JohnSmith, who sailedthe New Englandcoast in 1614,found it "well inhabitedwith a goodly,strong and well proportioned people." Five years later,Thomas Dermer found only "some antient Plantations, not long sincepopulous now utterly void."56 Similar accounts of rapidand severe 53 The disparateestimates reflect different assumptions about the natureof AmericanIndian life.Low estimatesassume that precontact disease, unsophisticated social arrangements,and limitedexploitation of ecologicalpotential kept populations low. High estimatesassume little precontact disease, limited warfare, high fertility, and fullutilization of the ecologicalpotential of Americanenvironments; European epidemics wiped out 95% of these populations beforeEuropean censuses. See Michael H. Crawford,The Originsof Native Americans: Evidence fom Anthropological Genetics(Cambridge, 1998), 33-39; Dobyns, "EstimatingAboriginal American Population," 395-416; Dobyns, TheirNumber Become Thinned: Native American PopulationDynamics in EasternNorth America (Knoxville, 1983); David Henige, Numbersfrom Nowhere: The American Indian ContactPopulation Debate (Norman, Okla., 1998); Ann F. Ramenofsky,Vectors of Death: TheArchaeology of European Contact (Albuquerque, 1987), 1-21; and Douglas H. Ubelaker, "Patterns of Demographic Change in the Americas," Human Biology,64 (June 1992), 361-79. 54 Newson, "Indian Population Patterns," 41-74; Stannard, "Disease and Infertility,"325-26; Dean R. Snow, "Microchronologyand DemographicEvidence Relatingto theSize of Pre-ColumbianNorth American Indian Populations," Science, 268 (16 June 1995), 16oI-o4; Taylor, American Colonies,40. 55 For a populationof initialsize PO and a growthrate of r, the populationat timet can be calculatedsimply: P=Poert To findthe rate needed to produce90% loss over1oo years,rearrange the equation and solvefor r to geta rateof 2.3%. 56 Las Casas, Devastationof theIndies, 29-31; Smith,A Descriptionof New in Works England ... (1616), Barbour, ed., Complete of Captain John Smith, I:330; Dermerto SamuelPurchas, 1619, in Purchas,ed., HakluytusPosthumus, or Purchas His

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 722 WILLIAM AND MARY QUARTERLY mortalityemerged time and time again, fromthe "destroyingangel" of smallpoxin 1837that converted the NorthAmerican interior "into deso- late and boundless cemeteries,"to epidemics of measles, whooping cough, and meningitis in Alaska in 1942 and I943.57 Though epidemicsdid bringrapid decimationto manygroups, they did not monopolize the mortality.Europeans and Americans killed countlessAmerican Indians throughwar, starvation,neglect, and even hunting. Some commentatorshave accused Columbus of introducing four centuries of genocide.58 However, with account after account describingappalling epidemics from Quebec to Peru,it is impossiblenot to assign a dominantrole to infectiousdiseases. In some cases, diseases struckpopulations weakened by the chaos of colonization. In others, they spread by trade or with isolated missionaries,wreaking havoc on seeminglyintact Indian groups.As Diamond argues,"Their destruction was accomplishedlargely by germsalone."59 Because of the importanceof theseepidemics, physicians and historians have long struggledto diagnose each epidemic. Colonists often identified the outbreaks as fevers, plague, or smallpox. Modern researchershave exhaustivelyreviewed these descriptionsto establish specificdiagnoses, with varying success.60 Whatever the exactpathogens, manyof the diseasesarrived in the Americaswith the Europeans(or, as has recentlybeen suggested,with the Chinese): AmericanIndians, from the Huron to the Maya, claimed to have had little disease before European arrival.61Some historianshave used these claims and selected

Pilgrimes(1625), 20 vols. (Glasgow,1906), 19:129. Emptyvillages did not necessarily meandead Indians:they might have withdrawn from the coastas partof theirnor- mal seasonalmigrations, in responseto the epidemics,or in responseto the threat posedby Europeans. 57 Quoted in H. EvansLloyd, preface to Maximilian,Prince of Wied, Travelsin theInterior of North America, in ReubenGold Thwaites,ed., EarlyWestern Travels, 1748-1846,32 vols. (Cleveland,1904-1906), 22:33. For Alaska,see McNeill, Plagues and Peoples,I8I. 58For genocide,see Thornton,American Indian Holocaust and Survival;Ortiz, "AboriginalPeople and Imperialism,"I-I3; Stannard,American Holocaust; and Ward Churchill,Indians Are Us? Cultureand Genocidein NativeNorth America (Toronto, 1994), 11-63.For huntingIndians, see Lee Miller,ed., Fromthe Heart: Voicesof the AmericanIndian (New York,1995), 306. 59 Diamond, Guns,Germs, and Steel,373-74. See also Calloway,New Worldsfor All, 33; Dobyns, "EstimatingAboriginal American Population," 413-14; and McNeill,Plagues and Peoples,18o-81. 60 For these debates, see Timothy L. Bratton,"The Identityof the New EnglandIndian Epidemicof 1616-19," Bulletinof theHistory of Medicine, 62 (Fall 1988), 351-83;Spiess and Spiess, "New EnglandPandemic," 71-83; and Williams, ofNew "Epidemicof theIndians England,"340-49- 61 For Mayanclaims, see theaccount of ChilamBalam of Chumayel,quoted in Crosby,Columbian Exchange, 36. For Huron claims,see Paul le Jeune,"Relation of

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 723 paleopathologicalevidence to assertthat American Indians lived in a "disease freeparadise."62 This paradisemay even have been of the Indians'making. James Shreeve argues that American Indians doomed themselveswhen they hunted the large mammals of NorthAmerica to extinction:"If those first Native Americans had beenless adept hunters, theirdescendants might have been able to domesticatethe indigenous Americanhorse and camel,providing them with an invisiblearsenal of microbesof theirown whenColumbus made his firstfateful landing thousandsof yearslater."63 These notions have been weakened by care- fulanalyses of skeletalremains that have documented the existence of a hostof diseasesbefore European arrival. However, American Indians beforeColumbus do seem to have been sparedfrom the ravagesof smallpox,measles, influenza, bubonic plague, diphtheria,typhus, cholera,scarlet fever, whooping cough, and malaria.64These new dis- easescaused considerable mortality. Despitedisagreements over the subtleties of the pace, role, and diag- nosis of the epidemics,consensus has long existedthat American Indianssuffered severe mortality from epidemics caused by newly introduced Europeanpathogens. In thislimited sense, American Indians werea virginsoil. Controversybegins with the arguments of causeand effect.Did virginitymake Indians vulnerable? Did centuriesof isolation fromEurasian pathogens leave them with ill-equipped immune systems? Manywriters assert that lack of exposureleft American Indians without geneticprotections, acquired immunities, or both.These claimsmerit carefulscrutiny.

The exceedingcomplexity of thehuman immune system provides a dauntingobstacle to historianswho want to understandAmerican

What Occurredin New Francein the Year 1637," (1638) in Thwaites,ed., Jesuit Relations,II:193. For the possibilitythat the Chinesebeat the Europeansto America and broughtdiseases with them, see GavinMenzies, 1421: The YearChina Discovered America(New York, 2003), 114,412, and Crawford, Americans,88. 62 OriginsofNative Ortiz, "AboriginalPeople and Imperialism,"2. For similarclaims, see McNeill,Plagues and Peoples,176; Martin,Keepers of the Game, 48-49; and Cronon, Changesin theLand, 85. 63 Shreeve,"Dominance and Submission,"New YorkTimes Book Review, June 15, 1997, 13. For theArctic passage, see Cronon,Changes in theLand, 85; Storey,Life and Death in theAncient City of Teotihuacan,42-43; and Taylor,American Colonies, 41. For a discussionand critiqueof the theory,see Crawford,Origins of Native Americans,51-52. For the role of animals and cities,see Cronon, Changesin the Land, 85; Diamond, Guns,Germs, and Steel,213; McNeill, Plagues and Peoples,178; Taylor,American Colonies, 41; and Williams, "Epidemic of the Indians of New England," 241. 64 Howard S. Russell,Indian New EnglandBefore the Mayflower (Hanover, N. H., 1980), 35, 104-o5; Stannard, AmericanHolocaust, 53; Taylor, American Colonies, 41; Ubelaker,"Patterns of DemographicChange," 364.

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Indiansusceptibility. It is easierto remainabove the molecular fray and makesimple claims of no immunity.In theyears since McNeill and Crosbybegan emphasizing the importance of diseaseand immunityin humanhistory, humans (and theirimmune systems) have faced perhaps the gravestchallenge yet: HIV and AIDS. The epidemichas fueled unprecedentedresearch into the structure and functionof theimmune system,which has producedcrucial insights that can help resolvethe uncertaintiesthat have confoundedearlier discussions of American Indiandepopulation. Human tissues,seen froma microbe'sperspective, provide a rich varietyof nutrients.Even in health,humans support a fertileecosystem of microorganisms,with a typicalperson harboring more bacteria than humancells. Four broad classes of microorganisms can maketheir home in humantissues. Bacteria, which play a seriesof usefulroles (such as in digestion),cause many infections, from strep throat and pneumoniato cholera,anthrax, and tuberculosis.Viruses range from the nuisanceof thecommon cold to thedevastation of polio,smallpox, and HIV. Viral pneumoniaand diarrhearemain the leading infectious causes of death worldwide.Fungi, responsible for dandruff and yeast infections, can also causesevere pulmonary and systemicinfections. The lastgroup, lumped togetheras parasites,include the single-and multi-celledorganisms responsiblefor malaria, giardia, and countlessother infestations.65 In the absenceof functioningimmune systems, human bodies would be overrunwith microorganisms. In responseto thischallenge, animals developed elaborate systems of surveillanceand protectionthat keep most parts of thebody sterile (suchas thebrain, liver, kidneys, muscles, bones, and blood),and the otherparts of the body colonized but healthy (skin, lungs, mouth, stom- ach,intestines).66 The skinand otherbody surfaces provide the first line ofdefense, with secretions, barriers, and normalcolonizing microorgan- ismsthat usually prevent dangerous pathogens from entering the body. Once insidethe body,microorganisms face an immunesystem com- posed of specializedcells and chemicals.The cellularimmune system includeslymphocytes (B-lymphocytes make antibodies; T-lymphocytes 65Writers sometimes confuse these groups, for example discussing the "smallpox bacillus."See Stannard,American Holocaust, 77. 66 TheNew EnglandJournalof Medicine published a seriesof reviewarticles on immunologythat are accessibleto nonexpert,but motivated,readers: Peter J. Delves and Ivan M. Roitt,"The ImmuneSystem: First of Two Parts,"N. Eng.J. Medicine, 343 (July6, 2ooo), 37-49; Delves and Roitt,"The ImmuneSystem: Second of Two Parts,"ibid., 343 (July13, zooo), 108-17; RuslanMedzhitov and CharlesJaneway, Jr.,"Innate Immunity,"ibid., 343 (Aug. 3, 2000), 338-44; Rolf M. Zinkernagel, "MaternalAntibodies, Childhood Infections, and AutoimmuneDiseases," ibid., 345 (Nov. I, 2001), 1331-35.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 725 organizeimmune responses and can kill microbesdirectly) and phagocytes(cells, such as neutrophils,monocytes, and macrophages,that can ingestand destroymicrobes or infectedcells). The humoralimmune system,so namedbecause its chemicalcomponents can be separatedfrom the cellularimmune system, includes antibodies (which recognize and labelinvading microbes), cytokines (which modulate immune responses), and complement(which can identifymicrobes, modulate responses, and killmicrobes directly). The componentsinteract in manyways. Each humancell produces specificproteins and carbohydratesand ingestsothers from its environment.Some of thesemolecules are broken down into small pieces, bound to structuresknown as themajor histocompatibility complex (MHC), and thendisplayed on theouter surface of the cell, a processknown as antigen presentation.Lymphocytes and macrophagestravel throughout the body and evaluatethe presented antigens. If theydetect foreign antigens, they can respondby proliferating,by releasingantibodies or cytokines,or by attackingthe microbe directly. Some componentsof theimmune system specializein detectingand removingintracellular pathogens (viruses and certainbacteria), while other components specialize in dealingwith extra- cellularpathogens (parasites and most other bacteria). Immunefunction hinges on theability to distinguishself from non- self.67A bodyneeds an immunesystem that leaves normal, healthy cells intact,but thatrecognizes and killspathogenic bacteria, parasites, and viruses,as wellas cellsthat have been invaded by viruses or intracellular bacteria.The distinctionbetween self and non-selfis madeby two differ- entmechanisms, which characterize the "innate" and the"adaptive" componentsof the immunesystem. Innate (sometimes labeled "natural") immunityis basedon theability of phagocytes,natural killer cells, and complementto recognizea smallset of antigens(fragments of proteins, carbohydrates,or nucleicacids) producedonly by bacteriaor other microorganisms(for example, components of bacterialcell walls and spe- cificforms of bacterialDNA and RNA). This systemquickly recognizes and respondsto manypathogens regardless of whetherthey have been encounteredbefore. The adaptive(often confusingly labeled "acquired") immunesystem, in contrast,is not preprogrammedto respondto pathogens.Instead, through a processof randomgenetic rearrangements,

67 Althoughimmunologists treat the distinctionof selfversus non-self as self- evident,this concept has an interestinghistorical and philosophicaldevelopment. See AlfredI. Tauberand ScottH. Podolsky,"Frank Macfarlane Burnet and theImmune Self,"Journal of the History of Biology, 27 (1994), 531-73.Confusion between self and non-selfand an unbalancedimmune system contribute to allergiesand autoimmune disease. See StuartE. Turvey,"Atopic Diseases of Childhood,"Current Opinion in Pediatrics,13 (Oct. 2001), 487-95.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 726 WILLIAM AND MARY QUARTERLY each lymphocytegenerates a differentantibody or antigenreceptor. An individual'smillions of lymphocytesgenerate an extraordinarydiversity of antibodiesand receptorsthat recognize nearly every conceivable antigen(both self and non-self,but a healthyimmune system quickly learns to ignoreself antigens). This systemresponds slowly to initialinfection with a specificpathogen. On subsequentencounters, however, it respondsmuch more rapidly, potentially preventing symptomatic reinfection. The technicaldistinctions between innate and adaptiveimmunity correlateloosely with the populardistinctions between "genetic" and "acquired"immunity. At somelevel, both components are genetic. The processesthat generate the antibodies of adaptive immunity are encoded in our genes.However, the specific antibodies produced by individuals arenot subject to naturalselection: every person generates the full diversityof antibodies;the specific antibodies produced by an individualat anymoment are purelya functionof thatindividual's prior exposures; and thespecific antibodies that are active against relevant pathogens are notpassed genetically from one generationto thenext (though transient antibodyprotection is passedfrom mother to childacross the placenta and in breastmilk). In contrast,the components of innate immunity are subjectto naturalselection. An individualwhose preprogrammed innate receptorsrespond more powerfully to local pathogenshas a survival advantage.Over time, innate immunity can evolveand achievea better fitwith the local burden of infectious diseases. Other components of the immunesystem also evolve.Different MHC moleculeshave different affinitiesfor microbial antigens, affecting how well theseantigens are presentedto innateand adaptivereceptors. Variations in othermole- cules expressedby macrophages,lymphocytes, or othertissues can changesusceptibility to infection.Each of theseforms of heritabledif- ferenceprovides substrate for natural selection. Meanwhile, microbes undergoa parallelprocess of naturalselection to evadethese evolving defenses.68 This emergingmodel of immunefunction has manyimplications for understandingAmerican Indian susceptibilityto European pathogens.The frequentlystated claims of no immunity,as well as occa- sionalcomparisons of AmericanIndians to peoplewith AIDS or other immunodeficiencies,have no substance.69With the exception of persons bornwith rare genetic immune diseases, all humanscan mounta power- 68 Medzhitov and Janeway,"Innate Immunity,"338-39. 69 For comparisons of American Indians and Hawaiians to people with AIDS or other immunodeficiencies, see Hurtado et al., "Epidemiology of Infectious Diseases," 429; Stannard, "Disease and Infertility,"339; and Tierney, Darkness in El Dorado, 56.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 727 ful defenseagainst viruses, bacteria, fungi, and parasites.No one is immunologicallydefenseless, and authorswho make claims of no immu- nityprobably do notmean them this literally. Instead, they presumably meanthat Indians' lack of priorexposure to Old Worldpathogens left themwith deficient immunity compared to Europeans.Several possible formsof deficient immunity might have existed. First, American Indians mighthave lacked specific genes that gave Europeans resistance to spe- cificdiseases. Second, they might have had generalimmunodeficiencies thatleft them vulnerable to a rangeof infections.Third, their genetic homogeneitymight have left them vulnerable to adaptablepathogens. Fourth,regardless of their state of innate immunity, they might have ini- tiallylacked adaptive immunity to Old Worlddiseases. Fifth, they might havesuffered from synergistic effects of simultaneousinfections. Each differentmechanism of impaired immunity must be assessedseparately. Knowledgeof the linksbetween genetics and immunityhas been transformedin the yearssince scientistsrecognized the connection betweenmalaria and sicklecell disease.Geneticists have continued to studythe immune responses of isolatedhuman populations. New tech- niquesof molecular biology and epidemiologyhave identified a range of geneticmechanisms that mediate responses to infectiousdiseases. Such studieshave shown how different versions of a gene(each known as an allele) and the receptors,cytokines, and MHC moleculesthat they encode can makea host moreor less vulnerableto infection.Many gene-diseaseconnections have been proposed.70Sickle cell trait, thalassemia(another inherited anemia), G6PD deficiency(an enzyme involvedin glucosemetabolism), and specificMHC alleles protect Africans,Mediterraneans, and Asiansagainst malaria. The Tay-Sachs mutation,which causes a rapidlyprogressive neurological disease in chil- drenwho possesstwo copies of the gene,granted protection against tuberculosisto Ashkenazicarriers of a singlecopy. Cystic fibrosis pro- tectednorthern Europeans against cholera. Specific MHC alleleshave beenassociated with infection by hepatitisB, hepatitisC, dengue,and HIV. A recentlydiscovered mutation in a macrophagereceptor confers protectionagainst HIV to Europeanswho possess it.71 Smallpox left tan-

70 For overviews,see Diamond, Guns,Germs, and Steel,2ox, and AdrianV. S. Hill, "The Immunogeneticsof Human InfectiousDiseases," Annual Reviewof Immunology,I6 (1998), 593-617. 71Sarah A. Tishkoffet al., "HaplotypeDiversity and LinkageDisequilibrium at Human G6PD: RecentOrigin of AllelesThat ConferMalarial Resistance," Science, 293 (July20, 2oo00),455-62; D. M. Rodman and S. Zamudio, "The Cystic Fibrosis Heterozygote-Advantagein SurvivingCholera?" Medical Hypotheses,36 (Nov. 1991), 253-58; Mary Carrington et al., "HLA and HIV-I: Heterozygote Advantage and B*35-Cw*o4 Disadvantage," Science, 283 (Mar. 12, 1999), 1748-52; Hill, "Immunogenetics and Genomics," Lancet, 357 (June 23, 2001), 2037-41; J. Claiborne

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 728 WILLIAM AND MARY QUARTERLY talizingclues about its impact on humangenetics before its eradication in the 1970s.A studyof childrenin India foundthat severe smallpox mortality-acase-fatality rate of 52 percent-wasnot distributedran- domly.Instead, children who had typeA bloodhad seventimes the risk of contractingsmallpox and twicethe risk of dyingfrom smallpox than childrenwith other blood types. Such evidence convinced Diamond that infectiousdiseases shaped human genetic evolution: "Natural selection is nota theoreticalpostulate, but a grimlycontinuing reality."72 Dozens of geneshave now been associated with resistance or susceptibilityto infectiousdiseases. Tuberculosishas been studiedmost carefully. Specific genes that modifythe behaviorof lymphocytesand macrophagesappear relevant forresistance to initialinfection, while others influence the progression of thedisease.73 In mousemodels, a singlemutation in one geneunder- minesmacrophage function and increasessusceptibility to infection with the bacteria that cause tuberculosis.74Human variants of this macrophagegene have been shown to increasethe risk of active tuberculosis.75Many other genes influence the impact of tuberculosis,including MHC alleles,cytokines, and thevitamin D receptor.76These genetic dif- ferencesprovide possible mechanisms for the described racial differences in susceptibilityto tuberculosis.77 Aspectsof thiswork could be relevantfor the studyof American Indiansusceptibility. Continuing study of theYanomami has suggested thatthey are a virginsoil fortuberculosis. The diseasestruck them with an unusuallyhigh attack rate and withatypical symptoms, "indicating a high susceptibilityto disease." Detailed studies of theirimmune responsesshowed that they had weakcellular immunity, leaving their "immunesystem ill-equipped to handlethe bug." Researchers concluded thatthe "immunologicallynaive" Yanomami demonstrated how "the

Stephenset al., "Dating the Originof the CCRS-A32AIDS-Resistance Allele by the Coalescenceof Haplotypes,"American Journal of Human Genetics,62 (June1998), 1507-15. 72 Diamond, "A Pox upon Our Genes," Natural History,99 (Feb. 1990), 30. 73 ChristianG. Meyer,Jiirgen May, and Klaus Stark, "Human Leukocyte Antigens in Tuberculosis and Leprosy," Trendsin Microbiology,6 (Apr. 1998), 153. 74 Rima McLeod et al., "Immunogeneticsin the Analysisof Resistanceto IntracellularPathogens," CurrentOpinion in Immunology,7 (1995), 544-46. 75 RichardBellamy et al., "Variationsin the NRAMPi Gene and Susceptibility to Tuberculosis in West Africans,"N. Eng. J. Medicine, 338 (Mar. 5, 1998), 640-44. 76 These are reviewedin Marc Lipsitchand AlexandraO. Sousa, "Historical Intensityof NaturalSelection for Resistance to Tuberculosis,"Genetics, 161 (Aug. 2002), 1599-1607. 77 For one claim of racial differencein tuberculosis susceptibility,see William W. Stead et al., "Racial Differencesin Susceptibilityto Infection by Mycobacterium tuberculosis,"N. Eng.J. Medicine,322 (Feb. 15, 1990),422-27.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 729 humanimmune system first responded to M. tuberculosiseons ago."78 A studyof an AmericanIndian family in Canadafound a specificgenotype associatedwith the macrophagegene thatincreased tuberculosis risk tenfold.79Such work provides suggestive evidence that American Indians mighthave lacked protective genes that Europeans possessed. It provides an initial foundationfor the conclusionsof manyhistorians that AmericanIndians were vulnerable because their isolation from Old Worldplagues had "preventednatural selection of resistant survivors and theirdescendants."80 However,claims of naturalselection producing resistant human populationshave manylimitations. Despite the assumptionsabout indigenouspopulations worldwide having particular susceptibility to Eurasianpathogens, scientists have not documented any "racial susceptibility"to smallpoxor chickenpox. The socialand economicdisruptions that accompaniednew diseaseshave confoundedanalyses of initial responsesto measlesand tuberculosis.81One fundamentalquestion is whetherthese diseases have existed long enough to allownatural selec- tionto producesignificant differences in specific populations' resistance to differentdiseases. Many diseases, including measles, influenza, and smallpox,emerged with the first cities. Smallpox and measleslikely did not reachEurope until the secondor thirdcentury A. D. Plaguefirst struckEurope in themid-fourteenth century. Could resistantEurasians have evolvedby the sixteenthcentury, in timeto have a competitive advantageagainst American Indians? This seems unlikely.82

78Sousa et al., "An Epidemicof Tuberculosiswith a High Rate of Tuberculin Anergyamong a PopulationPreviously Unexposed to Tuberculosis,the Yanomami Indiansof theBrazilian Amazon," Proceedings of the National Academy of Sciences, 94 (Nov. 25, 1997), 13227 ("high susceptibility"), 13231 ("immunologically naive"); KathleenFackelmann, "Tuberculosis Outbreak: An AncientKiller Strikes a New Population," Science News, I53 (Jan. 31, 1998), 73 ("first responded"), 75 ("ill- equipped"). 79 Celia M. T. Greenwoodet al., "Linkageof Tuberculosisto Chromosome 2q35 Loci, IncludingNRAMPi, in a LargeAboriginal Canadian Family,"American JournalofHuman Genetics,67 (Aug. 2000), 405-14. 80Jennings, Founders ofAmerica, 130. 81 No "racial susceptibility":Abram S. Benenson,"Smallpox," in AlfredS. Evans,ed., ViralInfections of Humans: Epidemiology and Control,3d ed. (New York, 1989),642; ThomasH. Weller,"Varicella-Herpes Zoster Virus," in Evans,ed., Viral Infections,669. Social confounding:Francis Black, "Measles,"ibid., 459; Masahiro Kushigemachi,Lawrence J. Schneiderman,and ElizabethBarrett-Connor, "Racial Differencesin Susceptibilityto Tuberculosis: Risk of Disease afterInfection," Journalof Chronic Disease, 37 (1984),853-60. 82 In the 1970osFrancis Black estimatedthat acute epidemicdiseases, which requirehuman populations of certainthreshold sizes, had onlybeen presentfor 200 generations,too shorta time forsignificant natural selection: Black, "Infectious Diseases in Primitive Societies," Science, 187 (Feb. 14, 1975), 515-I8. For recent refinementsof thisestimate, see Lipsitchand Sousa, "HistoricalIntensity of Natural

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Specifichypotheses also erodeunder scrutiny. The selectiveadvan- tageof carriersof cysticfibrosis against cholera seems far-fetched since choleradid notappear in Europeuntil 1832.83 Although researchers have linkedseveral genes to tuberculosissusceptibility, they explain only a smallamount of theapparent genetic component and theirclinical rele- vanceremains unclear.84 When data do notturn out as expected,scientistshave turnedto post hoc explanationsto supporttheir faith in naturalselection. One groupidentified variations in a receptorused by malariaparasites to enterred blood cells. People deficient in thisreceptor should,in theory,be resistantto malaria.The oppositeturned out to be true.The researchershad to concludethat "unidentified selection pres- sures"explained the prevalence of this costly deficiency.85 Explanationsof American Indian susceptibility run into similar diffi- culties.Diamond's discussion of type A bloodand smallpoxsusceptibility has littlerelevance for American Indians, who are nearlyall type0.86 ImmunologistFrancis Black has found that the Yanomami and othervir- gintribes of the Amazon valley mount normal immune responses against measles,as well as againstvaccines for measles, mumps, rubella, polio, yellowfever, pneumonia, and bacterialmeningitis. His teamconcluded that"deficiency at the immunogeneticloci we have examinedcannot explainthe poor survivalof New Worldpeople."87 Although other researchershave found that the Yanomami did mountatypical responses to tuberculosis,they admit that this could simply reflect the high burden of parasiticinfections among the Yanomami, something that activates humoralimmunity at theexpense of cellular immunity.88 Physicians have

Selection,"1599-1607; Paul Schliekelman,Chad Garner,and MontgomerySlatkin, "NaturalSelection and Resistanceto HIV: A GenotypeThat LowersSusceptibility to HIV ExtendsSurvival at a Time of Peak Fertility,"Nature, 411 (May 31, 2oo0), 545-46; Stephenset al., "Dating the Origin,"I513; and Tishkoffet al., "Haplotype Diversity,"455-62. 83 Cysticfibrosis heterozygotes may have had protectionagainst non-cholera secretorydiarrheas, which likely did existin Europe.See SherifE. Gabriel,response to Paul Fontelo,"Protection Against Cholera," Science, 267 (Jan.27, 1995),440. 84 Bellamy,"Identifying Genetic SusceptibilityFactors forTuberculosis in Africans:A Combined ApproachUsing a Candidate Gene Studyand a Genome- Wide Screen,"Clinical Science, 98 (2ooo), 245-50; Greenwoodet al., "Linkageof Tuberculosis,"406, 414. 85 TimothyJ. Aitman et al., "Malaria Susceptibilityand CD36 Mutation," Nature, 405 (June29, 2000), IOI5-I6. 86Diamond, "A Pox upon Our Genes,"26-30. 87 Black, Gerald Schiffman,and JanardanP. Pandey, "HLA, Gm, and Km Polymorphismsand Immunity to Infectious Diseases in South Amerinds," Experimentaland Clinical Immunogenetics,12 (1995), 214. See also Black, "An Explanationof High Death Ratesamong New WorldPeoples When in Contactwith Old WorldDiseases," Perspectives in Biology and Medicine,37 (Winter1994), 294-95. 88 Hurtado et al., "Epidemiologyof InfectiousDiseases," 426; Sousa et al., "Epidemicof Tuberculosis," 13231.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 731 long observedthat American Indians and Alaskannatives have high susceptibilityto certainbacteria, especially Haemophilus and Streptococcus. Yet despiteextensive study it remainsunclear to whatextent these differences reflectgenetic vulnerabilities or social conditionssuch as malnutrition,overcrowding, and exposure to recurrentinfections.89 Even if tuberculosisresistance genes prove relevant now, it will be difficult,perhaps impossible,to connectthem to specificoutbreaks of tuberculosisin the nineteenthor twentiethcenturies. A second potential mechanismis that American Indian evolution amid the (alleged) relativehealth of Americaenabled the persistenceof inheritedimmune deficienciesthat left Indians vulnerable to a wide rangeof infections.The Navajos and JicarillaApaches, for instance, have an increased incidence of a serious inheritedimmunodeficiency. This disease leaves its victimsvulnerable to viral,bacterial, and fungalinfec- tions; mostdie withinthe firstyears of lifeunless they receive aggressive medical treatment.While such immunedeficiencies have been described among some groups,they are not widespreadamong AmericanIndians. It is also unclear whether such inherited immune deficiencies contributedto demographiccollapse, or resultedfrom random genetic fluc- tuationsamong the ensuingremnant populations.90 The thirdpotential mechanism of inheritedvulnerability arises from genetic homogeneity.American Indians have long been known to be remarkablyhomogeneous for type O blood. Subsequentstudy has found similarlylimited variability for a series of differentgenes, especiallya limiteddiversity of MHC molecules.91Francis Black suggeststhat this lack of geneticdiversity left New World populationsmore susceptible to certaininfections. Measles, forinstance, can adapt itselfto the immune systemof its host. If its nexthost has a similarimmune system (that is, a similarassortment of MHC molecules),then the infectionwill be more virulent.When faced with a population of geneticallysimilar individuals, measles"can adapt to each populationas a whole and cause unusual damage." Based on this theory,Black arguesthat "limitedgenetic diversity,not 'bad genes' may be the fatalchink in the immunologicalarmor of the New World people."92Recent studies have also foundthat limited 89John B. Robbinsand RachelSchneerson, "Evaluating the Haemophilus Influenzae b Vaccine N. Type Conjugate PRP-D," Eng.J. Medicine,323 (Nov. Iy, 1990), 1415-16. 90Robert P. Erickson,"Southwestern Athabaskan (Navajo and Apache) Genetic Geneticsin Diseases," Medicine, I (May-June 1999), I51-57. 91Crawford, Origins of Native Americans, 88-148. However, he notedthat new DNA markershave shown more diversity than previous estimates. 92 Black, "Why Did They Die?" Science, 258 (Dec. ii, 1992), 1739-40; Black, "Explanationof HighDeath Rates," 301 ("can adapt"); Black et al., "HLA,Gm, and Km Polymorphisms,"215 ("limited genetic diversity"). This theory has been picked

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 732 WILLIAM AND MARY QUARTERLY diversityof MHC moleculescan leaveindividuals more susceptible to otherinfections, including HIV and hepatitisB.93 While such theories areplausible and supportedby specific evidence, they remain only spec- ulationabout the impactof measles,smallpox, and tuberculosison AmericanIndians. The fourthmechanism of no immunitydistinguishes between innateand adaptiveimmunity. In some cases, mostfamiliarly with chickenpox but also with smallpox and measles,the protection provided by antibodiesof theadaptive immune system prevents reinfection after an initialepisode. In earlymodern Europe, where these viruses were endemic,most people were exposed as infantsand children.Since many viralinfections are milder in children,since infants receive some protec- tionfrom maternal antibodies, and sinceparents could provide nursing care,most children survived these childhood infections and developed adaptiveimmunity. In settingswhere the diseases were not endemic, ter- riblemortality could ensue. Iceland, for instance, supported too smalla populationto allowsmallpox to persistas an endemicinfection. When it wasintroduced in 1707 aftera longabsence, it killed36 percentof the population(18,ooo out of roughly50,000) in a singleyear. Similarly highmortality occurred when smallpox was introducedintermittently intoBoston and other British colonies during the eighteenth century.94 AmericanIndian populations easily could haveexperienced severe epidemicsbecause of theirinitial lack of adaptiveimmunity. The entire populationof Indianvillages, young and old,would have been vulnerable to thefirst appearance of smallpox, measles, or otherinfections. Few peoplemight have been healthyenough to providenursing care, tend the crops,or maintainessential subsistence activities.95 Many of these infectionsalso cause moresevere mortality in adultsthan in children. This would have been especiallydamaging since theseadults were responsiblefor crucial social roles.96 Each of thesefactors, the result of up by some historians: Fenn, Pox Americana, 26-27, 141;Robert McCaa, "Spanish and NahuatlViews on Smallpoxand DemographicCatastrophe in Mexico,"Journal ofInterdisciplinaryHistory, 25 (1995), 419-20. 93 Carrington et al., "HLA and HIV-I," 1748-52; Hill, "Defence by Diversity," Nature, 398 (Apr. 22, 1999), 668-69. 94Benenson, "Smallpox," 634; Zinkernagel,"Maternal Antibodies," 1331. 95Crosby, "Virgin Soil Epidemics,"293-96. 96 Some historianshave arguedthat influenza and otherepidemics single out youngadults for the highestmortality, stripping vulnerable societies of theirmost productiveindividuals. In fact,most infectionshave U-shaped mortalitycurves: highin infants,low in school-agedchildren and adolescents,then increasing steadily withage: Benenson,"Smallpox," 641; Anne A. Gershon,"Measles Virus (Rubeola)," in GeraldL. Mandell,John E. Bennett,and RaphaelDolin, eds., Mandell,Douglas, and Bennett's Principles and Practice of InfectiousDiseases, 5th ed. (Philadelphia, 2ooo), 1801-09; Weller, "Varicella-Herpes Zoster Virus," 668.

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absent adaptive immunity,could have produced high mortalityregard- less of AmericanIndian innateimmunity. The magnitudeof this effectdepends on two crucial factors.First, which diseaseswere trulynew to AmericanIndians? Smallpox, measles, and influenzalikely did arrivein the Americaswith Europeans. Analysis of AmericanIndian skeletalremains, however, has shown thatmany diseases existed in pre-Columbian America, including tuberculosisand pneumonia, and possiblyherpes, chicken pox, and otherviruses.97 As one review concludes, "The concept of a pristine,disease-free, pre- Columbian New World environmentis no longer credible."98As a result,the breadthof AmericanIndian adaptive immune vulnerability remainsunclear. Second, the notion of trulyprotective immunity only applies to a small numberof viral infections.Influenza, which shiftsits antigensover time, can reinfectindividuals even in endemicareas. Other viruses,such as those that cause common colds or gastroenteritis,can infectthe same individualover and over again. Most bacterialdiseases, meanwhile,generate little or no protectiveimmunity: individuals can sufferendless recurrencesof skin infectionsor pneumonia. Although thesediseases, especially viral pneumonia and diarrhea,are less visiblein the historicrecord than smallpox and measles, they mighthave been dominant causes of mortalityfor which adaptive immunitymight not have been relevant.99 The last mechanismdepends on disease synergy.When Europeans arrived,they brought many new diseases to the Americas.Epidemics of

97 Many authorslist tuberculosis,treponematosis, pneumonia (streptococcus), staphylococcus,typhoid, shigellosis, salmonella, leishmaniasis, Chagas' disease, toxo- plasmosis,amebiasis, giardiasis, tinea, blastomycosis, tapeworm, whipworm, pin- worm,roundworm, and hookworm.See SuzanneAustin Alchon, Native Society and Diseasein ColonialEcuador (Cambridge, 1991), 20o-24; Boyd,Coming of the Spirit of Pestilence,I5; and Starna,"Biological Encounter," 512. These diseaseswere found in someplaces; they were not likelyendemic everywhere. 98Arthur C. Aufderheide,"Summary on Disease beforeand afterContact," in John W. Verano and Ubelaker, eds., Disease and Demographyin theAmericas, (Washington,D. C., 1992), I65. For otherrebuttals of the disease-freeparadise, see Calloway,New Worldsfor All, 25; ClarkSpencer Larsen, "In theWake of Columbus: Native Population Biology in the PostcontactAmericas," Yearbookof Physical Anthropology,37 (I994), 109, II4; Ubelaker, "Patternsof Demographic Change," 372; or manyof theother essays in Veranoand Ubelaker,eds., Disease and Demography. 99For theimpact of commonbacterial pathogens on a disease-experiencedpop- ulation,see Walsh McDermott,with David E. Rogers,"Social Ramificationsof Control of Microbial Disease," JohnsHopkins Medical Journal, I5i (1982), 305. In 1990,viral pneumonia and diarrhearemained the leading causes of infectiousdeaths. See ChristopherJ. L. Murrayand Alan D. Lopez,eds., TheGlobal Burden ofDisease: A ComprehensiveAssessment ofMortality and Disabilityfom Diseases,Injuries, and Risk Factors in Ip99 and Projectedto 2020 (Cambridge, Mass., 1996), 176. It is tempting, but impossible,to extrapolatethis prevalence back to pre-contactAmerica.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 734 WILLIAM AND MARY QUARTERLY measles,smallpox, and influenzaoften circulated simultaneously among AmericanIndians. When new diseases reached a village,not only could everyonefall sick at thesame time, but everyperson could suffer from severalinfections. As was well demonstratedwith the influenzapan- demicof 1918,co-infection with multiple pathogens (in thatcase, viral and bacterialpneumonia) can havesynergistic effects on mortality.Some diseasesalso cause immunesuppression. Measles, for instance, sup- pressescellular immunity and leavesits victims more vulnerable to other diseases,especially tuberculosis.100 Although synergistic epidemics could havecontributed to Americandepopulation, the magnitude of thesyn- ergyremains unknown. Takenas a whole,recent immunological research offers many clues aboutthe stateof Indianimmunity. American Indians could certainly mount immuneresponses to European pathogens.Perhaps their "naivete"left them without protective genes, making them incrementally susceptible.Perhaps their homogeneity left them vulnerable to adaptable pathogens.Research about these questions continues on thecutting edge of immunology.It is possiblethat definitive evidence of demographi- callysignificant resistance genes will emerge. The historicalexperiment, however,has runits course. European and Americanpopulations mixed forover five hundred years before scientists could studythem ade- quately.The opportunityfor further research on firstcontact popula- tionsremains remote. As a result,the stateof virginimmunity will foreverremain contested. This leavesthe literatureon geneticsand immunitypromising, but unsatisfying.101 Genetic arguments of population-widevulnerability must therefore be made withgreat caution. Otherimmunological mechanisms remain plausible, but problematic. Initiallack of adaptiveimmunity likely left American Indian societies vulnerableto certainpathogens, but certainlynot to all of them,and adaptiveimmunity does not seemto havebeen relevant for the domi- nantcauses of mortality in developingsocieties.

100 Eric T. Sandberg,Mark W. Kline,and WilliamT. Shearer,"The Secondary Immunodeficiencies,"in E. RichardStiehm, ed., ImmunologicDisorders in Infants and Children, 4th ed. (Philadelphia, 1996), 553-60oi; Christopher L. Karp et al., "Mechanismof Suppressionof Cell-MediatedImmunity by MeaslesVirus," Science, 273 (July12, 1996), 228-31. 101The phenomenaof obesitydemonstrate the impact of socialfactors even on diseasesthat have strong genetic components. Studies have shown that 50o% to 90% of thevariance of obesitycan be attributedto genetics.But theexpression of genetic tendenciesdepends on social context:famine will preventthe expression of obesity, regardlessof genetic predilection. Similarly,the prevalence of obesity in the United States has increased rapidly over recent decades, in the absence of significantgenetic change; Gregory S. Barsh, I. Sadaf Farooqi, and Stephen O'Rahilly, "Genetics of Body-Weight Regulation," Nature, 404 (Apr. 6, 2000), 644-51.

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Furthermore,the mechanismsof adaptiveimmunity, along with the impactof simultaneousand successivesynergistic infections, emphasize the importanceof the diseaseenvironment, and not onlythe populationitself, in shapinga population'ssusceptibility to infection.Other featuresof the environment,defined broadly, also have profoundeffects on immunity.A population'sphysical, social, economic, and politicalenvironments all inter- act to createpatterns of vulnerability, regardless of itsgenetic substrate. Such vulnerabilitieshave long been recognized. Even as observers began assertingracial argumentsof disease susceptibilityin the nineteenthcentury, they saw that a wide rangeof social factorscreated susceptibilityto epidemic disease. Afterstudying an outbreak of measles among the indigenouspopulations of Fiji in 1875,W. Squire concluded, "We need invokeno special susceptibilityof race or peculiarityof consti- tutionto explainthe greatmortality." He blamed social conditions,especially "want of nourishmentand care." In I909, anthropologistAles Hrdlicka reached a similar conclusion about American Indians: "Doubtless much of what now appears to be greaterracial susceptibility is a resultof otherconditions." Sherburne Cook came to believethat disease amongstindigenous populations worldwide "acted essentiallyas the outletthrough which many other factors found expression."102 Malnutritionprovides the mostobvious, and prevalent,demonstration of the linksbetween social conditions,environmental conditions, and disease. In additionto causingdeficiency diseases, such as ricketsand pellagra, malnutritionincreases susceptibility to infection.Some vitamindeficiencies cause skinbreakdown, eroding the firstbarrier of defenseagainst infection. Protein deficiencies impair both cellular and humoral responses. Malnutritionduring infancy and childhood has particularlydevastating effectson subsequentimmune function. Certain diseases have morespecific connectionsto nutrition.Malnutrition, especially vitamin A deficiency, increasesmortality from measles. Malnourished children are morelikely to die fromchicken pox. Such interactionscreate "a viciouscircle. Each episode of infectionincreases the need forcalories and proteinand at thesame time causes anorexia;both of theseaggravate the nutritionaldeficiency, making the patienteven more susceptibleto infection."Understanding these rela- tionships,scientists have realizedthat malnutrition "is the most common causeof secondaryimmunodeficiency in the world."103

102 Squire,"Reports of Societies:The EpidemiologicalSociety," Medical Times and Gazette,I (1877),324; Hrdlirka,Tuberculosis among Certain Indian Tribesof the UnitedStates (Washington, D. C., 1909), 3I; Cook, "The Significanceof Disease in the Extinctionof the New EnglandIndians," Human Biology,45 (Sept. 1973),5o6. See also AugustHirsch, Handbook of Geographicaland HistoricalPathology, trans. CharlesCreighton (London, 1883-1886), 167. 103Sandberg, Kline, and Shearer,"Secondary Immunodeficiencies," 565. See also Black, "Measles," 451; Gershon, "Measles Virus (Rubeola)," I805; and Weller, "Varicella-HerpesZoster Virus," 674.

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Historianshave thoroughly documented the impact of malnutrition on diseasesusceptibility.104 Such connectionshave clear importance for AmericanIndians, who facedboth disease and socialdisorder following Europeancolonization. As Cronondescribes, villages disrupted by disease and social breakdown"often missed key phases in theirannual subsistence cycles-the corn planting,say, or the fall hunt-and so were weakened when the next infectionarrived."'05 This would have been particularly damagingfor the many populations that eked out onlya precarioussubsis- tence beforeEuropean arrival.Although some writershave described AmericanIndians livingin bountifulharmony with theirenvironment, archaeologistsand physicalanthropologists have shownthat many groups were terriblymalnourished. The accomplishmentsof the Mayan civiliza- tion mighthave been undoneby climatechange, crop failures, and famine. Disease, malnutrition,and violencemade Mesoamericancities as unhealth- fulas theirmedieval European counterparts, with life expectancies of 21 to 26 years.The Arikarashad lifeexpectancies as low as 13.2 years.Careful studyof skeletalremains has foundwidespread evidence of nutritionaldefi- ciencies,with health conditions worsening in theyears before contact with Europeans.106 Baseline malnutrition,especially in the large agricultural societiesin Mexico and the Andes, leftAmerican Indians vulnerable-at the outset-to European diseases.107When the conditionsof colonization disruptedsubsistence, the situationonly grew worse. Malnutritionmay be the most obvious factor,but it was only one of many.Environmental historians have shown how physicalenvironments 104For an overview,see RobertDirks, "Famineand Disease," in KennethF. Kiple, ed., The CambridgeWorld History of Human Disease (Cambridge,1993), 157-63.For a specificexample (tuberculosis during the siegeof Paris),see David S. Barnes, The Makingof a Social Disease: Tuberculosisin Nineteenth-CenturyFrance (Berkeley,1995), 6-9. Malnutritionremains the major risk factorfor mortality worldwide,accounting for 11.7% of the attributablerisk (comparedto 6% for tobacco,5.8% forhypertension, 5.3% forsanitation and hygiene,and 1.5% foralco- hol). See Murrayand Lopez, GlobalBurden ofDisease, 311. 105 Cronon,Changes in theLand, 88. See also Chaplin,Subject Matter, 158, and White,"Western History," 2o8. 106John H. Coatsworth,"Welfare," American Historical Review, ioi (1996),1-12 (generaldiscussion); Crawford, Origins of Native Americans, 53 (Arikara);Larsen, "In the Wake of Columbus,"109-54 (worseninghealth); Storey, Life and Death in the AncientCity of Teotihuacan,253-66 (cities); Ann L. W. Stodderet al., "Cultural Longevityand BiologicalStress in theAmerican Southwest," in RichardH. Steckel and JeromeC. Rose, eds., The Backboneof History:Health and Nutritionin the WesternHemisphere (Cambridge, 2002), 481-505 (ill-health). 107Steckel and Rose, "Patternsof Health in the WesternHemisphere," in Steckeland Rose, eds., Backboneof History,563-79. While agriculturalsocieties (e.g., Mexico, Andes) experiencedpoor health,rural areas (e.g., coastal Georgia, Brazil) did better.Societies with a pre-contactlife expectancyof 40 yearscould moreeasily absorb new pathogensthan societies with a lifeexpectancy of 20 years; S. RyanJohansson and Owsley,"Welfare History on theGreat Plains: Mortality and SkeletalHealth, 1650 to 1900,"in Steckeland Rose,eds., Backbone ofHistory, 556.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 737 can leave populationssusceptible to disease. Lowland Ecuadorians,weakened by endemic parasitesand intestinaldiseases, were more vulnerable to European infectionsthan their highland compatriots.After Spanish arrivalin Mexico, a "plague of sheep" destroyedMexican agricultural lands and leftMexicans susceptibleto famineand disease. Colonization introduceda host of damagingchanges in New England. Deforestation led to wider temperatureswings and more severe flooding. Livestock overranIndian crops and requiredpastures and fences,leading to fre- quent conflictand widespread seizure of Indian land. Europeans also introducedpests, including blights, insects, and rats.All of thesechanges fueled rapid soil erosion and underminedthe subsistenceof surviving Indian populations. More dramaticenvironmental events also wreaked havoc. Drought, earthquakes,and volcanic eruptionsundermined resistance to disease in Ecuador in the 169Os.A devastatinghurricane struck Fiji in 1875, exacerbatingthe measles outbreakthere. As one observer commented,"Certainly for the last 16 yearsthere has been experienced no such weather,and nothingcould be more fatal to a diseased Fijian thanexposure to it."108 Historiansand anthropologistshave also documentedmany cases in which the varied outcomesof specificpopulations depended on specific social environments.The Lamanai Mayas, heavily colonized by the Spanishregime, had highermortality than the moreisolated Tipu Mayas. While much of Peru sufferedseverely, the regionof Huamanga lost only 20o percentof its populationbetween 1532 and I570, the resultof "a high birthrate, the relativeimmunity of remotehigh-altitude areas to disease, shrewd politics, and good luck." The Pueblos sufferedwhen "the endemic problemsof droughtand faminewere superimposedupon the economic disruptioncaused by the Spanish drain on food and labor." Severe outbreaksof and in Peru from to smallpox erysipelas i8oo ISo5 reflecteda combinationof drought,crop failures,famines, mining failures, and economic collapse. The introductionof specific epidemics reflectedspecific historical events. Dauril Alden and JosephMiller traced outbreaksof smallpoxfrom West Africandroughts, through the middle passage of the slave trade, to Brazil. Measles raced down the political hierarchyin Fiji in 1875as a seriesof conferencescarried news of a treaty with the Britishempire, along with the virus,from the royalfamily to regionaland local leadersthroughout the island.109Local variabilityand

108 Newson, "Highland-Lowland Contrasts," 1191-94 (Ecuador); Melville, Plague of Sheep(Mexico); Cronon, Changesin theLand, 107-56 (New England); Alchon, NativeSociety and Disease in ColonialEcuador; "Occasional Correspondent"to The Times,Apr. 23, 1875, quoted in Cliff,Haggett, and Smallman-Raynor,"Island Populations,"163 (Fiji). 109Larsen, "In theWake of Columbus,"137 (Maya); SteveJ. Stern,Peru's Indian Peoplesand the Challengeof SpanishConquest: Huamanga to 1640,zd ed. (Madison,

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 738 WILLIAM AND MARY QUARTERLY contingencyled Linda Newson to conclude that "levelsof decline and demographictrends were influencedby the size, distribution,and char- acterof populations,especially their settlement patterns, social organiza- tion, and levels of subsistence."110Even in the late twentiethcentury, specificsocial factorsleft isolated indigenouspopulations vulnerable to European pathogens.Magdalena Hurtado,who has witnessedfirst-contact epidemicsin South America,emphasizes the adverseconsequences of "sedentism,poverty, and poor access to healthcare.""111 Studies of North Americantribes in the nineteenthand twentieth centurieshave found similarlocal variability.Geographer Jody Decker shows how a singleepidemic among the northernPlains tribeshad dis- parateeffects, "even for contiguous Native groups,"depending on "population densities,transmission rates, immunity,subsistence patterns, seasonalityand geographiclocation." Drought and famineleft the Hopis particularlysusceptible to an epidemic in 1780. The Mandans suffered severelyfrom smallpox in 1837:famine since the previouswinter had left them malnourished,and cold, rainyweather confined them to their crowded lodges. When smallpox struck,they had both high levels of exposureand low levels of resistance.As Clyde Dollar concludes,"It is no wonder the death rate reached such tragicallyhigh levels." Once North Americantribes came under the care of the federalgovernments in the United Statesand Canada, theyoften suffered from malnutrition and poor sanitation.Mary-Ellen Kelm, who has studiedthe fatesof the Indians of BritishColumbia, concludesthat "poor Aboriginal health was not inevitable"; instead, it was the product of specific government policies.112

1993),44 (Huamanga); Stodderand Debra L. Martin,"Health and Disease in the Southwestbefore and afterSpanish Contact," in Veranoand Ubelaker,eds., Disease and Demography,63 (Pueblo); EnriqueTandeter, "Crisis in UpperPeru, I800-1805," HispanicAmerican Historical Review, 71 (I99I), 40-51;Alden and Miller,"Unwanted Cargoes: The Originsand Disseminationof Smallpoxvia the Slave Trade from Africato Brazil, c. 156O-I830," in Kiple, ed., The AfricanExchange: Toward a BiologicalHistory of Black People (Durham, N. C., 1987),35-109; Cliff,Haggett, and Smallman-Raynor,"Island Populations," 148-56 (Fiji). 110Newson, "Highland-LowlandContrasts," 1194. See also Newson, "The DemographicCollapse of NativePeoples of theAmericas, 1492-1650," Proceedings of theBritish Academy, 81 (1993),247-88. 111Hurtado et al., "Epidemiologyof InfectiousDiseases," 428. See also Marcos Cueto, The Returnof Epidemics:Health and Societyin Peru duringthe Twentieth Century(Burlington, Vt., z001). 112Decker, "Depopulation of the NorthernPlains Natives," Social Scienceand Medicine,33 (1991), 383; Fenn, Pox Americana,162, 187; Dollar, "The High Plains Smallpox Epidemic of 1837-38,"Western Historical Quarterly, 8 (Jan. 1977), 29; Kelm, ColonizingBodies: Aboriginal Health and Healingin BritishColumbia, 1goo-5o (Vancouver,1998), 177. See also Maureen K. Lux, MedicineThat Walks:Disease, Medicine,and CanadianPlains Native People, 188o-1940 (Toronto,2001).

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Comparative studies have particularpower for demonstratingthe local specificity of depopulation. Stephen Kunitz has shown that Hawaiians sufferedmore severelythan Samoans, a consequence of dif- ferentpatterns of land seizureby colonizingEuropeans. The Navajo did betterthan the neighboringHopi because theirpastoral lifestyle adapted more easily to the challenges imposed by American settlers.In these cases similar indigenous populations encounteredsimilar colonizers, with very differentoutcomes: "The kind of colonial contact that occurredwas of enormousimportance." Kunitz's cases demonstratethat "diseasesrarely act as independentforces but insteadare shaped by the differentcontexts in whichthey occur."113 Parallelingthis work, some historianshave begun to provideinte- gratedanalyses of the manyfactors that shaped demographicoutcomes. Any factorthat causes mentalor physicalstress-displacement, warfare, drought,destruction of crops,soil depletion,overwork, slavery, malnutrition,social and economicchaos-can increasesusceptibility to disease.114 These same social and environmentalfactors also decreasefertility, pre- ventinga populationfrom replacing its losses.115The magnitudeof mortality depended on characteristics of precontact American Indian populations(size, density,social structure,nutritional status) and on the patternsof European colonization(frequency and magnitudeof contact, invasivenessof the European colonial regime).As anthropologistClark SpencerLarsen argues, scholars must "move away from monocausal explanations of population change to reach a broad-basedunderstanding of declineand extinctionof NativeAmerican groups after 1492.))''116 The final evidenceof the influenceof social and physicalenvironments on disease susceptibilitycomes from their ability to generate remarkablemortality among even the supposedly disease-experienced Old World populations.Karen Kuppermanhas documentedthe synergy of malnutrition,deficiency diseases, and despairat Jamestown,where 8o percentof the colonistsdied between1607 and 1625. Smallpoxmortality, 113 Kunitz,Disease and Social Diversity:The EuropeanImpact on theHealth of Non-Europeans(New York, 1994), 5, 73. See also Crawford,Origins of Native Americans,41-49. 114Cook, "InterracialWarfare and PopulationDecline among the New England Indians," Ethnohistory,20 (Winter 1973), 1-24; McCaa, "Spanish and Nahuatl Views," 429; Newson,"Indian PopulationPatterns," 47-65; Snow and Kim M. Lanphear, "EuropeanContact and Indian Depopulationin the Northeast:The Timingof the First Epidemics," Ethnohistory,35 (Winter 1988), 17; Trimble, "1837-I838 Smallpox Epidemic,"82; Ubelaker,"Patterns of Demographic Change," 364-69. 115 Stannard, "Disease and Infertility,"325-50; Ubelaker, "Patterns of DemographicChange," 364. 116Larsen et al., "PopulationDecline and Extinctionin La Florida,"in Verano and Ubelaker,eds., Diseaseand Demography,35. See also Larsen,"In the Wake of Columbus," 124.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 740 WILLIAM AND MARY QUARTERLY nearly40 percentamong Union soldiers during the Civil War, reflected livingconditions and notinherent lack of innateor adaptiveimmunity. Mortalityamong soldiers infected with measles, which exceeded 2o percentduring the United States Civil War, reached 40 percentduring the siegeof Parisin theFranco-Prussian War.117 Poverty and socialdisrup- tioncontinue to shapethe distribution of disease,generating enormous globaldisparities with tuberculosis, HIV, and all otherdiseases. Is it possibleto quantifythe variability, to delineate the relative contributionof potentialgenetic, developmental, environmental, and social variables?Detailed studies have documented "considerable regional variability"in AmericanIndian responsesto Europeanarrival.118 Many AmericanIndian groupsdeclined for a centuryand then began to recover.Some, such as thenatives of the Bahamas,declined to extinction.Others, such as theNavajo, experienced steady population growth afterEuropean arrival.More precisedata exist for select groups. Newson,for instance, has compileddata aboutdie-off ratios, the pro- portionof thosewho died to thosewho survived.While die-off ratios wereas highas 58:I alongthe Peruvian coast, they were lower (3.4:I) in thePeruvian highlands. In Mexicothey varied between 47.8:I and 6.6:I, againdepending on elevation.They ranged from 5.1:1 in Chiapasto 24:1 in Hondurasand 40:I in Nicaragua."9Mortality rates from European diseasesamong South Pacific islanders ranged between 3 percentand 25 percentfor measles, and 2.5 percentto 25 percentfor influenza.120 Such variabilityamong relatively homogeneous populations, with die-off ratiosdiffering by an orderof magnitude, most likely reflects the contingencyof social variables.But mostof thesenumbers are, admittedly, enormous:a 4:I die-offratio indicates that 75 percentdied. Why did so manypopulations suffer such high baseline mortality? Does thisreflect a sharedgenetic vulnerability, whose final intensity was shapedby social variables?Or does it reflecta sharedsocial experience,of pre-existing nutritionalstress exacerbated by the widespread chaos of encounterand colonization?Both positions are defensible. The variabilityof outcomesreflected in thedifferent fates of different Indian populations provides powerfulevidence against the inevitabilityof mortality.It underminespopular claims, made most influentiallyby HenryDobyns, that American Indians suffered universal

117 Kupperman, "Apathy and Death in Early Jamestown," JAH, 66 (1979), 24-40; Crosby, "Virgin Soil Epidemics," 292-93 (smallpox); Squire, "Reports of Societies," 324 (measles). 118 Ubelaker and Verano, "Conclusion," in Verano and Ubelaker, eds., Disease and Demography,281. 119Newson, "Indian Population Patterns,"42-44- 120 Cliff,Haggett, and Smallman-Raynor,"Island Populations," 147.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions VIRGINSOILS REVISITED 741 mortalityfrom infectious diseases.121 Noble David Cook, for instance, argues that the vulnerabilitywas so general that Indians died equally whateverthe colonial context,"no matterwhich European territorywas involved,regardless of the location of the region.It seemed to make no differencewhat typeof colonial regimewas created."122Such assertions, which reduce the depopulation of the Americas to an inevitable encounterbetween powerfuldiseases and vulnerablepeoples, do not match the contingencyof the archaeological and historical records. These, instead,tell a storyof populationsmade vulnerable. One could arguethat the differencesin Americanand Europeandis- ease environments,the nutritionalstatus of precontactAmericans, and the disruptions of colonization created conditions in which disease could only thrive.Only a time travelerequipped with a supplyof vac- cines could have altered the demographicoutcomes.123 But it is also possible that outcomes might have been different.Suppose Chinese explorers,if theydid reach the Americas,had introducedEurasian diseases in the 1420s, leaving American populations two generationsto recoverbefore facing European colonization. Suppose smallpox struck Tenochtitlanafter Cortds's initial retreat and not duringhis subsequent siege of the city.An epidemic then mighthave been bettertolerated than duringthe siege. Or suppose that the epidemicsof 1616-1617and 1633-1634struck New England tribesduring the nutritionallybountiful summersand not duringthe starvingtimes of winter(or perhapsit was because of those starvingtimes that the epidemicstended to appear in winters).The historicrecord of epidemic afterepidemic suggeststhat high mortalitymust have been a likelyconsequence of encounter.But it does not mean that mortalitywas the inevitable result of inherent immunologicalvulnerability. Consider an analogous case, the global distributionof HIV/AIDS. From the earliestyears of the epidemic,HIV has exhibitedstriking dis- paritiesin morbidityand mortality.Its prevalencevaries betweensub- Saharan Africa and developed countries and between different populations within developed countries. Few scientistsor historians would argue that these disparitiesbetween African and Europeans or between urban minorities and suburban whites exist because the afflictedpopulations have no immunityto HIV. Instead,the social contingencyof HIV on a local and global scale has long been recognized.124 121 Compare Dobyns, TheirNumber Become Thinned, 13-16, to a critique, Aldenand Miller,"Unwanted Cargoes," 37. 122Cook, Born to Die, 5. 123This storyof sciencefiction has been told in Orson ScottCard, Pastwatch: TheRedemption of Christopher Columbus (New York,1996). 124 Jonesand Allan M. Brandt,"AIDS, Historical,"in JoshuaLederberg, ed., EncyclopediaofMicrobiology, 2d ed., vol. I. (San Diego, 2000), 104-I5, esp. 114.

This content downloaded from 128.103.149.52 on Fri, 09 Oct 2015 14:47:39 UTC All use subject to JSTOR Terms and Conditions 742 WILLIAM AND MARY QUARTERLY

We shouldbe justas cautiousbefore asserting that no immunityled to thedevastation of the American Indians. Historiansand medical scientistsneed to reassesstheir casual deploymentof deterministicmodels of depopulation.The historic recorddemonstrates that we cannotunderstand the impact of European diseaseson theAmericas merely by focusingon Indians'lack of immunity.It is certainlytrue that epidemics devastated American Indian populations. It is also likely that genetic mechanisms of disease susceptibilityexist: theyinfluence the susceptibilityof American Indians-and everyoneelse-to infectiousdisease. What remainsin doubtis the relativecontributions of social,cultural, environmental, and geneticforces. Even when immunologists demonstrate that a wide varietyof genescontribute to susceptibilityto infectiousdisease, it will likelyremain unknown how thesefactors played out amongAmerican Indiansin pastcenturies. Demographic data, meanwhile, provide con- vincingevidence of thestrong impact of socialcontingency on human disease.This uncertaintyleaves the door open forthe debatesto be shapedby ideology.125 Althoughunprecedented in their widespread severity, virgin soil epi- demicsmay have arisenfrom nothing more unique than the familiar forcesof poverty,malnutrition, environmental stress, dislocation, and social disparitythat cause epidemicsamong all otherpopulations. Wheneverhistorians describe the depopulation of the Americas that fol- lowedEuropean arrival, they should acknowledge the complexity,the subtlety,and the contingencyof the process.They need to replace homogeneousand ambiguousclaims of no immunitywith heteroge- neous analysesthat situate the mortalityof the epidemicsin specific social and environmentalcontexts. Only thencan theyovercome the widespreadpublic and academicappeal of immunologicdeterminism and do justiceto thecrucial events of the encounter between Europeans andAmericans.

125 My own perspectiveis shapedby awarenessof how social factorsdetermine contemporarypatterns of disease, by skepticismof the relevanceof increasingly detailedgenetic information, and by concernthat observers often seek to blamevic- timsto avoid responsibilityfor disparities in healthstatus.

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