human adaptation to the control of fire

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Human Adaptation to the Control of Fire

RICHARD WRANGHAM AND RACHEL CARMODY

Charles Darwin attributed human evolutionary success to three traits. Our

social habits and anatomy were important, he said, but the critical feature was

our intelligence, because it led to so much else, including such traits as lan-

guage, weapons, tools, boats, and the control of fire. Among these, he opined,

the control of fire was probably the greatest ever [discovery] made by man,

excepting language.1:48 Despite this early suggestion that the control of fire

was even more important than tool use for human success, recent anthropolo-

gists have made only sporadic efforts to assess its evolutionary significance.2,3

Here we use recent developments in understanding the role of cooked food in

human diets to support the spirit of Darwins offhand remark. We first consider

the role of fire in increasing the net caloric value of cooked foods compared to

raw foods, and hence in accounting for the unique pattern of human digestion.

We then review the compelling evidence that humans are biologically adapted to

diets that include cooked food, and that humans have a long evolutionary history

of an obligate dependence on fire. Accordingly, we end by considering the influ-

ence of fire on various aspects of human biology. We pay particular attention to

life history, and also briefly discuss effects on anatomy, behavior, and cognition.

Foraging serves multiple purposes,including obtaining amino acids,

vitamins, and minerals, but energygain is consistently found to be themost important criterion for animal

foraging decisions because maximi-zation of energy gain tends to havedirect consequences for fitness.4 Thisassumption has been validated bynumerous studies of primates show-ing that even small increases in netenergy gain lead to increases infemale reproductive rate and/or off-spring survival, such as in humans,5

chimpanzees,6 and baboons.7

An obvious implication from opti-mal foraging theory is that, like dietchoice, patch choice, and foragingtime, methods of processing foodshould be designed to maximize

energy gain. Among humans, thepredominant form of food processingis cooking, which has long been knownto be a cultural universal that demandstime, energy, and care (Fig. 1). Yetwhen Levi-Strauss8 hypothesized thatcooking has no significant biologicaleffects, no one objected to his idea.Only in the last decade has abundantevidence emerged that cooking consis-

tently increases the energy obtainablefrom most foods.

Two kinds of evidence are particu-

larly informative, though research onboth is still at an early stage. First,

body weight data show that humans

who eat cooked diets have a more

positive energy balance than do thosewho eat raw diets.9 In the most exten-

sive study, a cross-sectional survey of

513 long-term raw-foodists living in

Germany, Koebnick and colleagues10

found that body mass index wasinversely correlated with both the

proportion of raw food in the diet

and the length of time since adoption

of raw-foodism. All studies of humanraw-foodists, as well as many com-

parisons of domestic or wild animals

that eat cooked versus raw diets, lead

to the same conclusion: The morecooked food in the diet, the greater

the net energy gain.9,11

By studying the effects of cooking

on specific nutrients, in vivo experi-ments have begun to reveal themechanisms underlying the benefi-

cial effects of cooking on energy

availability. Until recently, research-ers generally assumed that raw

nutrients such as starch and proteinare well digested by humans, given

that when humans eat these nutrients

raw, very little to none of the nutrient

reaches the feces in an undigestedform. The inference of 100% digesti-

bility was flawed, however, becausestudies of ileostomy patients show

that both raw starch and raw proteinare only partially digested by thetime they reach the end of thehuman small intestine. After leavingthe ileum and entering the largeintestine, residual nutrients are notdigested by the gut. Instead, they arefermented by intestinal microbes,which consume a proportion of theresulting energy. The proportion ofenergy used by the microflora isunavailable to humans; that fraction

ARTICLES

Richard Wrangham is a professor in the Department of Human Evolutionary Biology at Harvard

University. Since 1987 he has directed a study of chimpanzee behavioral ecology in KibaleNational Park, Uganda (current co-director, Martin Muller). He is the author ofCatching Fire: HowCooking Made Us Human (2009, Basic Books). E-mail: [email protected].

Rachel Carmody is a Ph.D. candidate in Human Evolutionary Biology at Harvard University. Herdissertation focuses on the energetic significance of cooking and nonthermal food processing inhuman evolution and related consequences for modern human nutrition.E-mail: [email protected].

Key words: cooking; life history; anatomy; behavior; cognition

VVC 2010 Wiley-Liss, Inc.DOI 10.1002/evan.20275Published online in Wiley Online Library (wileyonlinelibrary.com).

Evolutionary Anthropology 19:187199 (2010)


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of loss to humans ranges from 100%for protein12,13 to an estimated 50%for carbohydrates.14,15 Accordingly,based on the proportion of nutrientdigested by the time it reaches thelarge intestine, cooking appears toincrease digestibility substantially.Current experiments suggest that the

associated caloric gain due toimproved digestibility as a result ofcooking is 12%35% for starches (me-dian 30%: oats, wheat, plantain,potato and green banana), and 45%78% for protein (chicken egg).11 Theenergetic costs of cooking food arecurrently unmeasured, but wouldhave to be very high to negate thesebenefits. For individuals able to obtaintheir food cooked without excessivedifficulty in finding fuel and defendingtheir fireplaces, these effects imply alarge fitness advantage.

Cooking also increases net energygain by reducing the metabolic workdone by humans when digesting.Evidence for this claim comes fromanimal studies. Other things beingequal, rats eating softer food expendless energy in digestion, and aretherefore heavier and more obesethan rats eating harder diets havingthe same number of measured calo-ries.16 Cooking consistently softensplant food,9 and gelatinizes collagen

and therefore reduces the physicalintegrity of meat,17 so that similareffects can be expected as conse-quences of cooking. Although thishypothesis has not been directlytested in mammals, pythons fedcooked meat have been found to ex-perience 12%13% lower costs of

digestion than do pythons fed equiv-alent meals of raw meat.18

Various other mechanisms arepotentially important but have beenless well studied.11 Cooked lipids arelikely to be digested more easily thanare raw lipids because they tend tooffer a greater surface area for diges-tion. Cooking may offer importantbenefits by reducing the energeticcosts of detoxification or immunedefense against pathogens. Cooking alsoallows more dry weight to be ingestedbecause it reduces water content.

Given these energetic benefits ofcooking, in addition to other advan-tages such as making food safer,more accessible, and more appetizing,why do people worldwide ever eatany of their diet raw? Two reasonsappear to be particularly important.First, many fruits are designed to beeaten raw. That is, they are biologi-cally and, in some cases, agriculturallyadapted to be as attractive as possibleto consumers because, as in the case

of wild fruits, consumers disseminateswallowed or expectorated seeds. Theprincipal attractant is most oftensugar, as in apples and grapes. Cook-ing presumably does little to increasethe digestibility of such items.

Second, cooking is sometimesimpractical, particularly when indi-viduals are on trek or foraging. Forexample, Australian aborigines wouldeat a variety of roots, eggs, or animals(such as mangrove worms) raw dur-ing the day, but if they found enoughof the same items to bring back tocamp, they would cook them afterreaching home. Likewise Inuit hunt-ers would rarely attempt to cookwhile foraging, since wood fuel wasin short supply and most cookingrelied on seal-oil burners that

required several hours of use. Inuitmen therefore ate various raw ani-mal foods by day, including cachedfish and caribou. On their return tocamp, however, a cooked eveningmeal was the norm.9

BIOLOGICAL ADAPTATION

TO COOKED FOOD

While most animals, whether wildor domestic, appear to resemblehumans by gaining more energy from

cooked food than from raw food, cur-

rent evidence points to a remarkabledifference between humans and allother species in the ability to thrive onraw food. Every animal species investi-gated to date fares acceptably on rawdiets. Only humans do not. Thus, nocases are known to us of humans liv-ing on raw wild food for more than afew weeks. Raw domesticated foodcan provide a sustaining diet for con-temporary urban raw-foodists, but thefew studies of health status all indicatethat urban raw-foodists are at risk ofchronic energy shortage.

Inadequate energy gain from a rawdiet probably explains a particularlytelling result. Koebnick and col-leagues10 found that most women ona 100% raw diet were sub-fecund:approximately 50% of their subjectswere amenorrheic. Indeed, likeenergy deficiency, the incidence ofamenorrhea varied positively withthe percentage of raw food in thediet and the duration of raw-foodism(Fig. 2). The odds of energy defi-

Figure 1. Baboon being prepared for cooking in a Hadza camp, northern Tanzania. Fol-

lowing a widespread practice, the hunters have laid the prey on the fire in order toremove the hair by singeing. After the hair has gone, they sometimes leave the carcass

on the fire and let it roast in situ. Alternatively, they boil the meat in a pot. Photograph

and information courtesy of Frank W. Marlowe. [Color figure can be viewed in the online

issue, which is available at wileyonlinelibrary.com.]

188 Wrangham and Carmody ARTICLES


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ciency or amenorrhea were notreduced in subjects who ate animalfoods, suggesting that these resultswere driven by the lack of cookingrather than diet composition. It isnotable that reproductive failureoccurred in these women eventhough their urban raw diets hadcritical energetic advantages overraw diets that they hypothetically

might have attempted to consume inthe wild. First, since the urban foodswere primarily domesticates (bothplant and animal), they were likelyhigh in digestible nutrients and lowin indigestible components or toxinscompared to wild raw foods. Second,the urban raw-foodists would have

suffered little seasonal variation infood quality since they obtained foodfrom global sources. Third, raw dietswere extensively processed nonther-mally (for example, in blenders) oreven by drying over low heat. Many

raw-foodists treat foods that havebeen heated below 468C as accepta-ble items. An additional advantageappears to come from the urbanraw-foodists taking less exercise thanforagers do.

The evidence that the averagewoman eating a diet of 100% rawhigh-quality foods is amenorrheicsuggests an important conclusion:Human populations are not adaptedto survive on a diet of raw wild food,

even when it is extensively processedusing nonthermal methods. This isconsistent with the fact that nohuman population has ever beenfound living on raw wild food. Theonly alternative possibility is thathunter-gatherers in the unknownpast were consistently able to findwild raw foods of higher quality thanthose eaten by contemporary urban

raw-foodists. The challenge for thosewho are skeptical about the impor-tance of cooking in human evolutionis therefore to identify such diets.Even though honey, marrow, liver,and some exceptional other kinds ofmeat, fruit, or social insect might, intheory, sustain a population wheneaten raw for a few weeks ormonths, we know of no raw diet thatcould provide predictable year-roundadequacy. Until such a diet has beenidentified, we conclude that humansdiffer from all other species in being

biologically committed to a diet ofcooked food.

This proposal is easily understoodin terms of our current biology. Mostimportantly, the few available meas-urements indicate that the intestinesof humans are small compared tothose of other primates, being about60% of the expected weight/volumefor a species of our body mass.19

More data are needed to assess thevariation in gut dimensions within

species, but current information sug-gests that once our ancestors hadpredictable access to cooked food,there would have been little benefitin retaining a relatively capacious co-lon designed to allow fermentation

of long-chain carbohydrates. Sincegut tissue is energetically expensiveto maintain, selection would havefavored reduction of colonic tissueand other parts of the gut that wereno longer useful for individuals eat-ing a cooked diet.

Human molars are also smallerthan those of other primates.9 Theaction of cooking in reducing foodtoughness suggests that tooth sizereduction is adaptive.20 Other fea-tures of the mouth that have beeninterpreted as evolutionary responses

to cooked foods include reduction ofjaw-muscle myosin, increased salivaryamylase production, and reduced oral

cavity volume.21

Many other adaptations to cookeddiets can be expected. Very little isknown about the comparative enzy-mology of the human and ape diges-tive systems, but the relatively highquality of cooked food suggests thathuman-specific adaptations are likely.Reductions in toxin intake due to thedestructive effect of heat may haveled to increased sensitivity to plant

xenobiotics in humans compared tomany primates. Increased ingestionof Maillard compounds (potentiallytoxic complexes of sugars and aminoacids that form under heat catalysis)could have selective consequences fordetoxification systems. The ingestionof relatively high calorie loads inmeals, particularly late in the day, sug-gests modifications to the insulin sys-tem in humans as compared to apes.Such possibilities make the evidencethat humans are uniquely adapted toa high-quality diet of cooked food a

provocative claim for understandingvarious aspects of human digestivephysiology in a new way.

WHY HOMO ERECTUSAPPEARS

TO HAVE NEEDED FIRE

Given evidence that all humans arebiologically adapted to a cooked diet,when did fire use begin? The arche-ological evidence gives us a mini-mum age of at least 250 kya. Several

Figure 2. Energy deficiency among raw-foodists, adapted from Koebnick and col-

leagues.10 Age-adjusted body mass index (left axis, n) and percentage of nonpregnant

female subjects


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sites dated to 250 kya or older con-tain evidence of fire use by hominins,including burned deposits, fire-cracked rocks, reddened areas, bakedclay, ash, charcoal, fire-hardenedwood, burned lithics and bone, and

even some indication of hearths.

22

Older dates for fire use are alsowidely acknowledged at sites such asBeeches Pit in England23 and Scho-ningen in Germany,24 dated to 400kya, as well as Gesher Benot Yaaqovin Israel, dated to 790 kya.25

Unfortunately, the archeological re-cord may never tell us when fire wasfirst controlled. There is a decreasingprobability of finding evidence of anytype as time increases, and this isparticularly true with fire use, sincetraces of fire can vanish quickly.9 For

example, Sergant, Crombe, and Per-daen26 have reported that burnedbone, shells, and other artifacts have

been found at almost all Mesolithicsites in the northwest EuropeanPlain, yet direct evidence of controlof fire is extremely limited.26

Biology provides an alternativemethod of inferring the origin ofcooking. Animals show that anatomycan adapt very quickly to a changein diet.2729 Fast adaptation rates arealso known for hominins. Amonghuman populations with a history of

dairying, lactase persistence (that is,the ability to digest lactose intoadulthood) has evolved at least twicein the last 7,000 years.30,31 In addi-tion, populations with a recent his-tory of consuming starch-rich foodsexhibit higher copy numbers of thegene encoding for salivary amylase.32

Consequently, we can reasonablyinfer the origin of cooking from theemergence in hominins of biologicaltraits that are consistent with theconsumption of cooked food.

The predictable effects of cooking,

as noted earlier, include food soften-ing (including enhanced fracturabil-ity) as well as increased digestibilityand reduced costs of digestion. Fromthese we can hypothesize that theadoption of cooking should have ledto corresponding reductions in mas-ticatory and gastrointestinal anat-omy. In what hominin, if any, didsuch reductions take place?

We can eliminate Homo sapiens asa candidate, since fire was almost

certainly controlled prior to theiremergence 300200 kya. Also, theanatomical differences betweenH. hei-delbergensis and H. sapiens were notobviously diet-related, involving pri-marily a smaller face, a rounder head,

and a somewhat larger brain.

33

Homo heidelbergensisappears to bea reasonable candidate from an ar-cheological perspective, since itsemergence 800600 kya corre-sponds to the earliest widelyaccepted date for the control offire.25 H. heidelbergensis differs fromits precedessor, H. erectus, primarilyby its larger cranial capacity andother aspects of cranial shape,including a higher forehead anda flatter face.9 These features arenot irrelevant: A less prognathic face

can indicate reduced masticatorystrain,34 while a larger brain suggestsa higher energy budget, since the

brain is a metabolically expensive tis-sue.19 It is therefore likely that someimprovement in diet did occur at this

junction. However, the anatomicalchanges appear too slight a responseto a dietary shift as significant as cook-ing was likely to have been. In addi-tion, the transition from H. erectus toH. heidelbergensis appears to haveinvolved no major changes in denti-tion or gastrointestinal anatomy, in

contrast to what would be predictedifH. heidelbergensis had been the firstspecies to consume a cooked diet.

In contrast, the transition fromlate australopithecines or early Homo(Homo habilis, H. rudolfensis) to H.erectus is associated with significantchanges in diet-related features thatare consistent with the predictedeffects of a cooked diet. Postcaninetooth area is smaller in H. erectusthan in any previous hominin on anabsolute basis, and so small as to beequivalent to H. sapiens when

adjusted for body size.35

Correspond-ingly, H. erectus exhibits a relativelysmaller mandible36 and other aspectsof facial shortening, which suggestreduced masticatory strain.34 To-gether, these craniodental featuresindicate that H. erectus was consum-ing a softer diet. Gut size alsoappears to conform to the expectedpattern. For instance, H. erectusappears to have had a barrel-shapedthoracic cage similar to that of later

Homo and distinct from the funnel-shaped thoraces of previous homi-nins.37 H. erectus is therefore recon-structed as having a smaller gut thanits ancestors did.19 Given consistenttrade-offs in gut versus brain size

among primates,

19

larger cranialcapacity in H. erectus (849 cm3) thanin H. habilis (601 cm3) or H. rudol-fensis (736 cm3)35 is also consistentwith a smaller gut. Despite thesereductions in digestive anatomy, H.erectus shows signals of increasedenergy use, including larger bodysize,38 adaptations for long-distancerunning,39 and possibly reduced inter-birth intervals.40 The apparently softer,more digestible, and higher energy dietofH. erectus are all consistent with theexpected effects of cooking.

Locomotor adaptations also pointto the control of fire by Homoerectus. It is generally accepted thatH. erectuswas the first obligate biped,with multiple adaptations for terres-trial locomotion that came at theexpense of arboreal capability.39,4144

Obligate terrestriality would haveexposed H. erectus, with a reducedcapacity to scramble up a tree, to abroader array of predators, includinglions, leopards, hyenas and saber-toothed cats.45 Whereas H. erectusmight have defended themselves with

weapons during the day, it is hard toimagine how they would havedefended themselves at night withoutthe protection of fire.46 Indeed, pri-mates almost never sleep terres-trially. The main exceptions to thisrule are humans, who universallyrely on fire for protection in naturalhabitats; some gorillas (especiallyadult males), which are probably lesssusceptible to predation than wereH. erectus on account of their largerbody size and predator-poor foresthabitat; and some cliff-sleeping

baboons.47

We therefore suggestthat the control of fire was a prereq-uisite for the transition to obligateterrestriality.

ADAPTIVE CONSEQUENCES

OF THE CONTROL OF FIRE

Life History

Life history theory predicts causalrelationships between age-specific ex-



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trinsic mortality rates and the pace

of life history. For example, higher

extrinsic mortality in adults due to

increased rates of predation or dis-

ease results in a smaller proportion

of the population surviving to older

age. Increased extrinsic mortality inadults is therefore expected to

weaken selection on genetic factors

that delay senescence.48,49 As a

result, investments in growth and

maintenance are less likely to pay off

in terms of increased fecundity. For

this reason, populations with high

adult extrinsic mortality tend to

evolve fast life history patterns that

feature earlier and heavier overall

investments in reproduction. Corre-

lated life history traits include

shorter gestation, smaller size at

birth, earlier weaning, a reducedgrowth period, smaller adult body

size, earlier sexual maturity, shorter

interbirth intervals, and a shorter life

span. In contrast, species with low

adult extrinsic mortality can afford

to allocate more energy to growth

and maintenance, favoring a life

history pattern that features slow

maturation, increased adult body

size, late reproduction, high invest-

ment in each of a relatively small

number of offspring, and longer life.

These relationships have been exten-sively supported both in the wild5052

and experimentally.5355

Compared to other mammals, pri-mates tend to fall along the slow endof the life history continuum, evencontrolling for body size.56 Humans,however, are unique among primatesin having a mixed-pace life history(Fig. 3). In some respects, humansepitomize the slow strategy. Forexample, compared to chimpanzees,humans have larger infants, pro-tracted juvenility (childhood), and

longer adult life expectancy. Yethumans also wean early and repro-duce at a much faster rate thanwould be expected by the pace of ourlife history. As Dean and Smith57:115

have described it, reproduction inhumans (hunter-gatherers) works indouble time compared to our closestrelatives, the great apes, with meaninterbirth intervals in human for-agers being just 24 years comparedto 56 years in chimpanzees.58,59

Two main hypotheses have beenproposed to explain the unusualcombination of slow and fast fea-tures in human life history. Bothnote that humans are evolutionarilycommitted to a high-quality diet that

is difficult to procure. They thereforeconclude that weaned juveniles can-not easily feed themselves. As aresult, juveniles need to be provi-sioned by mothers or other kin.58

The first hypothesis, proposed byHawkes and colleagues,60 emphasizesthe role of skilled postreproductivewomen in provisioning juveniles andhelping with child care. According totheir idea, known as the grand-mother hypothesis, women can addto their inclusive fitness after meno-pause by facilitating reproductive

success in their daughters and otheryounger kin. In this scenario, longer-lived women contribute more to thegene pool via indirect fitness, leadingnatural selection to favor increasedlongevity. Interbirth intervals arereduced because the procurement,preparation, and provision of appro-priate foods by grandmothers meansthat dependent offspring are weanedsooner, while mothers are better atand spend less energy in foraging,thus facilitating the resumption ofmenstrual cycling. Hawkes and

colleagues60

suggest that the high fit-ness benefits of being a grandmothermay explain the evolution of post-menopausal longevity in humans.Thus, with respect to the life historyparadox, the grandmother hypothesissuggests that, thanks to certainunique human traits, a long life pro-motes fast reproduction and vice

versa.The second hypothesis, which was

proposed by Kaplan and col-leagues,58 emphasizes the age-spe-cific pattern of productivity. Accord-

ing to their idea (the embodied capi-tal model), productivity of food inadulthood is so high that it can pre-dictably compensate for the negativeproductivity in early life through theintergenerational transfer of resour-ces. Under this model, longevity isextended because the return fromdelayed investments increases as theproductive life span increases. Inter-birth intervals decrease through thesystem of intergenerational transfers

(from any kin, not just grandmothers)that allow women to weight energyallocation toward reproduction ratherthan food production during theirfecund years. Similar logic has beenemployed to argue for the inclusive

fitness contributions of children andadolescents in shaping the unexpect-edly fast component of the humanlife history pattern.61,62

Here we complement these ideasby proposing that the control of fireand consumption of cooked foodalso contributed to the evolution ofthe paradoxical human life historypattern. In our control-of-fire hy-pothesis the slow components ofhuman life history were favored bytwo main consequences of using fire.First, fire use led to reduced extrinsic

mortality as a result of lower preda-tion and disease. Second, cookingraised the nutritional value of provi-sioned food, increasing the value ofassistance from older individuals andthereby strengthening the selectionpressures on senescence. The fastcomponents of human life history,early weaning and short interbirthintervals, were likewise supported bycooking. In our model, earlier weaningwas made possible by cooked foodsbeing softer, more easily digestible,and less pathogen-bearing than raw

foods. Reduced interbirth intervalswere favored by both the energeticadvantages of a cooked diet and theprovisioning that cooking facilitates,allowing for greater stability in thenutritional status of mothers. Theseideas are elaborated briefly below.Box 1 summarizes the commonal-ities and distinctions among the grand-mother hypothesis,60 embodied capitalmodel,58 and control-of-fire hypothesis.

Slow Life History via Reduced

Extrinsic Mortality and Increased

Productivity in the Elderly

The human transition to obligate ter-restriality, apparently beginning withHomo erectus, should theoreticallyincrease extrinsic mortality due tohigher rates of predation, disease, andenvironmental hazards on the ground.As expected, a phylogenetically con-trolled analysis of 776 mammalian spe-cies has found that terrestrial taxa tendto have shorter maximum longevity

ARTICLES Human Adaptation to the Control of Fire 191


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than do arboreal taxa.63 Yet despite ourterrestriality, modern humans werefound to exhibit the highest longevityper body size of any mammal in thedataset, arboreal or terrestrial (Fig. 4).This is especially remarkable given thatall other terrestrial primates reducenocturnal predation by sleeping in treesor on cliffs. Aiello and Key40:562 pro-posed that the solution to the problemof extended human longevity most

probably lies in the developing socialorganization and expanding brain thatprovided a cultural buffer to the ele-

vated mortality risks of the savanna.We suggest that a particularly impor-tant cultural buffer was fire use.

The control of fire would havereduced extrinsic mortality by atleast two means. First, the presenceof fire appears to be a powerfuldeterrent of predators. Although nostudies have formally quantified the

deterrent effect of fire, demographicdata support this claim. For example,the causes of 4,993 deaths in a popu-lation of 8,008 !Kung hunter-gather-ers of the Nyae Nyae area, from ca.1900 to 2005, were systematicallycollected by John Marshall, ClaireRitchie, and Polly Wiessner, andcompiled into a database by Wiess-ner. Because predator attacksbecome legendary, Wiessner (perso-

nal communication) suspects thatfew, if any, are missing from therecord. Wiessners database includes10 deaths or serious maulings by lionor leopard from 1910 to 1960, all butone of which occurred in the absenceof fire. As these data imply, Wiessnerreports that the !Kung regard anight-time fire as importantly protec-tive. Thus, even though getting fire-wood can be a laborious task, the!Kung normally keep fires going all

night and stoke them well whenpredators are in the vicinity, solelyfor protection. The danger of sleep-ing without a fire is illustrated bysome of the fatal attacks, such as thedeath of /Asa: Her mother and fa-ther were sleeping and had let thefire go dead. /Asa was sleeping ashort distance away from them. Thestory goes that lions came and sat bythe family, watched the parents, saw

/Asa and took her (P. Wiessner, per-sonal communication).

Second, control of fire shouldreduce extrinsic mortality by lower-ing rates of disease. Controlled burn-ing of campsites controls pest infes-tations.64 In addition, cooking signifi-cantly reduces the incidence offoodborne illness, particularly fordiets that include meat.11 Heat killsthe most common foodborne bacte-ria, including Escherichia coli, Salmo-

Figure 3. The human life history puzzle. In most species, different life history parameters are consistent in their pace, as illustrated here for

nonhuman primate species (solid circles) by correlations among four life history variables. Unusually, hunter-gatherers (large diamond)

are slow in two variables (life span, age at first birth), but fast in two others (weaning, interbirth interval). A: Nonhuman primates with

long maximum life span tend to have late age of first birth (r2 0.56, n 36, p < 0.001). Humans are here assigned a conservative esti-

mate of 70 years for maximum life span, following Harvey, Martin, and Clutton-Brock,92 and fall close to the primate line. B: Nonhuman

primates with later weaning have longer interbirth intervals (r2 0.80, n 36, p < 0.001). Hunter-gatherers conform to the primate

trend. C: Nonhuman primates with a late age of first birth tend to have long interbirth intervals (r 2 0.61, n 41, p < 0.001); however,

hunter-gatherers have shorter interbirth intervals than expected. D: Nonhuman primates with a late age of first birth tend to wean later

(r2 0.82, n 29, p < 0.001), but hunter-gatherers have an earlier weaning age than expected. The puzzle about humans is why they

combine fast reproduction (short interbirth interval and early weaning) with slow growth (late age at first birth). Data sources: non-

human primates, Harvey, Martin, and Clutton-Brock92

; hunter-gatherers, Marlowe89

(Table 2, warm-climate, nonequestrian only). Num-ber of hunter-gatherer societies contributing to mean values: age at first birth, 6; interbirth interval, 9; weaning age, 18.



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Box 1. Summaries of Three Solutions to the Human Life History Paradox: The grandmotherhypothesis,60 the embodied capital model,58 and the control-of-fire hypothesis.

A. Common framework. Thethree solutions are not mutuallyexclusive. All three models share aframework in which reduced extrin-sic mortality (1) is responsible forslow aspects of human life history,notably slow maturation (2) andhigh longevity (3). An inverse rela-tionship between extrinsic mortality(M) and time to maturity (a) isexpected under Charnovs dimen-sionless approach to life history, inwhich aM is approximately constantacross related taxa.93 Slow matura-tion, in turn, promotes increasedadult body mass.a Reduced extrinsic

mortality will also favor increasedlongevity, as the average adult lifespan is roughly 1/M.94 All threemodels also share the concept thatthe intensive provisioning of youngerkin (4) allows for fast aspects ofhuman life history, including earlierweaning of infants (5) and an earlierreturn to fecundity by women afterweaning, which in turn favors ashort interbirth interval (6) and highfertility overall. Whether stated orimplied, all three models also inferthat high fertility contributes to

high longevity, since the inclusivefitness benefits that result from pro-visioning by older kin will act tostrengthen natural selection on fac-tors delaying senescence.

B. Grandmother hypothesis.60

This model focuses on the inclusivefitness contributions of seniorwomen as the critical factor allow-ing for high longevity and high fer-tility in humans. Extractive foragingby skilled postreproductive womengenerates food in excess of self-

maintenance requirements (1) andthis surplus is shared with juvenilerelatives. This surplus food, as wellas other contributions by post-reproductive women in the form of

food processing and child care,allows for higher fertility of repro-ductive-aged kin. Since inclusive fit-ness rises for postreproductivewomen who provision, long-livedhelper genes increase in frequencyin the gene pool, contributing tolongevity. In addition, continuedprovisioning by postreproductivewomen lowers the susceptibility todisease (2) of juvenile kin, furtherselecting for increased longevity.Hawkes and colleagues60 argued thatthese relationships may explain theevolution of postmenopausal longev-ity in humans. The complementarity

between the grandmother hypothesisand the control-of-fire hypothesis isillustrated by the fact that OConnell,Hawkes, and Blurton Jones77 dis-cussed the importance of cooking asa mechanism that helped enable pro-

visioning of kin.

C. Embodied capital model.58

This model emphasizes the timerequired to learn to subsist ef-fectively on a diet of high-quality,nutrient-dense foods. Here, slowmaturation allows for the acquisi-

tion of knowledge, skill, andstrength (1) which lead to profitablehunting and extractive foraging (2).The productivity of older individu-als far exceeds that of younger indi-

viduals, leading to a system ofresource transfers from old toyoung within kin groups. In addi-tion, since hunting is a low-successbut high-return activity, a dietaryniche that involves hunting favors abroader culture of food sharing (3)(kin-based and nonkin-based).Jointly, kin provisioning and food

sharing act to minimize volatility innutritional status, resulting in lessdisease (4). In addition, such foodtransfers lead to less predation (5),since provisioning reduces theamount of time that juveniles mustspend out of camp and since food

sharing reduces the costs of groupliving, leading to larger group size.Increased knowledge, skill, andstrength can further limit predation

as they allow better defense. Theresulting reduction in extrinsicmortality selects for the slowaspects of human life history, withhigh longevity subject to especiallystrong selection because cumulativeresource production increases non-linearly with longevity. Kaplan andcolleagues58 argued that these rela-tionships lead to co-evolutionbetween the human patterns of lifehistory and extreme intelligence.

D. Control-of-fire hypothesis.We propose that the control of fireincreases the efficiency of provision-

ing and reduces extrinsic mortality,thus contributing to the evolution ofthe human life history pattern.Increased efficiency of provisioning:

Fire use (1) allows for the cookingof food (2), which reliably enhancesfood energy, digestibility, and soft-ness (3) by the mechanisms dis-cussed in this paper. Suitable infantfoods are generated, allowing earlierweaning. In addition, the high nutri-tive value of cooked food likely con-tributes to a short interbirth inter-

val, given data illustrating the sup-

pressive effect of a raw diet onovarian function in modern raw-foodists.10 Importantly, the effectsof cooking improve the efficiency ofprovisioning, with fewer raw resour-ces required to achieve the samebenefit. This enhances the value ofkin provisioning, thus broadeningthe number of potential provi-sioners. Moreover, the act of cook-ing represents a means of contribu-tion. This may enable juveniles whoare not yet efficient hunters or for-agers to contribute meaningfully to

kin provisioning and thereby gaininclusive fitness benefits. Jointly,these characteristics favor the fastaspects of human life history.

Reduced extrinsic mortality:Other effects of cooking includefood detoxification and the killing offoodborne pathogens. These features,coupled with stable nutritional statusas a result of a high-quality cookeddiet and a culture of provisioning,

aBody mass increase in Homo is compli-cated by a reduction in sexual dimor-phism, so that only females experience theincreased mass. Reduction in sexualdimorphism in Homo is thought to be dueto sexual selection,95 which we do not dis-cuss in the present paper.



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nella, Campylobacter, Staphylococcus,Listeria, and Clostridium botulinum,all of which are potentially lethal. In

urban societies, the incidence of food-borne illness arising from meat con-sumption was recently estimated tobe 99.98% lower due to cooking thanit would have been if the same meatswere consumed raw, suggesting thatmeat consumption at current levelswould be energetically infeasiblewithout cooking.11 Finally, the factthat heat dramatically improves theenergetic value of widely availablefood resources, such as tubers,

reduces fluctuations in energy bal-ance that might otherwise compro-mise immune functions.65

Importantly, beyond extrinsic fac-tors, fire use can influence the selec-tion pressures governing senescence.Two mechanisms have been proposedfor senescence. The mutation accumu-lation theory, developed by Meda-war,48 states that the force of naturalselection weakens with increasing agesince extrinsic mortality will lead tofewer individuals alive in older agegroups, even in a theoretically immor-tal population. Williams observed that

antagonistic pleiotropy can also con-tribute to this effect, since traits thatincrease fitness early in life but bear a

cost later in life will be positivelyselected for, given that more individu-als are alive at young ages than at oldages.49 According to these theories,any feature that increases the propor-tion of individuals surviving to laterages and allows aged individuals toincrease their contributions to fitnesswill strengthen selection on geneticfactors that delay senescence, leadingto a slowing of life history. We suggestthat cooking meets both criteria.

lead to lower rates of disease (4).Disease risk may be lessened furtherby fire use, independently of theeffects of cooking, if campsites are

burned to eradicate pests. As dis-cussed in this paper, fire use resultsin less predation (5) due to theeffects of fire as a predator deterrent

and potential weapon. Jointly, thesuppressive effects of fire use on ex-trinsic mortality contribute to theslow aspects of human life history.



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For example, it is well establishedthat edentulous or denture-wearingindividuals have lower masticatoryefficiency than do fully dentate indi-

viduals.66 In addition, masticatoryefficiency can be affected by age-related decreases in biting and chew-ing force,67 which are attributable to

deterioration in muscle strength.68

Masticatory disability of this type hasbeen shown to increase mortality,even after controlling for other riskfactors.69,70 By softening foods andreducing their toughness, cookingshould improve the ability of agedindividuals to meet their energy needsand thereby increase the proportionof individuals surviving to later ages.

In addition, by improving the ener-getic value of food resources, cookingshould increase the advantages of assis-tance given to reproductive women bygrandmothers60 and other aged kin.58

This increased contribution should leadto slower life history. Under the muta-tion accumulation model, it wouldstrengthen selection against late-act-ing deleterious mutations by increas-ing the contribution to descendantgene pools of longer-lived individualsthrough the increased reproductivesuccess of their female kin. Underthe antagonistic pleiotropy model, itwould increase payoffs for late so-matic performance and therefore

perturb the equilibrium in favor ofhigher longevity.

High Fertility via Cooked

Food Consumption

By transforming plant and animal

source foods into nutrient-dense,soft, and digestible forms via themechanisms discussed above, cookinghelps make foods accessible to theimmature dentition and gastrointesti-nal tracts of potential weanlings. More-over, unlike all other forms of process-ing, cooking reliably kills foodbornebacteria. Studies in developing coun-tries have found that weaning diets areoften contaminated with fecal patho-gens due to improper food preparationand contact with animal feces, withmicrobial counts further worsened by

prolonged storage at high ambienttemperatures,71,72 The difficulty oflocating fuel for proper cooking orreheating of food has been identifiedas a key problem hindering the preven-tion of related enteric infections thatare a primary cause of malnutritionamong weanlings.73 By increasing theavailability of suitably nutritious andsafe foods, cooking should facilitateweaning, shortening the duration oflactational amenorrhea.

Beyond lactational amenorrhea, itis well established that the primaryecological mediators of fecundity inwomen are energetic: net energy bal-ance (that is, energy stores), ener-getic expenditure, nutritional intake

(current weight gain or loss) and theenergetic costs of lactation are allimportant.74 For example, studies ofnatural fertility populations havefound interbirth intervals to be nega-tively correlated with maternal post-partum weight, controlling for theduration of lactation.75,76 By improv-ing the energetic value of foods, par-ticularly that of starch-rich foodsthat are consistently available, cook-ing enables a woman to resume ovar-ian cycling sooner. Indeed, given thehigh rates of ovarian suppression

observed among female raw-foodistsof reproductive age,10 we posit that acooked diet is necessary for routine

fertility in female hunter-gatherers.Since cooking improves the nutritive

value of foods, fewer raw resources arerequired to achieve the same benefit.Given the well-established impact ofcooking on starchy plant foods, whichare the resources routinely collected bywomen among tropical hunter-gather-ers, cooking should substantially lowera womans foraging effort and increaseher own net productivity. Therefore,

unlike other models, our scenario forthe impact of fire on human life historydoes not necessarily depend on extra-maternal provisioning of raw foodresources or processing effort. Never-theless, our scenario is highly compati-ble with extra-maternal provisioning.As discussed by OConnell, Hawkes,and Blurton Jones,77 this is because thepositive effects of cooking increase theefficiency of kin provisioning, therebybroadening the range of provisionerswho would achieve commensurate in-clusive fitness benefits for their effort.

Moreover, the act of cooking itself rep-resents a means of contribution. Thismay enable juveniles who are not yetefficient hunters or foragers to contrib-ute meaningfully to kin provisioningand thereby gain inclusive fitness bene-fits, provided that the inclusive fitnessreturns justify the costs in terms oftime and energy. Observations of cook-ing behavior in Hadza juveniles asyoung as five, though limited to the ex-ploitation of fires kindled by elders,77

Figure 4. Maximal life span plotted against body mass for humans (closed circle) and 151

primates (open circles), compared to the ordinary least squares regressions for 189 arbo-

real mammals (dashed line: 0.25x 1.64, r2 0.50, p < 0.001) and 469 terrestrial mammals

(y 0.22x 1.39, r2 0.76, P < 0.001). Modified from Figure 2 in Shattuck and Williams.63



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support the idea that contributions arepossible even at very early ages. Thus,according to our model, provisioningby grandmothers, grandfathers, and

juvenile kin can all be expected to playa role in the evolution of the unique

human life history pattern.

Anatomy

As with their effects on life history,cooking and other consequences ofthe control of fire appear to haveinfluenced anatomy in multiple ways(Box 2). We have already suggestedthat cooking led to reduction of thedigestive system in relation to bodymass. Features of the human diges-

tive system that have been reportedto be relatively small include teeth,

jaw musculature, oral cavity volume,total gut volume, and the surfaceareas of the stomach, large intestine(colon), and cecum.9,7880 The small

intestine is the only major componentof the human gut that is close to theexpected size (smaller than in 62% of42 measured primate species78), per-haps because it is the major site fornutrient absorption. No gut compo-nents are larger than expected. Thediminution of the digestive systemconforms to humans having a lowdaily dry weight intake of food com-pared to nonhuman primates.81 Onthe other hand, total daily energy ex-

penditure appears to be high forhumans compared to other apes.82

The contrast between reduced diges-tive structures and higher energy useis explicable only by human diets pro-

viding exceptional energy.

Aiello and Wheeler

19

proposed thatgut reduction, and hence a reductionin the energetic cost of maintaininggut activity, contributes to solvingthe puzzle of large brains; that is, theproblem of how humans satisfy thehigh energy demands of a big braindespite having the same relative ba-sal metabolic rate as smaller-brainedprimates. Aiello and Wheeler consid-ered that two dietary changes wereresponsible for the reduction of gut

Box 2. Fire and anatomical change.

Changes in anatomy putativelyinfluenced by the control of fire.Although Pan and Australopithecushad important differences (such aswalking quadrupedally and biped-ally respectively) both are portrayedas having similar body mass, adap-tations for climbing (e.g. robust,curved fingers and toes, narrowshoulders) and large guts, signaledby the flared shape of the rib-cageand wide pelvis. Based on suchtraits we assume that like Pan,

Australopithecus slept at night intrees, climbed to eat fruits andsome other arboreal items, and atelarge volumes of food of relatively

low caloric density compared tohuman diets. Critical changesresulting from the control of fireoccur between Australopithecus andHomo erectus, withH. erectus show-ing the following features asdescribed in the text. (1) Increasedbrain volume, supported by areduction in gut volume made pos-sible by the improved digestibilityof cooked food. While there is evi-dence of increased brain volume inHomo erectus, the rise in cranial

capacity was prominent throughoutthe Pleistocene and most noticeablein Homo sapiens. (2) Increasedbody mass, especially in females,

promoted by reduced mortality dueto fire use. (3) Reduced molar area,a result of food being softened byheat. (4) Reduced gut volume, indi-cated by a narrowing of the rib-cage and pelvis. (5) Loss of arborealadaptations in the shoulders, arms,legs, hands and feet as arborealfoods grew less important thancooked terrestrial foods, andbecause Homo erectus could sleepon the ground following the controlof fire. (6) Reduced body hair, with

extra warmth achieved at night byresting near a campfire. (Anatomi-cal drawings courtesy of LucilleBetti-Nash).



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costs and corresponding increases inbrain size: more meat around1.9 mya, followed by cooking around0.6 mya. In contrast, our argumentthat cooking likely arose with Homoerectus suggests that cooked food sup-

ported the rise in brain size from 1.9mya onwards. As with many conse-quences of cooking, other factors mayalso play a role. In this case, reductionin skeletal muscle may also contributeto explaining how extra energy couldbe diverted to the brain.83

The problem of reducing heat losswhen inactive suggests an effect ofthe control of fire on body hair. AsPagel and Bodmer84 suggested, theability to sleep next to a campfirewould have solved the problem ofmaintaining warmth when asleep

and therefore allowed the reductionof body hair. Loss of body hair couldbe favored by various factors, includ-ing reduced vulnerability to para-sites84 and increased ability to loseheat by day,85 as well as at least nineother possibilities.86 If Wheelersheat-loss hypothesis is correct, thewarmth provided by fire can thereforeultimately be considered vital in ena-bling humans to acquire the ability torun long distances. Anatomical evi-dence that long-distance runningbegan with Homo erectus39 is thus

consistent with the idea that H. erec-tus controlled fire. Babies, being rela-tively inactive by day, would still needto be protected from hypothermia:this might explain why, unlike adults,they have a thick layer of heat-gener-ating fat close to the skin.87

Behavior and Cognition

One of the most striking behav-ioral apomorphies of humans isthat we spend much less time eatingthan nonhuman apes do. Great

apes spend 47 hours per day chewing,much as expected from their largebody mass. In contrast, humans spendless than one hour per day chewing,according to studies of U.S. residents,the Yekwana of Venezuela, Kipsigis ofKenya, South Pacific Samoans, andnine other societies.9 In some ways,the abbreviated human chewing pat-tern makes us seem like a carnivore,since carnivores, as compared to planteaters, spend a similarly small

amount of time chewing their food.88

However, carnivores achieve their lowchewing time by rapidly slicing andswallowing large chunks of meat, whichis unlike the human pattern of finelycomminuting food. The short chewing

time of humans is therefore betterexplained by the effect of cooking andnonthermal processing in reducing thetoughness and hardness of food, thanby the incorporation of increasedamounts of meat in the diet.

Low chewing time in humans hasseveral important consequences.Critically, individuals can afford toforego chewing for long periods dur-ing the day and instead compressmuch of their food intake into a rela-tively brief evening meal. As a result,instead of spending the majority of

daylight hours with guts that areactively digesting, humans can mini-mize gut activity in favor of aerobicexercise. This allows relatively effi-cient multi-hour locomotion andlong day journeys. Thus, male chim-panzees have average day ranges of35 km, with an occasional maxi-mum around 10 km, whereas malehunter-gatherers average around 914 km per day.89 Such long dayranges appear to be facilitated by thecombination of short chewing timesand relatively quiescent guts.

In addition, the fact that humanscan eat more than 2,000 calories in anhour of chewing means that theycan cover their energetic needs evenafter returning to camp at the endof a largely unproductive day. Thisdepends, of course, on food being avail-able following their return. Among con-temporary foragers, the household sys-tem means that married men canexpect a cooked meal to be available ev-ery evening. This system, which allowsmen to forage for high-risk, high-gainfood by supporting them nutritionally

on days when they fail to produce, thusdepends on the use of a food type thatcan be consumed rapidly; that is,cooked food. The tendency for mentoforage more for high-risk, high-gain foods, while women specializeon low-risk, low-gain foods, musttherefore have been strongly pro-

moted by the control of fire.The relationship between the con-

trol of fire and cognitive ability isspeculative, but considerable mental

ability clearly was important forlaunching the control of fire. Themanagement of fire requires prob-lem-solving (for example, to capturefire) and planning (for example, toget fuel). While chimpanzees and

bonobos can control fire in limitedways,9 it seems likely that homininencephalization, possibly as a resultof increased meat-eating by habil-ines, made the stable control of firecognitively possible. After the controlof fire was achieved, life historyeffects favoring a long period ofchildhood development would havecreated further opportunities forenhanced cognitive function. Variousconsequences would have followed.Even if the initial control of fire didnot necessitate a stable home base

for weeks at a time, central-place for-aging was likely adopted to allowboth fireside cooperation in cookingand food distribution, as well as car-ing for relatively immobile offspring.Reliance on fire also suggests a rela-tively high level of coordination com-pared to great apes. Given that greatapes demonstrate a preference forcooked food,90 we assume that thecontrol of fire would have led rapidlyto cooking, which then favoredincreased patience (to wait until thefood is ready), cooperation, and

respect for ownership in reducingthe problem of scroungers takingfood from a poorly guarded fire.Complex co-evolutionary pressures,including social pressures arisingboth from the opportunity to provi-sion each other and from the abilityto steal from each other, thereforeseem likely to have shaped the rela-tionship between fire and cognition.

CONCLUSION

We have presented evidence that

the first species adapted to the con-trol of fire was Homo erectus. Wehave also proposed various conse-quences of using fire, including con-tributions to the unique patterns ofhuman life history. In some ways, weregard these ideas as conforming toexisting theory. For instance, the hy-pothesis of early fire use does notchallenge the idea that increasedmeat-eating played an important rolein human origins. Nor do we con-



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clude that the life style and life his-tory of H. erectus were fully modern.The value of fire to humans and thenature of its use probably changedafter fire was first controlled, thanksto advances both in cooking methods

and other technologies, such as theeffectiveness of fire-based defenseagainst predators. The postulatedeffects of fire may therefore alsohave developed in stages. For exam-ple, while the initial control mighthave allowed hominids to sleep onthe ground without experiencing anincrease in predation rates comparedto sleeping in trees, fire need not havehad any immediate effects in loweringextrinsic mortality. The effects of con-trolling fire thus need to be consideredwithout assuming that they were

always the same as they are now.Nevertheless, while the consequen-ces of controlling fire have evolved,the acquisition of fire is clearlyexpected to have had large effects onnumerous aspects of human biology,and in some ways our ideas confrontconventional wisdom. For example,our hypothesis lies in contrast to the

view that fire was controlled first bya relatively late member of thehuman lineage (that is, within thelast half-million years), since thatidea also necessitates the notion that

fire use had little impact on humanevolutionary biology. Likewise, itchallenges the idea that humans aresuch ecological generalists that theyare not adapted to any specific com-ponents of their habitats. Potts91:129

exemplified a widely held view: It ispatently incorrect to characterize thehuman ancestral environment as a setof specific repetitive elements, statisti-cal regularities, or uniform problemswhich the cognitive mechanismsunique to humans are designed tosolve. In contrast, we claim that

humans are biologically adapted toeating cooked food. Accordingly, thehuman ancestral environmentrequired the presence of controlledfire and cooked meals, and thus pre-sented humans with a specific andconsistent set of problems relevant totheir biology, behavior, and cognition.

The cooking hypothesis could bedisproved by the discovery of somepreviously unknown combination ofraw, nonthermally processed foods

that provides an adequate human dietin diverse and variable habitats. Sucha discovery would be provocative andinformative. But if the cooking hy-pothesis is right, it presents numerousexciting challenges for understanding

the evolutionary impact of the controlof fire. Either way, further attention tothe unique aspects of human dietaryadaptation promises large rewards forunderstanding human evolution.

ACKNOWLEDGMENTS

This paper is based on a presenta-tion at the Arizona State UniversityWorkshop on Human Uniquenessand Behavioral Modernity (February1922, 2010), organized by Kim Hilland Curtis Marean. We thank JohnFleagle for the invitation to contrib-ute to Evolutionary Anthropology,Scott Williams and Milena Shattuckfor helpful discussion and for shar-ing their dataset on longevity, PollyWiessner for data on the sources andcontexts of !Kung mortality, FrankMarlowe for documentation on Hadzacooking practices, Lucille Betti-Nashfor providing the anatomical drawingsin Box 2, and Kristen Hawkes, JohnShea, John Fleagle and an anonymousreviewer for constructive commentson our manuscript.

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