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Natural Histories of Infectious Disease: Ecological Vision in Twentieth-Century Biomedical

ScienceAuthor(s): Warwick AndersonSource: Osiris, 2nd Series, Vol. 19, Landscapes of Exposure: Knowledge and Illness in ModernEnvironments (2004), pp. 39-61Published by: The University of Chicago Press on behalf of The History of Science SocietyStable URL: http://www.jstor.org/stable/3655231 .

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N a t u r a l Histor ies o f Infect ious D i s e a s e :

EcologicalVisionin Twentieth-CenturyBiomedicalScience

By WarwickAnderson*

ABSTRACT

Duringthe twentieth

century,disease

ecology emergedas adistinct

disciplinarynet-

work within infectious diseases research. The key figures were Theobald Smith,F. Macfarlane Bumet, Rene Dubos, and Frank Fenner. They all drew on Darwinianevolutionism to fashion an integrative (but rarely holistic) understanding of disease

processes, distinguishing themselves from reductionist "chemists" and mere "mi-crobe hunters."They sought a more complex, biologically informed epidemiology.Their emphasis on competition and mutualism in the animated environment differedfrom the physical determinism that prevailed in much medical geography and envi-ronmental health research. Disease ecology derived in part from studies of the in-teraction of organisms-micro andmacro-in tropical medicine, veterinarypathol-ogy, and immunology. Itdeveloped in postcolonial settler societies. Once a minorityinterest, disease ecology has attractedmore attention since the 1980s for its expla-nations of disease

emergence,antibiotic

resistance, bioterrorism,and the health im-

pacts of climate change.

INTRODUCTION

The end of the twentieth century found Joshua Lederberg reflecting on the history of

infectious diseases research. "Duringthe early acme of microbe hunting, from about

1880 to 1940," he wrote, "microbes were all but ignored by mainstream biologists."Moreover, "medical microbiology had a life of its own, but it was almost totally di-

vorced from general biological studies." Bacteriologists "had scarcely heard of the

conceptual revolutions in genetic and evolutionary theory."Although germs had long

been "recognized as living entities . . . the realization that they must inexorably beevolving andchanging"was slow to penetrate public health and medical practice.1Yet

Lederberg could identify a few conceptual bridges linking bacteriology and general

*Departmentof MedicalHistoryandBioethics,Universityof WisconsinMedicalSchool, 1440 Medi-cal SciencesCenter,1300UniversityAve.,Madison,WI53706-1532; [email protected].

I would like to thankGreggMitman,MichelleMurphy,andChrisSellers foraskingme to write this

essayfor theconferenceon "Environment,Place,andHealth,"at theUniversityof WisconsinatMadi-son. Susan Craddockprovidedhelpfulcommentsatthe meeting.BarbaraGutmannRosenkrantzandMarkVeitchhave fromthe startguidedmy work on diseaseecology. I amalsogratefulto David Aber-

nathy,Nick King,LindaNash,CharlesRosenberg,andConeveryBoltonValenciusfor theiradviceonearlierversions of this

essay.FrankFenner,Joshua

Lederberg,Steve

Boyden,and

TonyMcMichael

cheerfullycorrectedsome misconceptions,thoughthey maynotagreewithall thatremains.JoshuaLederberg,"InfectiousHistory,"Science 288 (2000): 287-93, on 288, 291.

2004 by TheHistoryof Science Society.All rightsreserved.0369-7827/04/1901-0003$10.00

OSIRIS2004, 19: 039-061 39



WARWICKANDERSON

biology (most of them, admittedly, constructed after 1940). Once O. T. Avery, at

the Rockefeller Institute, discovered that nucleic acid was the transmissible factor

responsible for pneumococcal transformation, bacteria and bacterial viruses had

"quickly supplanted fruit flies as the test-bed for many of the subsequent develop-

ments of molecular genetics and biotechnology."2Indeed, in 1956 Lederberg himselfhadbeen awardeda Nobel Prize for his work in microbial genetics. He noted, too, that

the synoptic texts of Macfarlane Bumet and Rene Dubos had described the nexus of

microbiology and general biology; their pioneering integrative work characterized

the relations of disease, environment, and evolutionary processes in newly fashion-

able ecological terms.3

Increasing confidence in antibiotic and vaccine development during the 1960s and

1970s, however, led to the neglect of such ecological interpretationsof infectious dis-

ease. In the 1980s, nature struck back. Emergent diseases, such as AIDS, and prob-lems of microbial resistance to antibiotics, prompted "widespread re-examination of

our cohabitationwith microbes."It was time, Lederbergwrote in the year 2000, for usto abandon the old metaphor of a war between germs and humans, replacing it with

"a more ecologically informed metaphor, which includes the germ's-eye view of in-

fection."Above all, he concluded, we need more "researchinto the microbial ecologyof our own bodies."4

Historians generally have neglected ecological traditions in biomedical science.

Like most of the scientists and physicians they study, historians have chosen instead

to emphasize the development during the twentieth century of simplified laboratorymodels for complex pathophysiological mechanisms. Moreover, diagnosis and pre-vention are commonly framed in terms of "microbe hunting,"and treatmentin terms

of "magic bullets." Sometimes the story will conclude with a monitory account of thepitfalls of progress: technically biomedicine is doing better than ever, but at the cost

of its interpretive or exegetical power, its ability to define and represent our place in

nature. Medical science, in these accounts, has concentrated on elucidating mecha-

nisms of disease, abandoning the older efforts-frequently associated with the

names of Hippocrates and Sydenham-to make sense of life forms and their rela-

tions to the environment. It is easy to find examples of such cautionary tales, with

their typical mixture of satisfaction with contemporary achievement and nostalgiafor a more integrative, or holistic, worldview. 5When Charles-EdwardAmory Wins-low came to write his history of the "conquest" of epidemic disease, he admitted

that "the practical triumphs of bacteriology did indeed tend to over-simplify theproblem and to cause medical men for nearly half a century to ignore the true many-sidedness of disease."6 Following a similar line of reasoning, Mirko Grmek has

2 Ibid.,288. See Ren6 J. Dubos. TheProfessor,TheInstitute,andDNA(NewYork,1976).3F. M. Buret, Biological AspectsofInfectiousDisease (NewYork,1940);andRen6J.Dubos,Man

Adapting(New Haven,Conn., 1965). See also JoshuaLederberg,"J.B. S. Haldane(1949) on Infec-tious Disease andEvolution,"Genetics 153 (1999): 1-3.

4 Lederberg,"InfectiousHistory"(cit. n. 1), 289, 290, 293. Evenin 1988,Lederberg,citingBuret,hadurgedus "tocome to gripswith therealitiesof ourplace in nature"("MedicalScience, InfectiousDisease, and the Unity of Humankind,"Journalof the American Medical Association 260 [1988]:

684-5, on 684).5 Formy own contributionto this literature,see WarwickAnderson,"Diseaseand Its Meanings,"Lancet 2000 354 (1999): SIV49.

6 C.-E.A. Winslow,TheConquestof EpidemicDisease: A Chapterin theHistory of Ideas (1943;reprintedMadison,Wis., 1980), 335.

40



NATURALHISTORIESOFINFECTIOUSDISEASE

pointedout that since PasteurandKoch,"muchmoreimportanceis attachedto in-

vestigationsof thebiology of germsthanto knowledgeof the influenceof milieu."7

Recently,MichaelWorboyshasarguedthatevenif germtheoriesdid not leadphysi-cians simplyto switchfrom holism to reductionism,interestin social andenviron-

mentalinfluencesgraduallydeclined,andincreasingly"disease was constitutedinrelationsbetweenbacteriaandindividualbodies."8Thepacemaybe slower,butthedestinationis the same:medical science eventuallybecomestriumphantly,yet per-haps meretriciously,reductionist.Anyonewould think that modem biomedicineis

just a matterof culturinggermsin thelaboratory,identifyingtheirphysicochemicalproperties,andtrackingthemin the community-that is, little more thanmicrobe

hunting.Inthisessay,however,I wantto reviewthehistoryof infectious diseases research

in the twentiethcenturyto recover variousemergingforms of ecological under-

standingfromwhat has sometimes seemed an aridwaste of reductionism.In par-

ticular,I would like to sketchoutpersonalconnectionsbetweenthemajoradvocatesof the ecology-or "naturalhistory"-of disease, to describe an internationalre-searchnetwork,and to explorethevariousinstitutionalandsocial niches these sci-entists occupied. Reconstructingthis social ecology of ecological knowledge inmedical science is no easy task.9For one thing, each of the majorpioneers of abroaderbiological conceptionof disease processes tended to representhimself as

singular,as the sole authorof the idea, andrarelycited others,even those linkedtohim by educationandfriendship.Formanyearly proponents,this rhetoricof sin-

gularityandmarginalitywas a crucialaspectof theargumentandpartof theirown

propheticself-fashioning.Yet the trainingand the careerpathsof key figuressuch

as TheobaldSmith,F. MacfarlaneBurnet,and Rene Dubos structuredan intricatenetworkof influence,counsel,andcriticism.This is not to say thata uniform,well-defined school of disease ecology existedin the twentiethcentury.The differencesbetweenmanyof these scientists can at times be as greatas any similarity:Dubos,for example,was by the end of his career a significantoutlierfrom this clusterofscholars.But anemphasison singularity,and on variationin laboratorywork,orin

argumentandappeal,often disguiseda fundamentalsimilarityin approach,a fam-

ily resemblancein theory, perspective,and career.These scientists had common

pointsof referenceanda sharedrhetoricalrecourseto ecological and otherbroadlyintegrativeapproachesto understandingdisease. That is, the intellectual interac-

tionsof theseand otherscientistsforgeda recognizablesubdiscipline,a sharedcon-ceptualframeworkandrhetoric,withininfectious diseases research,even if theirownlocal commitmentsandlaboratorystyle sometimes differed.

Itis importanttodistinguishthisassertionof an "environmental"perspectiveinmedi-cal sciencefroman earlierconcernwithmedicalgeography,therole of thephysical

7 MirkoGrmek,"G6ographiemedicale et histoiredes civilisations,"Annales:Economies,Societes,Civilisations 18 (1963): 1071-89, on 1085. For similarstatements,see Fielding H. Garrison,"TheNewerEpidemiology,"MilitarySurgeon53 (1923): 1-14, 10;andErwinH.Ackerknecht,HistoryandGeographyof theMostImportantDiseases (NewYork,1965), 1.

8Michael Worboys, Spreading Germs: Disease Theories and Medical Practice in Britain,

1865-1900 (Cambridge,2000), 285.9CharlesE. Rosenberg,"TowardanEcology of Knowledge:OnDiscipline, Context,andHistory,"in TheOrganizationof Knowledgein ModernAmerica, 1860-1920, ed. AlexandraOleson and JohnVoss(Baltimore,1979),440-55.

41



WARWICKANDERSON

milieuincausingdisease.0TheworkofBurnet,inparticular,was structuredmorearoundabiologicallymediatedenvironmentandderived,inpart,fromtheparasitologicaltradi-tionin tropicalmedicineandveterinarypathology,whichwaspreadaptedto ecologicalexplanationsof thissort,not fromolderHippocraticnotionsof directenvironmentalde-

terminism.Unlikemostmedicalgeography-which persistedinthetwentiethcenturyinmedicalhistoryandin geographyitself-disease ecology postulatedan evolutionarytimescale,modelsthatwereintegrativeandinteractive,anda global scope.Moreover,diseaseecologywas less explicitlyracialin itsarguments,thougha concernwithpopu-lationqualityundoubtedlypersisted.Ingeneral,thespatialimaginaryof diseaseecologywas moreabstractandbiologicallyanimatedthanmedicalgeography,andtheprocessesit describedusuallywerevisibleonlytoexperts,notreadilydiscernedorexperiencedbythegeneralpublic.Thatis, the finepatternof microbialinteractionwasgenerallylessev-identthana changein seasonor a shiftin thewinddirection.But theecologicalunder-

standingoftheglobalas a siteof infectiousdiseaseemergencecouldnonethelessbecom-

pelling:it was,afterall,Duboswhocoinedtheslogans"OnlyOneEarth,"and"ThinkGlobally,ActLocally."Furthermore,itwouldbe diseaseecologythatprovidedthemost

plausibleexplanationfortheemergenceof "new"diseasesinthe 1980s.The diseaseecologistswhose careersI traceherewerenot,of course,theonlyones

seekingtoreinterpretthe relationsof healthandenvironmentinthe twentiethcentury.Therewereresearchers,forexample,intoxicologyandoccupationmedicine,who,as

ChristopherSellers has pointedout, transformedthose fields into "environmentalhealth"afterWorldWarII, a metamorphosismost forcefully expressed,perhaps,instudiesof theetiologyof cancerandrepresentedpopularlyin RachelCarson'sSilent

Spring.1 Althoughoftennotexplicitly "ecological"-the termis usedonly twice in

SilentSpring-studies of the effect of the physicalenvironmenton humanhealthcould,attimes,drawextensivelyon workin animalecology,andtheemphasisonthebalanceof natureandthedarkside of modernityconveyedabroadlyecologicaltone.12It is remarkable,then,justhowrarelytheproponentsof anecology of infectiousdis-eases andtheexpertson thehealthimpactof thephysicalenvironmentreferto one an-other.Theymayhave sharedintellectualinterests,evenpoliticalconcerns,buttheirsocialnetworks,careertrajectories,andinstitutionalniches seemverydifferent.Suchbasicsimilarityalliedwithself-styleddifferenceatteststo boththebroadsalienceandthe interpretiveflexibilityof notions of "environment"and"ecology"in twentieth-

centuryexplanationsof healthanddisease.

Therelationshipof diseaseecology to medicalholism,orconstitutionalmedicine,and to theoriesof thepathogenicpotentialof civilizationis just as ambiguous.BothBurnetand Dubos severelycriticizedwhatthey saw as an exclusivelyreductionist

10See Grmek,"G6ographiemedicale"(cit. n. 7); CarolineHannaway,"Environmentand Mias-mata,"in CompanionEncyclopediaof theHistoryofMedicine,ed.W.F BynumandRoy Porter(Lon-don, 1993),292-308; ConeveryBoltonValencius,"Historiesof MedicalGeography,"in MedicalGe-

ographyinHistoricalPerspective,ed. NicolaasA. Rupke(London,2000), 3-29; andFrankA. Barrett,Disease and Geography:TheHistoryof an Idea (Toronto,2000).

" ChristopherC. Sellers,Hazardsof theJob:FromIndustrialDisease toEnvironmentalHealth Sci-ence (ChapelHill, N. C., 1997).

12 1 am gratefulto GreggMitmanandChris Sellers for insistingon this. Carsonobservesthatdis-ease is "a problemof ecology, of interrelationships,of interdependence"(Silent Spring [1963; re-printedHarmondsworth,1974], 169). But as Sellers suggests, "[E]venas [Carson's]own ecologicalhabitsof mindprovedcrucialto hersynthesis,notecology itselfbutthesciences of humanhealthsup-plied the core of herargument"(Hazardsof the Job [cit.n. 11], 2).

42




trendin modembiomedicine,buttheydid notdisplaymuchinterestin holismat thelevelof thehumanorganism,andtheirecologicalmodelsalwayscontainedsomekeyreductionistelements.'3Rather,they distrustedunnaturallynarrowandoverlysim-

plifiedaccountsof any sort,especiallythose revealinga preoccupationwith phys-

icochemicalmechanism,promotinginstead a more inclusiveandintegratedunder-standingof natureandsociety.Theirannoyancewith reductionismanddismayat the

emergingcharacterof modernitywere notunrelated.'4CertainlyDubos becamea fa-mous criticof the dangersof industrialcapitalismandenvironmentallyinsensitive

modernity.By theend of his career,condemnationof a destructivecivilization,andits associatedalienatedrationalism,dominatedhis writing,and his argumentscameto assume a moretraditionallyholistic, humanistic,andeven mystical,cast.Buret,too,displayedambivalencetowardmodernity,pointingto thedangersof overpopula-tion,biologicalwarfare,antibioticresistance,and environmentaldegradation,all, inhis opinion,the fruitsof a narrowlyreductionist-even obscurantist-worldview.

As CharlesE. Rosenberghassuggested,anxietiesabouttheriskof modernwaysoflife were,duringthe courseof thetwentiethcentury,"explainedincreasinglyintermsnot of thecityas apathogenicenvironment,butof evolutionaryandglobalecologicalrealities."15It is thepurposeof thisessay to explainhow one partof thiscomplexex-

planatoryframeworkwas assembledandeventuallymadepopular.

THENEWEREPIDEMIOLOGYANDHOST-PARASITEINTERACTIONS

Writingin 1940,Iago Galdston,a New Yorkpsychiatristand historianof medicine,remarkedon thecrudereductionismof most"post-Pasteurian"medicine.16Epidemi-

ology,thestatisticalstudyof the characterandcauseof disease,hadonceprovidedarichlytextured,multifactorialaccountingof the environmentalconcomitants,andthesocial andmoralcircumstances,of epidemicsthatravagednineteenth-centuryEuropeand NorthAmerica.Since thedemise of medicalgeographyandthegeneralaccept-anceof germtheories,however,anintricateandexactingcalculushad dwindledintomeremicrobehunting.Thislamentationhadbecomecommonplaceand,bythistime,wasperhapsmorea necessaryritualthana realisticdescription.It wascertainlycon-venientfor reformersto representthe statusquo as a collectionof narrow-minded

13 Moregenerally,

on holism in thetwentiethcentury,

see CharlesE.Rosenberg,

"Holismin Twentieth-CenturyMedicine,"in Greaterthan the Parts:Holism in Biomedicine, 1920-1950, ed. ChristopherLawrenceandGeorgeWeisz (NewYork,1998), 335-55.

14 Nor aretheyunrelatedto the concernsthatpromptedsocial medicine,thoughthe styles of anal-ysis, andpolicy implications,were often quite different.Yet in his earlierwork,JohnA. Ryle couldclaim that"therearebetterinspirationstothoughtfulmedicineto be foundintheOriginofSpeciesthanin a modem textbook of bacteriology"(The NaturalHistory of Disease [1936; reprintedLondon,1988], 382). See alsoIago Galdston,TheMeaning of Social Medicine (Cambridge,Mass., 1954);GeorgeRosen,"WhatIs Social Medicine?A GeneticAnalysisof theConcept,"Bulletinof theHistoryofMedicine21 (1947): 674-733; andDorothyPorter,"ChangingDisciplines:JohnRyle andtheMak-ing of Social Medicinein Twentieth-CenturyBritain,"Historyof Science 30 (1992): 119-47.

15 Charles E. Rosenberg,"Pathologiesof Progress:The Idea of Civilizationas Risk,"Bull. Hist.Med.72 (1998):714-30, on 723. Rosenbergdescribes"a moreexpansiveglobalperspectivein whichinclusive andecological styles of analysishavebecome increasinglypervasive"(726), citing Buret.

Fora helpfuldiscussion of theepidemiologicaltropesof "contamination"and"configuration"(i.e., amoreecological understandingof epidemics),see Rosenberg,"ExplainingEpidemics,"in ExplainingEpidemics,and OtherStudies in theHistoryof Medicine(Cambridge,1992),293-304.

16Iago Galdston,Progress in Medicine:A Critical Reviewof the Last One HundredYears(New

York,1940).

43



WARWICKANDERSON

technicians, to represent the old guardas cloistered laboratoryscientists dutifully cul-

tivatingtheirgerms or as public health officials glibly documenting disease outbreaks,

tracing germs through the community. The benefits of complexity and integrative

analysis surely would stand out most clearly against such alleged routinism and art-

lessness.But those who studied tropical medicine and veterinary pathology-and, indeed,

most field epidemiologists-understood thattrackingthe microbial cause of a disease

outbreakrarely proved as easy as one might hope. Otherbiological factors had to be

taken into account. The development of the notion of "carrier status" during the

1890s-the idea that susceptibility to germs might vary in a human population, al-

lowing some individuals to spreada germ without succumbing to it-had alreadypre-sented a challenge to more simplistic efforts to track microbes.17The full complexityof host-parasite relations, however, was perhapsbetter revealed in studies of tropicalmedicine and veterinary pathology, in which various life forms were commonly in-

volved in disease processes. Just before WorldWarI, Ronald Ross had tried to get hiscolleagues in tropical medicine to accept a sophisticated dynamic-equilibrium model

of disease transmission, but by then few of them took his work seriously.'8 It was

instead Theobald Smith, a comparative pathologist at Harvard,who became the ma-

jor advocate of the study of disease as a general biological problem.Smith, the codiscoverer of the role of a tick in transmittingthe parasite thatcauses

Texas cattle fever, was fond of emphasizing the mutual dependence of host and mi-

croorganism, whether in health or disease. In an address at the 1904 St. Louis Uni-

versal Exposition, he had claimed that the "social and industrial movement of the hu-

manrace is continually leading to disturbancesof equilibrium in nature,one of whose

direct or indirect manifestations is augmentationof disease."19Later,Smith would ar-gue that the study of disease was no longer "in the hands of professional mystics" be-

cause "disease has become a biological problem.... [I]t is ranging itself among nat-uralphenomena in our mind."He also positioned his comparative work in pathologyandimmunology, with its concern for dynamic biological processes, against the work

of investigators trying to dig toward the "more fundamental concepts embodied in

physics and chemistry."20Smith described health and disease as consequences of a

struggle for existence between living things, predatoryand parasitic. He reported onthe life cycle of parasites, host-parasite conflict, symbiosis and mutualism, cell para-sitism and phagocytosis, and variation and mutation among parasites. "Parasitism

17 Onthe"healthycarrier,"seeWinslow,ConquestofEpidemicDisease (cit.n. 6);andJudithWalzerLeavitt,TyphoidMary:Captiveto thePublic's Health(Boston, 1996).

18 RonaldRoss, "SomeQuantitativeStudies in Epidemiology,"Nature 87 (1911): 466-7. See alsoJ. AndrewMendelsohn,"FromEradicationto Equilibrium:How EpidemicsBecame ComplexafterWorldWarI,"in LawrenceandWeisz, Greaterthanthe Parts(cit. n. 13), 303-31. Onthe practiceofdisease ecology in African tropicalmedicine during this period, see Helen Tilley, "Ecologies ofComplexity:TropicalEnvironments,AfricanTrypanosomiasis,andtheScience of Disease ControlinBritishColonialAfrica, 1900-1940" (this volume).

19 TheobaldSmith,"Some Problemsin the Life Historyof PathogenicMircoorganisms,"Science,n.s., 22 (1904): 817-32, on 817. See also his "Parasitismas a Factor in Disease,"Science, n.s., 54(1921): 99-108. Smith becamedirectorof the Division of AnimalPathologyof theRockefellerInsti-

tute,in Princeton,New Jersey,in 1914. See BarbaraGutmannRosenkrantz,"TheobaldSmith,"Amer-ican NationalBiographyOnline,Feb.2000, http://www.anb.org/articles/12/12-00861.html;andHansZinsser,"BiographicalMemoir of TheobaldSmith, 1859-1934," BiographicalMemoirs(NationalAcademyof Sciences) 17 (1936): 261-303.

20TheobaldSmith,ParasitismandDisease (Princeton,1934),viii, x.

44



NATURALHISTORIESOF INFECTIOUSDISEASE

may be regarded,"Smith wrote in 1934, "notas a pathological manifestation, but as anormal condition having its roots in the interdependence of all living organisms."The

prevailing modus vivendi was always temporary, always evolving: the "face of natureand of civilization is steadily changing and thereby changing the host-parasite rela-

tions."21Here was a naturalistic andevolutionary understandingof the interactions oforganisms-micro and macro-in which human disease was decentered and envi-

ronment, or milieu, became animated. Ultimately, "all that can be postulated is theuniversal struggle of living things to survive, and in this struggle the fundamentalbi-

ological reactions gradually range themselves by natural selection under ... cate-

gories of offence and defence." The environment that mattered most was alive, and

any effect of climate or topography would be mediated throughthe interactions of or-

ganisms. Smith reflected on the difference between his dynamic modeling and thework of earlier medical geographers:

Sanitarianslookedto thevariationsinatmosphericmoistureandtemperature,the rise andfall of the waterin subsoil,greatfluctuationsin temperatures,as favoringcausesof epi-demics.Todaywe areinclinedtonarrowthemdownto thehumanandanimalworld,theirintercourse,migrations,thecontinualfluctuationsin habitsandmodes of life, butespe-ciallyin theincreasingsusceptibilityof populationsduringthedisease-freeperiods.22

If "the human race is in a ratherdelicate, unstable relation to its environment,"asSmith contended, then a more complex epidemiology was required. Hans Zinsser, inhis obituaryof Smith, saw his friend and colleague struggling against a tendency "for

bacteriological investigation to segregate isolated fractions of a problem for analysis,with frequent neglect of the correlation of results with the problem as a whole."23

Complex, integrative statistical studies of disease were necessary.The relation of illness to population mobilization and host resistance, evident dur-

ing WorldWar I and in the subsequent influenza pandemic, had already attunedmanyepidemiologists to such appeals for a more intricate and naturalistic accounting ofdisease patterns. MajorGreenwood, a statistician at the Ministry of Health in Britain,and later the first professor of epidemiology at the London School of Hygiene and

Tropical Medicine, claimed that in the nineteenth century William Farrand John Si-mon had recognized that "the conditions of human life-both, as we now say, en-vironmental and eugenic-were quite as importantto the epidemiologist as the ma-teria morbi."24Since then, however, epidemiology had become oversimplified, too

close to a mere addendum on bacteriology. Greenwood wanted more complex and

evolutionary studies of disease in populations, not mere microbe hunting. Epidemics,he believed, were the consequence of a disturbancein biological equilibriumandthusnot reducible to invasion stories.25Simon Flexner, directorof the Rockefeller Instituteand an admirer of Smith's work, also observed a reaction against a facile bacterio-

logical epidemiology during the 1920s. He noted that "each generation receives its

21 Ibid.,2, xi.22 Ibid., 162.23 Zinsser,"TheobaldSmith"(cit.n. 19),284.24 MajorGreenwood,"TheEpidemiologicalPointofView,"BritishMedicalJournal(hereafterBMJ)2

(1919):405-7. Formoreon Greenwood,see J. RosserMatthews,QuantificationandtheQuestforMedi-cal Certainty(Princeton,1995),chap.5;andMendelsohn,"FromEradicationtoEquilibrium"(cit.n. 18).

25MajorGreenwood,Epidemicsand CrowdDiseases: An Introductionto the Studyof Epidemiol-

ogy (London,1935).

45



WARWICKANDERSON

particularimpressionof epidemicdiseases"andthatthepostwargenerationwasmak-

ing an effortto "defineepidemiologyin termswiderthanthoseof the microbicinci-tants of diseasealone."26Accordingto Flexner,this would meandevelopingan ex-

perimentalepidemiologyin which thehost-parasiteinteractionsSmithhadsketched

outmightbe exploredfurther.Studies of thebiologicalcomplexitiesof host-parasiteinteractionsoon reacheda

morepopularreadership,which wantedto learnaboutthelatestscientifictheoriesonman'splacein nature.InRats,Lice,andHistory,HansZinsserrecountedthe"biog-raphy"of typhusfever,tracingthe impactof the diseaseon therise and fall of civi-lizations.Zinsser,aprofessorof bacteriologyandimmunologyatColumbiaand lateratHarvard,wasrespectedfor his investigationsof leucocytefunctionand theprecip-itinreaction,andhe wroteextensivelyon allergyandthe immuneresponse.Havingtrainedinitiallyas a biologist-with E. B. Wilsonat Columbia-Zinsser knewthat

"physicochemicalanalysiswill nevergive the final clue to life processes"and that

TheobaldSmith'sstudyof "complexsystems"wasrequiredinstead."Infectiousdis-easeis one of thegreattragediesof livingthings,"Zinsserwrote,"thestruggleforex-istence betweendifferentformsof life."27A similarlytragicbiologicalview could beseen in PercyAshbur's The Ranksof Death,a popularbook on the contributionofdiseaseto theEuropeanconquestofAmerica.InfluencedbyZinsser,Ashburnevoked

Europeanmigrationto theWesternHemisphereas "thegreatestmobilizationof dis-ease,of its introductionto new andsusceptiblepeoples,the moststrikingexampleofthe influenceof diseaseupon history,of which we canspeakwithanycertainty."Thenativepeoplesof theAmericashad littleimmunityto the diseasesEuropeansbroughtwiththem:thepreexistingbiological equilibriumwasupset,withdevastatinghuman

consequences.Ashburn,who hadservedinthePhilippines,worriedthatwhitesmightyet meet theirmatchif exposedto the "yellowman,"who was even moreimmuno-

logicallycompetent,theresultof "thegeneraldearthof sanitationinAsia,andtheun-rivaledopportunitiesfor ingestinga neighbour'sdung."Ashbur's understandingofthenaturalhistoryof infectiousdisease led himto wonderif, in thecomingcenturies,it would be "machineryor science or immunityto disease thatwill most influenceracialdominance?"28

Diseasehistory,usuallyshornof its raciallinks,would continueto appealto bio-

logicallyinclinedhistorians,atfirstthroughtheAnnalesschool andthen,in the1970s,throughAmericanhistoriansseeking a broadconceptualframeworkfor ambitious

surveys.InTheColumbianExchange,forexample,AlfredW.CrosbyJr.expressedadesireto understandmanabove all as a "biologicalentity."InspiredbyAshburnandZinsser,andcitingHenrySigeristandGaldston,CrosbydescribedhowEuropeanin-vadershaddisruptedtheecological stabilityof the New World,spreadingdisease tovulnerablepopulations.Hechartedthetransferof plants,animals,andgermsbetween

EuropeandtheAmericas,arguingthatthis"Columbianexchangehas leftus withnot

26 Simon Flexner, "ExperimentalEpidemiology,"Journal of ExperimentalMedicine 36 (1922):9-14, on 9, 11.

27 HansZinsser,Rats,Lice, and History:A StudyinBiography(1934; reprintedBoston, 1963), 16,7. DuringWorldWarI, Zinsserhad been a memberof theRed CrossSanitaryCommissionin Serbia,

organizedto controltyphus by RichardP. Strong,laterprofessorof tropicalmedicine at Harvard.Strongwas a minorcontributorto thedevelopmentof diseaseecology atHarvard.See Tilley,"Ecolo-gies of Complexity"(cit. n. 18).

28 P.M. Ashburn,TheRanksof Death:A MedicalHistoryof the ConquestofAmerica(New York,1947), 5, 211, 212. Most of thebook was finishedbefore 1937.

46




a richerbuta moreimpoverishedgeneticpool."29A few yearslater,WilliamH. Mc-Neill alsotriedtoapplythe theoriesof SmithandZinsserto the historicalstudyof dis-ease outbreaks.McNeill was concernedabouthumanpersistencein "tamperingwith

complexecologicalrelationships."Since WorldWarII, a new generationof disease

ecologists,inparticularMacfarlaneBurnetandReneDubos,hadbeenwarningof thebiologicaldangersof populationgrowth,biologicalwarfare,andenvironmentaldegra-dation.Like them,McNeill fearedthat "asequenceof sharpalterationsandabruptoscillationsin existingbalancesbetweenmicroparasitismand macroparasitismcanthereforebe expectedin the nearfutureas in the recentpast."30

MACFARLANEBURNETAND

THE NATURALHISTORYOF INFECTIOUSDISEASE

InMelbourne,Australia,duringthe 1930s,MacfarlaneBuret, a youngvirologist,was

readingtheworksof TheobaldSmithandHansZinsserwithgreatinterest.GrowingupinruralVictoria,Burnethadtakendelightinnaturalhistory,whichwouldremainasourceofpleasurefor therestof hislife.In hisyouth,hebecameanavidcollectorof beetlesand

participatedenthusiasticallyinthe local naturestudymovement.31While a medicalstu-dentat theUniversityof Melbourne,hecontinuedhisbeetlingandfurtherdevelopedhis

biologicalinclinationsunderthetutelageofWilfredE.Agar,theprofessorof zoology.Agar,an experton the role of chromosomesin heredity,had becomeincreasingly

preoccupiedwithwide-rangingbiological speculation.Inspiredby hisreadingof Al-fredNorthWhitehead,theprofessorhadfashionedhimselfas anopponentof physic-ochemicalreductionismand anadvocateof vitalismandholism."Surelyit is not sci-

entific,"hepleadedin 1926,"toinsistthatbiologistsmustinterpretall theirphenomenain thesametermsas thosefoundsufficientin physicsandchemistry."32FamiliarwithGestaltpsychologyand new work in ecology, Agartransmittedhis enthusiasmsto

manyof hisstudents,includingBurnet.ForAgar,as forBurnet,allorganisms,evenmi-crobes,were"linksinthe causalprocesswhichis thecourseof natureitself."33

As a young doctor,beginninghis researchon animalviruses andbacteriophages,Burnet also readJulianHuxley's Essays of a Biologist, and all of The Science of Life,by H. G. Wells, Huxley, and G. P. Wells.34"In one way or another,"Burnet later

29Alfred W.Crosby

Jr.,The ColumbianExchange:Biological

and CulturalConsequencesof

1492(Westport,Conn., 1972),xiii, 219.

30WilliamH. McNeill, Plagues and Peoples (NewYork,1976), 254, 257.31 TomGriffiths,Huntersand Collectors:TheAntiquarianImaginationinAustralia(Melbourne,1996).32 W. E.Agar,"SomeProblemsof EvolutionandGenetics,"PresidentialAddress,SectionD.-Zo-

ology,"in Reportof the 17thMeetingof the AustralasianAssociationfor theAdvancementof Science,Adelaide,1924 (Adelaide, 1926), 347-58, on 358. Whitehead'sargumentsforcreativeforce, interre-lations,andprocessin natureinfluenceda numberof ecologists in the 1930s: see his Process and Re-ality:An Essay in Cosmology(NewYork,1929), 127-97.

33W. E.Agar,A Contributionto theTheoryof theLivingOrganism(Melbourne,1943).Agarrepeat-edly cites RaymondPearl,D'A. W.Thompson,andC. M. Child.Agar'sinterestin populationpolicyandeugenics also infected Burnet.See Agar,"SomeEugenic Aspectsof AustralianPopulationProb-lems,"in ThePeoplingofAustralia,ed. P. D. PhillipsandG. L. Wood(Melbourne,1928), 128-44.

34JulianHuxley,Essays of a Biologist (London, 1923);andH. G. Wells, JulianHuxley,andG. P.

Wells,TheScienceof Life,2 vols. (1929;reprintedNewYork,1931).See F. M. Burnet,ChangingPat-terns: An Atypical Autobiography(Melbourne, 1968); F.J. Fenner, "FrankMacfarlaneBurnet,1899-1985,"BiographicalMemoirsof Fellows of theRoyal Society33 (1987): 100-62; and Christo-pherSexton,TheSeedsof Time:TheLifeof SirMacfarlaneBurnet(Melbourne,1991).Burnetalso re-called (ChangingPatterns,75-6) the influenceof SinclairLewis,Arrowsmith(London, 1925).

47



WARWICKANDERSON

recalled,Wells,Huxley,andWells"broughtme intobiologicalscience andprobablygavethatecologicalslant to thestudyof humandisease which I thinkis characteris-tic of whatI havewritten."35H. G. Wells and hiscoauthorsprovidedan extensiveac-count of the new science of ecology, whichtheydefinedas "theobservationof ani-

malsintheirpropersurroundingsandof theirnormalinteractionandwaysof life, andwhat one may call field physiology."36They describedthe gradualtransitiononKrakatoafrom devastationto the "richnessof tropicalclimaxvegetation,"theimpor-tanceof parasitechains and food chains,the life cycle of lemmings,the biologicalcontrolof pricklypearin Australia,andtheproliferationof introduceddeerin NewZealand.Accordingto The Scienceof Life,"unrestrainedbreeding,for man and ani-malsalike,whethertheyaremice,lemmings,locusts,Italians,Hindoos,orChinamen,is biologicallyathoroughlyevil thing."Burnetwouldtaketo heartexplanationsof the

"struggleforLife,""thetangledweb of interrelationships,"andthedangersof over-

crowdingandhumanmobility.37Wells warnedthat

freedomof intercourseandcommunicationstimulatesbothtradeandthought;butitgivesdisease-germsnew facilities forrapidspreading.... Thus thegrowthof civilizationhasbeen markedby a trailof plagues,moreexplosiveand morewidespreadthananythingwhichprimitivemancanhaveexperienced.38

Yetin its treatmentof healthanddisease,TheScienceofLifemostlypresenteda con-ventionalversionof bacteriology.Buret musthavebeendisappointed,but thebookwould stimulatehimtothinkmoreabouttheecologyof the viruseshewascultivatingin the WalterandElizaHallInstituteduringthe 1930s.

At the Hall InstituteinMelbourne,

Burnetcompleted

his studiesof the interac-tions of bacteriaandbacteriophage,stimulatedduringan earliervisit to the ListerInstitutein London,and examinedthebehaviorof viruses,especiallythe influenza

virus,in the chick embryo.In 1935, an opportunityto investigate psittacosiscon-firmedhis growinginterestin biological aspectsof infectiousdisease. Burnetwasable to demonstratethat asymptomaticinfection with psittacosis was common

among wild parrots,but when the birds were confined and stressed, the illnesswould become manifest.39Such latent, inapparentinfection drew Burnet into abroaderconsiderationof disease ecology and immunity.The small scale of themedical researchenterpriseinAustraliawouldfrequentlycompelthe HallInstituteto take on a

microbiologicalservicerole for

government,muchof which involved

field studies of disease outbreakssuch as psittacosis.As a consequence,Burnet,thougha brilliantlaboratoryexperimentalist,was neverable to limit his researchtobench work. His presence in a "peripheral"settlersociety-a place preoccupiedwithpopulationproblemsand its fragileenvironment-and the occasionalneedto

35 F M. Bumet, "Life'sComplexities:Misgivings aboutModels,"AustralianAnnalsof Medicine4(1969): 363-7, on 364. William B. Provine arguesthat "Huxley'sdiscussion of evolution was thesinglemost encompassingpresentationof aneo-Darwinianviewpointavailablein 1930,"and he sug-gests that "theinfluence of TheScience of Lifeon scientists and theeducatedpublicdeservescarefulstudyby historians"("England,"in TheEvolutionarySynthesis:Perspectiveson the UnificationofBi-ology,ed. Erst MayrandWilliamB. Provine[Cambridge,Mass., 1980], 332).

36 Wells,Huxley,andWells,Scienceof Life (cit. n. 34), 1:22.37 Ibid., 2:974, 1012, 1010, 1012.38 Ibid.,2:1016.39 F M. Bumet, "EnzooticPsittacosis amongstWild AustralianParrots,"Journal of Hygiene 35

(1935):412-20.

48




undertakefield microbiologyled himrepeatedlytowardan ecological perspectiveon disease.

In 1937, Buret began to writeBiological Aspects of Infectious Disease, a book de-

signedforthenonspecialistreader.He wantedtodemonstratethat"infectiousdisease

canbethoughtof withprofitalongecologicallines asastrugglefor existencebetweenman andmicro-organisms."Thatis, he wouldarguethattherewas a natural

conflictbetweenman andhis parasiteswhich,in a constantenvironment,wouldtend toresultin a virtualequilibrium,in which bothspecies wouldsurviveindefinitely.Man,however,lives inanenvironmentconstantlybeingchangedbyhis ownactivities,andfewof his diseaseshaveattainedsuchanequilibrium.40

Buret regardedhis workas acombinationofepidemiologyandimmunologyviewedfrom a wide biologicalperspective.Examininga numberof commondiseases,he

soughttoprovideanevolutionaryexplanationof therelationsbetweenhumanpopula-tions andtheirparasites.Infectiousdiseasewas,heclaimed,nothingmoreor less than"a manifestationof the interactionof living beings"in a changingenvironment.Pro-cessessuchasmigration,urbanization,andgeneralpopulationincreasethuswouldleadto redistributionof old diseasesand theemergenceof "new"diseases."Wars,internalandexternal,financialdepressionsand labourtroubles,"he wrote,"areall breedersofinfectiousdisease,andthefutureof diseasewilldependon theessentiallyfortuitouscir-cumstances which will let loose or withhold these calamities."41In conclusion, Buretwarned(perhapspresciently)of thedangersof biologicalwarfare,thedeploymentof

germssuchasanthrax.Invitedto

givetheEdwardK. DunhamLecturesat Harvardin

1944,Burnetdistin-

guishedhis recentworkfrom those disciplines"whichdealessentiallywith the or-

ganismin isolationandwhich arechieflyconcernedwith its structure,chemicaland

morphological,andwith its functioningas a single unit."Rather,he associatedhisownresearchinterestswith "thescienceswhoseobjectis to interpretandcontrolthe

phenomenaof living thingsas theyare,in suchenvironmentsas thepresenceof na-tureand the activitiesof mankindhaveallottedthem."Burnetwantedto understandhow organismsare"distributedin spaceandtime"andthe "long-termhistoricalas-

pectsof theinteractionbetweenorganismandenvironment."42Hehadbegunto viewhimself as a contributorto the new evolutionarysynthesisthatJulianHuxley de-scribedin the

early1940s. The

synthesiswas

initiallya combinationof

Mendelism,chromosometheory,mathematicalstudiesof heredityin populations,andnaturalse-lectionism;aconsequenceof the revivalof Darwinisminthe 1930s,itbroughtexper-imentalgeneticiststogetherwith naturalistswho studiedevolutionin thefield.43In asense, then, Burnet was extending the synthesis to microbiology and immunology.

40 Buret, Biological Aspects of InfectiousDisease (cit. n. 3), 3, 23. See also idem, "ChangesinTwenty-FiveYearsin Outlookon InfectiousDisease,"The Medical Journalof Australia(hereafterMJA)2 (1939): 23-8; andidem, "CharlesMackayLecture:BiologicalApproachesto InfectiousDis-ease,"MJA2 (1941): 607-12.

41 Buret, BiologicalAspects of InfectiousDisease (cit. n. 3), 4, 307.42 F. M.Bumet,Virusas Organism:EvolutionaryandEcologicalAspectsofSomeHumanVirusDis-

eases (Cambridge,Mass., 1945),3.43MayrandProvine,EvolutionarySynthesis(cit. n. 35). See JulianHuxley,Evolution:TheModern

Synthesis(London,1942);R. A. Fisher,The GeneticalTheoryof NaturalSelection(1930; reprintedNew York,1958);andTheodosiusDobzhansky,Geneticsand the Originof Species (1937; reprintedNewYork,1951).

49



WARWICKANDERSON

Huxley recognizedBurnet'scontributionin the second edition of Evolution:TheModernSynthesis,thoughhe emphasizedmostlythe researchon microbialgeneticsandantibodyproductionratherthanthe morespeculativeecological modelingof dis-easeprocesses.44

Burnet'santipathytofacile reductionismandhisdiscomfortwith industrialmoder-nitybecame morepronouncedin later editions of his surveyof diseaseecology,re-titled the Natural History of Infectious Disease. In 1953, he lamented that "the older

generationof bacteriologistswho weremostlytrainedasmedicalmen has nowalmostbeenreplacedby workerstrainedprimarilyas biochemists."The newgenerationhadlittleor no interestin ecological aspectsof infectious disease.The adventof antibi-otics had furthernarrowedthefocus of medicalresearch,andsimplifiedthe clinicalencounter.In this and latereditions, Buret, an admirerof Malthus,amplifiedhis

warningsof anincreaseinpopulationnumbers,andadeclineinpopulationquality,asinfectious diseasebecame a less significantsocial factor.He was also moreworried

duringthe cold war that the great powerswouldresort to biologicalwarfare.Theprospectof germwarfarewas,hewrote,"astrangeandgloomy endingof this accountof thenaturalhistoryof infectiousdisease."45

In 1972,DavidO. White,theprofessorof microbiologyat theUniversityof Mel-

bourne,joined Buret as the authorof the fourthedition of the NaturalHistory ofInfectiousDisease, but the conceptualframeworkhardlyaltered.This last editionincludedsome additionalintroductorychapterson susceptibilityandresistance,thetransmissionof infection,evolutionand the survivalof host andparasite,antibiotics,andhospitalinfectionsandiatrogenicdisease.Theantireductionistthemecontinued,alongwith thedisparagementof geneticsandthenewmolecularbiology."Thefasci-

nationwith molecularbiology andits implicationsat all levels of biology has per-sisted,"Buret andWhitewrote,"andamongstbacteriologistsandvirologiststherehasbeen a trendawayfrom whatmaybe called theecologicalaspectsof infectiousdisease."In the fourthedition,ecology was againdefined as "theinteractionof or-

ganismswith theirenvironmentandespeciallywithotherorganismsof theirown ordifferentspeciesin that environment."46 Morethaneverbefore,the text was strewnwith termssuchas "climaxstate,""niche,""virgin-soilepidemics,"and"ecosystem."Thus"everyorganismis itself a productof evolutionandecologicallyrelatedto al-mosteveryotherorganismin the ecosystem."Urbanization,overcrowding,and hu-manmobilitywerecausingever-greaterdisruptionto suchecosystems.All thesame,

antibioticsseemedin the 1970s to havecontrolledinfectiousdiseases,whose futurelooked dull. "Theremaybe some wholly unexpectedemergenceof a new and dan-

gerous infectious disease, but nothing of the sort has marked the last fifty years."47Buret andWhiteremainedconcerned,however,thatnuclearorbacteriologicalwar-farewas imminentand thatmoderncivilizationwas environmentallyunsustainable."Thereis uneaseeverywhereamongstresearchmicrobiologistswith a social con-

44 JulianHuxley,Evolution:TheModernSynthesis,2d ed. (London, 1963), xxx-xxxi, 1.45 F. M. Buret, NaturalHistory of InfectiousDisease, 2d ed. (Cambridge,1953),3, 351. The third

edition,publishedin 1962,was little altered.46 F. M. Burnet and David O. White, NaturalHistoryof InfectiousDisease, 4th ed. (Cambridge,

1972), 3, 4.47 Ibid., 138, 263. Duringthe 1960s, Burnetalso explainedthat "communicabledisease has more

thana humansignificance;it is also a manifestationof the way of life of anotherorganism,the re-sponsiblepathogen"("TheNaturalHistoryof InfectiousDisease,"in TheTheoryandPracticeofPub-lic Health,2d. ed., ed.W.Hobson[London, 1965], 121).

50




science,"theynoted.It seemedthat"theadvanceof science is allowingthedevelop-mentof whollyunnaturalmodes of humandominationand mass destruction."48

Buret andWhitepointedto immunologyas one of the few branchesof "medical"researchto embraceecologicalapproaches."Themedicalaspectsof immunityhave

movedawayfromthecentreof scientificinterestas in the last tenyearsimmunologyhasbegunto developits full statusaspartof fundamentalbiology."49Apparently,thestimulusto thisdevelopmentwasBurnet'sclonal selectiontheoryof antibodyforma-tion,andhis explanationof immunologicaltolerance,whichhad earnedhimandSirPeterMedawarthe 1960 Nobel Prize forphysiologyor medicine.In the late 1950s,Bumet had encounteredNiels Jere's "selective"hypothesis,which stated thatan

antigenwould combinewiththe best fitamongtheorganism'sdiversenaturalglobu-linsandtransportit to antibody-producingcells, readyto makemultiplecopiesof the

presentedglobulin.Buret reconfiguredthisidea,arguingthatit wouldmakesenseifcells produceda patternof globulinfor geneticreasonsand the arrivalof thecorre-

spondingantigenicdeterminantcaused theproliferationof theappropriateglobulin.Thetheoryimpliedageneticpolymorphismof thelymphocytes,with avarietyof sur-face receptorsandcoding for antibodyglobulinsarisingfromsomatic mutationorfrom some otherprocessoccurringin differentiationanddevelopment.50This "bio-

logical"conceptreplacedLinusPauling'searlier"instructive"hypothesis,whichsug-gestedthattheantigenacteddirectlyas atemplateforantibodyproduction-this ideahadbeen far too "chemical"forBurnetto countenanceit. The clonalselectiontheorywould come to representtheculminationof Burnet's"ecological"thinking.

"Inmore senses thanone I havealwaysbeen a humanbiologist,"Buret declaredin 1966,"andI knowthatto lookatmanas aproductof evolution,aspartof thewhole

livingworld,hasgivenme some usefulinsightintomy owncharacteristicsand diffi-culties, and added a special intensity to my appreciationof the world as it is."51In Bur-net's lexicon "biological,"or "ecological,"signaledattentionto an integrative,Dar-winian conceptualframework;a biological approachdid not thereforeimply theabandonmentof reductionistmethodsso muchastheirintegrationintoadynamicandinteractivemodelof therelationsof organismandenvironment.Buret generallyusedhis interpretationof prewarecology as a metaphoricresourceratherthanananalytictool.AfterBuret readWellsandHuxleyandstudiedwithAgar,hisunderstandingof

ecologyhadacquireda moreorlesspermanentform.Despitetheoccasionalreferenceto "ecosystem" in the fourth edition of the Natural History of Infectious Disease, he

48 Buret andWhite,NaturalHistory of InfectiousDisease, 4th ed. (cit. n. 46), 266, 267. Buret inparticularhopedthatethology mightprovidesomeinsightintohumanaggressionandsuggesta meansof channelingit into moreconstructiveactivities.He communicatedextensivelywith KonradLorenzandfrequentlyvisitedhim.

49BurnetandWhite,NaturalHistoryof InfectiousDisease (cit. n. 46), 31.50F.M. Bumet, "A Modificationof Jere's Theoryof AntibodyProductionUsing the Conceptof

Clonal Selection,"AustralianJournalof Science 20 (1957): 67-9; and idem, The Clonal SelectionTheoryofAcquiredImmunity(Nashville, 1959).Foranearlierversionof thetheory,see F M. Buretand F.J.Fenner,TheProductionofAntibodies,2d ed. (Melbourne,1949).See alsoJoshuaLederberg,"TheOntogenyof the Clonal SelectionTheoryof AntibodyFormation:Reflectionson DarwinandEhrlich,"Annalsof the New YorkAcademyof Sciences 546 (1988): 175-87; ArthurSilverstein,His-

toryofImmunology(SanDiego, 1989);Anne-MarieMoulin,Le derier langagede la medecine:His-toire de l'immunologiede Pasteurau Sida(Paris, 1991);andEileen CrustandA. I.Tauber,"Selfhood,Immunity,and the Biological Imagination:The Thoughtof FrankMacfarlaneBuret," Biology andPhilosophy15 (2000): 509-33.

51 F M. Burnet,Biologyand theAppreciationof Life.BoyerLectures 1966 (Sydney, 1966), 1.

51



WARWICKANDERSON

appearsto havedisregardedthe mathematicalmodelingandsystems theoryof post-warecology.52Indeed,althoughmanyof thescholarswho shapedtwentieth-centuryecology workedinAustralia,thereis no evidencethatBuret interactedwiththem.53ForBurnet,the term"ecology"continuedto suggestageneralappreciationof natural

complexityandevolutionaryprocesses,thetranscendenceof merephysicochemicalmechanism;he would use some olderecological insights,but he did notembarkon

systematicecologicalresearch.

RENEDUBOSANDMANADAPTING

In 1943, Rene Dubos,the professorof comparativepathologyat Harvard,hadrec-ommendedBuret as the nextDunhamlecturerat the medicalschool.Dubos,thoughhe had not met the Australianscientist,was interestedin Buret's views on disease

ecology.54Afterdoctoralstudiesin bacteriologyat Rutgerswith SelmanWaksman,

Dubos hadinvestigatedthepropertiesof soil microorganisms,concentratingon therole of competition,and its biochemicalmediators,in limiting populations.55Later,settledat the RockefellerInstitute,he extracteda bacteriostaticsubstance,gramicidin,fromBacillusbrevis,anddemonstrateditsuse inthe treatmentof externalinfections.Suchinvestigationsof soil microbiologyandbacterialcompetitionquicklyattunedDubosto an interactiveandecologicalvisionof humanhealthand disease.56

Surprisingly,Dubos even foundsupportfor his emergingecological views from0. T.Avery,his mentorat theRockefellerInstitute,who otherwisepreferredto con-ductcloisteredlaboratorystudiesof immunochemistryand bacterialtransformation.DubosthoughtthatAvery'swork had little influenceon medicalpractice;rather,he

contributedto "theunderstandingof biologicalphenomena.""WhenAverybecameinterestedin abiological phenomenon,he firstobservedit forthesheerfunof it, as anaturalist."57The studyof microbiologyshouldbe morethana meremedical instru-ment;it shouldalso helpto illuminatea widerangeof biologicalproblems.The sci-entist should thereforeacquirea broadbiological perspectiveon diseaseprocesses.Accordingto Dubos,his seniorcolleaguewas convincedthat"theinterplaybetweenthelife processesof the hostandthose of theparasitewas theway of the future."58

52 See, e.g., W.C. Allee et al., Principles of AnimalEcology (Philadelphia,1949); and EugeneOdum,Fundamentalsof Ecology(Philadelphia,1953).For more on thehistoryof ecology, see GreggMitman,The State

ofNature:

Ecology, Community,and AmericanSocial

Thought,1900-1950

(Chi-cago, 1992).53See A. J.Nicholson, "TheBalance of AnimalPopulations,"JournalofAnimalEcology2 (1933):

551-98; andH. G. AndrewarthaandL. C. Birch, TheDistributionandAbundanceof Animals(Chi-cago, 1954). The leadingAustralianecologists arediscussedin SharonE. Kingsland,ModelingNa-ture:Episodesin theHistoryofPopulationEcology(Chicago,1985), 116-23, 171-2; andMartinMul-ligan and StuartHill, Ecological Pioneers: A Social Historyof AustralianEcological ThoughtandAction(Cambridge,2001), chap.7.

54 AlexanderN. Zabusky,"EcologicalOdyssey:The IntellectualDevelopmentof RendJ. Dubos"(seniorhonorsthesis,HarvardUniversity,1986).Dubos was at Harvardonly between 1942and1944;otherwisehe workedat theRockefellerInstitute.

55BernardD. Davis describesWaksman,who was awardeda Nobel Prizeforhis discoveryof strep-tomycin,as "primarilyanaturalhistorianof thesoil, cataloguingthemicro-organismsfoundthere,andfocusingon theirtaxonomyand theirecological effects"("TwoPerspectives:OnRendDubos,and on

AntibioticActions,"Perspectivesin BiologyandMedicine35 [1991]:37-48, on 40).56 BarbaraGutmannRosenkrantz,"ReneJulesDubos,"AmericanNationalBiographyOnline,Feb.

2000, http://www.anb.org/articles/12/12-01795.html.57 Dubos, TheProfessor,theInstitute,and DNA(cit. n. 2), 89, 113.58Ibid., 100.

52




Intheearly 1940s,Dubosbeganto formulatea morecomplexbiologicalaccountof host-parasiterelationships,drawingcertainlyon TheobaldSmith'spreviousworkandprobablyonBumet'srecentmonograph.InTheBacterialCell,publishedin 1945,Dubos described

the organizationof those moleculargroupingswhich,on accountof theirchemicalac-tivity,conditionthe behaviorof thecell bothas anindependentfunctioningunitandinitsrelationto the environment.The ultimateunderstandingof the naturalhistoryof infec-tiousdiseases,and the rationaldevelopmentof methodsfortheircontrol,dependuponthisknowledge.59

It was an effortto placebacteriain anevolutionarytimeframe,reporton bacterial

variabilityandmutation,and indicatethe biochemicalmanifestationsof organismiccompetition.Dubos claimed thatin the past, microbiologistshad narrowlystudied

"bacteriological'events'ratherthanbacteriathemselves."Theseresearcherswere "al-

mostuninfluencedbythedoctrinesandmethodsof classicalbiology."Dubossoughtto

remedythisdeficiency."Itis necessary,"he declared,"toabandontheanthropomor-phicattitudewhichcharacterizedearlierefforts;bacteriamustbe studied,notonlyinthe effectswhichtheyhaveonpracticalhumanproblems,butalso forwhattheyareandwhattheydo as independentlivingorganisms."60

Dubos,however,was graduallymovingawayfromlaboratoryinvestigationand re-

fashioninghimselfas apopularwriterandcommentator.Ina seriesof books,he would

arguefor a moreintegrativesocialandbiologicalunderstandingof humandisease.61Hisdominantthemewasthat"thestatesof healthanddiseasearetheexpressionsof the suc-cess orfailureof theorganisminits effortstorespondadaptivelyto environmentalchal-

lenges."LikeBumet,he believed"organismicand environmentalbiology"neededasmuchattentionas"physicochemicalbiology."Hewrote,"Incomparisonwiththe enor-mous effortdevotedto the componentsof thebodymachine,livingas a processhas

hardlybeenstudiedbyscientificmethods."62InbookssuchasMirageofHealthandMan

Adapting,Dubossoughttoexplore"thecomplexinter-relationshipsbetweenmanandhis

physicochemicalandbiologicalenvironment."63Manyofhisargumentswouldhavebeenfamiliarto readersof Bumet's work:the "interplay"betweenorganismsreachingan

equilibrium,thebalancebetweenparasitismandpredation,thedeterminantsof bacterialvirulence andhost resistance, the impact of increasingpopulationdensity,and the gen-eral evolution of microbialdiseases. However,Dubos, unlikeBuret, would increasinglyfocus on more directphysical influences on humanhealth,referringbackto Hippocratesand medical geographyandpointingto the dangersof environmentalpollution.

59Ren6 J. Dubos, The Bacterial Cell: In its Relation to Problems of Virulence,Immunity,andChemotherapy(Cambridge,Mass., 1945), 17.The bookwas basedon a series of lecturesdeliveredin1944 at the Lowell Institutein Boston.

60 Ibid., 339, 342. See also Rene J. Dubos, "Utilizationof Selective MicrobialAgents in the Studyof Biological Problems,"Bulletinof the N.Y.AcademyofMedicine 17(1941):405-22; idem, "Micro-biology,"AnnualReviewof Biochemistry11(1942):659-78; andidem,"TrendsintheStudyandCon-trol of InfectiousDiseases,"Proceedingsof theAmericanPhilosophicalSociety88 (1944): 208-13.

61 The firstof these was Ren6DubosandJeanDubos,TheWhitePlague: Tuberculosis,Man,and So-

ciety(1952;reprintedNew Brunswick,N.J., 1987),whichdescribestheimpactof povertyand war onthe incidence of this "socialdisease."

62 Dubos,ManAdapting(cit. n. 3), xvii, xix, xx, 333.63 Ibid.,xxi. See also Ren6J. Dubos,Mirage of Health: Utopias,Progress,andBiological Change

(London,1959).

53



WARWICKANDERSON

Althoughsome of Dubos's and Buret's interestsand approachescontinuedto

overlap,theirpathsbeganto divergeas well, as Dubosemphasizeda critiqueof cap-italism and civilization.In his work,monitorycommentoften overcameecologicalscruples.Hismessagewasbecomingever-moretraditional:

To a surprisingextent,modem manhas retainedunalteredthebodilyconstitution,phys-iological responses,andemotionaldriveswhich he has inheritedfromhis Paleolithican-cestors.Yethe livesinamechanized,air-conditioned,andregimentedworldradicallydif-ferentfromthe one in whichhe evolved.64

Dubos's condemnationof "thepathologyof urban and suburbanlife, of anti-

physiologicalleisurein a mechanized,automatedandcrowdedenvironment,"res-onatedwith the sensibilityof the 1960s protestmovements,and he soon becamea

prophetof the"counterculture."65Hebegantotalkmoreaboutthe moralcostof adap-

tationto degradedconditions."Alltoooften,"he lamented,"thebiologicaland socialchangesthatenablemankindtoovercomethe threatsposedbythe modemworldmustbe eventuallypaidforata cruelpricein termsof humanvalues."Adaptability,there-fore,was "oftenapassiveacceptanceof conditionswhichreallyare not desirableformankind."This led Dubos to arguethat "thebiologicalview of adaptationis inade-

quatefor humanlife"-a statementthatBurnetwasunlikelyto utter.66Dubos continuedin muchthe same vein throughoutthe 1960s and the 1970s. In

1968, he warned,"[M]anwill ultimatelydestroyhimself if he thoughtlesslyelimi-natestheorganismsthatconstituteessentiallinks in thecomplexanddelicateweb oflife of whichhe is apart."Increasingly,he representedhimselfas anheir of theHip-

pocratictradition:

"today,as in

Hippocrates'time,goodmedical care

impliesatten-

tion notonly to thebodybut to the wholepersonandto his totalenvironment."67Al-

thoughhe was nowcallingattentionto his"holistic"understandingof disease,Dubosstillarguedthatthisgeneralconceptualframeworkhadto be informedby preciselab-

oratoryknowledge.He triedto resist,not always successfully,environmentaldeter-minismand to hold on to a moreinteractive,ecologicalmodel. "Allnaturalphenom-ena,"he wrote,"arethe result of complex inter-relationships;all manifestationsofhumandisease are the consequencesof theinterplaybetweenbody,mind,andenvi-ronment."68Butincreasingly,he alsowantedto condemnthedamageindustrialcapi-talismwasdoingto "humanvalues,"counterposingradicalhumanismto hisecologi-cal

sensibility."Medical

problemsposed bythe environmentalstimuliand insults of

modem civilizationhaveacquireda criticalurgency,"he asserted.Indeed,his main

worryhadbecome "thethreatto mankindposedby technologiesderivedfrom mod-em physicochemicalandbiologicalsciences."69

FRANKFENNERAND THEECOLOGYOF VIRUSERADICATION

FrankFenner,an Australianmicrobiologist,workedin Dubos's laboratoryat theRockefellerInstitutein 1948 and1949.Therehestudiedtheproductionof BCG,since

64Dubos, ManAdapting(cit. n. 3), xviii. See Rosenberg,"Civilizationas Risk"(cit. n. 15).65 Dubos,ManAdapting(cit. n. 3), 252.66 Ibid.,275, 279.67 Ren6J.Dubos,Man,Medicine,andEnvironment(NewYork,1968),9, 61.68 Ibid.,61.69

Ibid., 88, 111.

54




Dubos was thinkingmoregenerallyabouttuberculosisat thetime.70JustafterWorldWarII,Fennerhadgone to theHall Institutein Melbourneto investigatetheexperi-mentalepidemiologyof infectiousectromeliaof mice andto conductresearchmore

generallyon poxviruses.It was Buret who suggestedthatFennermightappreciate

workingwithDubos. Fennerwas, in a sense, preadaptedto this intellectualterrain.While studyingmedicine at the Universityof Adelaide,he attendedthe lecturesofJ. B. Cleland,theprofessorof pathologyandlaterauthorof anessayon thenaturalistin medicine,and C. StantonHicks,theprofessorof physiologyand a pioneerecolo-

gist.71As a medicalstudent,Fennerevenattachedhimselftothe SouthAustralianMu-seum as its firstandlast"craniologist"-a joke title,he laterrecalled.Workingin anoldertraditionof thenaturalhistoryof man,Fennerhadusedhis skullmeasurementsto challengeprevailingtheoriesof Aboriginalhomogeneity,postulatinginsteada hy-bridorigin.As therewasno futurein craniology,duringthewarhe retrainedas a mi-

crobiologist,completinga diplomaof tropicalmedicine,and thentreatingmalaria,

scrubtyphus,anddenguein PapuaNew Guinea.Throughouthis subsequentcareer,Fennerwould retainhis interestin naturalhistoryandin therelationsof humansandtheirenvironment,especiallythe animatedenvironment.7

In 1949,Fennertookupthe foundationchairof microbiologyat the newAustralianNationalUniversity,thoughhe continuedfora few yearsto workat the HallInstituteonMycobacteriumulceransanditspeculiarterrestrialrelations.Inthe1950s,asmyx-omatosis,apoxvirus,was introducedinto therabbitpopulationof southernAustralia,Fennerdecidedto investigateevolutionarychangein theorganism'svirulenceandinthe resistanceof rabbitsto it. Itwas,he believed,"thebestnaturalexperimenton theco-evolutionof viralvirulenceand host resistanceavailablefor a disease of verte-

brates."73At first,99 percentof rabbitsdied from infection withthe myxomavirus.Thevirus,however,actedas apowerfulselectionpressureandthenextgenerationofrabbitswas far less susceptible.In this researchproject,FennercollaboratedwithFrancisRatcliffe,a zoologistattheCSIRO.RatcliffehadtrainedwithCharlesEltonandJulianHuxleyinEnglandbeforeventuringto Australiawhereinitiallyhe studiedthedistributionof thefruit-eating"flying-fox"andlatertheproblemof soil erosioninthe outback.74Fenner'secological orientationwas confirmedand enrichedthroughhisassociationwithRatcliffe,who since the 1940s hadbeenseekingbiologicalmeansto controlrabbitpopulations.75

70Rene J. Dubos, F.J. Fenner,and C. H. Pierce,"Propertiesof a Cultureof BCG Grownin LiquidMediaContainingTween80 andthe Filtrateof HeatedSerum,"AmericanReviewof Tuberculosis61(1950): 66-76; and F. J. Fenner,"BacteriologicalandImmunologicalAspects of BCGVaccination,"Advances in TuberculosisResearch4 (1951): 112-86.

71 Ontheenvironmentalistandsometimesneo-Lamarckiancastof theAdelaidemedicalschool, seeWarwickAnderson,TheCultivationof Whiteness:Science, Health,and Racial Destiny in Australia(NewYork,2003), chap.7. See also J. B. Cleland,"TheNaturalistin Medicine,withParticularRefer-ence to Australia,"MJA 1 (1950): 549-65; and C. StantonHicks, Soil, Food and Life (Melbourne,1945).Fenner'sfather,Charles,a geographerwho earnedhis living as superintendentof educationinSouthAustralia,was perhapsa moreimportantinfluence.

72 F J. Fenner,"Nature,Nurture,and My Experiencewith SmallpoxEradication:A CareerInflu-encedby ChanceEvents,"MJA 171(1999):638-41. Whenhe was attheHallInstitute,Fennerbecamethejuniorauthor,withBumet,of the second edition of The ProductionofAntibodies(cit n. 50).

73Fenner,"Nature,NurtureandMy Experiencewith SmallpoxEradication"(cit. n. 72), 639. Seealso idem, ed., History of Microbiology in Australia (Canberra, 1990).

74F.N. Ratcliffe,FlyingFoxandDriftingSand:TheAdventuresofa Biologist inAustralia(London,1938).JulianHuxleywrote the introductionto thisbook.

75F.J. Fennerand F.N. Ratcliffe,Myxomatosis(Cambridge,1965).

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WARWICKANDERSON

Duringthe 1960s,thewritingof booksandaccumulatingadministrativedutiestookFennerawayfromthelaboratorybench.76TheBiologyofAnimalViruses,a majorre-vision of Buret's Principles of AnimalVirology,was Fenner'sfirstattemptto de-scribe in detailthe "broaderbiologicalprinciplesof animalvirology."77In a chapter

on the transmissionof viruses,he arguedthat "theepidemiologyof infectiousdis-eases is a branchof ecology concernedwith the spreadand survivalof infectious

agentsin nature."Hereportedonroutesof entryinto thebodyandexit fromit, thedif-ferencesbetweensingle-hostandmultiple-hostviruses,variationsin immunity,theinfluenceof weatherconditionson diseasemanifestation,and theimportanceof ex-

perimentalepidemiology(forwhich he citedGreenwood)."Animalviruses,"Fennerconcluded,"survivein natureas partof an ecosystem."78In a laterpartof the same

chapter,he consideredthe evolution of virulence and host response. Focusingon

myxomatosis,influenza,anddengue,he emphasizedtheprocessesof naturalselec-tion,adaptation,andgeneticdrift.

Even in 1968,Fennerwas concernedthatincreasinghumanmobilityandenviron-mental alterationwouldlead to the emergenceof new diseases.His warningswere

amplifiedin thesecond editionof TheBiologyofAnimalViruses,publishedin 1974."Man'sdisturbanceof thebiosphere,andsome medicalinnovations,"wrote Fennerandhis coauthors,"havecreated'new' viraldiseases for man himselfandfor his do-mesticatedanimals."Itwas clearbythenthat"thegreatincreasein thenumbersof hu-manbeings,theircrowdingintoeverlargercities,and theincreasingcommunication

bymen betweenthese cities all overtheworld,aretendingto makethe 'human'worldinto a single ecological unit."79Rare,or previouslyunknown,microbesmight pro-liferatewithrapidityin thesecircumstances.In anespecially prescientpassage-in

viewof the outbreakof bovinespongiformencephalopathyinBritainadecadelater-Fennerandhis colleaguessuggestedthat"thegreatconcentrationsof livestockthatcharacterize'industrialagriculture'in someWesterncountries,andthe widespreadshipmentandaggregationof largenumbersof animalsforfattening,providegreatlyincreasedopportunitiesfor thespreadof 'rare'virusesthroughlargenumbersof ani-malsandfor theemergenceof viraldiseases of livestock."80Inthe 1970s,Buret mayhavethoughtthatthe outlookforinfectiousdiseasewas still reassuringly"dull,"butFennerwas increasinglypessimistic.

Theprospectsfor smallpoxeradication,however,did seem to improve.Dubos'sdistasteforhumaninterventionin the environmenthad led himto dismiss efforts to

eradicatediseases;he urged,rather,theircontrol,by whichhe meanta "proper,skil-fulhandlingof theecologicalsituation."He assertedin 1965:"Eradicationof micro-bialdiseaseis a will-o'-the-wisp;pursuingit leads into a morassof hazy biologicalconceptsandhalf-truths."This vain pursuitencouraged"the illusion that mancan

76 In 1967 Fennerbecame dean of theJohnCurtinSchoolof MedicalResearchat theAustralianNa-tionalUniversity.From1973until 1979,he was directorof theCentreforResource andEnvironmentStudiesthere.

77 E J.Fenner,TheBiologyofAnimalViruses,2 vols. (NewYork,1968),2:v. See also F M. Burnet,PrinciplesofAnimalVirology,2d ed. (NewYork,1960).Elsewhere,Fennerclaimedthat Bumet'sBi-ologicalAspects of InfectiousDisease "shareswithTheobaldSmith'sParasitismandDisease thedis-tinction of being the firstattemptto apply ecological principlesto infectious diseases" ("Brahma,

Shiva,andVishnu:ThreeFaces of Science,"AustralianAnnalsofMedicine4 [ 1969]:351-60, on 351).78Fenner,Biology ofAnimalViruses(cit. n. 77), 2:760, 758.79E J.Fenner,B. R.McAuslan,C. A. Mims et al., TheBiology ofAnimalViruses,2ded. (NewYork,

1974),618, 635.80Ibid.,635.

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controlhis responsesto stimuli and can makeadjustmentsto new waysof life with-outhavingto payfor theseadaptivechanges.""Havingstudiedbiologicaleffortstoeradicaterabbits,Fennerwas not so surethatcompletefailurewasinevitable,thoughhe, too, couldbe doubtful.Becausethegermsof malariaandyellow feverhad mul-

tiplehosts,Fennerbelievedany attemptto eradicatethese diseases was "biologicallyunsound."He could,however,conceive of the biological possibilityof eradicatingsmallpox,since the virus was monotypicandhadno animalhost, the disease was

readilyidentified,immunityafterinfection was life long, andvaccinationwas rela-

tively easy.In 1968,theyearafterthe launchof theIntensifiedSmallpoxEradication

Campaign,he still thought"technicaldifficulties"stoodin the way of the completeeradicationof smallpox,butby 1974he wasmorehopeful.82Hisexpertiseinpoxvirusresearch,as well as his understandingof theecologicaldynamicsof vaccination,hadattractedtheattentionof D. A. Henderson,the chief of theSmallpoxEradicationUnitof theWorldHealthOrganization,who invitedFennerto serveon the committeeover-

seeingtheeradicationprogram.Later,as chairmanof the GlobalCommissionfor theCertificationof SmallpoxEradication,Fenner,in 1979,was able to confirmthe dis-

appearanceof the diseasesince 1977.83In 1968, S. V.Boyden,an immunologistwho hadworkedwithDubosand thenin

Fenner'sdepartmentat theANU,organizedaconferenceinCanberraoncivilization's

impacton humanbiology.ThemeetingbroughtBumet,Fenner,andDubostogetheragain.Boyden,the headof a new"urbanbiology"group,haddevelopedaninterestinthe social andbiologicalcausesof humanmaladjustment.It was notsurprisingthathe

joinedDubosin condemningthecosts of culturaladaptationto anunnaturalciviliza-tion.AccordingtoBoyden,"[W]henthe conditionsof life of an animalpopulationde-

viatefromthoseto whichit hasbecome,throughnaturalselection,geneticallyadapted,some signsof biologicalmaladjustmentarealmostinevitable."84Predictably,Dubosassertedthat"inapplyingtheconceptof adaptationtothe humanspecies,it is ... nec-

essary to use criteriadifferentfrom those used in Darwinianpopulationtheory."Instead,hebelieved,humansneededto "decidewhatkindsof adaptationarecompat-ible withthemaintenanceof desirablehumanvalues."85Buret, inhis introductiontothesymposium,avoidedsuchtalkof "humanvalues,"focusingon thechangingdis-tributionof humangenotypes secondaryto civilization.His old enthusiasmfor eu-

genicsneverfarbelow thesurface,Bumet worriedthataspopulationsincreasedtheir

qualitywas declining;the "overbreeding"of American"Negroes"especially dis-

mayedhim.86Fennerprovidedwhat was perhapsthe most thoroughly"ecological,"or least

anthropocentric,of the papers."Fromthe pointof view of infectiousdiseases,"he

wrote,"themostimportantfeaturesof man'sculturaldevelopmentarethesize of the

81Dubos,ManAdapting(cit.n. 3), 381. See SocratesLitsios,"Ren6Dubos andFredL. Soper:TheirContrastingViews on VectorandDiseaseEradication,"Perspect.Biol. Med.41 (1997): 138-49. Soper,withthe RockefellerFoundation,led the campaignto eradicatemalariain the 1950s and 1960s.

82 Fenner,Biology ofAnimalViruses(cit. n. 77), 2:784.83 F.J. Fenner,D. A. Henderson,I. Arita et al., Smallpoxand its Eradication(Geneva,1988).84 S. V.Boyden, introductionto TheImpactof Civilisationof theBiology of Man,ed. S. V.Boyden

(Toronto,1970),xiii-xiv, on xiii.85Rene J. Dubos, "TheBiology of Civilisation-With Emphasison PerinatalInfluences,"in Boy-

den,Impactof Civilisation(cit. n. 84), 219-29, on 220, 222.86F.M. Bumet, "HumanBiology as the Studyof HumanDifferences,"in Boyden,Impactof Civil-

isation(cit. n. 84), xv-xx.

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WARWICKANDERSON

individualcommunitiesof men,the numberandproximityof suchcommunities,andthe extentof movementandinterchangebetweenthem."87Fennerdiscussedchangesin

host-parasiteinteractionsinmalaria,salmonellosis,cholera,measles,smallpox,yellowfever,andpoliomyelitis.New viraldiseaseshadbeen"recognizedrelativelycommonly

duringthiscentury:mostbut notall of thesehave beendueto humaninterventioninsomenaturalsituation,ortochangesinthesocialhabitsof man."Urbanization,human

colonization,andairtravelseemedespeciallytopromotethespreadof disease.InFen-ner'sopinion,thebest solutionto theproblemof disease was "theeradicationof thesourcesof infectionbytheeliminationof poverty."88IndiscussingFenner'spaper,S. D.Rubbo,theprofessorof microbiologyatMelbourne,warnedof selectionforantibioticresistanceamongmicrobes."Theappearanceof thesenewstrainsof bacteriaintheaf-fluentsocietiesillustratesanunusualeffect of thechangingsocialorganizationon theinfectiousdiseasesof man."89Inresponse,Fennerdrewhisaudience'sattentionbacktotheemergenceof "new"diseases."Iam surewe will witness the appearanceof anti-

genicallynovel virusesin the nextfiftyyears,andI do not meanonlyinfluenzaviruses;possiblywemayalsowitnesstheappearanceofvirusesof novelpathogenicpotential."90

CONCLUSION

While some othermedicalinvestigatorsin the twentiethcenturyhadturnedto sociol-

ogy to gaina widerperspectiveon health anddisease,advocatesof diseaseecologydrewontheirknowledgeof biologicalprocesses.Forthem,eventhesocialmightbe-come a figmentof biology.Manyof thesescientistshad trainedin tropicalmedicine,veterinarypathology,or agriculturalscienceand were thuspreadaptedto seeingthe

broaderbiologicaldeterminantsof apparentlyspecificor idiosyncraticpathologicalevents.91Commonly,they hadacquiredin youthan enthusiasmfor naturalhistory,whichcontinuedto inflecttheirmedicalstudies;andtheproblemstheyinvestigated-Texas cattlefever,psittacosis,soil microbiology,myxomatosis-tended to confirmtheirecologicalinclinations.Residentinsettlersocieties suchasthe UnitedStatesandAustralia,pioneerdiseaseecologistswereespeciallyattunedto thepersistingimpactof colonialdevelopmentpolicies,to thelastingeffects of agriculturalchangeandhu-manresettlement.Burnet,inparticular,neverlosthis interestin thequalityandquan-tity of populations,a eugenic preoccupationfosteredby the intensedebatein the1920s overAustralianpopulationpolicy-or "carryingcapacity."92Diseaseecology

87 F.J.Fenner,"TheEffectsof ChangingSocial Organisationon the InfectiousDiseases of Man,"inBoyden, Impactof Civilisation(cit. n. 84), 48-76, on 48.

88 Ibid.,on 63, 66.89 S. D. Rubbo,quotedin ibid., 69.90Ibid.,76.91Experienceof tropicalpracticeclearlyinfluencedthe ideas of JacquesM. May,a disease ecolo-

gist who mixed mostly with geographersbut was also on the marginsof the groupI describe. In the1940s and1950s,with thesupportof theAmericanGeographicalSociety, Maytriedtorefashionmedi-cal geographyas disease ecology. See his "MedicalGeography:Its Methods and Objectives,"Geo-graphicalReview40 (1950): 9-41. OnMay'stropicalcareer,see JacquesM. May,Siam Doctor (Gar-denCity,N.Y., 1949).

92 I discuss this debate in The Cultivationof Whiteness(cit. n. 71). Interestingly,Buret seems to

have followed atrajectorysimilarto thatof RaymondPearl.InBuret's case, it led himawayfromthe"AustraliaUnlimited"partisansof theMelbournemedicalschool, towarda concern with"overpopu-lation."OnPearl,see GarlandE.Allen, "OldWine in New Bottles: FromEugenicstoPopulationCon-trol in theWorkof RaymondPearl,"in TheExpansionofAmericanBiology,ed. KeithR. Benson,JaneMaienschein,andRonaldRainger(New Brunswick,N.J., 1991), 231-61.

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thusemergedas alegacyof settlercolonial anxieties.93ForBuret andothersitwould

providea cogentexplanationof diseasepatternsin a worldshapedby humanmobil-

ity;it also allowedthem to expresstheirambivalencetowardthemodernitycolonial-ism hadapparentlymadeglobal.

In the 1980s, furtherchangesin the naturalandconceptualenvironmentswouldprovidea largerniche for ecological reasoningin medical science. Above all, the

emergenceof aglobalepidemicof HIV/AIDSshook thosepreviously"nonecologi-cal"scientistswhohadbecomecomplacentaboutinfectiousdiseaseinthedevelopedworld.Justasepidemiologistssuch asFlexnerandGreenwoodhadcalled for a more

complexunderstandingof disease transmissionin the wake of the influenzapan-demic of 1918-1919, manymicrobiologistsnow soughta moreintegrativeexplana-tion for the emergenceof AIDS andotherdiseases,includinglegionnaires'disease,Lyme disease, denguehemorrhagicfever, and new variantCreutzfeldt-Jacobdis-ease. Of course,disease "emergence,"usuallya matterof old diseases conquering

newterritories,washardlyanoveloccurrence,as Fennercould havetold them.Sincethe late nineteenthcentury,many"new"diseases had spreadwidely, amongthem

nontyphoidsalmonellosis,poliomyelitis,kuru,andeven the pandemicform of in-fluenza.All of theseemergentconditionshad at the time stimulatedspeculationontheirunderlyingbiologicalorsocialcauses,butAIDS would exertan evenmorepro-foundimpactonbiomedicalscience,as it struckaftera longperiodof complacency,when the futureof infectiousdiseases,in Burnet'sopinion,lookedexceedinglydullin the developedworld. In the developingworld, however,therehad never beenmuch causeforcontentment,for therethe impactof economicdevelopmenton mi-crobialabundanceanddistributionwas stilldemonstrateddaily.94Ecologicalinsight

wasrarelyabsentfromtropicalmedicine;thus,in a sense,"mainstream"biomedicalscience was simplycatchingup, recognizingthatdiseaseeven in Europeand NorthAmericamightbe the outcomeof dynamic processes in a global ecosystem. The

complacencyshatteredin the 1980s was not so much overconfidencein the globalcontrolof infectiousdisease,as the conventionalassumptionthatEuropeand NorthAmericahadmanagedsomehowto removethemselvesfrom the naturalprocessesthatdiseaseecologists described.

93 This echoes RichardGrove'sargumentfor the emergenceof a generalenvironmentalconscious-ness fromconcernsabout colonial environmental

degradation:see his Green

Imperialism:Colonial

Expansion, TropicalIsland Edens, and the Origins of Environmentalism,1600-1860 (Cambridge,1995).See also LibbyRobin,"Ecology:A Science of Empire,"in Ecologyand Empire:Environmen-talHistoryof SettlerSocieties,ed. TomGriffithsandLibbyRobin(Melboure, 1997),63-75; ThomasR. Dunlap,"EcologyandEnvironmentalismin the Anglo SettlerColonies,"in GriffithsandRobin,Ecologyand Empire,76-86; JohnMackenzie,"Empireand the EcologicalApocalypse:The Histori-ographyof theImperialEnvironment,"inGriffithsandRobin,EcologyandEmpire,215-28; andPederAnker,ImperialEcology:EnvironmentalOrderin theBritishEmpire,1895-1945 (Cambridge,Mass.,2001). By "Britishempire,"AnkermeansOxfordandSouthAfrica.

94 Muchof thisworkhasfocused on schistosomiasis andtrypanosomiasisin Africa.See CharlesC.Hughesand John M. Hunter,"Disease and 'Development'in Africa,"Social Science and Medicine 3(1970):443-93; andDuncanPedersen,"DiseaseEcology at a Crossroads:Man-MadeEnvironments,Human Rights, and Perpetual Development Utopias,"Social Science and Medicine 43 (1996):745-58. HelenTilleyhasdiscussed thepersistingecological perspectiveof Africantropicalmedicine

in more detailin "Ecologiesof Complexity"(cit. n. 18). See also StephenJ. Kunitz,Disease and So-cial Diversity:TheEuropeanImpacton theHealthofNon-Europeans(NewYork,1994).Inthe 1960sand1970s,medicalanthropologyfrequentlydemonstratedan"eco-social"approachto understandingdiseasein the"ThirdWorld."See MarciaC. InhomandPeterJ.Brown,TheAnthropologyof nfectiousDisease: InternationalHealthPerspectives(Amsterdam,1997).

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Fenner's prediction in the 1960s of the emergence of "new" diseases in the devel-

oped world was fulfilled in the 1980s. JoshuaLederbergwas among those who finallyread the ecological lesson. A colleague of Dubos's at the Rockefeller University,

Lederberghad worked with Buret at the Hall Institutein the 1950s, so theirwork was

familiar to him. In 1993, though, Lederberg complained that "the historiography ofepidemic disease is one of the last refuges of the concept of special creationism"-

pioneering ecological approacheshadlargely been ignored.95Now, however,many sci-

entists were preparedto admit thatevolutionary processes operating on a global scalewere responsible for the emergence of "new"diseases. As environments changed, as

urbanization, deforestation, and human mobility increased, so, too, did disease pat-terns alter, with natural selection promoting the proliferation of microbes in new

niches. But pessimism should not overwhelm us. "Werecall thatsince Frank Macfar-lane Buret, Theobald Smith, andothers,"wrote Lederberg, "we have understood that

evolutionary equilibrium favors mutualistic rather than parasitic or unilaterally de-

structive interactions. Naturalselection, in the long run, favors host resistance, on theone hand, and temperate virulence and immunogenic masking on the parasite's parton the other."All the same, Lederberg, echoing Dubos, remained concerned that too

good a humanadaptationto anincreasingly degradedenvironment might yet be detri-mental to human values. "In a biological sense," he mused, "we may achieve new ge-nomic equilibria with these radically alteredenvironments;but the price of natural se-lection is so high that I doubt we would find it ethically acceptable: it conflicts

violently with the nominally infinite worth that we place on every individual."96

During the 1990s, amplifiedconcern aboutemerging infectious diseases, along withfears of increasing antibioticresistance andthe health effects of climate change, would

boost interest in disease ecology. Stephen S. Morse, a virologist and immunologist atthe Rockefeller University, joined Lederberg in arguing that since "most 'new' or

'emerging'viruses are theresultof changes in trafficpatternsthatgive viruses new high-ways,"we need "ascience of trafficpatterns,partbiology andpartsocial science."97In-terestin the emergence of "new" diseases soon led to a proliferationof conferences and

symposia; it gave rise to numerous reportsand to popularbooks, such as Laurie Gar-rett's The ComingPlague.98Thejournals EmergingInfectiousDiseases andEcosystemHealth were launched in the mid-1990s.99At the end of the century,clinicians and sci-entists were also coming to recognize antibioticresistance as a growing problem, and

95 JoshuaLederberg,"Virusesand HumanKind:IntracellularSymbiosisandEvolutionaryCompe-tition,"in EmergingViruses,ed. StephenS. Morse (New York, 1993), 3-9, on 3. This book derivedfrom a 1989 conferenceonemergingvirusessupportedby the RockefellerUniversityandthe NationalInstitutesof Health,andattendedby D. A. Henderson,FrankFenner,WilliamH. McNeill, andRobertM. May.See also JoshuaLederberg,R. E. Shope, and S. C. OaksJr.,eds., EmergingInfections:Mi-crobialThreatstoHealthin theUnitedStates(Washington,D.C., 1992).LikeBurnetagenerationear-lier,Lederbergwas profoundlyshapedby Wells andHuxley:"TheScience of Lifewas themost influ-entialsourceof myperspectiveonbiology andman'splaceinthecosmos,seen asevolutionarydrama"("GeneticRecombinationin Bacteria:A DiscoveryAccount,"in TheExcitementand FascinationofScience,ed. JoshuaLederberg[PaloAlto, Calif., 1990],vol. 3, part1, 893-915, on 895).

96Lederberg,"VirusesandHumanKind"(cit. n. 95), on 8, 4.97 StephenS. Morse,"EmergingViruses:DefiningtheRules forViralTraffic,"Perspect.Biol. Med.

34 (1991): 387-409, on 388, 404. Morse thanksFrankFennerfordiscussingthispaperwith him.98 LaurieGarrett,TheComingPlague: NewlyEmergingDiseases in a WorldOutof Balance (Lon-

don, 1994).99See Nicolas B. King,"TheScale Politicsof EmergingDiseases"(thisvolume).Kingrelatesfears

of biologicalwarfare-a problemthathauntedBurneteven in 1940-to thegrowinginterestinemerg-ing diseases.

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theyattributedit to evolutionaryprocesses.Accordingto S. B. Levy,a microbiologistatTufts,profligateantibioticuse haddelivereda selectionpressureon microbes"un-

precedentedin the historyof evolution."'??"We mustsomehow,"he wrote,"findameans to reversetheecologicalimbalancethathas occurredin termsof resistantand

susceptiblestrains."'01Otherssawusreapingtheecologicalwhirlwindof climatechange.Alterationsin the abundanceand distributionof microorganismsand theirvectors

might,to a largeextent,mediatethe influenceof climatechangeand otherphysicaltransfigurations.Thus as mosquitoesextended theirrange so, too, would malaria,

dengueandothersupposedly"tropical"pathogens.InHumanFrontiers,Environments,andDisease,A. J.McMichael,whooccupiedGreenwood'schairat the LondonSchoolof HygieneandTropicalMedicine,declaredthat"ashumaninterventionin theglobalenvironmentandits life processesintensifies,we needbetterunderstandingof thepo-tentialconsequencesof... ecologicaldisruptionsforhealthanddisease."'02

Informandfunction,theunderstandingof diseaseecology emergingatthe end of

the twentiethcenturyoftendepartedquiteradicallyfromtheantecedenttheories,andmetaphoricborrowings,of Smith,Buret, andDubos.However,therewas stilla com-mon interestin mitigatingfacile reductionismin medicalresearch,a desireto as-semble a morecomplexandintegrativeexplanatoryframeworkfordiseasepatterns.Proponentsof anecological perspectiveon infectiousdiseasessoughta meansto re-latemicrobiologicalprocessesto largerenvironmentalorbiologicalforces,a waytodescribetheinteractive,dynamicrelationshipsbetweenhost andparasiteandphysi-cal milieu.In so doing, they conventionallyinvokedanevolutionarytimeframeanda globalcompass.Indeed,it is hardto imaginethe developmentof diseaseecologywithout the concomitanteconomicandpolitical globalizationoccurringduringthe

twentiethcentury.Now,asbefore,theleadinginstigatorsof wide-rangingecologicalapproachesarguethattheirviews aremarginalin biomedicalresearch.Yettheycon-tinue to occupy key positionsat elite researchinstitutions,andthey continueto ac-

quireNobel Prizesat anenviablerate.Despiteclaimsof marginality,speculationondiseaseecology hasoftenfunctionedto distinguishscientistsfrommere techniciansor fromtheallegedreductionismandroutinismofjuniorcolleaguesandcompetitors.Buttheoreticalspeculationof thissort,oncelittlemorethanamarkof intellectualdis-tinction,a flashybitof plumage,wouldeventuallybecome a majorselection advan-

tagein therapidlychanging,andperplexing,naturalandconceptualenvironmentsofthe late twentiethcentury.

100S. B. Levy,"AntibioticResistance:An EcologicalImbalance,"inAntibioticResistance:Origins,Evolution,SelectionandSpread,CibaFoundationSymposium207 (Chichester,U.K,, 1997), 1-14, on2. See also idem, TheAntibioticParadox:HowMiracleDrugsAreDestroyingthe Miracle(NewYork,1992).Dubospredictedselection for antibioticresistanceasearlyas 1942.See CarolL.Moberg,"ReneDubos:A Harbingerof MicrobialResistancetoAntibiotics,"Perspect.Biol.Med.42 (1999):559-80.

101Levy,"AntibioticResistance"(cit. n. 100), 8.

102A. J. McMichael,HumanFrontiers,Environments,and Disease: Past Patterns,UncertainFu-tures(Cambridge,2001), xiv. The WHOopenedan office to studythe healthimplicationsof climatechangein 1990. It is also importantto recognizethecontributionsince the late 1970s of mathematicalmodeling of host-parasiteinteractionsandpopulationdynamics.See R. M. May,"Ecologyand theEvolution of Host-VirusInteractions,"in Morse,EmergingViruses(cit. n. 95), 58-68; R. M. Ander-son andR. M. May,"PopulationBiology of InfectiousDiseases,"Nature280 (1979): 361-7,455-61;

and R. M. May and R. M. Anderson,"TheTransmissionDynamics of HumanImmunodeficiencyVirus,"in TheEpidemiologyandEcologyof InfectiousDisease Agents,ed. R. M.Andersonand J. M.Thresh(London, 1988), 239-81. MayregardedFrankFenneras the "realhero"of thebiologicalanal-ysis of diseasebecauseof his classic mathematicalanalysisof myxomatosis(May,"Ecologyand theEvolutionof Host-VirusInteractions,"63).

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anderson 2003 - natural histories of infectious disease - ecological vision in twentieth-century...

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