The Osteological Paradox Reconsidered Author(s): Mark Nathan Cohen, James W. Wood, George R.

Milner Source: Current Anthropology, Vol. 35, No. 5 (Dec., 1994), pp. 629-637 Published by: The University of Chicago Press on behalf of Wenner-Gren Foundation for Anthropological Research Stable URL: http://www.jstor.org/stable/2744088 Accessed: 06/12/2010 14:07
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to thatthe rules may be so lax (at least with regard the that the arof overall morphology the lithic artifacts) chaeologistmay be unable to ascertainfromthe lithics that theywere made accordingto such rules. I suspect (althoughI do not speak as a lithics specialist)that we MARK NATHAN COHEN State University New of recognizethe symbolicnatureof the archaeologicalrec- Departmentof Anthropology, Plattsburgh, N.Y. I2901, its ordofearlyUpperPaleolithicEuropemorefrom dec- York College at Plattsburgh, U.S.A. I5 VII 94 art orativeand representational than fromits lithics. Nevertheless, I am in complete agreement with of interpretation theMiddle-to-Upper-Paleolithic In i982 GeorgeArmelagosand I (Cohen and Armelagos Byers's fromskeletonsand in transition Europe with the one exceptionthat there i984) collected studies ofpathology and are more kinds or levels of symbolicbehaviorthan he mummies of prehistorichunter-gatherers farmers everyregionoftheworldthathad producedcompamentionsand that the originsof languageare as impor- from tant to understandas the originsof symbolic culture. rable data. We found a number of fairly consistent of outside trends:(i) that the frequency nonspecificchronicinAbove all, I am encouragedto see a scholarfrom Paleolithic archaeologytaking a serious and anything fection displayed by skeletons was commonly higher than among earlierhunter-gatherers; If among farmers (2) but naive interestin what archaeologyhas to offer. of the complimentby taking that the frequency specificinfectionssuch as yaws can return we archaeologists infectionusually in a seriousand ideallynot too naive interest what other and tuberculosisor tuberculosis-like disciplineshave to tell us about the evolutionofhuman increasedas groupsbecame largerand more sedentary; of and paracultureand ofthe human mind,ourdisciplinewill bene- (3) that the frequency intestinalinfections sites increased with group size and sedentism when fitenormously. mummies or feces were studied (see Allison I984; see Cited References also Reinhard,Hevly, and Andersoni987); (4) that the of frequency porotichyperostosis, skeletal lesion of the New York:BaR. I984. The evolution cooperation. of AXELROD, (childhood?)anemia, was almost always higheramong sic Books. vers farmersthan among earlier hunter-gatherers; that P. G. I987. Sp6cialisation la chasseet transition de (5) CHASE, LAnthropologie 9I:I75-88. sup6rieur. le Pal6olithique othersigns of malnutrition (retarded growthand osteoin and . I988. "Scavenging hunting theMiddlePaleolithic: porosis in children,prematureadult osteoporosis,reof prehistory in from Europe," UpperPleistocene The evidence Western Eurasia.EditedbyH. L. Dibble and A. Montet-White, duced toothsize, etc.) were more common amongfarmers than earlier hunter-gatherers; that the average (6) of Museum,University University pp. 226-32. Philadelphia: Pennsylvania. statureofmeasuredadult individualsdeclined throughsubsistence? out the Old Worldfrom was . I989. "How different MiddlePaleolithic the Paleolithicthrough Neothe A zooarchaeological on perspective theMiddleto UpperPaleo- lithicperiod;and (7) thatsignsofsystemicstressvisible lithictransition," The humanrevolution. in EditedbyP. R. pp. Uni- in teeth,includingmacroscopicenamel hypoplasiaand Edinburgh Mellarsand C. Stringer, 32I-37. Edinburgh: microscopicWilson bands, were usually more frequent Press. versity standardiza- and pronouncedin farmers . I99I. Symbols Style, and Paleolithic artifacts: than among earlierhunterof form. Journal Anthropo- gatherers. of tion,and theimposition arbitrary IO:I93-2 I4. logicalArchaeology I have interpreted these data as supporting concluthe P. G., AND HAROLD L. DIBBLE. archaei992. Scientific CHASE, (Coof A to Cam- sion that biological stress increased with farming ologyand theorigins symbolism: reply Bednarik. Journal 2:42-5 I. Archaeological bridge hen i989). I continue to interpret them this way, and I stonetoolsin Ethiopia: Im- note fromat least two papers in the I99OS that ArmeContemporary GALLAGHER, J. I977. for Journal FieldArchaeology of plications archaeology. 4: lagos and colleagues also continueto make thisinterpre407-I4. and alliancein Paleolithic so- tation (Armelagos 1990, Armelagos,Goodman, and JaCLIVE. I982. Interaction GAMBLE, cobs 1991; see also Goodman I993). Thisinterpretation ManI7:92-IO2. ciety. AND A. SONTZ. The lithicasI97I. R., D. KOSTER, GOULD, makes the implicitassumptionthatskeletonsin a cemof DesertAborigines Australia. of Ameri- etery, least on the average,are reasonablyrepresentasemblage theWestern at can Antiquity 36:I49-46. tive of the living populations that producedthem and W. D. I964. The genetical evolution socialbehavof HAMILTON, therefore that changes in skeletal assemblages reflect ior.Journal Theoretical Biology7:I-I6. of in B. I977. "Stonetool functions theWestern Desert," real changes in the health of once-livingpopulations. HAYDEN, in Stonetoolsas cultural markers: and Change,evolution, This is an assumption made implicitlyor explicitly, EditedbyR. V. S. Wright, I78-88. Canberra: pp. complexity. with varying degreesof caution,by most quantitatively Humanities Press. orientedpaleopathologists. and Lithictechnology ethnoreflections: . I979. Paleolithic The skeletal data and our interpretation themhave of Atlantic excavationamongtheAustralian Aborigines. graphic Humanities Press. Highlands: been challenged,however.In elaborating what theycall C. B., AND C. GAMBLE. I993. In searchof theNeSTRINGER, "the osteologicalparadox,"Wood et al. (CA 33:343-70; London: anderthals: Solvingthepuzzle ofhumanorigins. see also Harpendingiggo) suggestthat a numberoffacThamesand Hudson. hidden heterogeneity, Chimpanzee politics:Powerand sex among tors including nonstationarity, WAAL, F. DE. I989. Press. differential and selective mortality HopkinsUniversity Johns can bias the apes. Baltimore: frailty,

ter, SontzI97I; Gallagher and I977, I979) I977; Hayden

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sample ofskeletonsin a cemetery, makingit an unrepre- so the low rates of hypoplasia in prehistoricforagers sentativesample of a once-livingpeople and rendering should not be surprising. Tuberculosis and relateddisconclusions about the impact of economic change on eases occurprimarily archaeologicalsamples from in rehuman health unreliable. The points that they raise cent,relatively urbanenvironments, the mimicking patseem theoretically be valid, and I note that theyare tern of the disease of the present day (Cohen I989). to discussed positivelyby a number of my colleagues in Goodman (I993) has pointedout, also, that enamel hyskeletal analysis with reference the analysis of indi- poplasia, one of the few skeletal pathologies that can to vidual populations (see CA* comments). However, readilybe seen in livingindividuals, has repeatedly been theirtheoreticalarguments a lead them to offer reinter- foundto occur among livingpeople in the patternthat pretation health trendsassociated with the originsof our hypothesispredicts-it is regularly of more common agriculture a and which,from broadgeographic temporal in lower-class than in upper-class individuals, sugI perspective, finduntenableand refutable. gesting thatit reflects relativestressrather thanrelative Wood et al. begin by concedingthat Armelagosand I background nutrition resilience.Can it reallybe mere or maybe correct our interpretation the consequences coincidence that our directexplanation of paleopathoin of of early farming, but they argue that other interpreta- logical data fitsso well with these expectations? tions of the skeletal material are equally possible (and it Furthermore, is arguableat best whethernutrition equally difficult prove or disprove).They argue, in and healthimproved to withfarming sedentismamong and that the apparentincrease in pathologyas- prehistoric populations as Wood et al. assume or particular, sociated with early farming populations in fact could whethersurvivorship was significantly in greater early reflectan improvementin health. They suggest that agriculturalgroups than in hunter-gatherers. Optimal farmingpopulations may normally have been better- foraging data (reviewedin Cohen I989; see also Simms nourished and longer-lived than their hunting-and- I987, Russell i988) suggest that prehistorichuntergatheringforebears and thus better able to record gatherers were in a positionof descendingto agriculture stresses in their skeletons. By this interpretation, the as once-superior economic strategieshad to be abanfrequency infection(or otherpathology)did not in- doned (see, in particular, of Russell's description the efof crease with farming, its recordwas more fullypre- ficiencyof harvesting but wild and then domestic einkorn servedin the skeletons of better-nourished, more resil- wheat). Hunter-gatherers should typically have had betient,longer-lived farming populations.The skeletonsof ter backgroundnutrition(as well as fewerbackground foragers were relativelypathology-free because the infections) not thanfarmers and should normally have been foragers were healthybut because they died of insults the more resilienteven thoughthe stressesof mobility beforetheir skeletons could record them. Using this itselfmighthave workedagainstthem. logic,Wood et al. producea reevaluationofthe Dickson The perspective Wood et al. maybe affected their of by Mounds archaeologicalsequence spanningthe adoption (and our)familiarity with the !KungSan ofthe Kalahari, and intensification agriculture Illinois. They sug- whose caloric intake is marginal(at the low end of the of in gestthatlow averageages at death and highfrequencies modernhunter-gatherer spectrum and undoubtedly well of dental enamel hypoplasiain the latest,fullyagricul- below that of prehistorichunter-gatherers Cohen [see turalpopulation,previously read as a recordofdeclining i989]1)and who gain weight and resilience when they healthand longevity (Goodman et al. i984), mightactu- settle down under 2oth-century conditionswith 2othally be indicative of increased fertility and biological century benefits(Pennington i992). Under these condiprivilege. tions theyattain a success at rearing theirchildren that I respectfully disagree.Various typesof evidence sug- shouldimplypopulationgrowth ratesgreater thanthose gest that ours is the more probable interpretation. For displayedby eitherprehistoric hunter-gatherers preor one thing,the conclusions frompaleopathology,as I historicfarmers-so theiruse as an ethnographic analhave interpreted conformso closely to observations ogyforprehistory it, may be limited. ofhealth fromethnography predictions and fromepideIn general, populations settling down under 2oththat theyshould be taken as theyap- century miological theory conditionsoftendisplayeitherincreasedfertilpear. For example, epidemiological theorypredictsan ity or increasedsurvivorship both. However,neither or increase in infectionand parasiterates with sedentism can have occurredto any significant degreewith the beand largergroup size, supporting the directinterpreta- ginningof the Neolithic, as I will show. Perhapsmore tion ofthis pattern pathology the skeletons.More- to the point,neitherfertility survivorship have of in nor can over, the patternof increasinginfectionand parasites changed very much at the Neolithic transitionunless withgroupsize and sedentismoccursrepeatedly com- the two changed in opposite directions.The best estiin parisons of historical and modern populations (Cohen mates typicallysuggestthat the rate of growthforour i989). Similarly, modernhunter-gatherers display very species as a whole acceleratedfroman averageof about low rates of juvenile infection, and ane- o.oi% per year beforethe adoption of farming only malnutrition, to mia, just as theirprehistoric counterparts display low about o.i% after it (see, e.g., Hassan I98I, Bentley, rates of porotichyperostosis (see also Kent and Dunn's Goldberg,and JasienskaI993). Even if we assume that in [I993] discussion of hypoferremia newly settledSan thisentireacceleration resultedfrom increasedsurvivorin the Kalahari). Contemporary hunter-gatherers also ship with no contribution from increasedfertility, there display relatively low rates of weanling diarrhea, simplywas not enough of an improvement survivorin thought be a major contributor enamel hypoplasia, ship on the averageto accountforthe increasein visible to to

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pathology.For the !Kung San, forexample, an increase selectionforcolor in any one generation may be rather from44% to 45% of individualssurviving the mean small. to would suffice explainthe accelerated to In fact,the sample of deaths in a populationwill alage ofmaternity Neolithic growthrate of O.I%, but it alone could not ways include both a selected and a randomcomponent. explain the apparentincrease in pathologyamong early I suggestthat under most circumstancesthe effects of minorstatistifarmers-especiallybecause both ethnographic compar- selectionwill show up only as relatively isons and some paleodemographiclife tables suggest cal currentsagainst the backgroundof competingfacthatfertility often increasedwithfarming, further reduc- tors.I submitthat,except underveryextremeselective ing any possible averageNeolithic increasein survivor- conditions,the actual death cohortfora populationfor ship (Cohen I989, Buikstra,Konigsberg, Bullington any yearwill normally a fairly of and be good representation I986, Wood et al.) the living population fromwhich it came because of Further,prehistoric farmers also commonly have the randomnature of the unselected deaths,with only higher rates of dental caries than hunter-gatherers.a small bias foreach of various slightselective advanShould we conclude, as almost all scholarsdo, that the tages. In particular,most human deaths are probably farmers' diet was more cariogenicthan that of hunter- onlyweaklyrelatedto the chronicillnesses thathuman or gatherers, should we conclude that hunter-gatherersskeletons display (or those pathologies make only a normallyalso suffered died ofacute cariogenesis but be- small percentagecontribution the probability dyto of foretheirteeth had had the chance to develop lesions ing),and skeletonsmay therefore a relatively random be while farmers lived long enoughto develop caries?Con- sample with regardto visible skeletal pathologyin the versely,some prehistoric hunter-gatherers have greater population.(In fact,accidentsand zoonotic diseases [see skeletal robusticity and more arthritis than farmers. Is Fiennes I978], significant causes ofdeathamonghunterthis simply because the hunter-gatherers lived long gatherers and earlyfarmers which tend to strikeactive and arthritis farmers adults, would arguablykill those who were otherwise but enough to develop robusticity did not? We can reconcile these two contradictory pat- the most fitand the least frail).In specificinstances,of ternsonly by recognizing that each pathologyis telling course,severe selection or randomstatisticaldeparture us somethingof its own characterand the lifestyleof fromexpectedfrequencies("drift")may make any one its victimsby its patternin the skeletons.I submitthat skeletalsample a misleadingsample ofthe parentpopucaries and arthritis also chronicafflictions peri- lation. I protectmyselffromthis possibilityby using and like ostitisand porotichyperostosis should be interpreted as only trendsthat occur repeatedlyin different populadiseases whose skeletal pathologyis fairlystraightfor-tions. ward. Diseases like measles, which are known to kill One possible application of this reasoning is the withoutscarring skeleton,will unquestionably the have change in staturefromthe Paleolithic to the Neolithic to be dealt with in a different manner. the throughout Old World.If we considerthat only seaffects distribution heightsin the the of Perhaps we can resolve our differences pointing lectedmortality by out thatheterogeneity, differential and frailty, selective cemeteries,then, as Wood et al. claim, the declining mortality, althoughreal, do not play quantitatively as stature of Neolithic populations might representthe a of important selective role in the creation of cemetery overallgood healthand nutrition the populationfrom which they come. However, if we allow that a signifisamples as Wood et al. imply. If the individuals in a population were completely cant portionof the dead represent randomdeaths (with equal in their risk of dying fromall causes (or if all regardto stature),as they certainlymust, the implicaa causes of death were strictly accidental),we would ex- tion is thatthe Neolithic skeletonsrepresent universe a presumably population pect a death cohort or a cemeteryfull of such cohorts ofsmallerpeople and therefore to be a randomand usually representative sample ofthe with decliningnutrition-which is of course what the data suggestwe should find. living group,as the our hypothesisassumes. As Wood optimalforaging discussion, et al. point out, however,populationsare in realityhetAlthoughthereis ample room forfurther erogeneousin variousways; individualsare not at equal I suggestthat fornow, on the whole, the conclusions risk of dyingfromeach cause, and death is selective. of Cohen (i989) and Cohen and Armelagos (i984) can But,as is truewhen we studynaturalselectionand evo- stand. and lution,thatotherdomain ofdifferential frailty selecnot tive mortality, all or even most deaths are necessarily selected,nor are theyall selected forthe one traitor condition under consideration.For example, even in Reply thatfamousmodel of naturalselection,the British peppered moth whose color evolved to match the treeof trunks, presumably only a fraction the moths are ac- JAMES W. WOOD AND GEORGE R. MILNER PennsylvaniaState tually eaten or spared because of their wing color. DepartmentofAnthropology, University Park, Pa. I6802, U.S.A. 8 viii Otherspresumablyare eaten or escape being eaten de- University, spite theircolor-get caughton the wing,hit the wind- 94 screensoffast-moving trucks, too close to hot lights, fly in get steppedon, starveto death,or suffocate the smog Severalresponsesto our paperon "The OsteologicalParin that is darkening trees.The visible effect natural adox" (CA 33:343-70) have now appeared CURRENT the of

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and this may be a good time to reply of death by cardiovasculardisease. Because of selective to them all.' The commentators evenlydividedbe- mortality, are this one now-shattered vessel of clay, this tween those who heartilyloathed the paper and those kickerofbuckets,tells us littleabout the threeindividuwho basically liked it but wanted to make additional als who did not die. And this sortof selectivemortality points or to suggestways of tacklingsome of the prob- must occur whenever(i) individualsdiffer theirbioin lems we discussed. Since our intentionwas to spark logical (or even "lifestyle")characteristics (2) those and debate,we welcome all the comments,even those ac- characteristics bear some relationship the likelihood to cusing us of scientificsnobbery, nihilism, and aiding of death. Despite Cohen's assertionthat deaths are esand abettingsinisterpro-state, forces- sentiallyrandom,we suggest(and we are by no means pro-civilization although how we can be both nihilist and pro-civ- thefirst do so) thatthesetwo conditionsare universal to ilization is somethingof a mystery us. to in human populations. Our paperhighlighted severalproblemsthat can conThis example allows us to lay to rest one point of foundinferences drawnfromskeletal samples about the confusionin Goodman's comment(see his n. 7). Goodhealth of prehistoric populations.These difficulties are man equates the words "biological" and "genetic" in a now widelyrecognized epidemiology demography way thatwe do not. Surelyone's serumcholesterol in and level but have received insufficient attentionin researchon is a biological characteristic. Yet our friendwith the skeletons fromarchaeological sites. As Goodman (CA clogged arteriesmay have had elevated serum choles34:28i-88) and Saunders and Hoppa (I993) point out, terol because he had familial hypercholesterolemia (a and indeed as we pointed out ourselves, osteologists geneticcondition)or because he habituallyate fried egg have long acknowledged that they deal with samples sandwiches with pork drippings threetimes a day (the made up of life's failuresat any particular age. But con- ever-popular Elvis Diet). In eithercase, elevated serum traryto Goodman we see only limited progressbeing cholesterol a frailty is and factor, selectivemortality will made in the development formal of methodsforbuilding act upon it. Ifserumcholesterolis at least partially herithis insightinto the interpretation skeletal lesions. table (as, in fact,it is), then selective mortality the of in Ifproblemsof inference and interpretation have proven demographic sense will also constitute naturalselection for researchersworking with living popula- in the genetic sense. But demographicselectivitycan difficult tions,we cannotimaginethattheycan be any easier for occur in the complete absence of naturalselection. those dealing with bones dug up fromcemeteries. There are otherlessons to be drawnfrom thisparable. Most of the problemswe discussed in our paperstem The factis, the miserablecorpse at our feetdid not die fromheterogeneous frailty and selective mortality, the in childhoodfromdiphtheria, typhus,or smallpox,and effects which can be illustratedwith a he certainly not die frommarasmusprecipitated of confounding did by homelyparable. Suppose that one of the fourauthorsof weanling diarrhea.Thus, the fact that cardiovascular ouroriginal paperhas grossly elevatedserumcholesterol disease is responsibleforsuch a highfraction the obof levels, while the otherthreeare normal,at least in that serveddeaths(ioo% in our sample so far) partly is attribrespect.In thepopulationat large,serumcholesterol has utable to the comparativeunimportanceof other disa measurable,monotonic association with the risk of eases in the population-the paradox of proportional deathfrom heartdisease. Thus, an individual's mortality. coronary And the multipleischemic scars on his nowserumcholesterollevel can be considereda component stilledheartsuggestthathe lived underconditionsthat of frailty, and our tinypopulation of coauthorsis het- permitted him to survivewithhis disease fora considererogeneous for frailty.Now suppose that our high- able period beforethe fatal heart attack that lefthim cholesterolcolleague keels over dead one day on dis- piningforthefjords. Indeed,had he died not from heart a covering that he has been labeled a pro-civilization, attack but fromchronic congestiveheart failure-had snob in a majorjournal.An autopsy he not perused the pages of CURRENT ANTHROPOLOGY nihilistic,scientific reveals that this ill-starredanthropologistsuffered thatsore and dreadful a morn-he would have leftbehind fromthe plugging of a heartin really terribleshape, and that hideous lump myocardialinfarction resulting up his coronary arteries by atheroscleroticplaques, no of myocardialtissue would have been a sign,in all its doubt aggravatedby the arterialconstrictionthat can ugliness, that he had managed to live successfullyfor accompanyacute psychologicalstress.In addition,mul- manyyearsdespitehis illness. The worse the condition tiple ischemic lesions are found on his heart,signs of of the heart,the longerthe inferred survival-a kind of past cardiac "events." We now have a mortality sample myocardialparadox. on our hands, albeit a small one. What can we infer This example can be criticized,most obviously beabout the health status of the living population that cause the sample is ludicrouslysmall but moreinterestlaunched this lost soul on his journeyacross the Styx? inglybecause the otherthreecoauthorswill eventually Obviously not much, except that it contained at least die, and we will thenhave an opportunity bringtheir to one individual who was apparently an elevated risk blightedcarcasses under the pathologist'sknife.That, at one mightthink, would providean unbiasedview ofthe entirepopulation.But each and everydeathwill misrepi. Although response written only this is twooftheoriginal resentthe remaining by distribution frailty among the livthe two it. coauthors, other haveread endorsed Anadditional and ing at whateverage the death occurs-except, ofcourse, on issues article raised our in paper appeared the has in focusing the forthe verylast death,forthat particular Yearbookof PhysicalAnthropology (Saunders coauthorwill and Hoppa I993).
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Volume 35, Number 5, December I994 1633 be perfectly of representative himself.Acquired conditions,includingthose associated with aging,will partly regeneratethe upper tail of the frailtydistribution so amongthe survivors, that selectivemortality will always producecorpsesthatlook terrible, matter no what the generalhealth of the population.The factthat one in fiveAmericanswill eventuallydie ofcancerdoes not mean that 2o% of living Americans have cancer right now. Byers(CA 35:282-84) makes an interesting point in this connection.He suggeststhat it may be possible to assess the magnitudeof the selective mortality acting on a trait such as stature by examining shiftsin the distribution the trait among individuals who die at of later(presumably postselection)ages. The specifictests he advocates,however,are lacking in statisticalpower, as he is carefulto point out; they also make a strong presumption thatthetraitofinterest normally is distributed at the outsetofthe selectionprocess,forotherwise measuresof skew and kurtosisby themselvesare uninformative about selection. An assumptionof normality may be approximately correct staturebut is unlikely for to hold formanyfrailty factors (see Schork,Welder,and Schorkiggo). Still,Byers'sbasic idea is sound. Here we sketchan alternative approachto the same problem,an approachthatmay be both moregeneraland morepowerful.If z is a frailty factor,be it statureor whatever, of then.theconditionaldistribution z among survivors at age t (i.e., among those whose life span T is greater than t) is f(zl T > t)
=

f(z)S(tl z)/ ff(z)S(tlz)dz,

of wheref(z) is the densityfunction frailty the outset at of the selection process and S(tj z) is the survivalfunction conditionalon z. Given appropriate specifications of f(z) and S(tj z), the equation could be fittedto data on skeletal samples by straightforward maximumlikelihoodmethods,thus providing directestimateof a the effect selective mortality the trait.Of course, of on fora trait that changes with age, as does stature,we would have to rescale the f(zI T > t) function properly, perhapsby using the residuals fromone of the PreeceBaines model growthcurves ratherthan raw statureitself(see Preece and Baines I978). But thatis a secondary point. We believe that Byers'ssuggestionhas considerable merit and deserves further exploration.Incidentally,the equation tells us explicitlywhat we have to worryabout in this whole area of inquiry:how frailty affects mortalvaries,indicatedby f(z), and how frailty ity,capturedby S(tj z). The deeperproblem,alluded to in our paper,is what to do when we don't have a readilymeasurablefrailty factorsuch as statureor when measurablevariablesdo not capture all the variationin frailty. we tried to As convey in our paper, this is a tough nut but not, we think,an uncrackableone (see the extendeddiscussion in Wood et al. i992). But it can't be crackedby ignoring thatit doesn't matter it, wishingit away, or pretending in the populationof interest.

Pretending thatit doesn'tmatter precisely is what Cohis inhen (above) triesto do. As he remarks, preferred of terpretation the paleodemographicand paleopathological evidence "makes the implicit assumption that at skeletonsin a cemetery, least on the average,are reaof sonably representative the living populations that produced them and therefore that changes in skeletal assemblages reflectreal changes in the health of oncelivingpopulations.This is an assumptionmade implicitly or explicitly,with varyingdegrees of caution, by most quantitativelyorientedpaleopathologists."That was preciselythe point of our paper: paleopathologists do make this assumption,oftenwithoutexaminingits implicationsfortheirinferences. But accordingto Cohen, the assumptionthat the dead are representative of the livingis justifiable because mortality largelyranis dom with respectto individual characteristics: sub"I mit that, except under very extreme selective conditions, the actual death cohortfora population forany year will normallybe a fairlygood representation of the living population fromwhich it came because of the randomnature of the unselected deaths." Frankly, we don't know whetherto be terrified relieved by or this conclusion-terrifiedbecause even the healthiest for among us can drop dead tomorrow no good reason, relieved because we can all stop worrying about diet, exercise,and those annoyingannual check-ups.We respectfully suggestthat Cohen's assertionthatmortality is mostlyrandom(nonselective) with respectto individual characteristics one of the most remarkable is statements in the historyof population science. If it is true, epidemiologists may as well retire, no relativerisk for will ever be distinguishable fromi. And demographers well close down shop too: life tables are uncan pretty cannot be affected necessarybecause mortality significantlyby age, and sex-specific tables are even more life of a waste of time because they foolishlyassume that one's sex may influencethe risk of death. The claim that mortality largelyrandomand nonselectiveis so is profoundin its implications that it needs to be supportedby evidence, not merelyasserted.Afterall, the entireinsuranceindustry foundedon the premisethat is the risk of death varies among individuals in a potentiallypredictableway. But we agreewith Cohen that mortality stochashas eletic (random)as well as deterministic (nonrandom) ments.In fact,severalofus have spentmajorportionsof lives formulating models our professional demographic that include both stochastic and deterministic components (fora review,see Wood et al. i992). With respect such models are consistentin showingthe to mortality, followingpattern:Within a given risk group,the variance in life span is typicallylarge,and in that narrow sense therandomcomponentofmortality be considcan discuseredimportant (see Vaupel I988 foran insightful sion of this point). When risk groupsare pooled, howat ever,mortality any given age will still be dominated to bythoseindividualsofhighestriskwho survived that age (Manton,Stallard,and Vaupel i986). In otherwords, and epidemiologicalmodels make it clear demographic

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that substantial selective mortalitycan occur even in signs of debilitatinginjuries or active infectionsthat the face of nontrivialstochasticvariationin life span.2 would have reducedany chance theymighthave had to Cohen's claim thatmortality was largely nonselective fightor flee successfully.In this particularprehistoric in prehistoric societies appearsto be based on his belief setting, then,violentdeathwas not unrelatedto an indithat most deaths in such societies were accidental. vidual's age, priorlife history, current or health status. While reliable data on causes of death are notoriously In otherwords,even accidentsand violence can be selecdifficult obtain fromnonliterate to people, such data as tive on individualcharacteristics. exist suggestthat the overwhelming thatthere Jackes(CA 34:434-39) notes,quite rightly, majorityof deaths in all preindustrial populationsare infectious nature, are many serious problemsthatwe did not highlight in in with undernutritionbeing a frequent contributary our original paper, including but not limited to agecause. In our workwith the Gainj, a populationof swid- estimationand differential preservation. However,as we den horticulturalists the northern on fringes Papua pointedout, those issues have receivedfarmore attenof New Guinea's Central Highlands,we foundthat about tion in the literaturethan the ones we did raise.3But 70% of deaths were frominfectiouscauses, with diar- that does not mean that the issues we deemphasized rhealdisease beingmore common in childrenand acute have all been settled. As long as we are enumerating respiratoryinfections somewhat more common in additionalproblemsto worry about,we would mention adults; physicaltraumaaccountedforonly about 2% of threemore, without,however,meaning to imply that deaths (Wood ig80:i22). Broadlysimilar patternshave this is an exhaustive list. First,as many osteologists been reportedfor the !Kung (Howell I979:69) and the have noted, the disease processes that can leave obAka Pygmies(Hewlett,van de Koppel, and van de Kop- servable skeletal lesions representonly a tinyfraction pel i986:54-55). Infectiousdiseases are known to be of all the afflictions likely to be presentin the living highlyselective, especially with respectto nutritional population; focusingon them will almost necessarily status and immune function. a studyof the Turkana give a highlydistorted In view ofoverallhealthand disease ofnorthern Kenya,one of the most traditional groupsof in the population. The second problem is differential nomadic pastoralistsin the world,Shell-Duncan (I993, diagnosis-the difficulty assigninga skeletal lesion of importanceof gas- unambiguouslyto a particularcause; because of errors I994) has shown the overwhelming trointestinaland respiratorytract infections in de- in differentiating diseases, skeletal lesions are oftenof terminingpatterns of morbidityand mortality(with low specificity diagnosticmarkers. as The third problem malaria running a somewhat distant third); more is that skeletal lesions usually occur only in rare,often she important, has shown thatthese diseases are power- extreme,cases of the diseases that produce them; as a fullyselectiveon nutritional as statusand immunocompe- result,such lesions are of low sensitivity markersof tence as assessed by delayed-type statisticalmethtests. disease. As it happens,thereare formal hypersensitivity In none ofthese studies or any othersthatwe are aware ods forassessingboth specificity sensitivity and (Kelsey, of have accidents been shown to be a leading cause of Thompson, and Evans i986:286). If such assessments death. It is all verywell forCohen to dismiss evidence were done,we suspect thatmost skeletal lesions would on the !Kungfromthe discussion,but the factremains proveto be poor diagnosticmarkers. thatthereare veryfew studies of anthropological A superficial readingof our paper mightsuggestthat populations that have yielded high-quality information on we are being inconsistenton this point. Some of the causes of death, and none of them indicates that acci- timewe seem to be sayingthatmortality samples overdentspredominate. Perhapspeople were clumsierin pre- estimate the prevalenceof pathologicalconditions(bebut history, we doubt it. cause of selective mortality), and some of the time we Besides, there is no reason to believe that accidents seem to be sayingthatmortality samples underestimate are genuinelyrandom: "accident-proneness" a well- the prevalence of pathological conditions (because of is established epidemiologicalphenomenon.Nor can we low sensitivity).What we are actually saying is that assume that violent deaths as opposed to those from both biases are likely to be operatingsimultaneously, illness or any of the othervicissitudes of life are ran- and both make it difficult us to link lesion frequenfor domly distributed. The selectivityof violence can be cies in skeletons with disease prevalencein the living seen even in one of the veryfewosteologicalsamples in which a fairly largefraction least i 6%) ofindividuals 3. Infact, (at biases from ofbones arising thedifferential preservation died from beinghit with clubs or shot with arrows(Mil- in archaeological were deposits noted leasttwocenturies at ago. in in a mound Virginia thei 8th Thomas ner,Anderson,and Smith i99i). In this skeletal collec- Ondigging century, Jefferthat beingsoft, they tion from a cemetery geographicallyand temporally son (I788:io5) reflected "thebonesofinfants be whichmight thecauseso few probably decaysooner, werefound close to Dickson Mounds, most of the people who had here."Observations the differential on of preservation softtissue been slaughtered were adults,presumably because their are even older.WhenHamletasked the gravemaker, "How long daily activities put them at greaterrisk of being at- will a man lie i'th'earth he rot?"he was told: "Faith,if 'a be ere before die-as we have manypockycorpses 'a now-atacked. Furthermore, many of these skeletons showed not rotten
2. Foroutstanding reviews therelevant of models, Manton see and Stallard(i984: chap. 6; i988), Mode (i985: chaps. 3 and 4), and Namboodiri (I99I: chap. 9).

in-'a willlastyousomeeight daysthatwill scarceholdthelaying will last you nineyear"(Act 5, Scene yearor nineyear.A tanner and antiquarian allusionsare i). We onlyhope thattheseliterary nottoo pro-civilization some ofourreaders' for tastes(cf.Cohen, CA 33:359).

Volume 35, Number 5, December 994 1635 population in any straightforward way. Although the necessarytheoryand compile the necessaryevidence; two biases operate in opposite directions,it would be bald assertions and appeals to conventional wisdom foolish to assume that they must exactly cancel each won't take us veryfarin the rightdirection. ReadersofGoodman's commentsmightconcludethat otherout forany disease. In our view, a far more serious block to inference, we somehow missed the factthatskeletallesions attriband malnutrition take some time to which none of our criticsaddresses,is the factthat le- utable to infection sion frequenciesin the dead partlyreflect proportional develop,thatpeople oftenlive with those conditionsfor which in turnreflects whole spectrum of extendedperiods, and that some fractionof them remortality, the conditionsaffecting riskofdeath,not just those that coverfrom the theirillness. Yet it is preciselythisvariation caused the particularlesion or lesions in question.This in experiencethat makes the interpretation skeletal of is problem not solved byusingGoodman's (p. 28 I) "mul- lesions in mortality samples such a vexingtopic-and, tipleindicators health,"because the fullset oflesions if exploredfurther, of such a potentially enlightening one. potentiallydetectable in the skeleton still represents While it goes without sayingthat Goodman (p. 282) is only a small portionof that spectrum.Moreover,selec- correctwhen he writes that thereare many reasons to tive mortalitymay be operatingon all the indicators investigatethe "cultural and social repercussions"of disease,it is difficult see how morbidity mortality to simultaneously, and to differing degrees. and According Goodman (p. 282), "Wood et al. miss the can be disassociated fromone anotherin studies based to mark in theirexplication of the dynamicsof selective strictly individualsof a particularage who failed to on mortality partlybecause theyare committedto the no- survive.Afterall, the ability to live with a condition tionthatthe goal ofpaleoepidemiology understanding causing a pathologicalbonyresponseor to recoverfrom is cause of death. Paleoepidemiologistsare in factseldom it,perhapswith an impairedabilityto withstand further concerned withcause-of-death analysis,whichis exceed- illness,does not implythat the presenceof these skeleinglydifficult a numberofreasonsand is not at all es- tal lesions is not in some way associated with an elefor sentialto sayingsomething abouthealthand adjustment vated risk of death. in past populations." Surelypaleopathologists and espeGoodman makes extendedcriticisms severalof our of cially paleodemographersare very interested indeed illustrative exercises.In doingso, he misses the spiritof in causes of death, at least partof the time. But that is those exercises,which was to illustratepotentialprobbeside the point. If we want to say somethingabout lems and not to hold a mirror to nature.(Havingsaid up health and adjustmenton the basis of skeletal samples, that,we would contend that the assumptionsunderlythenwe have to own up to the factthatwe are looking ingourillustrations no less realisticthanthosemade are at samples of dead people, and presumably theirreason by Goodman, Cohen, and othersin theirmore "final" for dyinghad somethingto do with their health and analyses.) Goodman spends a long time on one espeWe would never draw inferences adjustment. about the cially simple-minded example thatwas merelyintended of distribution healthcharacteristics thegeneralpopu- to introducesome of the problems;but by doing so, he in uncoversone ofthemostfundamental diflationbyexclusivelyexamining hospitalpatients, among inadvertently in whom serious disordersapproach i oo%. Serious disor- ficulties this area ofstudy.In ourexample,we posited dersare even morecommonamongthedead: such disor- threesubgroupswithin a population and assumed that those subgroupswere exposed to low, moderate,and dersare what most ofthemdied of. We cannot stress this point too much. If a skeletal highlevels of "stress,"respectively. Undernot too unrelesion-or the conditionresponsible it, or a traitpre- alistic assumptions,we showed that the high-and lowfor disposingto thatcondition, anothertraithighly or corre- stress groups could display similar lesion frequencies lated with thatcondition-has anyrelationship whatso- and thus be difficult distinguishfromone another to everto the riskof death,the skeletal collectionmust be using skeletal samples alone. But Goodman says that a biased sample for the living population. The bias we willfully ignoredan important piece ofevidence:had caused by selection may be large or small; it may be we examinedthe mortality of patterns the threegroups, it positive or negative;but mathematically must exist. theywould have fallen out fromeach otherunambigWe would be more than happyto discoverthatthe bias uously. This claim is unassailable-provided that we is consistently small and, hence, untroubling, Saun- know beforehand as how many subgroupsthere are, are ders and Hoppa (I993) suggestfor the special case of able to assign skeletonsto the subgroups withouterror, But stature.4 at present, have neithertheory we nor em- and can reliablyreconstruct the mortalitypatternsof pirical evidence showing that the bias can always be the subgroups.Otherwisewe are presented with an unignored.It will take a lot of hard work to develop the known number of risk groups,each of unknown size, whose apparentpooled age-at-death distribution conis foundedby heterogeneous and nonfrailty demographic thatthelinkage between short stature 4. Goodman(p. 283) argues Alas, we fear that osteological samples to theconfounding stationarity. and theriskofdeathis partly spurious, owing and of effects "thecausal linkofbothwithimpoverished stressful more oftenapproximate the latterset of circumstances our reinforces basic than the former. Of conditions." courseit is, andthisfact living thatdirectly is point:mortality selectivenot onlyforconditions In his responseto our alternativeexplanationforthe socioeconomic traits cause deathbut also foranyother (including Dickson Mounds findings, Goodman criticizesthe aswith such condicorrelated that characteristics) are consistently sumptions of our model, dismissingmany of them as the tions,whatever sourceofcorrelation.

636 1CURRENT

ANTHROPOLOGY

maize was a late additionto diets alreadybased in large parton severalcultigens(see Smith I989). To date,only a fewDickson Mounds skeletonshave been analyzedfor stable carbon isotopes-an indication of maize conthe sumption-but skeletonsfrom throughout cemetery sequence yield figuresthat fall within the late prehistoric,or agriculturalist, rangeforeasternNorthAmerica

M. I984. "Paleopathology Peruvian in and Chilean in populations," Paleopathology theorigins agriculture. at of tion and intensification agriculture," use Cohen's of to EditedbyM. Cohen and G. Armelagos, 5I5-29. New York: pp. phrase.The full course of changes in diets and lifeways AcademicPress. relatedto an increasedreliance on cultivationactually ARMELAGOS, G. j. I990. "Health and diseasein prehistoric populationsin transition," Disease in populations transition. in in spanned a much longerperiod than the few centuries EditedbyA. Swedlund and G. Armelagos, I27-44. New pp. when the Dickson Mounds burialgroundwas used, and York:Bergin Garvey. and

unrealistic. While the reasonableness of our assumpto the tionsis difficult assess from osteologicalevidence Dickson Mounds (as Jackes rightly so emavailable from phasizes), this criticismagain misses the point of the exercise. Given the time, energy,and inclination,we suspectthatwe could come up witha much morerealisfor tic model (involving, example, more than two subgroups or continuously distributedfrailty).But that would not alterour fundamental point:we can interpret the osteological recordmeaningfully only if we do indeed have an explicit model for the formation the of mortality sample we are workingwith. As we said repeatedlyin our paper,the pointis not thatour model is right and othermodels are wrongbut thatmodels are in factnecessaryand forthe most partlacking. It is clear fromhis very firstsentence (p. 28I) that Goodman misunderstandsour position: we emphatifrom cally do not arguethat "health inferences paleodemographicand paleopathological data are impossible" are but merelysuggestthat such inferences more difficult thanwe all originally believed,and also moreinteresting.We are convincedthatthereare solutionsto the problemswe raised, but findingthe solutions will require some deep thinkingabout the processes linking frailty, stress,disease, tissue responses,and the formation of mortalitysamples. It will also require formal modelingofthoseprocesses.As Goodman (p. 282) notes, of "There is ... a mathematicaltethering individualand if group frailty; group frailty changes, then either the of size ofsubgroups the frailty one or moresubgroups or must change. Furthermore, can begin to interpret one if of the individualsignificance aggregate frailty one has and some idea a theoryabout the distribution frailty of of how groupsmightchangein size and how exposures contexmightchangesubgroups'healthrisks-in short, in written crititual information." Althoughapparently cism ofus, this is in factpreciselyour position.Indeed, if one adds the further stipulationthatwe need models ofthe linkagebetweenfrailty the riskofdeath,then and Goodman's statementsummarizesour view admirably. We are pleased thatGoodman underscores importhe tance of "culturalcontext"in the interpretation skelof etons fromcemeteries;in doing so, he again reiterates our position as expressed in the original paper. It is strange,however,that the Dickson Mounds skeletons continue to be misperceivedby Goodman and others (Goodman et al. I984; Goodman and Armelagos I985;

previouscharacterizations the Dickson Mounds samof ple, it does not encompass the fullspectrumof changes fromhunting-gathering through intensified agriculture. It is likewise difficult arguefrom available archaeto the ological evidencethatthelatestDickson Mounds people the of were sick because theysuffered ill effects an outflowoffoodto otherplaces (Goodmanet al. I984, Goodman and Armelagos I985). At present,it is simplynot clear what the changes over time in skeletal lesion frequencies observedat Dickson Mounds mightmean and what mighthave caused them. In general,both Cohen and Goodman seem to want to cast us as irredeemably opposedto the scientific positionstheyhave stakedout. This reactionis as surprising as it is unwarranted.As we took pains to say, "It is of important emphasize that our reinterpretation the to is healthconsequences ofearlyagriculture not necessarily more correctthan previousinterpretations. And, indeed, we suspect that both interpretations may be correct for different periods and locations. The point, however,is not that we are rightand otherauthorsare wrongbut thatthe data [bythemselves,i.e., unaided by models] supportboth interpretations equally well" (CA 33:357). Cohen and Goodman also tryto make us sound more pessimisticthan we actually are. We believe that advances can be made, but we reiterate thata necessary for of precondition advancementis the development statistical models forthe formation mortality of samples. Althoughwe do not underestimatethe difficulties of this work, we do not think they are insurmountable. And we are pleased to acknowledgethat the work has to alreadybegun, thanks in part (we are gratified say) to our paper. Byers'sidea on measuringselectivity, for as example, is a nice step in the rightdirection, is the more extendedanalysis of Saunders and Hoppa (I993). While neitherof these analyses can be consideredthe finalword on the subject,both at least show what can be done if the issues are taken seriously.Jackes's (p. 435) trenchant comment is relevant here: "Despair should arise only if osteologistsare not intellectually honest and able to withstand a reappraisal of their methods."

and (Buikstra Milner I992). Thus, despite I99I, Buikstra

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