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Wenner-Gren Foundation for Anthropological Research

TIe Expensive-Tissue HpolIesis TIe Bvain and lIe Bigeslive Sslen in Hunan and Fvinale
AulIov|s) LesIie C. AieIIo and Felev WIeeIev
Souvce Cuvvenl AnlIvopoIog, VoI. 36, No. 2 |Apv., 1995), pp. 199-221
FuIIisIed I TIe Univevsil oJ CIicago Fvess on IeIaIJ oJ Wennev-Oven Foundalion Jov
AnlIvopoIogicaI BeseavcI
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CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI I995
? I995 I TIe Wennev-Oven Foundalion Jov AnlIvopoIogicaI BeseavcI. AII vigIls vesevved OOII-3204/95/3502-0004$2.50
TIe Expensive-Tissue
TIe Bvain and lIe Bigeslive
Sslen in Hunan and Fvinale
I LesIie C. AieIIo and
Felev WIeeIev
Bvain lissue is nelaIoIicaII expensive, Iul lIeve is no signiJi-
canl covveIalion Ielveen veIalive IasaI nelaIoIic vale and veIa-
live Ivain size in Iunans and olIev encepIaIized nannaIs. TIe
expensive-lissue IpolIesis suggesls lIal lIe nelaIoIic vequive-
nenls oJ veIaliveI Iavge Ivains ave oJJsel I a covvesponding
veduclion oJ lIe gul. TIe spIancInic ovgans |Iivev and gaslvo-
inleslinaI lvacl) ave as nelaIoIicaII expensive as Ivains, and lIe
gul is lIe onI one oJ lIe nelaIoIicaII expensive ovgans in lIe
Iunan Iod lIal is navIedI snaII in veIalion lo Iod size. Oul
size is IigII covveIaled vilI diel, and veIaliveI snaII guls
ave conpaliIIe onI vilI IigI-quaIil, eas-lo-digesl Jood. TIe
oJlen-ciled veIalionsIip Ielveen diel and veIalive Ivain size is
nove pvopevI vieved as a veIalionsIip Ielveen veIalive Ivain
size and veIalive gul size, lIe Iallev Ieing delevnined I dielav
quaIil. No nallev vIal is seIecling Jov veIaliveI Iavge Ivains in
Iunans and olIev pvinales, lIe cannol Ie acIieved vilIoul a
sIiJl lo a IigI-quaIil diel unIess lIeve is a vise in lIe nelaIoIic
vale. TIeveJove lIe incovpovalion oJ incveasingI gvealev anounls
oJ aninaI pvoducls inlo lIe diel vas essenliaI in lIe evoIulion oJ
lIe Iavge Iunan Ivain.
LESLIE C. AIELLO iS Beadev in FIsicaI AnlIvopoIog al Univev-
sil CoIIege London |Oovev Sl., London WCiE 6BT, EngIand).
Bovn in I946, sIe vas educaled al lIe Univevsil oJ CaIiJovnia,
Los AngeIes |B.A., i967: M.A., I970) and lIe Univevsil oJ Lon-
don |FI.B., i98i). Hev veseavcI inlevesls cenlev on lIe evoIulion
oJ Iunan adaplalion: sIe is cuvvenlI coIIaIovaling vilI Bevnavd
Wood on lIe anaIsis oJ lIe poslcvaniaI JossiIs Jvon OIduvai
Oovge. SIe Ias puIIisIed |vilI M. C. Bean) An Inlvoduclion lo
Hunan EvoIulionav Analon |London Acadenic Fvess, i990),
AIIonelv and lIe AnaIsis oJ Size and SIape in Hunan EvoIu-
lion |JouvnaI oJ Hunan EvoIulion 22I27-47), TIe FossiI Evi-
dence Jov Moden Hunan Ovigins in AJvica A Bevised Viev
|Anevican AnlIvopoIogisl 9573-96), |vilI B. I. M. BunIav)
Neocovlex Size, Ovoup Size, and lIe EvoIulion oJ Language
|CUBBENT ANTHBOFOLOOY 34I84-93), and |vilI B. A. Wood)
CvaniaI VaviaIIes as Fvediclovs oJ Honinine Bod Mass |Anevi-
can JouvnaI oJ FIsicaI AnlIvopoIog, in pvess).
FETEB WHEELEB is Biveclov oJ BioIogicaI and EavlI Sciences,
LivevpooI JoIn Mooves Univevsil. He vas Iovn in i956 and edu-
caled al lIe Univevsil oJ BuvIan. His veseavcI Jocuses on pIsi-
oIogicaI inJIuences on Iunan evoIulion and lIevnoIioIog.
Anong Iis puIIicalions ave TIe InJIuence oJ BipedaIisn on lIe
Enevg and Walev Budgels oJ EavI Honinids |JouvnaI oJ
Hunan EvoIulion 2II07-I5), TIe InJIuence oJ lIe Loss oJ
FunclionaI Bod Haiv on lIe Enevg and Walev Budgels oJ EavI
Honinids |JouvnaI oJ Hunan EvoIulion 23379-88), TIe TIev-
noveguIalov Advanlages oJ Lavge Bod Size Jov Honinids Fovag-
ing in SavannaI Envivonnenls |JouvnaI oJ Hunan EvoIulion 23
35i-62), and TIe InJIuence oJ Slaluve and Bod Fovn on
Honinid Enevg and Walev Budgels A Conpavison oJ AuslvaIo-
pilIecus and EavI Hono FIsiques |JouvnaI oJ Hunan EvoIu-
lion 24I3-28).
TIe pvesenl papev vas sunilled in JinaI Jovn i5 VI 94.
MucI oJ lIe vovI lIal Ias Ieen done on encepIaIizalion
in Iunans and olIev pvinales Ias Ieen ovienled lovavd
vI queslions-vI diJJevenl pvinale laxa Iave diJJev-
enl veIalive Ivain sizes ov vI lIe Iunan Iine Ias un-
devgone sucI a pIenonenaI incvease in Ivain size duving
lIe pasl 2 niIIion eavs. HpolIeses lIal Iave Ieen pul
Jovvavd lo ansvev lIese queslions pvinaviI invoIe
socio-ecoIogicaI Jaclovs sucI as gvoup size |AieIIo and
BunIav I993),
sociaI |ov MacIiaveIIian) inleIIigence
|Bvne and WIilen I988), ov conpIexil oJ Jovaging slval-
eg |MiIlon I979,
FavIev and OiIson I979, CIullon-
BvocI and Havve I980, OiIson I986, MacNaI and Eisen-
Ievg I989). TIese queslions and lIeiv ansvevs ave un-
douIledI inpovlanl Jov an undevslanding oJ encepIaIi-
zalion, Iul lIeve ave olIev issues lIal nusl Ie laIen inlo
considevalion. Bvains ave nelaIoIicaII vev expensive
ovgans, and Iavge Ivains Iave speciJic cIenicaI and lIev-
noveguIalov vequivenenls |WIeeIev I984, FaII I990).
One oJ lIe nosl inlevesling queslions is Iov encepIa-
Iized pvinales, and pavlicuIavI Iunans, can aJJovd sucI
Iavge Ivains |Mavlin I983, FoIe and Lee I99I).
BeIaliveI Jev sludies Iave Ieen ovienled lovavd lIis
queslion oJ cosl. TIose lIal Iave suggesl a veIalionsIip
Ielveen dielav quaIil and veIalive Ivain size, nedialed
eilIev lIvougI lIe Ivain's cIenicaI vequivenenls and
speciJicaII Iong-cIain Jall acids |CvavJovd i992) ov
lIvougI IasaI nelaIoIic vale |BMB), veJIecling lIe en-
evg needed Jov Ivain gvovlI and nainlenance |Mavlin
I98I,I 983: Avnslvong i982, i983, i985a, I, I990: HoJ-
nan I983). TIvougI lIe anaIsis oJ lIe nelaIoIic ve-
quivenenls oJ vavious ovgans in lIe Iod, ve suggesl
lIe expensive-lissue IpolIesis lo expIain Iov en-
cepIaIized pvinales can Iave veIaliveI Iavge Ivains
vilIoul covvespondingI IigI IasaI nelaIoIic vales.
i. We lIanI Bavid CIivevs and Ann MacLavnon Jov suppIing un-
puIIisIed gul veigIls and Jov dvaving ouv allenlion lo inaccuvacies
in lIe puIIisIed pvinale gul veigIls in CIivevs and HIadiI |i980
laIIe 6). We ave gvaleJuI lo lIe JoIIoving peopIe Jov veading eavIiev
vevsions oJ lIis nanuscvipl and/ov discussing vilI us lIe ideas
pvesenled in il Felev Andvevs, BoIevl Bavlon, BoIin BunIav, BoI
FoIe, Maciej HenneIevg, KalIevine Honevood, Havv Jevison,
CalI Ke, BulI Mace, KalIevine MiIlon, Sava BandaII, Mavgavel
ScIoeningev, Fvancis TIacIeva, AIan WaIIev, and Bevnavd Wood.
We lIanI JoIn FIeagIe Jov naIing us avave lIal Siv AvlIuv KeilI
Iad poinled oul lIe invevse veIalionsIip Ielveen Ivain size and
slonacI size in pvinales in I89I |KeilI i89i) and Iad Ianenled
lIe Jacl lIal lIe Jindings in lIis oIscuve papev Iad gone, lo Iis
InovIedge, enliveI unciled |KeilI i950). An ovaI vevsion oJ lIis
papev vas pvesenled al lIe I993 FaIeoanlIvopoIog sociel neel-
ings in Tovonlo, Canada.
200 CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI 1995
z 4l CeIus &
Modevn Hunans
2 4
1.25 1.75 2.25 2.75 3.25 3.75 4.25 4.75
EncepIaIizalion Quolienl
FIO. I. EncepIaIizalion quolienls |genus avevages) Jov Iunans and olIev pvinales |n = 24) |Iunan Iod
nass =
65 Ig: Ivain nass = 1,300 g: olIev dala Jvon AieIIo and Bean 1990).
TIis IpolIesis aIso pvovides an expIanalion Jov lIe ap-
pavenl covveIalion Ielveen encepIaIizalion in lIe eavI
Ioninids and lIe incovpovalion oJ incveasingI Iavge
anounls oJ aninaI-devived Jood inlo lIe diel.
TIe FvoIIen
TIvee Jaclovs conIine lo pose a najov pvoIIen Jov lIe
undevslanding oJ Iov encepIaIized pvinales, and pavlic-
uIavI Iunans, can aJJovd lIeiv veIaliveI Iavge Ivains.
TIe Jivsl is encepIaIizalion ilseIJ. B deJinilion, an en-
cepIaIized pvinale Ias a Iavgev-lIan-expecled Ivain in
veIalion lo ils Iod size. One oJ lIe nosl connonI
used equalions Jov lIe pvediclion oJ Ivain size Jov pIacen-
laI nannaIs |Mavlin I983, I990) is

vIeve E is Ivain nass in niIIigvans and F is Iod nass
in gvans. In levns oJ lIis equalion, nodevn Iunans
Iave an encepIaIizalion quolienl |valio oJ oIsevved lo
expecled Ivain size [EQ]) oJ 4.6 vIiIe olIev pvinales av-
evage i.9
- o.6 |Jig. I). TIis neans lIal lIe avevage
Iunan Ias a Ivain lIal is 4.6 lines lIe size expecled
Jov lIe avevage nannaI and lIe avevage non-Iunan pvi-
nale anlIvopoid Ias a Ivain aInosl lvice as Iavge as
lIal oJ lIe avevage nannaI.
TIe second Jaclov is lIe nelaIoIic cosl oJ lIe Ivain.
On lIe Iasis oJ in vivo delevninalions, lIe nass-speciJic
nelaIoIic vale oJ lIe Ivain is appvoxinaleI I I.2 W.Kg-
|valls pev IiIogvan) |laIIe i: AscIoJJ, OuinlIev, and
Kvanev I 97 I). TIis is nine lines IigIev lIan lIe avevage
nass-speciJic nelaIoIic vale oJ lIe Iunan Iod as a
vIoIe |i.25 W.Kg-1). TIe najovil oJ lIis IigI IeveI oJ
enevgelic expendiluve, vIicI is conpavaIIe lo in vivo
neasuvenenls oJ Ivain lissue Jvon olIev nannaIian
species, appeavs lo Ie associaled vilI lIe ion punping
necessav lo nainlain lIe polenliaIs acvoss lIe axonaI
nenIvanes. In addilion, enevg is used in lIe conlinuaI
snlIesis oJ neuvolvansnillevs sucI as acelIcIoIine.
ConsequenlI, a Iavge-Ivained nannaI nusl Ie capaIIe
oJ conlinuaII suppIing lIe Ivain vilI lIe IigI IeveIs
oJ suIslvale and oxgen vequived lo JueI lIis expendi-
luve, a lasI nade nove diJJicuIl I lIe inaIiIil oJ lIe
Ivain lo slove signiJicanl enevg vesevves.
TIeve is no douIl lIal an incvease in Ivain lissue
vouId vepvesenl a considevaIIe enevgelic inveslnenl Jov
lIe aninaI concevned. Fov exanpIe, accovding lo equa-
lion i, lIe avevage |65-Ig) Iunan Ias a Ivain I.04 Ig
Iavgev lIan vouId Ie expecled Jov lIe avevage nannaI
oJ lIe sane Iod nass |oIsevved Ivain nass = I,300 g:
expecled Ivain nass = 268 g) and o.8s Iavgev lIan vouId
Ie expecled Jov lIe avevage pvinale oJ lIe sane Iod
nass. Assuning Jov lIe nonenl lIal lIe nelaIoIic cosl
oJ i i.2 W.Kg-1 is conslanl Jov Ivain lissue in aII nan-
naIs oJ conpavaIIe Iod nass, lIe inJevved BMB Jov lIe
expecled Ivain nass in lIe avevage nannaI oJ Iunan
Iod nass vouId Ie 3 valls. TIe oIsevved BMB Jov lIe
oIsevved, nucI Iavgev Ivain nass in Iunans is I4.6
Because lIe Iunan Ivain cosls so nucI nove in enev-
gelic levns lIan lIe equivaIenl avevage nannaIian
Ivain, one nigIl expecl lIe Iunan BMB lo Ie covve-
spondingI eIevaled. Hovevev, lIeve is no signiJicanl
AIELLO ANB WHEELEB TIe Expensive-Tissue HpolIesis 2oi
Ovgan Mass and MelaIoIic Bale in Hunans
Ovgan TolaI Ovgan
Ovgan Mass MelaIoIic Bale MelaIoIic Bale % TolaI
Ovgan |Ig) % Bod Mass |W.Kg-1) |W) Bod BMB
Bvain I.3 2.0 II.2 I4.6 i6.i
Heavl 0.3 0.5 32.3 9.7 IO.7
Kidne 0.3 0.5 23.3 7.0 7.7
Livev I.4 2.2
I7.I I8.9
Oaslvo-inleslinaI I.I I.7 J I I324 I4.8
TolaI 4.4 6.8 6I.7 68.i
SIeIelaI nuscIe 27.0 4I.5 0.5 I3.5 I4.9
Lung o.6 0.9 6.7 4.0 4.4
SIin 5.0 7.7 0.3 I.5 I.7
Ovand lolaI 37.0 56.9 80.8 89.i
NOTE Bala Jov a 65-Ig naIe vilI a BMB oJ 90.6 W |AscIoJJ, OunlIev, and Kvanev I971).
covveIalion Ielveen veIalive IasaI nelaIoIic vale and
veIalive Ivain size in Iunans and olIev encepIaIized
aninaIs |McNaI and EisenIevg I989). MannaIian
BMBs ave aIIonelvicaII veIaled lo Iod nass I an
equalion oJ lIe Jovn
BMB |W) = a nass |Ig)075. |2)
Mosl inlevspeciJic sludies Iave vepovled exponenl vaI-
ues vev cIose lo 0.75, and lIis is genevaII accepled
as lIe slandavd exponenl Jov conpavisons oJ species oJ
diJJeving Iod nass |BIaxlev I989, BIigI and JoInson
I973, KIeiIev I96I, ScInidl-NieIsen I984). SucI anaI-
ses Iave pvoduced siniIav eslinales Jov lIe nelaIoIic
IeveI |a in equalion 2) lIal vange Jvon 3.3 lo 4.I |BIaxlev
I989). One oJ lIe nosl videI used genevaI veIalionsIips
Jov naluve pIacenlaI nannaIs |eulIevians) is lIal caI-
cuIaled I KIeiIev |196I),
BMB |W) = 3.39 nass |Ig)075. |3)
TIeve is, Iovevev, considevaIIe vavialion Ielveen laxo-
nonic gvoups |BIaxlev I989, Hussen and Lac I985, Fe-
levs i983). Fov exanpIe, lIe vepovled nelaIoIic IeveIs
oJ sone inseclivoves |BIaxlev I989, WIeeIev I984) and
nusleIid cavnivoves |veaseIs) |Ivevsen I972, WIeeIev
I984) ave as IigI as 9.5 and
7.5, vespecliveI. In conlvasl,
lIose oJ sone cIivoplevans |Ials) ave as Iov as 2.o lo 2.5
|FoczopIo I97I, WIeeIev I984). AIlIougI sone eulIe-
vian laxa do lIeveJove deviale navIedI Jvon lIe KIeiIev
veIalionsIip, lIis is nol lIe case Jov pvinales, vIicI,
vilI a nelaIoIic IeveI oJ 3.36 |BIaxlev I989), dispIa
BMBs aInosl idenlicaI lo lIose pvedicled I lIe KIeiIev
equalion and olIev genevaI veIalionsIips Jov eulIevian
Fav nove expevinenlaI delevninalions Iave Ieen
nade oJ Iunan IasaI nelaIoIisn lIan Jov an olIev
nannaI |C. ScIoJieId I985). TIe exlensive dala avaiI-
aIIe cIeavI denonslvale lIal, aIlIougI inJIuenced I
Jaclovs sucI as age and sex |W. N. ScIoJieId I985), lIe
BMBs oJ naluve individuaIs ave lpicaI oJ pvinales and
consequenlI eulIevian nannaIs as a vIoIe |laIIe 2).
In Jacl, lIe nean BMBs oJ naluve nen and vonen
slvaddIe lIe vaIues pvedicled I IolI pvinale and eulIe-
vian equalions Jov nannaIs oJ conpavaIIe Iod nass
|Jig. 2). ConsequenlI, lIeve is no evidence oJ an incvease
in IasaI nelaIoIisn suJJicienl lo accounl Jov lIe addi-
lionaI nelaIoIic expendiluve oJ lIe enIavged Ivain.
WIeve does lIe enevg cone Jvon lo JueI lIe encepIa-
Iized Ivain?
TIe SoIulion
One possiIIe ansvev lo lIe cosl queslion is lIal lIe
incveased enevgelic denands oJ a-Iavgev Ivain ave con-
pensaled Jov I a veduclion in lIe nass-speciJic nela-
IoIic vales oJ olIev lissues. Fov exanpIe, iJ a signiJicanl
conponenl oJ BMB is endogenous Ieal pvoduclion spe-
ciJicaII veIaled lo lIe lIevnoveguIalov denands oJ lIe
nannaI, lIen an incveased conlviIulion nade I
Ivain nelaIoIisn lo ils lIevnaI Iudgel couId aIIov a
covvesponding veduclion in lIe vequivenenl Jov dedi-
caled lIevnogenesis eIsevIeve in lIe Iod.
An aIlevnalive and nol necessaviI conlvadiclov pos-
siIiIil is lIal lIe expansion oJ lIe Ivain vas associaled
vilI a conpensalov veduclion in lIe veIalive nass oJ
one ov nove oJ lIe olIev nelaIoIicaII aclive ovgans oJ
lIe Iod. AIlIougI nosl sludies oJ pvinale nelaIoIisn
Iave Jocused on lIe enevgelic cosls oJ encepIaIizalion,
lIe Ivain is jusl one oJ sevevaI ovgans vilI IigI enevgelic
denands. TIe Ieavl, Iidnes, and spIancInic ovgans
|Iivev and gaslvo-inleslinaI lvacl) aIso naIe a suIslanliaI
conlviIulion lo ovevaII BMB |laIIe i). Belevninalions
CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI 1995
OIsevved and Fvedicled BasaI MelaIoIic Bales Jov a 65-Ig
Conpaved vilI OlIev Fvinales and EulIevians
Fvedicled 65-Ig MannaI BMB
OlIev Fvinales EulIevians
|3.36 M0 75) |3-39
Sex and Age BMB |W) W BiJJ. |%) W BiJJ. |%)
I8-30 vs 80.9I4 76.9I6 5.20 77.603 4.25
30-6o vs 78.39I 76.9I6 I.92 77.603 I.02
I8-30 vs 70.2o8 76.9I6 -8.72 77.603 9.-53
30-6o vs 66.528 76.9I6 -I3-5I 77.603 -I4.27
I8-30 vs 75.56I 76.9I6 -1.76 77.603 -2.63
30-6o vs 72-460 76.9I6 -5.79 77.603 -6.63
SOUBCE Fov Iunans, W. ScIoJieId |i985).
oJ lIe oxgen consunplion vales oJ lIese ovgans in vivo
I pevJusion expevinenls indicale lIal, logelIev vilI
lIe Ivain, lIe accounl Jov 60-70% oJ BMB despile
naIing up Iess lIan 7% oJ lolaI Iod nass. TIe Ieavl
and Iidnes Iave nass-speciJic nelaIoIic vales consid-
evaII IigIev lIan lIal oJ lIe Ivain, lIe enevgelic de-
nands oJ vIicI ave conpavaIIe lo lIose oJ lIe spIancI-
nic lissues. TIe lissues vIicI naIe up lIe venaining
93% oJ Iod nass dispIa covvespondingI Iov vales oJ
enevg luvnovev. Fov exanpIe, lIe in vivo nass-speciJic
nelaIoIic vale oJ vesling Iunan sIeIelaI nuscIe is onI
aIoul 5% oJ lIal oJ lIe Ivain, and consequenlI, aI-
lIougI lIis lissue accounls Jov 4I.5% oJ lolaI Iod
nass, il conlviIules onI I4.9% oJ BMB on lIe Iasis oJ
lIe dala used Ieve |laIIe i).
TIese diJJevences in lIe conlviIulion oJ vavious lis-
sues lo BMB ave aIso veJIecled I neasuvenenls oJ lIe
oxgen consunplion vales oJ isoIaled lissues |laIIe 3).
SucI in vilvo delevninalions ave Inovn lo Ie inJIuenced
I Jaclovs sucI as lIe node oJ pvepavalion oJ lIe lissues
and lIe cIenicaI conposilion oJ lIe suspending nedia,
and lIeveJove cave is necessav in conpaving lIe aIso-
1 000
0.01 0.1 1 1 0 100
FIO 2. BasaI nelaIoIic vale and Iod nass, sIoving lIal 65-Ig
Iunan naIes and JenaIes |I8-30 eavs oId)
span lIe Iesl-Jil Iine Jov aII nannaIs |equalion 3).
AIELLO ANB WHEELEB TIe Expensive-Tissue HpolIesis
In vilvo Tissue Mass-speciJic MelaIoIic Bales
Mass-speciJic MelaIoIic Bale |W.Kg-1)
Mouse Bal Bal Bog
Tissue |I3 g) |150 g) |242 g) |19.I Ig)
Bvain I4.0 IO.3 I3.I 7.6
Heavl I6.4 |II7) io.8 |i05) I6.6 |126) 5.9 |78)
Kidne 22.0
23.0 |224) 24.9 |I90) I3.8 |i82)
Livev I6.3 |ii6) II.2 |I19) ii.6 |89) II.2 |I48)
Oaslvo-inleslinaI lvacl I7.4 |I24) 5.6 |55) IO.9 |83) 3.8 |50)
Lung 3.8 |27) 7.0 |68) - 3.0 |39)
SIeIelaI nuscIe 3.2 |23) 4.9 |48) 2-2 |I7) 3-2 |42)
SIin _ 2.3 |23) _ I.0 |Ii)
Bone - 0.9|8) - 0.4|5)
SOUBCES Fov nouse, WIeeIev |i984): Jov iso-g val, FieId, BeIding, and Mavlin I939:
Jov 242-g val, WIeeIev |i984) and unpuIIisIed dala: Jov dog, Mavlin and FuIvnan
NOTE NunIevs in IvacIels vepvesenl lIe lissue nass-speciJic nelaIoIic vale as a pev-
cenlage oJ lIe nass-speciJic nelaIoIic vale oJ lIe Ivain.
Iule vaIues vepovled I diJJevenl sludies. AIso, lIe aIso-
Iule nelaIoIic vales oJ individuaI lissues oJ species oJ
diJJeving size cannol Ie diveclI conpaved Iecause lIese
pavanelevs, IiIe BMB ilseIJ, ave aIIonelvicaII veIaled
lo Iod nass. TIe Iiniled nunIev oJ delaiIed sludies
conducled genevaII indicale lIal lIe nass-speciJic nel-
aIoIic exponenls oJ lIe diJJevenl lissues ave Ielveen o
and - o. I 5 |BevlaIanJJ and EaslvicI I 9 5 3, Ovande I 980,
KveIs I950, OiIava and Ilazova I984, WIeeIev i984),
and lIeveJove ceIIuIav nelaIoIisn is Iess dependenl
on lIe size oJ lIe nannaI lIan ovevaII BMB, vilI
ils nass-speciJic exponenl oJ avound -o.25. Hovevev,
vIen lIe diJJevenl lissues ave conpaved vilIin a slud,
lIe genevaI pallevn oJ lIeiv veIalive nelaIoIic vales is
vev siniIav lo lIal oIsevved Jov Iunans in vivo. As
expecled, an exceplion is lIe Ieavl, vIicI in vivo nain-
lains IigI IeveIs oJ conlvacliIe aclivil even in lIe vesl-
ing nannaI, vesuIling in nucI IigIev IeveIs oJ oxida-
live nelaIoIisn lIan lIose neasuved in isoIaled cavdiac
TIeveJove, IolI in vivo and in vilvo dala cIeavI den-
onslvale lIal, logelIev vilI lIe Ivain, lIe Ieavl, Iidne,
and spIancInic ovgans accounl Jov lIe najovil oJ BMB.
To delevnine vIelIev incveased encepIaIizalion is as-
socialed vilI a veduclion in veIalive size oJ an oJ lIese
olIev nelaIoIicaII aclive lissues il is necessav lo con-
pave lIe oIsevved nass oJ eacI ovgan in an aduIl Iunan
vilI lIal expecled Jov lIe avevage pvinale oJ covve-
sponding Iod nass.
TIe anaIsis is Iased on lIe ovgan nasses oJ a 6s-Ig
slandavd Iunan naIe. Oaslvo-inleslinaI lvacl nass,
excIuding oesopIagus and conlenls |Jood and digeslive
juices), Ias Ieen eslinaled lo Ie I,I50 g |Sndev I975).
TIe Iivev is eslinaled as lIe diJJevence Ielveen lIis
Jiguve and lIe spIancInic nass oJ 2.5 Ig given I
AscIoJJ, OunlIev, and Kvanev |I97 i) and is consislenl
vilI olIev eslinales oJ novnaI Iivev size in a slandavd
individuaI |Sndev I975). Ovgan nass in aduIl Iunans
vavies vilI age, IeaIlI, and nulvilionaI slalus |Sndev
I975), Iul dala Jvon conpIele disseclions oJ individuaI
cadavevs |e.g., MilcIeII el aI. I945, FovIes, Coopev, and
MilcIeII I956) suggesl lIal lIe genevaI size veIalion-
sIips Ielveen ovgans sIovn in laIIe i ave veasonaIIe
veJIeclions oJ lIe veIalionsIips in IeaIlI individuaIs. Il
is inpovlanl lo nole lIal lIis anaIsis is designed lo
veveaI onI genevaI lvends in oIsevved size and nelaIoIic
veIalionsIips oJ Iunan ovgans in veIalion lo lIose lIal
vouId Ie expecled in lIe avevage pvinale oJ ouv Iod
nass. Il is nol designed, and sIouId nol Ie inlevpveled,
lo vepvesenl a delaiIed size ov nelaIoIic anaIsis appIica-
IIe al lIe individuaI IeveI.
TIe ovgan nasses lIal vouId Ie expecled Jov lIe avev-
age pvinale oJ a Iunan Iod nass |65 Ig) veve con-
puled Jov lIe Ieavl, Iivev, and Iidnes on lIe Iasis oJ
lIe Ieasl-squaves equalions Jov pvinales given in SlaII
|i965). TIe covveIalion coeJJicienls in lIese veIalion-
sIips ave suJJicienlI IigI lo guavd againsl signiJicanl
Iias allviIulaIIe lo lIe use oJ Ieasl-squaves vegvession
valIev lIan veduced-najov-axis anaIsis |AieIIo I992).
Expecled Ivain nass and gul nass veve devived Jvon
veduced-najov-axis equalions conpuled Jov lIis anaI-
sis. TIe veIevanl equalions, aIong vilI sanpIe sizes,
covveIalion coeJJicienls, and dala souvces, ave given in
Jiguve 3.
TIe conIined nass oJ lIe nelaIoIicaII expensive
lissues Jov lIe veJevence aduIl Iunan is venavIaII
cIose lo lIal expecled Jov lIe avevage 6s-Ig pvinale |Jig.
3, laIIe 4), Iul lIe conlviIulions oJ individuaI ovgans
lo lIis lolaI ave vev diJJevenl Jvon lIe expecled ones.
AIlIougI lIe Iunan Ieavl and Iidnes ave IolI cIose
lo lIe size expecled Jov a 6s-Ig pvinale, lIe nass oJ
lIe spIancInic ovgans is appvoxinaleI goo g Iess lIan
expecled. AInosl aII oJ lIis sIovlJaII is due lo a veduc-
lion in lIe gaslvo-inleslinaI lvacl, lIe lolaI nass oJ
CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI 1995
c 2000
Kidne Kidnel
FIO. 3. OIsevved and expecled ovgan nass Jov a slandavd 65-Ig Iunan. Expecled ovgan nasses Jov Ieavl,
Iivev, and Iidnes Jvon SlaII |i965) Ieavl nass =
5.2M0987 |n = 32i, v =
o.99): Iivev nass = 32.2M094 |n =
293, v =
o.98): Iidne nass |IolI Iidnes logelIev) = 6.3M087 |n = 268, v =
0.95). Expecled Ivain size is Iased
on lIe veduced-najov-axis equalion conpuled Jov IigIev pvinales |excIuding Iunans) Jvon dala in SlepIan,
FvaIn, and Bavon |i98i) Ivain nass =
I.35 |N = 26, v = o.98). Expecled gul size is
Iased on lIe veduced-najov-axis equalion conpuled Jov IigIev pvinales Jvon dala in CIivevs and HIadiI
|I980) and CIivevs, pevsonaI connunicalion, I990 |lpeselling evvovs aJJecling dala accuvac in lIeiv laIIe 6
Iave Ieen covvecled, and nev species Iave Ieen added): gul nass, Iog1OOM
= o.85310g10M - I.27I |N = 22,
v =
o.96). OM, gul nass |Ig): W, olIev-ovgan nass |g) M, Iod nass |Ig): n, nunIev oJ individuaIs: N,
nunIev oJ species: v, pvoducl-nonenl covveIalion coeJJicienl.
vIicI is onI aIoul 6o% oJ lIal expecled Jov a siniIav-
sized pvinale. TIeveJove, lIe incvease in nass oJ lIe
Iunan Ivain appeavs lo Ie IaIanced I an aInosl idenli-
caI veduclion in lIe size oJ lIe gaslvo-inleslinaI lvacl.
TIese veIalionsIips ave size veIalionsIips valIev lIan
nelaIoIic veIalionsIips. WIelIev lIe enevgelic saving
allviIulaIIe lo lIe snaIIev gul is suJJicienl in ilseIJ lo
neel lIe nelaIoIic denands inposed I lIe incveased
encepIaIizalion depends on lIe veIalive nelaIoIic vales
oJ lIe lvo lissues. AIlIougI no Iunan dala ave avaiIaIIe
veIaling speciJicaII lo lIe in vivo oxgen consunplion
oJ lIe gaslvo-inleslinaI lvacl, lIe ovevaII nelaIoIic vale
oJ lIe spIancInic ovgans is appvoxinaleI I2.2 W.Kg-1
|AscIoJJ, OunlIev, and Kvanev
I97i). IJ lIe nass-
OIsevved and Expecled Ovgan MelaIoIic Bales
Mass |Ig) MelaIoIic MelaIoIic
Cosl Incvenenl
Tissue OIsevved Expecled OIsevved-Expecled |W.Kg-1) |W)
Bvain I .300 0.450 o.850 I I.2 9.5
Heavl 0.300 0.320 -0.020 32.3 -o.6
Kidne 0.300 0.238 o.o62 23.3 I.4
Livev I.400 I-563 -o.i63
-0.944 I2.2 -II.5
Oaslvo-inleslinaI lvacl I.Ioo i.88i -0.78I
TolaI 4.400 4.452 - I.2
SOUBCE AscIoJJ, OunlIev, and Kvanev |I97I).
NOTE Expecled nelaIoIic vales ave conpuled Jov a
Iunan on lIe Iasis oJ lIe equalions given
in Jiguve 3.
AIELLO ANB WHEELEB TIe Expensive-Tissue HpolIesis l 205
speciJic nelaIoIic vales oJ lIe Iivev and snoolI nuscIe
oJ lIe gul conlviIuling lo lIis ave conpavaIIe |and in
vilvo delevninalions oJ lissues Jvon olIev nannaIian
species suggesl lIal lIis is lIe case [laIIe 31), lIen lIe
veduclion in lIe size oJ lIe gul saves appvoxinaleI 9.5
W. ConsequenlI, lIe enevgelic saving allviIulaIIe lo
lIe veduclion oJ lIe gaslvo-inleslinaI lvacl is appvoxi-
naleI lIe sane as lIe addilionaI cosl oJ lIe Iavgev Ivain
|laIIe 4). TIeveJove, iJ lIe cIanges in lIe pvopovlions oJ
lIe lvo ovgans veve conlenpovav evoIulionav evenls,
lIeve is no veason lIal lIe BMBs oJ Ioninids vouId
evev Iave Ieen eIevaled aIove lIose lpicaI oJ olIev pvi-
nales as a consequence oJ lIe enevgelic cosls oJ encepI-
AIlIougI lIis anaIsis is concevned pvinaviI vilI
lIe conlviIulion oJ lIe nelaIoIicaII aclive lissues lo
BMB, sone considevalion sIouId Ie given lo lIe sig-
niJicance oJ lIe cosls oJ lIese ovgans in lIe conlexl oJ
lIe ovevaII enevg Iudgel oJ lIe aninaI. OIviousI, il is
inpossiIIe lo delevnine lIe lolaI daiI enevg expendi-
luve-lIe JieId nelaIoIic vale |FMB)-oJ eavIiev Ioni-
nids, Iul inJevences aIoul lIe IiIeI IeveIs oJ enevg uli-
Iizalion can Ie nade Jvon neasuvenenls oJ nodevn
Iunans and olIev Iiving nannaIs. CaIcuIalions oJ
FMB Jov I3 species oJ snaII nannaI, lIe najovil
veigIing Iess lIan ioo g, avevaged 2.65 lines BMB |Ka-
vasov I992). TIe valio is signiJicanlI Iovev in Iunans,
vanging Jvon I.5 5 lo lines BMB Jov individuaIs un-
devlaIing IigIl and Ieav occupalionaI vovI vespec-
liveI |FAO/WHO/UNU I985). IJ lIe daiI enevg ex-
pendiluve oJ eavIiev popuIalions oJ Hono sapiens is
laIen as appvoxinaleI i.8 lines BMB |lIe vaIue esli-
naled Jov suIsislence Javnevs in deveIoping counlvies
loda [FAO/WHO/UNU I985]), lIen even iJ lIe nela-
IoIic vales oJ lIe Ivain and gul venain al lIeiv IasaI
IeveIs lIeiv conIined conlviIulion, vIicI vepvesenls
3I% oJ BMB, sliII accounls Jov a IigII signiJicanl I7%
oJ lolaI enevg vequivenenls.
A signiJicanl pvopovlion oJ FMB is allviIulaIIe lo lIe
cosl oJ aclivil |Kavasov I992), duving vIicI lIe enevg
denands oJ lIe sIeIelaI nuscuIaluve incvease dvanali-
caII Iul lIose oJ lIe nelaIoIicaII expensive ovgans,
vilI lIe exceplion oJ lIe Ieavl, venain cIose lo lIeiv
vesling IeveIs |LeIningev I975). AnolIev najov conpo-
nenl oJ FMB is an incvenenl oJ Ieal pvoduclion vIicI
occuvs duving lIe assiniIalion oJ nulvienls, lIe sun-
naled eJJecl aIove IasaI nelaIoIisn oJ vIicI is levned
lIe speciJic dnanic eJJecl oJ Jood. TIe exlenl oJ lIis
incvease in enevg expendiluve depends on IolI lIe aI-
soIule quanlil oJ Jood ingesled and ils conposilion. Fov
exanpIe, Jov a vange oJ nannaIian cavnivoves, lIe avev-
age daiI cosl oJ assiniIalion Ias Ieen caIcuIaled as ap-
pvoxinaleI I 5 % oJ lIe lolaI ingesled nelaIoIisaIIe en-
evg |Kavasov i992), vIicI vepvesenls aIoul 40% oJ
BMB. TIe nuIlipIe causes oJ lIis suIslanliaI incvease
in enevg expendiluve ave inconpIeleI undevslood, Iul
conlviIulov Jaclovs incIude addilionaI nelaIoIic acliv-
il I lIe gul ilseIJ due lo lIe enevgelic denands oJ
pvocesses associaled vilI lIe lvanspovl oJ nulvienls
|BIaxlev I989). Since delevninalions oJ BMB ave nade
speciJicaII vilI lIe suIjecl in a poslaIsovplive slale,
lIe vale oJ enevg uliIizalion I lIe gul viII novnaII
Ie IigIev lIan ils IasaI IeveI. ConsequenlI, lIis ovgan
viII Ie vesponsiIIe Jov an even nove signiJicanl pvopov-
lion oJ lolaI enevg expendiluve lIan is indicaled I ils
aIsoIule conlviIulion lo BMB.
EvoIulionav InpIicalions
TIis anaIsis inpIies lIal lIeve Ias Ieen a coevoIulion
Ielveen Ivain size and gul size in Iunans and olIev
pvinales. TIe IogicaI concIusion is lIal no nallev vIal
is seIecling Jov Ivain-size incvease, one vouId expecl a
covvesponding seIeclion Jov veduclion in lIe veIalive size
oJ lIe gul. TIis vouId Ie essenliaI in ovdev lo Ieep lIe
lolaI Iod BMB al lIe lpicaI IeveI. IJ il vas necessav
Jov a pvinale lo Iave a Iavge gul, lIal pvinale vouId
aIso Ie expecled lo Iave a veIaliveI snaII Ivain.
TIis assunes lIal lIe pvinales veve nol IaIancing
lIeiv enevg Iudgels in olIev vas, sucI as opling Jov a
veIaliveI IigI BMB ov aIleving lIe size and/ov nela-
IoIic vequivenenls oJ olIev lissues. A veIaliveI IigI
BMB vouId vequive a covvespondingI IigI enevg in-
laIe, and, unIess lIe envivonnenlaI condilions veve un-
usuaI, lIis vouId nol onI vequive devoling a signiJi-
canlI Iavgev pevcenlage oJ lIe daiI line Iudgel lo
Jeeding IeIaviouv Iul aIso pul lIe aninaI in nove in-
lense conpelilion Jov Iiniled Jood vesouvces. FuvlIev, il
is unIiIeI lIal lIe size oJ olIev nelaIoIicaII expensive
lissues |Iivev, Ieavl, ov Iidnes) couId Ie aIleved suIslan-
TIe exlenl lo vIicI lIe Iivev can Ie veduced in size
duving encepIaIizalion is pvoIaII conslvained I lIe
pavlicuIav enevg vequivenenls oJ lIe Ivain, vIicI uses
gIucose excIusiveI as ils JueI. Since lIe Ivain eJJecliveI
conlains no enevg vesevves, il is cvilicaII dependenl on
lIe conlinuaI suppI oJ gIucose Jvon lIe IIood. IJ lIis
JaIIs appveciaII IeIov ils novnaI concenlvalion oJ
avound 4.5 nM Jov even veIaliveI sIovl peviods, sig-
niJicanl dsJunclion oJ lIe cenlvaI nevvous sslen can
vesuIl. A najov voIe oJ lIe Iivev is lo vepIenisI and nain-
lain lIese IeveIs, IolI I veIeasing gIucose Jvon lIe
IveaIdovn oJ ils gIcogen sloves, vesevves oJ vIicI can
conpvise up lo io% oJ lolaI Iivev nass, and I nanuJac-
luving il Jvon aIlevnalive enevg vesevves noIiIised Jvon
eIsevIeve in lIe Iod. ConsequenlI, lIe enevg de-
nands inposed I incveased encepIaIizalion cannol ex-
ceed lIe capacil oJ lIe Iivev lo slove and ensuve lIe
uninlevvupled suppI oJ lIe gIucose necessav lo JueI
lIis nelaIoIisn.
Since aInosl lIe enlive nass oJ lIe Ieavl consisls oJ
lIe vIlInicaII conlvacling cavdiac nuscIe, il is diJJi-
cuIl lo envisage Iov an signiJicanl veduclion in lIe
size oJ lIis ovgan couId laIe pIace vilIoul conpvonis-
ing ils aIiIil lo nainlain an adequale civcuIalion oJ
IIood avound lIe Iod. TIe nainlenance oJ IigI lissue
pevJusion vales viII Ie pavlicuIavI inpovlanl lo lIe
Ivain, vIicI, Jov lIe veasons discussed aIove, vequives
a conlinuous suppI oJ IigI IeveIs oJ gIucose and ox-
206 l CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI I995
gen. In speciJic veIalion lo Iunans, iJ aclivilies vequiving
a IigI aevoIic scope, sucI as pevsislence Iunling, veve
inpovlanl in lIe node oJ IiJe oJ Ialev Ioninids, lIen
lIis vouId Iave Ieen an addilionaI seIeclion pvessuve
Jov IigI cavdiovascuIav pevJovnance.
AIong vilI lIe Ivain, lIe Iidnes Iave an exlveneI
IigI nelaIoIic vale associaled vilI IigI IeveIs oJ aclive
ion lvanspovl. TIe enevgelic pvocess is nol lIe Jovnalion
oJ lIe pvinav uvine ilseIJ Iul lIe suIsequenl vesovp-
lion oJ valev and soIules Jvon lIis JiIlvale as il passes
lIvougI lIe nepIvons. Since lIe aIiIil oJ lIe Iidne lo
concenlvale uvine is veIaled lo IolI lIe IeveI oJ aclive
lvanspovl and lIe IenglI oJ lIese slvucluves |especiaII
lIe Ioops oJ HenIe), il is IiIeI lIal an veduclion in
eilIev ils enevgelic expendiluve ov ils size viII veduce
lIe naxinun uvine concenlvalion il is capaIIe oJ ex-
cveling. TIe pvoduclion oJ a nove diIule uvine vouId
Iave Ieen a pavlicuIav pvoIIen Jov Ioninids iJ lIe veve
expIoiling veIaliveI open equaloviaI IaIilals vIeve
dvinIing oppovlunilies veve scavce and lIevnoveguIalov
vequivenenls veve aIvead pIacing considevaIIe de-
nands on lIeiv valev Iudgels |WIeeIev i99i).
FinaII, a veduclion in lIe veIalive nass oJ sIeIelaI
nuscIe couId nol Ie used lo IaIance lIe enevg Iudgel
in lIe sane JasIion as veduclion in lIe nass oJ lIe ex-
pensive lissues, Iecause lIe nass-speciJic BMB oJ nus-
cIe lissue is considevaII Iovev lIan lIal oJ an oJ lIe
expensive ovgans and lIe avevage nass-speciJic BMB oJ
lIe Iod as a vIoIe. ConsequenlI, in ovdev Jov a veduc-
lion in sIeIelaI nuscIe nass lo conpensale Jov lIe in-
cveased enevg expendiluve oJ lIe enIavged Iunan Ivain,
appvoxinaleI i9 Ig oJ nuscIe, aIoul 70% oJ lIe lolaI,
vouId Iave lo Ie vepIaced I an equaI anounl oJ lissue
vilI no nelaIoIic cosl al aII.
IJ lIe IpolIesis oJ coevoIulion is covvecl, vIal is
essenliaI Jov undevslanding Iov encepIaIized pvinales
can aJJovd Iavge Ivains is idenliJing lIe Jaclovs lIal
aIIov lIen lo Iave veIaliveI snaII guls. TIe gul is lIe
onI one oJ lIe expensive nelaIoIic lissues lIal couId
vav in size suJJicienlI lo oJJsel lIe nelaIoIic cosl oJ
lIe encepIaIized Ivain. TIe veason Jov lIis is lIal, aI-
lIougI gul size is veIaled lo Iod size, ils size and pvo-
povlions ave aIso slvongI delevnined I diel |CIivevs
and HIadiI I980, I984: Mavlin el aI. I985: MacLavnon
el aI. I986a, I: Mavlin I990). Oul size is associaled vilI
IolI lIe IuII and lIe digesliIiIil oJ Jood |MiIlon I986,
I993: MiIlon and Bennenl I988). Biels cIavaclevized
I Iavge quanlilies oJ Jood oJ Iov digesliIiIil vequive
veIaliveI Iavge guls cIavaclevized I voIuninous and
eIaIovaled Jevnenling cIanIevs |slonacI and/ov snaII
inlesline). An exlvene exanpIe is lIe avliodaclI vuni-
nanls |e.g., covs), vIicI ave JoIivoves, usuaII suIsisling
aInosl enliveI on gvasses. ConvevseI, diels cIavaclev-
ized I snaIIev quanlilies oJ Jood oJ IigI digesliIiIil
vequive veIaliveI snaIIev guls and ave cIavaclevized I
sinpIe slonacIs and pvopovlionaleI Iong snaII inles-
lines |enpIasizing aIsovplion) |CIivevs and HIadiI
I980). Cavnivoves lpiJ lIis pallen.
TIe associalion Ielveen gul size and diel aIso IoIds
vilIin pvinales |CIivevs and HIadiI I984, Mavlin el aI.
I985). Fov exanpIe, MiIlon |I987) Ias enpIasized lIe
veIalionsIip Ielveen lIe veIaliveI snaII gul in CeIus
and a IigI-quaIil and lIeveJove veasonaII eas-lo-
digesl diel conposed oJ sugav Jvuils and pvolein- and
oiI-vicI seeds as veII as soJl-Iodied gvuIs, cicadas, and
snaII vevleIvales. SeavcIing Jov aninaI Joods laIes up
aIoul 40-50% oJ lIeiv Jeeding line Iudgel. TIe veIalive
gul size in lIis pvinale conlvasls slvongI vilI lIal oJ
AIoualla |Jig. 4) vIicI eals a poovev-quaIil diel con-
posed oJ a IigI pevcenlage oJ Ieaves as veII as IolI vipe
and unvipe Jvuils, a signiJicanl pevcenlage oJ vIicI ave
IigII JiIvous Jigs |CvocIell and EisenIevg I987, MiIlon
I988). TIe veIalionsIip Ielveen gul size and diel aIso
IoIds vilIin lIe OId WovId CoIoIinae, vIicI diJJev
Jvon lIe vesl oJ lIe anlIvopoid pvinales nol onI in
lIeiv genevaII veIaliveI Iavgev guls Iul aIso in lIeiv
exceplionaII Iavge slonacIs |CIivevs and HIadiI I980,
Mavlin el aI. I985). FvesIlis vuIicunda, vIicI Ias a
IigI-quaIil diel, conlvasls sIavpI in veIalive gul size
vilI F. cvislalus, vIicI veIies on a nucI poovev-quaIil
diel. WilIin lIe HIoIalidae, HIoIales Iav, vIicI
spends nove line Jeeding on Jvuils lIan on Ieaves, Ias
a veIaliveI snaIIev gul lIan H. sndaclIus, vIicI
spends nove line Jeeding on Ieaves lIan on Jvuils |MiI-
lon I987).
TIeve is aIso a cIose veIalionsIip Ielveen veIalive gul
size and veIalive Ivain size |Jig. 4). AninaIs vilI veIa-
liveI Iavge guls aIso Iave veIaliveI snaII Ivains, vIiIe
aninaIs vilI veIaliveI snaII guls Iave veIaliveI Iavge
Ivains. Hovevev, lIeve aIso appeavs lo Ie a gvade veIa-
lionsIip pvesenl. Fov a given veIalive Ivain size, lIe coIo-
Iines Iave a veIaliveI snaIIev gul lIan lIe ceIids and
IIoIalids: lIe na Iave Iovev veIalive BMBs ovevaII
ov guls vilI IigIev nass-speciJic nelaIoIic vales, ov
lIeiv olIev expensive ovgans na Ie veIaliveI Iavgev
and/ov enevgelicaII nove coslI. TIe vesoIving povev
oJ lIese conpavisons is Iiniled I lIe snaII nunIev oJ
species Jov vIicI gul dala ave avaiIaIIe, lIe snaII nun-
Iev oJ individuaIs sludied vilIin eacI species, and lIe
Jacl lIal Ivain and gul dala do nol cone Jvon lIe sane
individuaIs. Inlevpvelalion is aIso Iiniled I lIe aIsence
oJ dala on lIe aIIonelvies oJ nelaIoIic cosl oJ individuaI
ovgans in non-Iunan pvinales. Hovevev, even vilI
lIese Iinilalions, lIeve appeavs lo Ie a IinIage Ielveen
diel and lIe veIalive sizes oJ lIe gaslvo-inleslinaI lvacl
Iind lIe Ivain.
TIe veIalionsIip Ielveen gul size and Ivain size na
IeIp lo ansvev lIe queslion vI anlIvopoid pvinales
Iave veIaliveI Iavgev Ivains lIan lIe avevage Jov olIev
nannaIs vilIoul aIso Iaving a veIaliveI IigI BMB
|MiIlon I988, Avnslvong I990). TIe
equalion |Jig. 3) Jov lIe veIalionsIip Ielveen gul nass
and Iod nass in lIe anlIvopoid pvinales is
I27I, |4)
vIeve O is gul nass and F is Iod nass, IolI expvessed
in IiIogvans. TIis equalion Ias IolI a Iovev sIope and
a Iovev inlevcepl lIan lIe equalIon vIicI cIavaclevizes
lIe veIalionsIip in non-pvinale nannaIs |Bvod I 945),
AIELLO ANB WHEELEB TIe Expensive-Tissue HpolIesis l 207
I 75I
` 3 6 3
. *2
-0.3 -0.1 0.1 0.3 0.5
BeIalive Bvain Mass
FIO. 4. BeIalive Ivain nass vevsus veIalive gul nass in pvinales, delevnined on lIe Iasis oJ lIe IigIev-pvinale
equalions given in Jiguve 3 and expvessed as lIe vesiduaIs Ielveen lIe Iogged oIsevved and expecled sizes. TIe
covveIalion oJ lIe vesiduaIs is -o.69 |n = i8, p o.ooi, one-laiIed lesl). FiIIed squaves, ceIids: open squaves,
coIoIines: slavs, IIoIalids: 7's, olIev calavvIines: i, AIoualla senicuIus: 2, CeIus apeIIa: 3, FvesIlis cvislalus:
4, F. vuIicunda: 5, HIoIales sndaclIus: 6, H. Iav: 7, Hono sapiens.
TIese equalions suggesl lIal lIe avevage pvinale, vilI
a Iavgev veIalive Ivain size lIan lIe avevage nannaI,
aIso Ias a snaIIev veIalive gul size lIan lIe avevage
TIe veIalionsIip Ielveen veIalive Ivain size and diel
is oJlen nenlioned in lIe Iilevaluve on pvinale encepIa-
Iizalion |e.g., FavIev and OiIson I979: CIullon-BvocI
and Havve I980: OiIson I986: MiIlon I987, I988: Mac-
NaI and EisenIevg i989) and is genevaII expIained in
levns oJ lIe diJJevenl degvees oJ inleIIigence needed lo
expIoil vavious Jood vesouvces. Fov exanpIe, FavIev and
OiIson |I979: OiIson i986) Iave avgued lIal a veIaliveI
Iavge Ivain and neocovlicaI size covveIales vilI onnivo-
vous Jeeding in pvinales, vIicI vequives veIaliveI con-
pIicaled slvalegies Jov exlvacling IigI-quaIil JoodsluJJs.
AIlevnaliveI, CIullon-BvocI and Havve |I980) Iave
suggesled lIal Jvugivoves Iave veIaliveI Iavge Ivain sizes
Iecause lIe Iave veIaliveI Iavgev Ione vanges lIan
JoIivoves, necessilaling a nove sopIislicaled nenlaI
nap Jov Iocalion and expIoilalion oJ lIe Jood vesouvces.
TIe vesuIls pvesenled Ieve suggesl lIal lIe veIalionsIip
Ielveen veIalive Ivain size, and diel is pvinaviI a veIa-
lionsIip Ielveen veIalive Ivain size and veIalive gul
size, lIe Iallev Ieing delevnined I dielav quaIil |Jig.
5). TIis vouId inpI lIal a IigI-quaIil diel is necessav
Jov encepIaIizalion, no nallev vIal na Ie seIecling
......................... . ..............................
FIO. 5. HigI-quaIil diel and incveased
encepIaIizalion. BasIed Iine,
2o8 l CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI I995
1400 -
AvcIaic & nodevn Iunans
Hono eveclus
0 ? z o z Hono evgaslev

Hono IaIiIis/vudoIJensis
200 I I I I
0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5
Age in niIIions oJ eavs
FIO. 6. Incvease in aIsoIule Ioninoid cvaniaI capacil ovev line. Bvain sizes Jvon AieIIo and Bean |I990), ages
Jvon AieIIo and BunIav |I993).
Jov lIal encepIaIizalion. A IigI-quaIil diel veIaxes lIe
nelaIoIic conslvainls on encepIaIizalion I pevnilling
a veIaliveI snaIIev gul, lIeveI veducing lIe considev-
aIIe nelaIoIic cosl oJ lIis lissue.
TIese vesuIls ave conpaliIIe vilI lIe vecenl sugges-
lion I BunIav |i992, I993, n.d.: AieIIo and BunIav
I993) lIal a Iavge Ivain, and pavlicuIavI a Iavge neocov-
lex valio, is veIaled pvinaviI lo gvoup size in pvinales
valIev lIan lo Jeeding slvaleg. Il is cevlainI lvue,
lIougI, lIal a Iavge Ivain size na Iave JaciIilaled nove
conpIicaled exlvaclive Jovaging slvalegies |BunIav n.d.)
and acled as a secondav seIeclion pvessuve Jov encepIa-
Iizalion. A IigI-quaIil diel couId aIso Iave IeneJiled
encepIaIizalion I diveclI incveasing lIe lolaI enevg
avaiIaIIe lo JueI an incveased BMB. TIis vouId Iave
appIied, Iovevev, onI iJ lIe quanlilies oJ IigI-quaIil
Jood consuned veve al Ieasl equaI lo lIose oJ lIe Iovev-
quaIil Jood. In veIalion lo Iunans lIis does nol appeav
lo Ie lIe case. Hunans do nol Iave a veIaliveI IigI
BMB, and, JuvlIevnove, Bavlon |i992) Ias denonslvaled
lIal lIe Iave a signiJicanlI Iovev daiI Jood inlaIe
lIan non-Iunan pvinales vIose diel is oJ Iovev ovevaII
Bvain-Size CIange duving Hunan EvoIulion
Ovev lIe pasl 4 niIIion ov so eavs lIe Ioninid Ivain
Ias expanded Jvon appvoxinaleI 400 lo 500 cc esli-
naled Jov lIe auslvaIopilIecines lo I,400 cc Jov nodevn
Iunans |Jig. 6). TIeve Iave Ieen lvo najov peviods oJ
Ivain expansion. TIe Jivsl covveIales vilI lIe appeav-
ance oJ lIe genus Hono, appvoxinaleI 2 niIIion eavs
ago, vIen aIsoIule Ivain size incveased lo an avevage oJ
654 cc |s.d. = 96.2, n = 8) in H. IaIiIis/vudoIJensis and
appvoxinaleI 850 cc in lIe eavIiesl AJvican H. evgaslev.
TIe second is coincidenl vilI lIe appeavance oJ avcIaic
H. sapiens in lIe Iallev IaIJ oJ lIe MiddIe FIeislocene,
vIen Ivain size incveased lo ils nodevn IeveI |LeigI
I992, BigIlnive 198I). TIis peviod oJ expansion pvoIa-
II vepvesenls an acceIevalion oJ an enIavgenenl lIal
Iad Iegun eavIiev in lIe MiddIe FIeislocene |TvinIaus
and WoIpoJJ n.d.).
WIen Ivain size is covvecled Jov Iod size, eavI Ioni-
nid Ivain size JaIIs eilIev vilIin ov jusl aIove lIe uppev
vange oJ lIe Iiving pvinales |Jig. 7). Even lIe nosl en-
cepIaIized oJ lIe eavI Ioninids ave cIosev in lIeiv veIa-
live Ivain sizes lo lIe genevic avevage EQs oJ lIe non-
Iunan pvinales, pavlicuIavI CeIus and Sainivi, lIan
lIe ave lo lIe EQs oJ nodevn Iunans. BolI CeIus and
Sainivi ave veIaliveI snaII-Iodied pvinales. A considev-
aIIe pvoIIen Jov lIe eavI Ioninids vouId Iave Ieen
lo pvovide lIenseIves, as a Iavge-Iodied species, vilI
suJJicienl quanlilies oJ IigI-quaIil Jood lo pevnil lIe
necessav veduclion oJ lIe gul. TIe oIvious soIulion
vouId Iave Ieen lo incIude incveasingI Iavge anounls
oJ aninaI-devived Jood in lIe diel |SpelI i989: MiIlon
I987, I988).
AIlIougI aII Ioninids ave nove encepIaIized lIan
lIe najovil oJ Iiving pvinale geneva, lIe auslvaIopilIe-
cines sIov an ovevaII Iovev encepIaIizalion lIan nen-
Ievs oJ lIe genus Hono. TIe ave siniIav in degvee oJ
encepIaIizalion lo Fan, HIoIales, and Sainivi, vIicI
suggesls lIal lIe Iad a diel al Ieasl equaI in quaIil lo
lIal oJ lIese pvinales. OoviIIa Ias one oJ lIe Iovesl
IeveIs oJ encepIaIizalion oJ an IapIovIine pvinale, and
AIELLO ANB WHEELEB TIe Expensive-Tissue HpolIesis l 2og
H. IaIiIis H. sapiens
eveclus K
5- H. evgaslev
H. vudoIJensis
A. voIuslus
A. Ioisei
A. aJvicanus I
a3 A. aJavensis ` *I
* .0
--------2 \ \ CeIus

.1E Ai
- -

OoviIIa Fongo
0 34
FIO. 7. EncepIaIizalion quolienls Jov Ioninids, I species |open squaves), conpaved vilI olIev IigIev
pvinales, I genus-apes |pIuses) and nonIes |soIid squaves)-avvanged in ascending ovdev oJ nagnilude.
TIe Iovev EQ Jov nodevn Iunans is Iased on lIe Iod and Ivain nasses used in lIis anaIsis: lIe IigIev
is Iased on a Iod nass oJ 44 Ig and a Ivain nass oJ I,250 g |Havve, Mavlin, and CIullon-BvocI I986).
Honinid dala Jvon McHenv |i994).
lIe nucI IigIev IeveI oJ encepIaIizalion oJ aII oJ lIe
auslvaIopilIecines suggesls a diel oJ signiJicanlI IigIev
quaIil lIan lIal oJ lIis genus. TIis suggeslion oJ a veIa-
liveI IigI-quaIil diel Jov aII oJ lIe auslvaIopilIecines,
and pavlicuIavI Jov lIe voIusl auslvaIopilIecines, is
consislenl vilI evidence Jvon denlaI nicvoveav. Ka
and Ovine |i988) concIude lIal lIe nicvoveav on lIe
noIavs oJ lIe voIusl auslvaIopilIecines vesenIIes lIal
oJ exlanl pvinales lIal eal Iavd Jood ilens, vIiIe lIal
on lIe noIavs oJ lIe olIev auslvaIopilIecines suggesls
lIal lIe suIsisled nove on Ieaves and JIesI Jvuils. Il is
inlevesling lIal CeIus, lIe nosl encepIaIized oJ Iiving
non-Iunan pvinales, nol onI eals Iavd Jood ilens and
cIoseI vesenIIes lIe voIusl auslvaIopilIecines in ils
nicvoveav pallevn |Ka and Ovine i988) Iul aIso Ias a
IigI-quaIil diel |MiIlon i987) and vesenIIes Iunans
in ils gul novpIoIog |Mavlin el aI. I985, MiIlon i987).
Becenl anaIsis oJ IolI lIe slvonliun-caIciun and sla-
IIe cavIon isolope valios oJ AuslvaIopilIecus voIuslus
Jvon SvavlIvans |MenIev i) suggesls an onnivovous
valIev lIan a slviclI vegelavian diel Jov lIese Ioninids
|SiIIen I992, Lee-TIovp, van dev Mevve, and Bvain I994).
Because oJ lIeiv IigIev IeveIs oJ encepIaIizalion,
nenIevs oJ lIe genus Hono vouId Ie expecled lo Iave
Iad an even IigIev-quaIil diel lIan lIe auslvaIopilIe-
cines. SiIIen, Avnslvong, and HaII |n.d.) Iave avgued lIal
lIe diel oJ eavI Hono Jvon SvavlIvans pvoIaII diJ-
Jeved Jvon lIal oJ lIe voIusl auslvaIopilIecines in eilIev
lIe incovpovalion oJ nove undevgvound slovage ovgans
|soJl IuIIs, luIevs, elc.) ov lIe pveJevenliaI consunplion
oJ aninaIs Iaving veIaliveI IigI slvonliun-caIciun va-
lios sucI as Ivaxes. Meal consunplion I eavI Hono
nigIl aIso Ie inJevved Jvon poIisI on OIdovan looIs
|KeeIe and TolI i98i) and I culnavIs on Ione |Folls
and SIipnan I98I, SIipnan I986, Bunn and KvoII
i986), Iul lIeve is aIvas a cevlain degvee oJ uncevlainl
ovev vIicI oJ lIe Ioninids, auslvaIopilIecines ov eavI
Hono, acluaII nade and used lIe looIs. Evidence is
slvongev lIal eavI H. eveclus |H. evgaslev) vas nove
pvedalov and, I inJevence, incovpovaled nove aninaI
pvoducls inlo ils diel lIan lIe eavIiev Ioninids |SIip-
nan and WaIIev i989). Suppovl Jov lIis inlevpvelalion
vesls pvinaviI on lIe poslcvaniaI sIeIelon, vIicI sug-
gesls a nove eJJicienl adaplalion lo vapid Ioconolion.
SIipnan and WaIIev aIso suggesl lIal lIe AcIeuIian
looI lvadilion nigIl Ie inlevpveled as indicaling gvealev
veIiance on and incveased Jvequenc oJ lIe pvocessing oJ
aninaI lissues.
Il is diJJicuIl lo inJev veIalive gul size Jov lIe Ioninids,
Iecause, unIiIe lIe Ivain, lIe gul is nol encased in a
Ion capsuIe vIose voIune can Ie neasuved. Hovevev,
cevlain Jealuves oJ lIe poslcvaniaI sIeIelon oJ WT-i 5000
|H. evgaslev) suggesl lIal lIis Ioninid Iad a snaIIev
veIalive gul size |consislenl vilI ils IigIev IeveI oJ en-
cepIaIizalion) lIan did lIe auslvaIopilIecines, vepve-
senled I AL-288-I |A. aJavensis). TIe Iavge gul oJ lIe
Iiving pongids gives lIeiv Iodies a sonevIal pol-IeIIied
appeavance, IacIing a discevniIIe vaisl. TIis is Iecause
lIe vounded pvoJiIe oJ lIe aIdonen is conlinuous vilI
lIal oJ lIe Iovev povlion oJ lIe viI cage, vIicI is sIaped
IiIe an invevled JunneI, and aIso Iecause lIe IunIav
vegion is veIaliveI sIovl |lIvee lo Jouv IunIav vevleIvae)
|Jig. 8). TIe navvoving oJ lIe uppev povlions oJ lIe lIo-
vacic cage is associaled vilI lIe exlveneI povevJuI
2IO CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI I995
4 /
FIO. 8. TvunIs oJ a cIinpanzee |IeJl), a Iunan |cenlev), and AuslvaIopilIecus aJavensis |vigIl), sIoving lIe
pvolvuding viI cage in lIe Iallev. |A. aJavensis veconslvuclion aJlev ScInid I983, cIinpanzee and Iunan aJlev
ScIuIlz 1950.)
nuscIe conpIex oJ lIe peclovaI givdIe used duving avIo-
veaI Ioconolion |ScInid i99i). TIe veconslvucled viI
cage oJ A. aJavensis |ScInid i983) indicales lIal lIese
Ioninids velained a JunneI-sIaped lIovax siniIav lo lIal
oJ lIe cIinpanzee. A. aJavensis diJJevs Jvon lIe pongids
onI in Iaving a Iongev IunIav vegion |six IunIav vevle-
Ivae). AddilionaI cIues aIoul lIe pvopovlions oJ lIe aI-
doninaI ovgans oJ auslvaIopilIecines ave pvovided I lIe
slvucluve oJ lIe peIvis, vIicI, Iecause oJ lIeiv IipedaI
posluve, pvovided sone suppovl lo lIis vegion oJ lIe
Iod. BolI A. aJavensis |Tague
and Lovejo I986, BuJJ
1991) and A. aJvicanus |BoIinson I972) possessed vide
peIves veIalive lo lIeiv slaluve, lIe oulvavdI JIaved up-
pev navgins oJ vIicI ave consislenl vilI lIe pvesence
oJ a veII-deveIoped and pvoluIevanl aIdonen |ScInid
Fongid and auslvaIopilIecine lvunI novpIoIog con-
lvasls vilI lIal oJ nodevn Iunans. TIe IavveI-sIaped
lIovacic cage and veIaliveI snaIIev peIvis oJ H. sapiens
Iovdev a navvovev aIdoninaI vegion vilI a dislincl
vaisl aIsenl in lIe lvunI oJ apes. H. evgaslev is lIe Jivsl
Inovn Ioninid lo appvoxinale nodevn Iunan Iod
pvopovlions |BuJJ and WaIIev I993). TIe inJevence is
lIal il nosl pvoIaII aIso Iad a veIaliveI snaIIev gul.
Modevn Iunan lvunI pvopovlions in eavI Hono vouId
Iave Iad addilionaI signiJicance iJ aclive Iunling and/
ov Iong-dislance nigvalion vas inpovlanl lo lIe ecoIog
oJ lIese Ioninids. HigI IeveIs oJ suslained aclivil ve-
quive an exlveneI eJJicienl cavdiovascuIav sslen, lIe
Ie conponenls oJ vIicI ave Iocaled vilIin lIe lIo-
vacic cage. In apes and auslvaIopilIecines lIe conslvuc-
lion oJ lIe sIouIdev givdIe veslvicls lIe eIevalion oJ lIe
uppev povlion oJ lIeiv JunneI-sIaped viI cages duving ves-
pivalion |ScInid i99i). VenliIalion oJ lIe Iungs vas
pvoIaII nainI dependenl on lIe novenenls oJ lIe
diapIvagn and vouId lIeveJove Iave Ieen Iess eJJeclive
lIan in Hono, in vIicI lIe uppev pavl oJ lIe viI cage
can Ie vaised lo enIavge lIe lIovax duving inspivalion.
In addilion lo lIis pIsioIogicaI considevalion, ScInid
|i99i) Ias idenliJied IionecIanicaI advanlages oJ lIe
Hono Iod Jovn. A signiJicanlI navvovev vaisl lIan
in lIe auslvaIopilIecines vouId Iave aIIoved lIe avns
lo sving nove JveeI in lIe Ioveved posilion and pevnil-
led gvealev lovsion in lIe aIdoninaI vegion, IolI oJ
vIicI ave essenliaI in slaIiIising lIe uppev Iod duving
IipedaI vunning.
TIese oIsevvalions ave veIevanl lo lIe Jivsl navIed
incvease in Ioninid Ivain size. Fov lIe second incvease,
lIe inlvoduclion oJ cooIing na Iave Ieen an inpovlanl
Jaclov. CooIing is a lecInoIogicaI va oJ exlevnaIising
pavl oJ lIe digeslive pvocess. Il nol onI veduces loxins
in Jood Iul aIso incveases ils digesliIiIil |SlaII I984,
Sussnan i987). TIis vouId Ie expecled lo naIe diges-
lion a nelaIoIicaII Iess expensive aclivil Jov nodevn
Iunans lIan Jov non-Iunan pvinales ov eavIiev Ioni-
nids. CooIing couId aIso expIain vI nodevn Iunans
ave a Iil nove encepIaIized Jov lIeiv veIalive gul sizes
lIan lIe non-Iunan pvinales |see Jig. 4).
AIlIougI lIeve is sliII nucI lo Ieavn aIoul enevg IaI-
ances in Iunans and non-Iunan pvinales, a picluve is
enevging lIal is consislenl vilI a IinIage Ielveen
Ioninid diel and lIe veIalive sizes oJ lIe gaslvo-
inleslinaI lvacl and lIe Ivain. Ouv vovI conpIenenls
lIal oJ MiIlon |I986, I993: MiIlon and Bennenl i988),
vIicI suggesls lIal lIe enevgence oJ lIe Ioninids, and
pavlicuIavI oJ Hono, vas associaled vilI lIe incovpova-
lion oJ IigIev-quaIil JoodsluJJs inlo lIe diel. A IigI-
quaIil diel vas pvoIaII associaled vilI a veduclion in
AIELLO ANB WHEELEB TIe Expensive-Tissue HpolIesis
lIe size and lIeveJove lIe enevgelic cosl oJ lIe gul. IJ
lIis is covvecl, encepIaIizalion in lIe Ioninids vas aIIe
lo pvoceed vilIoul pIacing an addilionaI denands on
lIeiv ovevaII enevg Iudgels. FuvlIevnove, iJ lIe expIoi-
lalion oJ lIese IigI-quaIil Joods, sucI as aninaI pvod-
ucls, nuls, ov undevgvound luIevs, vequived nove con-
pIex IeIaviouvs, lIen lIis aIso couId Iave acled as one
oJ lIe seIeclion pvessuves Jov lIe oIsevved incvease in
Ivain size. FuvlIev incveases in Ivain size nigIl veII
Iave Ieen JaciIilaled I lIe inlvoduclion oJ cooIing lo
vendev Jood nove digesliIIe.
TIese concIusions ave devived Jvon lIe genevaI oIsev-
valion lIal lIeve is no signiJicanl covveIalion Ielveen
veIalive IasaI nelaIoIic vale and veIalive Ivain size in
Iunans and olIev encepIaIized nannaIs. IJ an encepI-
aIized aninaI does nol Iave a covvespondingI eIevaled
BMB, ils enevg Iudgel nusl Ie IaIanced in sone olIev
va. TIe expensive-lissue IpolIesis suggesled Ieve is
lIal lIis IaIance can Ie acIieved I a veduclion in size
oJ one oJ lIe olIev nelaIoIicaII expensive ovgans in
lIe Iod |Iivev, Iidne, Ieavl, ov gul). We avgue lIal lIis
can Iesl Ie done I lIe adoplion oJ a IigI-quaIil diel,
vIicI pevnils a veIaliveI snaII gul and IiIevales a sig-
niJicanl conponenl oJ BMB Jov lIe encepIaIized Ivain.
No nallev vIal vas seIecling Jov encepIaIizalion, a veI-
aliveI Iavge Ivain couId nol Ie acIieved vilIoul a covve-
spondingI incvease in dielav quaIil unIess lIe nela-
IoIic vale vas covvespondingI incveased.
Al a nove genevaI IeveI, lIis exevcise Ias denon-
slvaled olIev inpovlanl poinls. Fivsl, diel can Ie inJevved
Jvon aspecls oJ analon olIev lIan leelI and javs. Fov
exanpIe, an indicalion oJ lIe veIalive size oJ lIe gaslvo-
inleslinaI lvacl and consequenlI lIe digesliIiIil oJ lIe
Jood sluJJs Ieing consuned is pvovided I lIe novpIoI-
og oJ lIe viI cage and peIvis. Second, an dielav inJev-
ence Jov lIe Ioninids nusl Ie consislenl vilI aII Iines
oJ evidence. TIivd, lIe evoIulion oJ an ovgan oJ lIe
Iod cannol pvoJilaII Ie sludied in isoIalion. OlIev ap-
pvoacIes lo undevslanding lIe cosl oJ encepIaIizalion
Iave genevaII JaiIed Iecause lIe Iave lended lo IooI
al lIe Ivain in isoIalion Jvon olIev lissues. TIe expen-
sive-lissue IpolIesis pvoJilaII enpIasizes lIe essen-
liaI inlevveIalionsIip Ielveen lIe Ivain, BMB, and olIev
nelaIoIicaII expensive Iod ovgans.
CIesapeaIe InJovnalion Sslens, AnnapoIis, Md.
21401, U.S.A. |73o71.156iOconpusevve.con). 7 x 94
AieIIo and WIeeIev pvopose lIal a IigI-quaIil diel
aIIovs a Iavgev pevcenlage oJ an aninaI's lolaI enevg
vesevves lo go lo lIe Ivain lIan vouId olIevvise Ie lIe
case Iecause lIe nelaIoIicaII expensive gul is veduced
in size. TIeiv suggeslion pvovides a soIid Iead inlo lIe
queslion Iov nonIunan pvinales can aJJovd lo expend
aIoul lvice as nucI and Iunans aIoul Jouv lines as
nucI enevg on lIeiv Ivains as nosl olIev nannaIs
|Avnslvong 1985a, I, i990).
Queslions venain, Iovevev. AieIIo and WIeeIev pvo-
pose lIal Jov Iunan encepIaIizalion, lIe enevg saving
slenning Jvon a veduced gul size is suJJicienl lo eIini-
nale lIe need Jov olIev Jovns oJ consevvalion. One oJ
lIe allviIules oJ lIe Ivain is lIal il uliIizes gIucose and
does nol svilcI lo gIcogen vIen vesevves vun Iov, in
conlvasl lo nuscIes, vIicI can veadiI sIiJl Jvon one
Jovn oJ enevg lo anolIev. Bo lIe spIancInic ovgans ve-
senIIe nuscIe in lIeiv use oJ gIcogen, ov ave lIe, IiIe
lIe Ivain, veslvicled lo gIucose? IJ lIe use and slove
gIcogen, pavl oJ lIeiv veigIl is in lIe Jovn oJ pvepacI-
aged enevg, and sone sIavpening oJ lIe anaIsis na
Ie caIIed Jov.
TIe diJJevences Ielveen lIe expecled and oIsevved
sizes oJ Iunan ovgans and nelaIoIic cosls vepovled in
lIe papev ave Iased on pvinale dala. Oiven lIal pvinales
diJJev Jvon olIev nannaIs IolI in Iaving veIaliveI Iig
Ivains Jov lIeiv enevg vesevves and in uliIizing a Iavgev
pevcenlage oJ lIose enevg vesevves Jov lIeiv Ivains
|Avnslvong I985a, I, i990), does a cIange in veIalive
gul size accounl Jov Iov pvinale encepIaIizalion diJJevs
Jvon lIal in olIev nannaIs, ov is sone olIev necIa-
nisn ov slvucluvaI sIiJl inpovlanl Ieve?
HpolIeses aIoul JunclionaI IioIog lIal veIale lo a
singIe species ave veaIev lIan lIose vIicI can expIain
diJJevences in nan. TIe conneclion Ielveen diel and
lIe expensive-Ivain IpolIesis viII Ie slvenglIened iJ
AieIIo and WIeeIev can poinl lo siniIav Jindings in olIev
laxa. Bivds vilI Iov nelaIoIic vales Iave veIaliveI
snaIIev Ivains lIan lIose vilI slandavd nelaIoIic vales,
pavaIIeIing oIsevvalions anong nannaIs |Avnslvong
and Bevgevon i985). TIe veIalionsIip oJ ovIs lo olIev
Iivds, Iovevev, vesenIIes lIal oJ pvinales lo olIev
nannaIs: ovIs Iave veIaliveI Iavge Ivains given lIeiv
lolaI enevg suppI. Bo ovIs suppovl lIeiv veIaliveI Iig
Ivains vilI veduced guls? A posilive Jinding vouId
slvenglIen lIe aulIovs' IpolIesis. In olIev silualions,
negalive Jindings nigIl aIso slvenglIen lIe IpolIesis.
Bal species diJJev in nelaIoIisn, diel, and encepIaIiza-
lion, inseclivovous Ials Iaving veIaliveI snaIIev Ivains
and Iovev nelaIoIic vales lIan noninseclivovous ones.
TIe diJJevences in veIalive Ivain size disappeav, Iovevev,
vIen lIe diJJevences in nelaIoIisn ave laIen inlo ac-
counl: vIen lIe slandavd Iecones lolaI enevg vesevves
valIev lIan sinpIe Iod veigIl, lIe Ial species Iave
equivaIenl degvees oJ encepIaIizalion |Avnslvong i983).
In lIis case, one vouId nol expecl lo Jind a diJJevence
in gul size Ielveen dielav gvoups oJ Ials. TIus lesls Jov
lIe genevaIil oJ lIe IpolIesis na Ie Jound oulside oJ
lIe pvinale ovdev.
AIlIougI lIe vI oJ incveased Ivain size is oJ genevaI
inlevesl, IpolIeses concevning lIis allviIule viII Ie
veaI unliI ve cone lo undevslnd Iov Ivains can aJJovd
lo incvease in size and vIal slvucluvaI nodiJicalions ave
covveIaled vilI lIal incvease. TIis papev is a veIcone
addilion lo ouv InovIedge.
CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI I995
Bepavlnenl oJ AnlIvopoIog, Slale Univevsil oJ Nev
YovI al AIIan, AIIan, N. Y. I2222, U.S.A.
5 x 94
As AieIIo and WIeeIev poinl oul, a Jev vovIevs Iave
suggesled lIal Ivain size dala veveaI lvo peviods oJ
expansion ovev lIe pasl Jouv niIIion eavs oJ Ioninid
evoIulion. Hovevev, an eavIiev suvve oJ lIe Iilevaluve
JaiIed lo Jind vide suppovl Jov a punclualed-equiIiIviun
nodeI oJ Ioninid Ivain size evoIulion: in Jacl, vales oJ
evoIulionav cIange in cvaniaI capacil |niIIidavvins)
suggesl lIal Ivain enIavgenenl in Hono appeavs lo Ie
aulocalaIlic, lIe dala suppovling a souped-up vevsion
oJ lIe gvaduaIisls' nodeI |FaII i987). LeigI |i992ii),
exanining lvends in cvaniaI capacil, concIudes lIal
pveviousI pvoposed punclualed equiIiIviun nodeIs do
nol adequaleI descviIe Ialev Ioninid evoIulion. Fuv-
lIevnove, vales oJ Ivain size incvease in Hono eveclus
and eavI H. sapiens cannol Ie slalislicaII dislin-
guisIed. In sIovl, nove dala ave soveI needed lo assevl
lIal a Iuvsl oJ Ivain expansion coincided vilI lIe ap-
peavance oJ avcIaic Hono.
TIal said, il is nevevlIeIess lvue lIal lIe pasl lvo
niIIion eavs Iave vilnessed a dvanalic incvease in
Ivain size in lIe genus Hono. EIucidalion oJ lIe pvine
novevs Jov lIis incvease Ias Iecone a Javovile pasline
in paIeoanlIvopoIog |FaII i992). Candidales incIude
Iunling, looI pvoduclion, vavJave, vovI, sociaI inleIIi-
gence, and Ianguage. TIe pvoIIen vilI lIese IeIaviovaI
pvine novevs, Iovevev, is lIal lIe ave IigII specuIa-
live and do nol Iend lIenseIves veII lo IpolIesis lesl-
ing. In conlvasl lo nosl pvine-novev lIeovies, lIe pves-
enl avlicIe is gvounded in pIsioIog and conpavalive
analon. As a vesuIl, il is suppovled I quanliJied dala
and paves lIe va Jov coIIeclion oJ nove dala and JuvlIev
lesling oJ veIaled IpolIeses. TIe expensive-lissue I-
polIesis aIso diJJevs Jvon lIe aIove conjecluves in lIal
il suggesls a pIsioIogicaI/analonicaI conpIex lIal
acled as a pvine veIeasev pevnilling seIeclion Jov in-
cveased Ivain size valIev lIan specuIaling aIoul one I-
polIelicaI IeIaviov lIal vas lIe pvinav lavgel oJ lIal
seIeclion |i.e., a pvine novev).
In a nulsIeII, lIe expensive-lissue IpolIesis pvo-
poses lIal a IigI-quaIil diel pevnilled a veIaliveI
snaIIev gul and lIeveI veIaxed a nelaIoIic conslvainl
on Ivain size. EIsevIeve, I Iave pvoposed anolIev pIsi-
oIogicaI/analonicaI conpIex as a pvine veIeasev oJ Ivain
size in lIe genus Hono, naneI, evoIulion oJ a nelvovI
oJ cvaniaI veins |a vadialov) lIal sevves lo cooI lIe
Ivain undev condilions oJ IpevlIevnia |FaII 1990).
Heve I suggesl lIal lIe lvo IpolIelicaI veIeasevs ave
conpaliIIe Iecause ceveIvaI nelaIoIisn, veIalive Ivain
size, and lIevnoIlic needs ave aII inlevlvined. IJ IolI
veIeasevs veve inslvunenlaI duving Ioninid evoIulion,
pevIaps lIe undevIing IeIaviovaI Jaclovs |diel Jov ne-
laIoIisn, Ioconolion Jov vascuIav evoIulion) na Ie vo-
ven inlo a salisJing |iJ nol JaIsiJiaIIe) scenavio.
Bvains ave exquisileI Ieal-sensilive, and Iunan
Ivains Iave pavlicuIavI gveal cooIing needs. One veason
Jov lIis is lIal lIe valio oJ ceveIvaI lo Iod-vesling nela-
IoIic vales incveases vilI incveased Iod size in nan-
naIs, and Iunans ave veIaliveI Iavge nannaIs |Capula
i98i). |BMB decveases considevaII vilI incveasing
Iod size in nannaIs vIeveas ceveIvaI nelaIoIic vale
decveases onI sIigIlI vilI incveasing Iod size.) A sec-
ond veason lIal Iunan Ivains Iave gveal cooIing needs
is lIal Iunans ave IigII encepIaIized-lIal is, lIe
Iave veIaliveI Iavge Ivains genevaling polenliaII dan-
aging Ieal given lIeiv Iod sizes. Fov exanpIe, as AieIIo
and WIeeIev oIsevve, lIe acluaI nelaIoIic oulpul Jov
lIe Iunan Ivain |I4.6 W) is nucI Iavgev lIan lIe 3 W
expecled Jov a nannaI oJ siniIav Iod size.
TIe queslion, lIen, is nol onI WIeve does lIe en-
evg cone Jvon lo JueI lIe encepIaIized Ivain? Iul aIso
WIeve do lIe vesouvces cone Jvon lo cooI lIe encepIa-
Iized Ivain? AieIIo and WIeeIev pvopose a sIiJl lo a IigI-
quaIil diel |vilI a veduclion oJ gul) as an ansvev lo lIe
Jivsl queslion. I pvopose veJinenenl oJ IipedaIisn undev
Iol savanna condilions |vilI a cIange in cvaniaI vascu-
Ialuve) as an ansvev lo lIe second |FaII i990). Weaving
lIese lvo logelIev, ve na nov specuIale aIoul vIal
eavI Ioninids veve doing oul lIeve on lIe savanna-
naIe lIe veve vovIing oul and IooIing Jov veg-
gie Iuvgevs/Big Macs! TIis Jils vilI WIeeIev's |i988)
nidda-scavenging IpolIesis |vIicI sIouId pevIaps Ie
velilIed Sland TaII, Sla CooI, and Fig Oul). On a JinaI
nole, convevgenl evoIulion Jov incveased encepIaIiza-
lion Ias occuvved independenlI in cevlain vIaIes and
IigIev pvinales. TIe veIaliveI Iavge Ivains oJ vIaIes
genevale a good deaI oJ Ieal despile lIeiv aqualic IaIi-
lals. In Ieeping vilI lIis, a vecenl vepovl suggesls lIal
al Ieasl one species oJ vIaIe Ias independenlI evoIved
a nel oJ IIood vesseIs lIal connecl vilI lIe Iase oJ lIe
sIuII and pvolecl lIe Ivain Jvon IpevlIevnic IIood
JIov |Fovd and Kvaus i992). In IigIl oJ lIe expensive-
lissue IpolIesis, one vondevs vIal gul/diel dala
nigIl veveaI aIoul Iig-Ivained celaceans. Il venains lo
Ie seen iJ olIev pIsioIogicaI Jaclovs viII Ie idenliJied as
polenliaII inpovlanl Jov invesligaling Ioninid |Ivain)
evoIulion. I Iope so Iecause, in n opinion, pIsioIogi-
caI IpolIeses cevlainI Ieal slovleIIing.
BioIogicaI AnlIvopoIog BeseavcI Fvogvanne,
Univevsil oJ lIe Wilvalevsvand, MedicaI ScIooI,
FavIlovn 2I93, SoulI AJvica. 30 I7 94
TIe IpolIesis advanced I AieIIo and WIeeIev, aI-
lIougI lIe do nol expIicilI sa so, JoIIovs lIe oId
FisIevian lIeoven equaling Bavvinian Jilness vilI en-
evgelic eJJicienc oJ vepvoduclion |FisIev I930). Il does
nol pvelend lo idenliJ lIe causes oJ lIe incvease oJ lIe
Ivain size in Ioninid evoIulion: il sinpI poinls lo
vIal lIe aulIovs considev a condilio sine qua non Jov
lIal incvease. TIe Iogic is cIeav vilIin lIe pavadigns
and nunevicaI dala sels enpIoed.
AIlIougI il deaIs vilI evoIulion, lIe enlive papev
vovIs on lpoIogicaI pvincipIes. Enevg needs ave pve-
dicled Jov a lpicaI pvinale: IunanIind is vepvesenled
AIELLO ANB WHEELEB TIe Expensive-Tissue HpolIesis
I a slandavd naIe, and il seens Jvon lIe Iod veigIl
oJ 65 Ig lIal il is a vIile one. Vavialion in Iunan
Ivain size and Iod size is vev considevaIIe, pvoducing
an enovnous nunIev oJ conIinalions oJ Ivain, gul, and
lolaI Iod sizes and Ience vide vanges oJ encepIaIiza-
lion quolienls. TIe avevage veigIl seens lo Ie cIosev
lo 5 5 lIan lo 65 Ig |HenneIevg i990). TIe dala pvesenled
Ieve on lIe nass-speciJic nelaIoIic vales oJ vavious ov-
gans vav considevaII even iJ one aIIovs Jov inlevspe-
cies diJJevences and discvepancies in IaIovalov lecI-
niques |conpave laIIe i and laIIe 3). Il is lIus diJJicuIl
lo ascevlain Iov veIiaIIe lIe eslinales oJ nelaIoIic
incvenenls in laIIe 4 ave and Iov nan Iunan indi-
viduaIs vouId conJovn lo lIen.
TIeve is IillIe douIl lIal lIe aIsoIule size oJ lIe Ion-
inid Ivain incveased duving lIe Iislov oJ lIis Iineage
vIiIe veIiance on IigIev-quaIil Joods, especiaII neal,
incveased, Ieading lo lIe veduclion in lIe size oJ lIe
gaslvoinleslinaI lvacl. WIelIev lIis concuvvence indi-
cales inlevdependence is anolIev nallev. TIe cIanges
in BMB caused I lIe 850 g incvease in Ivain size ave
snaII- 9.5 W, covvesponding lo io. 5 % oJ lIe lolaI BMB,
as indicaled I lIe aulIovs, ov lo 5.8% oJ lIe FMB, caI-
cuIaled as i.8BMB. TIus a sinpIe dvop in FMB lo
I .7BMB vouId nove lIan conpensale Jov incveased
Ivain enevg consunplion. TIe anounl oJ enevg in
queslion equaIs lIal expended duving 45 ninules' Iei-
suveI vaIIing |4 In/Iv.) ov lIe cIange in BMB accon-
paning cIange in Iod nass I 6.8 Ig-Iess lIan lIe
diJJevence Ielveen lIe avevage Jov IunanIind |5 5-5 8
Ig [HenneIevg i990]) and lIe aulIovs' assuned
65 Ig.
A cIange oJ a Jev degvees in lIe lenpevaluve oJ lIe
innediale envivonnenl nigIl save lIe vequived
anounl oJ enevg, and so vouId a nodevale decvease
in IaIiluaI Jood inlaIe-dieling individuaIs can veduce
lIeiv vesling enevg expendiluve I as nucI as 30%
|LanI i984). Il seens lIal exlending lIe line laIen up
I sIeep vouId aIso do lIe lvicI. TIe posluIaled incvease
in enevg vequivenenl oJ lIe Iavgev Ivain couId Ie aI-
sovIed in nunevous vas olIev lIan lIe veduclion in
lIe size oJ lIe gaslvoinleslinaI lvacl.
TIe queslion venains, WI do ve need a Iavgev Ivain?
Musl il Ie aIsoIuleI Iavgev, as in a poov goviIIa scoving
so aIsnaII on lIe encepIaIizalion quolienl and el
consideved inleIIecluaII cIosev lo Iunans lIan ceIids,
ov sinpI veIaliveI Iavgev as indicaled I lIal quolienl?
In nosl neasuves oJ encepIaIizalion, Ivain size is ex-
pvessed as a |vaviousI caIcuIaled) Jvaclion oJ Iod size.
A Iavgev gul conlviIules lo lIe incvease in Iod size nol
onI diveclI Iul aIso lIvougI lIe vequivenenl oJ in-
cveased nuscIe and sIeIelaI nass lo cavv il avound.
TIus a Iavgev gul neans considevaII gvealev Iod nass
and Ience a Iavgev denoninalov Jov lIe encepIaIizalion
quolienl and a snaIIev quolienl-sinpIe avilInelic
valIev lIan sone IioIogicaI pIenonenon. Is Iiggev veaII
TIe lIveeJoId incvease in Ioninid Ivain size since lIe
FIiocene is pavaIIeIed I a 3.2 lines incvease in Ivain
size in equids |Jvon 270 g in FIioIippus lo 870 g in nod-
evn Iovse [Jevison I973]) and does nol seen exceplionaI.
TIe uniqueness oJ Ioninid evoIulion vesls in lIe IacI
oJ expecled incvease in Iod size-lIus a veduclion oJ
Iod size veIalive lo Ivain size. TIis ovevaII veduclion
vesuIls Jvon exlevnaIizalion oJ Junclions. AieIIo and
WIeeIev covveclI poinl lo cooIing as an exanpIe, Iul
lIe Iisl is nucI Iongev. ExlevnaIizalion Ieads lo a veduc-
lion in lIe ovevaII enevg vequivenenls oJ lIe Iunan
Iod-lIe anounl oJ nuscIe and consequenlI lIe vo-
Iuslicil oJ lIe sIeIelon and lIe size oJ lIe visceva sev-
vicing lIe Iod decvease ov, valIev, Jov nosl oJ Ioninid
evoIulion do nol incvease al a vale connensuvale vilI
lIe incvease oJ lIe Ivain. Fvon lIe levninaI FIeislocene,
Iovevev, unliI sevevaI Iundved eavs ago, lIe ovevaII
size oJ lIe Iunan Iod acluaII decveased |Fvaev I984,
JacoIs i985). Il seens lIal lIis genevaI slvucluvaI ve-
duclion oJ lIe Iunan Iod is vesponsiIIe Jov ouv Iavge
encepIaIizalion quolienl.
Bepavlnenl oJ AnlIvopoIog, CoIunIia Univevsil,
Nev YovI, N.Y. I0027, U.S.A. 26 7 94
TIis inlviguing papev ougIl lo pvovide considevaIIe Jod-
dev Jov lIougIl, veneved lesling, and, ideaII, snlIesis
vilI olIev aspecls oJ possiIIe Ivain-IeIaviov-gvovlI
conslvainls. As inlviguing as il is, Iovevev, I venain
sIeplicaI lIal lIese econonics-Iased nodeIs |incIuding
BunIav's ideas vegavding lIe neocovlex and Ianguage as
a cIeap Jovn oJ sociaI gvooning [see BunIav I993 and
n vesponse]) gel us an neavev lo undevslanding lIe
veIalionsIips Ielveen Ivains and IeIaviov lIal nigIl
Iave Ieen lavgels Jov pasl seIeclion pvessuves. M pvoI-
Ien evev since i 966, vIen I Jivsl puIIisIed on lIe ques-
lion oJ Ivain size in Iunan evoIulion, Ias Ieen lIal I
cannol see lIe Ivain as a unilav ovgan vilI a sinpIe
IeIaviovaI lasI lo acconpIisI sucI as inleIIigence,
Ianguage, adaplive IeIaviov, ov an olIev sucI ped-
agogicaI Jig IeaJ lo covev ouv ignovance aIoul Iov lIe
Ivain evoIved. To ne lIe Ivain is conposed oJ a nuIli-
lude oJ pavls lIal sevve nunevous IeIaviovaI Junclions
lIal can Iave IiJe-ov-dealI consequences depending on
Iov civcuils ave aclivaled ov inIiIiled, inJovnalion is
pvocessed, and aclion pallevns ave naniJesled in envi-
vonnenls vilI conpIex inlevdependencies Ielveen lIe
sociaI and naleviaI. Can sucI nacvoevoIulionav nod-
eIs possiII accounl Jov nill-gvill veaI-IiJe seIeclion
vaIIs lIal pavlicuIav Ioninid gvoups looI lIvougI a
niIIion ov so eavs |HoIIova I97984-85)?
I vondev iJ lIe aulIovs sIouId Ie so cevlain lIal
vIalevev lIe seIeclion pvessuves lIe evoIulion oJ pvi-
nale Ivains Iad lo JoIIov lIis pavlicuIavI inlevesling
sel oJ conslvainls. WIeve ave lIe dala lIal viII sIov
vavialion in lIese pavanelevs in a popuIalion and indi-
cale vIicI vavialions ave Javoved? WiII lIe appIicalion
oJ lIese econonic nodeIs expIain vI cIinpanzees |Io-
noIos and lvogIodles), goviIIas, ovangulans, elc., IeIave
as lIe do |since lIe onI neuvaI vaviale evev discussed
is lolaI Ivain size)? Can ve lIinI a Iil nove deepI aIoul
CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI I995
jusl vIal Ivain size is? Ave aII neuvaI lissues equaII as
enevg-Iungv and expensive?
Having vaiIed againsl vieving Ivain size as lIe end-aII
oJ lIe neuvaI suIslvale undevIing IeIaviov lIal vavies
and is evenluaII seIecled Jov |ov againsl) aII lIese eavs,
I an cIagvined lo adnil lIal I cevlainI Iaven'l cone
an cIosev lo sonelIing nove suIslanlive lIan nolions
oJ veovganizalion. I cannol IeIp Iul JeeI lIal ve ave
Iuvdened I ouv Jixalion on vIal ve can easiI neasuve,
Ivain size, and ovevIooI lIe veIalionsIips lIal Iave
enevged ovev lIe pasl 50 eavs Ielveen neuvaI nucIei
and lIeiv JiIev lvacls and IeIaviov. AieIIo and WIeeIev
oJJev a diJJevenl and inlviguing scenavio Ieve, and I IooI
Jovvavd lo Ieaving nove.
TIe exlvapoIalion lo Jeeding adaplalions Jvon viI cage
and peIvic novpIoIog |i.e., Ielveen A. aJavensis and
Hono) is inlevesling, Iul I vondev Iov Jeeding slvale-
gies and gul size can Ie veIaled lo nelaIoIic conslvainls
and Ivain size vilIin lIe Ioninids. As I see lIe vecovd,
lIeve ave lines vIen Ivain size seens lo Iave incveased
vilIoul nucI conconilanl Iod-size incvease |e.g.,
Hono eveclus lo avcIaic Hono, 800-goo
nI lo aIoul
I,200-I,300 nI) ov vIen lIe Ivain-size incvease nigIl
Ie veIaled |al Ieasl pavliaII) aIIonelvicaII lo Iod size
|e.g., Hono IaIiIis lo H. vudoIJensis ov AuslvaIopilIe-
cus aJavensis lo A. aJvicanus ov even, possiII, avcIaic
Hono lo H. neandevlIaIensis). TIe vecovd suggesls lo
ne lIal lIeve vas pIenl oJ Ielevogeneil oJ possiIIe
cause-eJJecl veIalionsIips Ielveen Ivains, Iodies, Jeed-
ing, and IeIaviovs vilIin an ongoing evoIulionav pe-
viod oJ lIe pasl 2 niIIion eavs |see, e.g., HoIIova 1980
II 9). I sinceveI douIl lIal Jeeding and Ivain-gul-size
inlevdependencies can expIain lIese inlevdependenl
Bepavlnenl oJ SocioIog and AnlIvopoIog, Miani
Univevsil, OxJovd, OIio 45056, U.S.A. II 7 94
AieIIo and WIeeIev's expensive-lissue IpolIesis is a
nuIliJacled nodeI oJ Iov Hono spp. couId aJJovd lo
incvease signiJicanlI lIeiv cvaniaI capacil Ieond lIal
oJ lIeiv pIIogenelic pvedecessovs, lIe auslvaIopilIe-
cines. TIe aulIovs expIain Iov |in a pIsioIogicaI, nel-
aIoIic, and analonicaI sense) lIe nenIevs oJ genus
Hono acconpIisIed lIis lvansJovnalion. TIe IpolIe-
sis vesls on a cvilicaI assunplion lIal AieIIo and
WIeeIev veadiI adnil cannol Ie diveclI denon-
slvaled-lIal lIe cIanges in lIe pvopovlions oJ lIe lvo
ovgans |Ivain and gul) veve conlenpovav evoIulionav
evenls. In lIeiv nodeI, as lIe Ivain enIavges, lIe gul is
veduced in size. A IincIpin in lIis evoIulionavio is a
cIange in lIe quaIil oJ Ioninid diels, vilI aninaI-
devived consliluenls Ieconing incveasingI inpovlanl.
TIe sIouId Ie conpIinenled Jov allenpling lIis inlev-
esling snlIesis, aIlIougI al lines il seens lIal evev-
lIing incIuding lIe IilcIen sinI |ov pevIaps slove, since
lIe suggeslion is aIso nade lIal cooIed Jood na Iave
pIaed a voIe in encepIaIizalion) Ias Ieen added lo lIis
vecipe Jov a Iiggev Ivain. TIe suggesl lIal eavIiev ex-
pIanalions ave insuJJicienl Iecause olIevs Iave lended
lo IooI al lIe Ivain in isoIalion Jvon olIev lissues, Iul,
as lIe nole, lIese olIev eJJovls Iave addvessed lIe vI
queslion valIev lIan lIe Iov queslion |AieIIo and
BunIav I993, Bvne and WIilen I988, MiIlon I979, and
In discussing lIe pallevn oJ cIanges in Ivain size in
Iunan evoIulion, AieIIo and WIeeIev suggesl lvo najov
peviods in vIicI lIis occuvved. One covvesponds lo lIe
appeavance oJ lIe eavIiesl nenIevs oJ genus Hono,
vIelIev IaIiIis ov vudoIJensis, and Ialev evgaslev. TIe
second peviod is associaled vilI avcIaic H. sapiens.
Leaving aside lIe issue oJ jusl Iov nan species ave
veaII vepvesenled in lIe Jivsl peviod |cJ. FoIe i99i), il
appeavs lIal lIe eavIiesl nenIevs oJ Hono veve nol
Iavgev in Iod size lIan auslvaIopilIecines and did nol
Iave nodevn IinI pvopovlions |JoIanson el aI. i987). Il
is nol al aII cIeav Iov nucI aninaI-devived Jood vas in
lIeiv diels ov vIelIev lIis vas vevleIvale ov invevle-
Ivale, and il is pevIaps pvoIIenalic lo IauncI lIe coevo-
Iulion oJ gul and Ivain on sucI a lenlalive Joundalion.
Hovevev, vilI species IiIe evgaslev and Ialev Ioninids
AieIIo and WIeeIev ave on nucI Jivnev gvound vilI ve-
specl lo nodevn novpIoIog and dielav pallevns and
In advancing lIeiv case Jov aclive Iunling and/ov
Iong-dislance nigvalion lIe suggesl lIal lIe vesIaping
oJ lIe viI cage Jvon a JunneI-sIaped |pongid and auslva-
IopilIecine) lo a nove IavveI-sIaped nodevn appeavance
vouId enIance lIe cavdiovascuIav sslen and nove eJ-
JicienlI venliIale lIe Iungs. TIis sounds a Iil IiIe lIe
nolion oJ pvogvess and is nol cvilicaI lo lIe IpolIesis
as pvesenled. AIlevnaliveI, sucI a cIange na Ie a
Junclion oJ lIe cIange Jvon quadvupedaI lo IipedaI Ioco-
nolion, as suggesled I Hunl
FieId IioIogisls
vIo vilness episodes oJ suslained Ioconolion and espe-
ciaII avIoveaI Iunling I viId cIinpanzees vouId nol
douIl lIeiv cavdiovascuIav Jilness ov lIeiv vespivalov
Junclioning |SlanJovd el aI. I994).
AieIIo and WIeeIev cone lo lIeiv inJevence oJ coevo-
Iulion oJ Ivain size and gul size I a pvocess oJ eIinina-
lion. TIal is, lIe exanine olIev expensive lissue
|Ieavl, Iidne, Iivev) and concIude lIal size veduclion in
an oJ lIen vouId Ie loo visI, vIeveas lIe gul Ias
nove JIexiIiIil in ils size |conlingenl on lIe necessav
dielav cIanges, oJ couvse). In eJJecl, lIe gul coevoIves
I deJauIl, a Iess lIan salisJaclov evoIulionav expIana-
lion and one lIal needs lo Ie addvessed iJ lIis IpolIesis
is lo Ie deveIoped JuvlIev.
Bepavlnenl oJ AnlIvopoIog, Univevsil oJ CaIiJovnia,
BevIeIe, CaIiJ. 94720, U.S.A. 7 x 94
Hov Iunans can aJJovd lIeiv Iavge Ivains Ias Iong Ieen
a queslion oJ inlevesl. Hunans ave vegavded as Iaving a
snaII gul Jov lIeiv Iod nass, an unusuaII Iavge Ivain,
and a novnaI nelaIoIic IeveI-a sel oJ condilions vIicI
AIELLO ANB WHEELEB TIe Expensive-Tissue HpolIesis
appeavs lo pose a pavadox, since Ivain lissue is vegavded
as enevgelicaII expensive. AieIIo and WIeeIev descviIe
lIe case oJ lIe incvediIIe sIvinIing gul as a soIulion
lo lIis appavenl pavadox, Iul lIe JunclionaI necIanisn
IinIing lIese pIenonena in an evoIulionav palIva is
nol nade cIeav. TIougI avaiIaIIe dala indicale a snaII
gul in Iunans |e.g., Mavlin I98I, MiIlon and Bennenl
i988), neasuvenenls oJ Iunan gul pvopovlions oJlen
appeav lo Iave Ieen nade on individuaIs Jvon Weslevn
nalions ealing veJined Weslevn diels. SpecuIalions on
Iunan gul pvopovlions and gul size in Iunans and olIev
pvinales sIouId Ie advanced vilI caulion, as vovI on
olIev aninaI species sIovs lIal diJJevenl seclions oJ lIe
gul can vapidI aIlev in vesponse lo cIanging dielav con-
dilions, even vilIin lIe IiJe span oJ lIe individuaI |e.g.,
Ovoss, Wang, and Wundev i986). Sone non-Weslevn vu-
vaI Iunan popuIalions vIicI consune Iavge anounls
oJ dielav JiIev ave eslinaled lo oIlain as nucI as io%
oJ lIeiv lolaI caIovic inlaIe eacI da Jvon lIe voIaliIe
Jall acids pvoduced in cecaI and coIon Jevnenlalion:
in conlvasl, lIis Jiguve Jov lIe Iov-JiIev Weslevn diel is
avound 0.7% |Van Soesl el aI. I982, MiIlon i986). TIis
nagnilude oJ diJJevence suggesls lIal sone Iunan pop-
uIalions na Iave considevaII Iavgev coIons lIan olI-
evs and lIus pevIaps a Iavge ovevaII gul. WouId AieIIo
and WIeeIev lIen pvedicl a covvespondingI snaIIev
Ivain size in sucI popuIalions? I douIl il. IJ I venenIev
covveclI, lIe Iunan Ivain and nevvous sslen ave esli-
naled lo accounl Jov onI sone 20% oJ daiI enevg
luvnovev, Ieaving a voIusl 8o% lo laIe cave oJ olIev
Hovevev, even iJ sone Iunan popuIalions do Iave
Iavgev coIons and guls, I vouId sliII pvedicl lIal nodevn
Iunans as a species Iave a snaII gul Jov lIeiv Iod
nass. In n opinion, vIen using an evoIulionav pev-
speclive il is aIvas Iesl lo lv lo accounl Jov IolI lIe
Iov and lIe vI, since lIe lvo ave inlevlvined |MiIlon
i988). As is poinled oul I Jevison |I973), pvinales ap-
peav lo Iave Ieen veIaliveI Iavge-Ivained nannaIs
since lIe inceplion oJ lIe ovdev, vIicI suggesls lIal
lIe Iave Iong lended lo seeI IeIaviovaI |Ivain-Iased)
soIulions lo lIeiv dielav pvoIIens and lIus Iave Iong
Ieen aIIe lo aJJovd lIe nenlaI soIulion-lIal is, aJJovd
lo Iave a sonevIal Iavge Ivain veIalive lo Iod nass. I
Iave pvoposed lIal lIis cane aIoul Iecause lIe ances-
lvaI Iineage uIlinaleI Ieading lo Fvinales vas sone-
Iov aIIe lo enlev lIe as-el-unJiIIed avIoveaI pIanl-
Iased dielav nicIe pvovided I lvopicaI-Jovesl
angiospevn lvees and vines and lIen vadiale in sucI a
va as evenluaII lo conlvoI a Iavge pvopovlion oJ lIe
IigIesl-quaIil pIanl Joods |nev Ieaves, vipe Jvuils, and
JIovevs) in lIis avIoveaI envivonnenl |MiIlon I98794-
95). Enlv inlo lIis dielav nicIe appeavs lo pIace consid-
evaIIe pvessuve on lIe Jeedev lo Iovev lIe cosls associ-
aled vilI pvocuvenenl oJ lIese palcIiI dislviIuled
pIanl Joods-a soIulion vIicI in ouv ovdev appeavs lo
Iave Ieen vesoIved in Iavge pavl I lIe deveIopnenl oJ
ceveIvaI conpIexil, vilI lIe allendanl IeIaviovaI pIas-
licil, nenov, Ieavning, and sociaI sIiIIs vequived lo
Iovev Jood acquisilion cosls and inpvove Jovaging ve-
luvns |see, e.g., MiIlon I979, I98I, I987, I988, I993).
ManuaI dexlevil and lIe use oJ lIe Iand in pvepaving
Jood and in Jeeding ave aIso inpovlanl Fvinale lvails
vIicI sevve lo Ivoaden lIe ovevaII Fvinale dielav nicIe
and conlviIule lo Jovaging success |see, e.g., OiIson
i986). Il isn'l so nucI lIal guls sIvanI, giving Fvinales
exlva nelaIoIic scope lo aJJovd lIeiv Ivains: valIev, il
vouId appeav lIal lIe deveIopnenl oJ lIe Ivain in divecl
associalion vilI an unusuaII IigI-quaIil diel and lIe
Jovaging sIiIIs vequived lo oIlain il na gvaduaII Iave
JaciIilaled sone veduclion oJ ovevaII gul nass. TIis is
an inpovlanl dislinclion.
Hov did lIe Iunan genus IveaI inlo ils unusuaII
pvoJilaIIe dielav nicIe-one vIicI I Iave levned lIe
nicIe oJ lIe cuIluvaI onnivove |MiIlon n.d.)-so lIal
il couId gel I vilI a snaIIev gul? Lel's inagine a pvolo-
Iunan anceslov Iiving in a cIanging envivonnenl in
vIicI, Jov vIalevev veason, IigIev-quaIil pIanl Joods
Iecone incveasingI diJJicuIl lo oIlain. TIeve ave lvo
pvincipaI soIulions lo lIis pvoIIen. One is lo luvn lo
Iovev-quaIil Joods lIal ave veIaliveI aIundanl Iul
JaivI eas lo oIlain |lIeveI, in lIe Ioninoid Iineage,
vilI ils cIavaclevislic Ioninoid gul novpIoIog, sacvi-
Jicing noIiIil and nan IeIaviovaI aspecls |e.g., ovang-
ulans and goviIIas veIalive lo cIinpanzees): lIe olIev is
lo IoId lIe Iine vilI vegavd lo dielav quaIil and Jind
sone va lo covev lIe incveasing cosls oJ pvocuving vave
Iul Jav nove nulvilionaII concenlvaled, IigI-quaIil di-
elav ilens |Jov discussion see Bennenl I983: MiIlon
I986, I987, I988, I993: MiIlon and Bennenl i988).
OIviousI, il is lIis second soIulion vIicI vas Ja-
voved in ouv Iineage. We Jind cvude slone looIs and ve-
duced denlilion as cIavaclevislic lvails oJ eavI nenIevs
oJ ouv genus-lvails vIicI lesliJ lo lIe incveasingI in-
povlanl voIe oJ lecInoIog in levns oJ lIe anceslvaI Iu-
nan diel |MiIlon I987, I993:
MiIlon and Bennenl
i988). TIe veduced denlilion oJ eavI Iunans indicales
lIal lecInoIog Iad Iegun lo inlevvene in Iunan di-
elav IeIaviov, in eJJecl pIacing a IuJJev ov Iavviev Ie-
lveen Iunan denlaI novpIoIog and lIe Iunan gul
|and lIus seIeclion pvessuves) and Joods consuned.
Slone looIs couId Iave JaciIilaled access lo JovnevI un-
avaiIaIIe Joods, IolI pIanl and aninaI, ov upgvaded ex-
isling Jood quaIil. EIsevIeve |MiIlon i987) I Iave dis-
cussed lIe pvoIaIIe voIe oJ neal ealing in Iunan
evoIulion, poinling oul lIal lIougI aninaI pvolein is
an exceIIenl anino-acid souvce Jov Iunans, il is Iess
desivaIIe as an enevgelic suIslvale.
BalIev lIan suggesling, as AieIIo and WIeeIev do, lIal
lIe Iavge Ivain in ouv Iineage veIales lo gvoup size valIev
lIan Jeeding slvaleg |an avgunenl vIicI seens Jovced
in IigIl oJ lIeiv papev's conlenl), I vouId avgue lIal eavI
Iunan sociaIil as veII as gvoup size is Iesl vieved as
anolIev lpe oJ dielav looI. In lIe genus Hono, a divi-
sion oJ IaIov and Jood sIaving appeav lo Iave Ieen lIe
sociaI looIs conlviIuling lo dielav suJJicienc |e.g., MiI-
lon i987). Hunans in nodevn lecInoIogicaI socielies
oJlen Jovgel jusl Iov pvoIIenalic gelling one's daiI
Jood can Ie, Iul, as BicIavds |I948) noled Iong ago, il is
Jood nol sex lIal naIes lIe vovId go vound. TIougI
216 CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI I995
veduclion oJ gul nass na veII Jvee up sone enevg lo
suppovl olIev ovgans, lIe Ivain is Iosl vilIoul a conslanl
and dependaIIe enevgelic suIslvale. TIus il vouId Ie
evoIulionaviI ivvesponsiIIe lo casl oJJ gul lissue unliI
nenlaI conpIexil vas suJJicienlI deveIoped lo nove
ov Iess ensuve dielav quaIil. Indeed, onI vIen seIec-
lion is veIaxed sIouId an veduclion in gul size occuv.
TIe gul is cevlainI an inpovlanl pavl oJ lIe evoIulion-
av picluve IolI Jov nonIunan Fvinales and Jov Iu-
nans, Iul il seens poinlIess lo lv lo viev gul cIanges
apavl Jvon lIe Jovaging slvaleg and dielav nicIe in
vIicI lIe ave evoIulionaviI enIedded.
Bepavlnenl oJ AnlIvopoIog, Havvavd Univevsil,
I I Bivinil Ave., CanIvidge, Mass. 02138, U.S.A.
II 7 94
Ovganisns can'l aJJovd Iong-levn deIl. Since lIe vecog-
nilion lIal lIe cosls oJ encepIaIizalion ave especiaII
IigI, lIeveJove, nelaIoIic conslvainls Iave Ieen a polen-
liaI souvce oJ expIanalion oJ vavialion in Ivain size. Bul iJ
lIe idea lIal incveased expenses nusl Ie nel I veduced
cosls is oId nevs, AieIIo and WIeeIev's pvesenlalion oJ
lIe expensive-lissue IpolIesis is nevevlIeIess noveI.
TIe Ie avgunenl -is lIal lIeve ave Jev dinensions oJ
Jveedon in pvinale enevg Iudgels and lIal oJ lIese
onI gul cosl is IiIeI lo vav enougI lo accounl Jov lIe
oIsevved diJJevences in Ivain size. TIe Jind lIal veIalive
gul size vavies invevseI vilI veIalive Ivain size and inJev
lIal onI species vilI cIeap guls can aJJovd Iavge Ivains
and lend lo Iave lIen.
Because il pvovides a cIeav accounl oJ IolI lIe naluve
and diveclion oJ causalion, lIis is a vev vaIuaIIe I-
polIesis. TIe evidence Jov a dielav expIanalion oJ Ion-
inid Ivain expansion is conpeIIing. TIe IpolIesis de-
sevves vigovous exaninalion lo lesl poinls oJ veaIness.
We suggesl lvo.
Fivsl, lIeve appeavs lo Ie a Iidden assunplion lIal
lIe enevg Iudgel oJ an aninaI al IasaI nelaIoIic vale
|BMB) is conslvained-lIal lIe BMB is lIe nininaI vale
oJ enevg luvnovev al vIicI ovgans can Ie nainlained.
IJ nelaIoIic vale couId JaII IeIov BMB, Iovevev, and
cevlain ovgans couId suvvive, lIen lIe oIsevved pallevn
oJ enevg dislviIulion anong ovgan sslens al BMB is
nol nandalov. Il is onI iJ BMB is conslvained lIal
lIe AieIIo-WIeeIev Iogic vovIs. Is il lvue, lIeveJove, lIal
BMB is conslvained-lIal il is lIe nininaI possiIIe
vale? No. BMB is JovnaII neasuved on vaIing suIjecls.
Buving sIeep, nelaIoIic vale JaIIs I aIoul io% |BIaxlev
i989). Il aIso JaIIs in olIev conlexls, sucI as duving slav-
valion. Il can diJJev Ielveen Iunan popuIalions I as
nucI as I7% |BIaxlev i989I44). SucI vavialion neans
lIal lIe anounl oJ enevg consuned I diJJevenl ovgans
opevaling al BMB is IigIev lIan lIal diclaled I suv-
vivaI. TIeveJove, il is iIIegilinale lo inJev lIal lIe oI-
sevved dislviIulion oJ enevg lovavds diJJevenl ovgans
al BMB vepvesenls lIe nininaI IeveIs needed I lIose
ovgans. Fov sone sucI ovgans lIe enevg luvnovev al
BMB na Ie lIe nininun: Jov olIevs il na nol Ie.
One escape Jvon lIis Iine oJ lIinIing couId Ie lo sug-
gesl lIal lIe BMB vepvesenls nol lIe nininaI Iul an
avevage nelaIoIic vale, a vale vIicI sIovs Iov aninaIs
dislviIule enevg lo ovgans al a lpicaI vovIing IeveI.
Bul lIis escape vouId Ie a JaIse one, Iecause as soon as
ve lIinI in levns oJ acluaI expendiluves oJ enevg ve
nusl acInovIedge lIal BMB does nol pvedicl lIe lolaI
enevg inlaIe |daiI enevg expendiluve). Hov IigI lIe
avevage nelaIoIic vale is aIove BMB vavies Ielveen spe-
cies in vas nol pvedicled I BMB ilseIJ.
We concIude lIal BMB cannol in lIeov Ie used lo
index lIe lolaI ov avevage ov nininun anounl oJ enevg
JIoving lIvougI lIe sslen ov lo diJJevenl ovgans. TIis
doesn'l nean lIal AieIIo and WIeeIev's concIusions ave
vvong, Iul il does nean lIal lIeve ave IogicaI and enpiv-
icaI issues nissing Jvon lIe avgunenl. A Ie queslion
is Iov nucI polenliaI vavialion lIeve is in lIe nela-
IoIic vales oJ ovgans opevaling al BMB.
Second, AieIIo and WIeeIev Iave Ieen Jovced lo as-
sune lIal lIe nelaIoIic cosls oJ ovgans scaIe isonelvi-
caII vilI lIeiv veigIls, Iul lIis veIalionsIip is un-
Inovn. WIal is lIe lvue cosl oJ evoIving a Iavgev Ivain,
and Iov nigIl lIis cosl Ie suppovled? Using lIeiv Jiguve
3, ve can inJev lIal a slandavd Iunan needs onI aIoul
5% nove daiI enevg lo nainlain ils enIavged Ivain
ovev lIal oJ a snaII-Ivained individuaI oJ equivaIenl
Iod size. CouId Iavgev Ivains Ie nainlained vilIoul
gul-size veduclion I dielav conpensalion? Il is cuvious
lIal oJ lIe expensive ovgan sslens onI lIe Ivain scaIes
vilI an exponenl suIslanliaII Iess lIan i |Felevs I983).
IJ Iavgev species Jind lIe enevg lo suppovl lIese veIa-
liveI Iavgev ovgans, vI can'l lIe suppovl Iavgev, Iess
coslI |in levns oJ nass-speciJic enevg) Ivains?
In sun, lIis is an exciling and slinuIaling vesuIl. We
IooI Jovvavd lo seeing lIe AieIIo-WIeeIev Iogic JIesIed
oul vilI Iellev dala and appIied lo laxa sucI as Ials |do
Jvuil Ials Iave snaIIev guls lIan inseclivovous Ials?),
celaceans |ave odonloceles snaIIev-gulled lIan nsli-
celes?), and vodenls. We aIso IooI Jovvavd lo lIe vesoIu-
lion oJ vIal appeavs, on lIe Jace oJ il, lo Ie a pvoIIen.
Hov do AieIIo and WIeeIev veconciIe lIeiv concIusion
vilI lIe aIIonelv oJ aduIl Ivain nass in nannaIs,
Iivds, and vepliIes? In aII lIvee gvoups, gul nass scaIes
isonelvicaII vilI Iod nass. Yel in nannaIs Ivain
nass scaIes lo lIe 0.75 exponenl, conpaved vilI a o.56
exponenl Jov Iivds and vepliIes |Mavlin i98i). An expIa-
nalion oJ lIese pallevns in levns oJ lIe expensive-lissue
IpolIesis vouId Ie a suIslanliaI acIievenenl.
London, EngIand. I3 7I 94
TIe expensive-lissue IpolIesis is a IpolIesis lo ex-
pIain lIe coevoIulion oJ lIe Ivain, lIe digeslive ss-
AIELLO ANB WHEELEB TIe Expensive-Tissue HpolIesis
len, and diel. We ave pIeased lo nole lIal lIe najovil
oJ lIe connenlalovs Jind il noveI, inlevesling, and
veIevanl and aIso lIal lIe vecognize lIal ve ave nol
cIaining lIal dielav cIange and lIe associaled cIange
in gul size veve necessaviI pvine novevs in Ioninid
encepIaIizalion. As FaII Ias cIeavI slaled, ve viev
lIese Jaclovs, Jov lIe nosl pavl, as pvine veIeasevs
vIicI naIe avaiIaIIe lIe nol inconsidevaIIe enevg ve-
souvces lIal ave a necessav conconilanl oJ encepIaIi-
HoIIova connenls lIal lIe expensive-lissue I-
polIesis does nol gel us an neavev lo undevslanding lIe
veIalionsIip Ielveen Ivains and IeIaviouv, Iul lIal vas
nol ouv inlenlion. NonelIeIess, MiIlon Ias pvoposed
lIal incveased conpIexil oJ Jovaging IeIaviouv associ-
aled vilI lIe cIange in diel couId Ie a pvine novev
Jov lIe incvease in Ivain size in pvinales, a viev aIso
expvessed in olIev guises I, Jov exanpIe, FavIev and
OiIson |I979: OiIson i986) and CIullon-BvocI and Hav-
ve |i980). MiIlon's connenls Ieve give lIe inpvession
lIal ve vejecl lIis viev: on lIe conlvav, il vas nol ouv
inlenlion lo cone dovn on lIe side oJ an one oJ lIe
vavious IpolIeses lIal ave cuvvenl in lIe Iilevaluve. In-
deed, in Jiguve 5 ve cIeavI indicale lIal lIeve na Iave
Ieen a causaI conneclion Ielveen nove conpIex Jovag-
ing slvalegies and Ivain size incvease, Iul ve aIso veaIize
lIal lIe causaI naluve oJ sucI veIalionsIips is aIvas
diJJicuIl lo delevnine. We cevlainI do nol vanl lo give
lIe inpvession lIal ve ave suggesling lIal gul cIanges
sIouId Ie vieved apavl Jvon lIe Jovaging slvaleg and
dielav nicIe in vIicI lIe ave evoIulionaviI enIed-
ded. Bul ve aIso vanl lo naIe cIeav lIal ouv IpolIe-
sis does nol vequive dielav cIange lo Ie lIe pvine
novev ov even one oJ lIe pvine novevs Jov encepIa-
Iizalion. Il cIeavI vouId aIso Ie conpaliIIe vilI gvoup-
size IpolIeses |BunIav I992, I993: AieIIo and BunIav
I993), sociaI-inleIIigence IpolIeses |Bvne and WIilen
i988), ov, pevIaps nove veaIislic, a conIinalion oJ
causes. Ouv nain poinl is lIal lIe veduclion in gul size
is a conconilanl oJ a cIange lo IigIev-quaIil diels. TIe
Iovev enevg vequivenenls oJ snaIIev guls veve a ve-
Ieasev lIal enevgelicaII pevnilled an associaled in-
cvease in lIe size oJ lIe Ivain.
AIlIougI ve considev lIe veIalionsIip Ielveen a
IigI-quaIil diel and and a veIaliveI snaII gul lo Ie an
inpovlanl conconilanl oJ encepIaIizalion, ve aIso do
nol vanl lo give lIe inpvession lIal il is lIe onI pvine
veIeasev. OlIev Jaclovs, analonicaI as veII as enevgelic,
Iave aInosl cevlainI conslvained Ivain size duving
Ioninid evoIulion. Fov exanpIe, as is noled I FaII, lIe
pvoIIen oJ suppIing lIe Ivain vilI lIe IigI IeveIs oJ
cIenicaI enevg il vequives is inlinaleI IinIed vilI
lIal oJ venoving lIe vesuIlanl Ieal Jvon lIis exlveneI
lenpevaluve-sensilive ovgan. In lIis conlexl, il Ias Ieen
pvoposed lIal lIe lIevnaI pvoleclion pvovided I a na-
Ied sIin and ils associaled sveal gIands slaIiIising lIe
lenpevaluve oJ lIe avleviaI IIood suppI lo lIe Ivain
|WIeeIev i984) and lIe eIaIovalion oJ enissav veins
aJJovding cooIing lo lIe deIicale oulev Iaev oJ lIe covlex
|FaII i990) veve cvuciaI Jaclovs in aIIoving lIe expan-
sion oJ lIe Ivain lIal Ias laIen pIace duving lIe evoIu-
lion oJ lIe genus Hono.
A Ie poinl vaised in delaiI I sone oJ lIe connenla-
lovs |HennenIevg, WvangIan el aI.) is vIelIev vIoIe-
Iod BMB is conslvained lo lIe exlenl lIal encepIaIiza-
lion vouId vequive lIe conpensalov veduclion in size
oJ anolIev nelaIoIicaII expensive ovgan. TIis is a vaIid
queslion. Il is videI assuned lIal lIe lolaI enevg
avaiIaIIe lo and uliIized I ovganisns is an inpovlanl
Iiniling Jaclov lo suvvivaI and vepvoduclive success. In-
deed, lIis Jovns lIe Iasis oJ nucI cuvvenl evoIulionav
and ecoIogicaI lIeov. ConsequenlI, ve Iave endeav-
ouved lo sIov lIal lIe cosl oJ encepIaIizalion is a sig-
niJicanl conponenl nol onI oJ BMB ilseIJ Iul aIso oJ
lIe lolaI enevg Iudgel oJ Iunans. TIe exlva cosl Jov
Iunans appeavs lo Ie in lIe vange oJ a 5 % incvease in
lolaI nelaIoIic enevg vequivenenls. We vouId avgue,
conlva HenneIevg and WvangIan el aI., lIal lIis vaIue
is nol insigniJicanl. An individuaI vilI an incveased en-
evg Iudgel viII Ie al a signiJicanl disadvanlage in levns
oJ conpelilion and vepvoduclive success.
As ve indicaled, ve concuv vilI lIese connenlalovs
lIal, in lIeov al Ieasl, lIe cosl oJ lIe addilionaI Ivain
lissue couId Iave Ieen nel I slvalegies olIev lIan a
veduclion in gul size. Fov exanpIe, iJ suJJicienl dielav
vesouvces veve avaiIaIIe, ovevaII BMB couId Iave Ieen
covvespondingI incveased and/ov lIe enevgelic cosls as-
socialed vilI olIev conponenls oJ lIe enevg Iudgel
veduced. WIal slvaleg vouId naxinise lIe vepvoduc-
live success oJ ovganisns vouId depend on lIe ovevaII
ecoIogicaI conlexl in vIicI lIe Iived. Il is quile possi-
IIe lIal olIev laxononic gvoups Iave soIved lIe pvoI-
Ien oJ lIe enevgelic cosls associaled vilI encepIaIiza-
lion in olIev vas lIan I a veduclion in lIe size oJ lIe
gul. Fov exanpIe, il is possiIIe al Ieasl in pavl lIal lIe
cosl oJ lIe Iavgev lIan avevage Ivains oJ nusleIids |Jevi-
son I990) is veJIecled in lIeiv IigIev lIan avevage BMB
|WIeeIev I984, Ivevson I972): vIelIev lIeve ave aIso cov-
vesponding veduclions in lIe sizes oJ olIev expensive
ovgans is cuvvenlI unInovn. SevevaI connenlalovs
|Avnslvong, FaII, WvangIan el aI.) nole lIe polenliaI
vaIue oJ exlending lIe anaIses lo olIev laxononic
gvoups |e.g., celaceans, Ials, Iivds), and ve vecognize
lIal, vIeve adequale dala sels can Ie oIlained, lIis is
JevliIe gvound Jov nucI Juluve veseavcI.
BegavdIess oJ vIal slvalegies ave uIlinaleI sIovn lo
Iave Ieen adopled I olIev gvoups and couId polenliaII
Iave Ieen used I Ioninids, ouv cenlvaI poinl venains
vaIid: Iunans possess a veIaliveI Iavge Ivain and a veIa-
liveI snaII gul and aIso Iave no covvesponding incvease
in BMB. ConsequenlI, lIeve is no need lo IooI Jov aIlev-
nalive expIanalions |sucI as veduced aclivil, incveased
sIeep, and veduced dielav inlaIe, as suggesled I Hen-
neIevg and WvangIan el aI.) Jov Iov lIe enevgelic cosls
associaled vilI Iunan encepIaIizalion Iave Ieen nel.
In Iunans IolI ovgan veigIl and in vivo ovgan nela-
IoIic dala slvongI suppovl lIe IpolIesis lIal lIe in-
cveased nelaIoIic cosl oJ lIe Iavge Iunan Ivain vas nel
speciJicaII I a decvease in lIe size oJ lIe gaslvoinlesli-
naI lvacl. TIe concIusion lIal can Ie dvavn Jvon lIis is
2i8 CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI 1995
lIal olIev soIulions veve nol as viaIIe in lIe adaplive
conlexl lIal conJvonled ouv evoIulionav anceslovs. Bul
ouv dala aIso suggesl lIal sone oJ lIe olIev Jaclovs na
Ie inpovlanl in oJJselling lIe cosls oJ encepIaIizalion
in olIev pvinales. AIlIougI lIeve is a slvong invevse
veIalionsIip Ielveen veIalive Ivain size and veIalive gul
size acvoss pvinales |Jig. 4), lIeve is aIso sone evidence
Jov gvade veIalionsIips in lIese dala. Fov exanpIe, lIe
coIoIines Iave a veIaliveI snaIIev conIined Ivain and
gul nass Jov lIeiv lolaI Iod nass lIan olIev pvinales,
and lIis couId Ie a veJIeclion oJ a Iovev lIan avevage
Sone oJ lIe connenlalovs expvess concevn ovev lIe
quaIil oJ lIe dala used in lIis anaIsis |HenneIevg,
WvangIan el aI., MiIlon). We JuII vecognize lIal lIe
dala sel is nol ideaI. In lIe inlevspeciJic pvinale conpav-
ison ve Iave cIeavI noled lIe pvoIIens vilI lIe dala
Iul nonelIeIess Iave Ieen inpvessed I lIe negalive
veIalionsIip Ielveen veIalive Ivain size and veIalive gul
size. Al lIe sane line ve Iave speciJicaII avoided laI-
ing inlevpvelalions oJ lIis veIalionsIip lo loo Jine a IeveI
oJ delaiI. FevIaps a nove sevious concevn is polenliaI
vavialion in lIe dala due lo veaI diJJevences in ovgan sizes
and Iod nasses vilIin Iunans and olIev pvinale laxa.
To ouv InovIedge dala sels do nol cuvvenlI exisl vIicI
vouId aIIov us lo lesl lIe inlvaspeciJic vavialion in BMB
and veIalive ovgan size. Hovevev, il sIouId Ie vecognized
lIal lIe expensive-lissue IpolIesis vesls squaveI on
lIe exislence oJ sucI vavialion. In pavlicuIav, vilIin spe-
cies ve vouId expecl lIal encepIaIized individuaIs de-
vialing Jvon lIe ideaI Ivain/gul-size veIalionsIips vouId
aIso deviale in olIev aspecls oJ lIeiv enevg Iudgels. Be-
pending on lIe envivonnenlaI condilions in vIicI lIe
Jound lIenseIves, ve vouId JuvlIev expecl lIal lIis de-
vialion vouId Iave Iad advevse consequences Jov lIeiv
vepvoduclive success. On lIe individuaI IeveI lIis vouId
Ie lIe seIeclive necIanisn dviving lIe oIsevved
Ielveen-laxa veIalionsIips.
In veIalion lo dala quaIil, HenneIevg aIso noles lIe
IigI vaviaIiIil in lIe nass-speciJic nelaIoIic vales Jov
individuaI ovgans acvoss species |laIIes i and 3) and ac-
covdingI queslions lIe veIiaIiIil oJ ouv vesuIling esli-
nales oJ lIe nelaIoIic IaIance in laIIe 4. Il sIouId Ie
noled, Iovevev, lIal lIe IigII vaviaIIe in vilvo dala
|laIIe 3) veve pvesenled Jov iIIuslvalive puvposes onI,
aIIoving lIe veIalive cosls oJ lIe diJJevenl lissues lo Ie
conpaved vilIin a species. Il is inpovlanl lo enpIasize
lIal lIe quanlilalive anaIsis vIicI sIovs lIal lIe
nelaIoIic cosl oJ lIe Iunan Ivain is IaIanced I lIe
veduced nelaIoIic cosl oJ lIe snaII Iunan gul |laIIe 4)
vas devived excIusiveI Jvon in vivo neasuvenenls oJ
Iunan suIjecls |laIIe I). FossiIIe inlevspeciJic vavialion
in nass-speciJic nelaIoIic cosl does nol Ieav on lIis
WvangIan el aI. aIso vondev Iov ve veconciIe ouv
concIusions vilI lIe diJJevenl ovgan aIIonelvies, pavlic-
uIavI Ivain and gul aIIonelvies, in nannaIs, Iivds, and
vepliIes. We do nol Iave lIe dala al pvesenl lo ansvev
lIis queslion, Iul laIIe 5 suggesls lIal Iivds, al Ieasl,
Iave adopled a vev diJJevenl enevg slvaleg Jvon pvi-
Mass |g) oJ lIe Expensive Tissues Jov a 500-g Fvinale
and a Bivd
Fvinale Bivd Bivd/Fvinale
Heavl 2.62 4.26 i.63
Livev I 6.78 I 7.97
I .07
Kidne 3.45 4.62
Bvain I3.59 4.75 0.35
Oul 29.66 3.54 O.12
ET/BM 0.I3 0.07
B&O/ET o.65 0.24
B&O/BM 0.09 0.02
NOTE ET/BM = nass oJ lIe expensive lissues as a pvopovlion oJ
Iod nass: B&O/ET = nass oJ lIe Ivain and gul as a pvopovlion
oJ lIe nass oJ lIe expensive lissues: B&O/BM = nass oJ lIe
Ivain and gul as a pvopovlion oJ Iod nass: pvinale pvediclions
Iased on lIe equalions pvesenled Ieve, Iivd pvediclions on equa-
lions in Felevs |i983).
nales. Fov exanpIe, lIe expensive lissues oJ an avevage
Iivd naIe up a snaIIev pevcenlage oJ Iod nass
lIan do lIe sane lissues in a siniIavI sized pvinale.
TIe Iivd Ias a nucI snaIIev Ivain lIan a siniIavI sized
pvinale and aIso a snaIIev gul vIiIe Iaving considev-
aII Iavgev Iidnes and Ieavl. TIese veIalionsIips oI-
lain lIvougIoul lIe veIevanl Iod-nass vanges. IJ lIese
size veIalionsIips nivvov lIe acluaI nelaIoIic cosls oJ
lIe lissues in Iivds as lIe do in Iunans, ve can poslu-
Iale lIal lIe denands oJ lIe vev diJJevenl IiJeslIe and
Ioconolov pallevn oJ Iivds govevn lIeiv diJJevenl ovgan
aIIonelvies. TIe pvincipIe is lIe sane, Iovevev. AII ov-
ganisns Iave lo acconnodale lIe veIalive cosls oJ lIeiv
expensive lissues vilIin IolI lIeiv BMB and lIeiv lolaI
enevg Iudgels. Il is IigII possiIIe lIal lIe enevgelic
denands oJ JIigIl, as veII as lIe eJJecl oJ lIese denands
on, Jov exanpIe, lIe size oJ lIe Ieavl, Iave pvecIuded
an degvee oJ encepIaIizalion conpavaIIe lo lIal Jound
in pvinales.
WvangIan el aI. aIso vaise lIe inlevesling queslion oJ
vI anong lIe expensive ovgans onI Ivain nass, IiIe
BMB, scaIes vilI an exponenl signiJicanlI Iess lIan
unil. Hovevev, lIe inpovlanl veIalionsIips ave acluaII
lIose Ielveen Iod size and lIe lolaI nelaIoIic cosls
oJ lIe expensive ovgans, nol jusl lIeiv nasses. In lIe
case oJ lIe Ivain lIe nelaIoIic vale and lIe ovgan nass
scaIe vilI valIev siniIav exponenls |o.69 and 0.76, ve-
specliveI), since lIe nass-speciJic nelaIoIic vale oJ
lIis ovgan is nol slvongI veIaled lo Iod size |Ovande
In conlvasl, aIlIougI lIe size oJ olIev expensive
ovgans na scaIe vilI exponenls cIosev lo i, lIeiv nass-
speciJic nelaIoIic vales na decIine nove vapidI vilI
incveasing Iod size, aIso vesuIling in an ovevaII expo-
nenl Jov lIe lolaI nelaIoIic cosl oJ lIe ovgan cIose lo
lIe 0.75 oJ BMB ilseIJ. Fov exanpIe, Iivev nass scaIes
vilI an exponenl oJ aIoul o.87 |Felevs i983), Iul ils
nass-speciJic nelaIoIic vale exponenl is -0.I2 |Ovande
I980), giving a conIined exponenl oJ 0.75 Jov lIe lolaI
AIELLO ANB WHEELEB TIe Expensive-Tissue HpolIesis
enevgelic cosl oJ lIis ovgan. Hovevev, vIelIev lIe aIIo-
nelvic veIalionsIips oJ gul size and nelaIoIisn JoIIov
a siniIav pallevn lo lIose oJ lIe Iivev is cuvvenlI uncev-
lain Iecause oJ lIe IacI oJ good dala sels veIaling nass-
speciJic lissue nelaIoIic vale lo Iod size.
Avnslvong JuvlIev vaises lIe queslion oJ suIslvale uli-
Iizalion pallevns I lIe Ivain and olIev ovgans and lIeiv
veIalionsIip lo ouv anaIsis. SpeciJicaII, sIe asIs
vIelIev gIcogen is sloved in gul lissue and, iJ so,
vIelIev lIis signiJicanlI adds lo lIe nass oJ lIe lissue
and lIeveI conJounds lIe anaIsis. We do nol JeeI lIal
lIis is a veIevanl concevn. Ouv anaIsis is Iased on vales
oJ enevg uliIizalion I lIe vavious ovgans expvessed as
lIe nass-speciJic ovgan nelaIoIic vale. OIcogen vouId
Ie nelaIoIicaII inaclive, and iJ il veve sloved in lIe
gul ils veigIl vouId Ie laIen cave oJ in lIe conpulalion
oJ lIe nass-speciJic nelaIoIic vale Jov lIal lissue. TIe
anaIsis vouId lIeveJove nol Ie inJIuenced I lIe spe-
ciJic suIslvales Ieing nelaIoIized.
Sone connenlalovs |FaII, MavcIanl, HoIIova, Hen-
neIevg) Iave IvougIl up poinls lIal ave speciJicaII veIe-
vanl lo Ioninid evoIulion. FaII Ias avgued lIal Ivain
expansion in lIe Ioninids na Iave Ieen gvaduaI valIev
lIan punclualed aJlev lIe appeavance oJ Hono:
MavcIanl suggesls lIal eavI Hono, pavlicuIavI H. Ia-
IiIis sensu slviclo, na nol Iave Iad a IigIev-quaIil
diel lIan lIe auslvaIopilIecines, and IolI HoIIova and
HenneIevg poinl oul lIal an incvease in aIsoIule Ivain
size in lIe Ioninids na acconpan an incvease in
Iod size ov na Ie independenl oJ il. TIese ave aII
evoIulionav delaiIs lIal ave suIjecl lo deIale slenning
Jvon lIe anIiguil oJ veIaliveI poov dala. TIe do nol
aJJecl lIe Iasic issue lIal vIen lIe Ivain expanded in
veIalion lo Iod size lIe enevgelic IaIance vouId Iave
Iad lo Ie adjusled. TIe queslion lIal is sliII open is
vIen in ouv evoIulionav Iislov lIis na Iave Iap-
pened. We suggesl lIal lIe cIange in Iod pvopovlions
in H. evgaslev in veIalion lo lIe auslvaIopilIecines na
Iave navIed a najov sIiJl lo a IigIev-quaIil Jood and
covvespondingI snaIIev guls. TIe Jacl lIal lIe cIange
in lIe sIape oJ lIe viI cage in Hono na aIso Ie associ-
aled vilI lIe adoplion oJ JuII IipedaI Ioconolion
|MavcIanl) does nol seviousI aJJecl lIis nolion. Ouv
poinl is lIal in veIalion lo Iod size lIe space avaiIaIIe
in lIe auslvaIopilIecine peIvic vegion |speciJicaII in
AuslvaIopilIecus aJavensis and A. aJvicanus) vouId ac-
connodale Iavgev guls in veIalion lo Iod size lIan lIe
covvesponding space in H. evgaslev.
We JeeI lIal lIe evidence pvovided lo suppovl lIe ex-
pensive-lissue IpolIesis is suJJicienl lo sIov lIal in
Iunans and pvinales lIeve Ias Ieen a coevoIulion oJ
lIe Ivain and lIe digeslive sslen. We do nol cIain lIal
a veduclion in lIe size oJ lIe gul is lIe onI va lo
IaIance lIe IigI enevg vequivenenls oJ a veIaliveI
Iavge Ivain: valIev, ve suggesl lIal il is lIe nosl pvoIa-
IIe neans I vIicI Iunans Iave acconpIisIed lIis.
TIeve is no douIl lIal lIe IpolIesis vouId IeneJil I
JuvlIev deveIopnenl and lesling, and ve Iope lIal lIis
conlviIulion viII Iave slinuIaled olIevs lo JoIIov ils
BeJevences Ciled
AIELLO, L. C. I992. AIIonelv and lIe anaIsis oJ size and
sIape in Iunan evoIulion. JouvnaI oJ Hunan EvoIulion
AIELLO, L. C., ANB M. C. BEAN. I990. An inlvoduclion lo Iu-
nan evoIulionav analon. London Acadenic Fvess.
AIELLO, L. C., ANB B. I. M. BUNBAB. I993. Neocovlex size,
gvoup size, and lIe evoIulion oJ Ianguage in lIe Ioninids.
ABMSTBONO, E. i982. A IooI al veIalive Ivain size in nan-
naIs. Neuvoscience Lellevs 34IOI-4.
.I983. BeIalive Ivain size and nelaIoIisn in nannaIs.
Science 220I302-4.
. I985a. BeIalive Ivain size in nonIes and pvosinians.
Anevican JouvnaI oJ FIsicaI AnlIvopoIog 66263-73.
. Ig8sI. AIIonelvic considevalions oJ lIe aduIl nanna-
Iian Ivain, vilI speciaI enpIasis on pvinales, in Size and
scaIing in pvinale IioIog. Ediled I W. L. Jungevs, pp.
II 5-46. Nev YovI FIenun Fvess.
.I990. Bvains, Iodies, and nelaIoIisn. Bvain, BeIaviouv,
and EvoIulion 36I66-76.
size in Iivds. Bvain, BeIaviov, and EvoIulion 26I4I-53. [EA]
IausIaIl und TenpevaluvveguIalion. MunicI UvIan and
BABTON, B. A. i992. AIIonelv oJ Jood inlaIe in Jvee-vanging an-
lIvopoid pvinales. FoIia FvinaloIogica 5856-59.
vespivalion oJ nuscuIaluve in veIalion lo Iod size. Anevican
JouvnaI oJ FIsioIog 17358-60.
BLA7TEB, K. I989. Enevg nelaIoIisn in aninaIs and nan.
CanIvidge CanIvidge Univevsil Fvess.
BLIOH, J., ANB K. O. JOHNSON. I973. OIossav oJ levns Jov
lIevnaI pIsioIog. JouvnaI oJ AppIied FIsioIog 3594I-60.
BBOBY, S. I945. Bioenevgelics and gvovlI. BaIlinove BeinIoId.
BUNN, H. T., ANB E. M. KBOLL. I986. Sslenalic IulcIev
I FIio/FIeislocene Ioninids al OIduvai Oovge, Tanzania.
BYBNE, B., ANB A. WHITEN. Edilovs. I988. MacIiaveIIian inleI-
Iigence. OxJovd CIavendon.
CHIVEBS, B. J., ANB C. M. HLABIK. I980. MovpIoIog oJ lIe
gaslvoinleslinaI lvacl in pvinales Conpavisons vilI olIev
nannaIs in veIalion lo diel. JouvnaI oJ MovpIoIog
.I984. Biel and gul novpIoIog in pvinales, in Food ac-
quisilion and pvocessing in pvinales. Ediled I B. J. CIivevs,
B. A. Wood, and A. BiIsIovougI, pp. 2I3-30. Nev YovI
FIenun Fvess.
CLUTTON-BBOCK, T. H., ANB F. H. HABVEY. I980. Fvinales,
Ivains, and ecoIog. JouvnaI oJ ZooIog, London I90309-23.
CBAWFOBB, M. A. i992. TIe voIe oJ dielav Jall acids in IioI-
og TIeiv pIace in lIe evoIulion oJ lIe Iunan Ivain. Nulvi-
lion Bevievs 503-II.
Vavialions in gvoup size and denogvapI, in Fvinale socie-
lies. Ediled I B. L. CIene, B. M. SeJavlI, B. W. WvangIan,
and T. T. SlvuIsaIev, pp. 54-68. CIicago Univevsil oJ CIi-
cago Fvess.
BEMMENT, M. I983. Feeding ecoIog and lIe evoIulion oJ Iod
size in IaIoons. AJvican JouvnaI oJ EcoIog 2I2I9-33.
BUNBAB, B. I. M. i992. Neocovlex size as a conslvainl on gvoup
size in pvinales. JouvnaI oJ Hunan EvoIulion 22469-93.
I993. Co-evoIulion oJ neocovlex size, gvoup size, and Ian-
guage in Iunans. BeIaviovaI and Bvain Sciences I668I-735.
. n.d. Neocovlex size and gvoup size in pvinales A lesl oJ
lIe IpolIesis. JouvnaI oJ Hunan EvoIulion. In pvess.
FALK, BEAN. I987. Honinid paIeoneuvoIog. AnnuaI Beviev oJ
AnlIvopoIog I6I3-30. [BF]
1i990. Bvain evoIulion in Hono TIe vadialov lIeov.
BeIaviovaI and Bvain Sciences I3333-8I.
CUBBENT ANTHBOFOLOOY VoIune 36, NunIev 2, ApviI I995
.i992. EvoIulion oJ lIe Ivain and cognilion in Ioninids
|TIe Sixl-Second Janes AvlIuv Lecluve). Nev YovI Anevi-
can Museun oJ NaluvaI Hislov. [BF]
FAO/WHO/UNU. I985. Enevg andpvolein vequivenenls Be-
povl oJ a joinl expevl consuIlalion. |WHO TecInicaI Bepovl Se-
vies 724.) Oeneva WovId HeaIlI Ovganisalion.
FIELB, J., H. S. BELBINO, ANB A. W. MABTIN. I939. An anaI-
sis oJ lIe veIalion Ielveen IasaI nelaIoIisn and sunnaled
lissue vespivalion in lIe val. I. TIe posl-puIevlaI aIIino val.
JouvnaI oJ CeIIuIav and Conpavalive FIsioIog I4I43-57.
FISHEB, B. A. I930. TIe genelicaI lIeov oJ naluvaI seIeclion.
OxJovd OxJovd Univevsil Fvess. [MH]
FOLEY, BOBEBT. I99I. Hov nan species oJ Ioninid sIouId
lIeve Ie? JouvnaI oJ Hunan EvoIulion 204I3-29. [LFM]
FOLEY, B. A., ANB F. C. LEE. I99I. EcoIog and enevgelics oJ
encepIaIizalion in Ioninid evoIulion. FIiIosopIicaI Tvansac-
lions oJ lIe BoaI Sociel, London B 334223-32.
TIe conposilion oJ lIe aduIl Iunan Iod as delevnined
I cIenicaI anaIsis. JouvnaI oJ BioIogicaI CIenislv
FOBB, T. J. ANB S. B. KBAUS. i992. A vele in lIe vigIl vIaIe.
Naluve 359680. [BF]
FBAYEB, B. I984. BioIogicaI and cuIluvaI cIange in lIe Euvo-
pean Lale FIeislocene and EavI HoIocene, in TIe ovigins oJ
nodevn Iunans A vovId suvve oJ lIe JossiI evidence. Ediled
I F. H. SnilI and F. Spencev, pp. 2II-50. Nev YovI AIan B.
Liss. [MH]
OIBSON, K. B. I986. Cognilion, Ivain size, and lIe exlvaclion
oJ enIedded Jood vesouvces, in Fvinale onlogen, cognilion,
and sociaI IeIaviov. Ediled I J. O. EIse and F. C. Lee,
pp. 93-I05. CanIvidge CanIvidge Univevsil Fvess.
OBANBE, F. I980. Enevg expendiluve oJ ovgans and lissues,
in Assessnenl oJ enevg nelaIoIisn in IeaIlI and disease. Ed-
iled I S. CaIvevl, pp. 88-92. CoIunIus Boss LaIovalovies.
OBOSS, J., Z. WANO, ANB B. A. WUNBEB. I986. Adaplalions
lo Jood quaIil and enevg need cIanges in gul novpIoIog
and capacil oJ Micvolus ovcIvogaslev. JouvnaI oJ MannaIog
I986. LiJe Iislovies in conpavalive pevspeclive, in Fvinale
socielies. Ediled I B. B. Snuls, B. L. CIene, B. M. SeJavlI,
B. W. WvangIan, and T. T. SlvuIsaIev, pp. I8I-96. CIicago
Univevsil oJ CIicago Fvess.
HENNEBEBO, M. 1990. Bvain size/Iod veigIl vaviaIiIil in
Hono sapiens Consequences Jov inlevpveling Ioninid evoIu-
lion. Hono 39I2I-30. [MH]
HOFMAN, M. A. I983. Enevg nelaIoIisn, Ivain size, and Ion-
gevil in nannaIs. QuavlevI Beviev oJ BioIog 5 8495-5 I2.
HOLLOWAY, B. L. I979. Bvain size, aIIonelv, and veovganiza-
lion Tovavd a snlIesis, in BeveIopnenl and evoIulion oJ
Ivain size BeIaviovaI inpIicalions. Ediled I M. E. HaIn,
C. Jensen, and B. BudeI, pp. 59-88. Nev YovI Acadenic
Fvess. [BLH]
.I980. WilIin-species Ivain-Iod veigIl vaviaIiIil A ve-
exaninalion oJ lIe BanisI dala and olIev pvinale species.
Anevican JouvnaI oJ FIsicaI AnlIvopoIog 5 3I09-2I. [BLH]
HUNT, KEVIN B. I994. TIe evoIulion oJ Iunan IipedaIil EcoI-
og and JunclionaI novpIoIog. JouvnaI oJ Hunan EvoIulion
26i83-202. [LFM]
HUYSSEN, V., ANB B. C. LACY. I985. BasaI nelaIoIic vales in
nannaIs Taxononic diJJevences in lIe aIIonelv oJ SMB and
Iod nass. Conpavalive BiocIenislv and FIsioIog
IVEBSEN, J. A. I972. BasaI enevg nelaIoIisn oJ nusleIids. Jouv-
naI oJ Conpavalive FIsioIog 8iA34I-44.
JACOBS, K. H. I985. CIinale and Ioninid poslcvaniaI sIeIelon
in Wuvn and EavI HoIocene Euvope. CUBBENT ANTHBOFOLOOY
265I2-I4. [MH]
JEBISON, H. J. I973. EvoIulion oJ lIe Ivain and inleIIigence.
Nev YovI Acadenic Fvess. [MH, KM1
. I990. WeIcone IigIl on a Iol lopic. BeIaviovaI and
Bvain Sciences I3360.
JOHANSON, BONALB C., ET AL. I987. Nev pavliaI sIeIelon oJ
Hono IaIiIis Jvon OIduvai Oovge, Tanzania. Naluve
327205-9. [LFM]
KABASOV, W. H. i992. BaiI enevg expendiluve and lIe cosl oJ
aclivil in nannaIs. Anevican ZooIogisl 32238-48.
KAY, B. F., ANB F. E. OBIN#. I988. ToolI novpIoIog, veav,
and diel in AuslvaIopilIecus and FavanlIvopus, in EvoIulion-
av Iislov oJ lIe voIusl auslvaIopilIecines. Ediled I F. E.
Ovine, pp. 427-48. Nev YovI AIdine de Ovulev.
KEELEY, L. M., ANB N. TOTH. I98I. Micvoveav poIisIes on
eavI slone looIs Jvon KooIi Fova. Naluve 297676-78.
KEITH, A. I89I. AnalonicaI noles on MaIa apes. Fvoceedings
oJ lIe Singapove BvancI oJ lIe BoaI Asialic Sociel 2377-89.
. I950. An auloIiogvapI. Nev YovI FIiIosopIicaI Li-
KLEIBEB, M. I96I. TIe Jive oJ IiJe. Nev YovI WiIe.
KBEBS, H. A. I950. Bod size and lissue vespivalion. BiocIinica
el BiopIsica Acla 4249-69.
LAMB, B. B. I984. FIsioIog oJ exevcise Besponses and adapla-
lions. Nev YovI MacniIIan. [MH]
I994. Biel oJ AuslvaIopilIecus voIuslus al SvavlIvans Jvon
slaIIe cavIon isolopic anaIsis. JouvnaI oJ Hunan EvoIulion
LEHNINOEB, A. L. I975. BiocIenislv. Nev YovI WovlI.
LEIOH, S. B. i992. CvaniaI capacil evoIulion in Hono eveclus
and eavI Hono sapiens. Anevican JouvnaI oJ FIsicaI AnlIvo-
poIog 87I-I4.
MC HENBY, H. I994. BeIaviovaI ecoIogicaI inpIicalions oJ eavI
Ioninid Iod size. JouvnaI oJ Hunan EvoIulion 2777-87.
I986a. Oaslvo-inleslinaI aIIonelv in pvinales incIuding nev
species, in Fvinale ecoIog and consevvalion. Ediled I J. O.
EIse and F. C. Lee, pp. 75-85. CanIvidge CanIvidge Univev-
sil Fvess.
. I986I. Sone aspecls oJ gaslvo-inleslinaI aIIonelv in pvi-
nales and olIev nannaIs, in BeJinilion el ovigines de
I'Ionne. Ediled I M. SaIIa, pp. 293-302. Favis Edilions du
MAC NAB, B. K., ANB J. F. EISENBEBO. I989. Bvain size and
ils veIalion lo lIe vale oJ nelaIoIisn in nannaIs. Anevican
NaluvaIisl I33I57-67.
MABTIN, A. W., ANB F. A. FUHBMAN. I955. TIe veIalionsIip
Ielveen sunnaled lissue vespivalion and nelaIoIic vale in lIe
nouse and dog. FIsioIogicaI ZooIog 28I8-34.
MABTIN, B. B. I98I. BeIalive Ivain size and nelaIoIic vale in
levveslviaI vevleIvales. Naluve 29357-60.
. I983. Hunan Ivain evoIulion in an ecoIogicaI conlexl
52nd Janes AvlIuv Lecluve on lIe EvoIulion oJ lIe Hunan
Bvain. Nev YovI Anevican Museun oJ NaluvaI Hislov.
1 990. Fvinale ovigins and evoIulion. London CIapnan
and HaII.
C. M. HLABIK. I985. OaslvoinleslinaI aIIonelv in pvinales
and olIev nannaIs, in Size and scaIing in pvinale IioIog.
Ediled I W. L. Jungevs, pp. 6I-89. Nev YovI FIenun Fvess.
MILTON, K. I979. SpaliaI and lenpovaI pallens oJ pIanl Joods
in lvopicaI Jovesls as a slinuIus lo inleIIecluaI deveIopnenl in
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. I98I. Bivevsil oJ pIanl Joods in lvopicaI Jovesls as a slin-
uIus lo nenlaI deveIopnenl in pvinales. Anevican AnlIvopoI-
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. I986. Fealuves oJ digeslive pIsioIog in Fvinales. Nevs
in FIsioIogicaI Sciences I76-79.
. I987. Fvinale diels and gul novpIoIog InpIicalions
Jov Ioninid evoIulion, in Food and evoIulion Tovavd a lIe-
ov oJ Iunan Jood IaIils. Ediled I M. Havvis and E. B. Boss,
pp. 96-I I6. FIiIadeIpIia TenpIe Univevsil Fvess.
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inleIIigence, in MacIiaveIIian inleIIigence. Ediled I B. Bne
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I993. Biel and pvinale evoIulion. ScienliJic Anevican
AIELLO ANB WHEELEB TIe Expensive-Tissue HpolIesis l2.2i
n.d. Food and diel, in TIe enccIopedia oJ cuIluvaI an-
lIvopoIog. Ediled I B. Levinson and M. EnIev. LaIeviIIe,
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MILTON, K., ANB M. BEMMENT. I988. Bigeslive and passage
Iinelics oJ cIinpanzees Jed IigI and Iov JiIev diels and con-
pavison vilI Iunan dala. JouvnaI oJ Nulvilion ii8285-305.
H. W. BEAN. I945. TIe cIenicaI conposilion oJ lIe aduIl Iu-
nan Iod and ils Ieaving on lIe IiocIenislv oJ gvovlI. Jouv-
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OIKAWA, S., ANB Y. ITAZOWA. I984. AIIonelvic veIalionsIip
Ielveen lissue vespivalion and Iod nass in lIe cavp. Conpav-
alive BiocIenislv and FIsioIog 77A4I5-i8.
FABKEB, S. T., ANB K. B. OIBSON. I979. A deveIopnenlaI
nodeI Jov lIe evoIulion oJ Ianguage and inleIIigence in eavI
Ioninids. BeIaviovaI and Bvain Sciences 2367-407.
FETEBS, B. H. I983. TIe ecoIogicaI inpIicalions oJ Iod size.
CanIvidge CanIvidge Univevsil Fvess.
FOCZOFKO, F. I97I. MelaIoIic IeveIs in aduIl IoneolIevns.
Acla TIevioIogica I6I-2i.
FOTTS, B., ANB F. SHIFMAN. I98I. CulnavIs nade I slone
looIs on Iones Jvon OIduvai Oovge, Tanzania. Naluve
BICHABBS, AUBBEY. I948. Hungev, vovI, and sex in a savage
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BIOHTMIBE, O. F. I98I. Fallevns in lIe evoIulion oJ Hono
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BOBINSON, J. T. I972. EavI Ioninid posluve and Ioconolion.
CIicago Univevsil oJ CIicago Fvess.
BUFF, C. B. I99I. CIinale and Iod sIape in Ioninid evoIulion.
JouvnaI oJ
Hunan EvoIulion
BUFF, C. B., ANB A. WALKEB. I993. Bod size and Iod
sIape, in TIe NavioIolone Hono eveclus sIeIelon. Ediled I
A. WaIIev and B. E. LeaIe. CanIvidge Havvavd Univevsil
SCHMIB, F. I983. Eine BeIonslvuIlion des SIeIelles von A.L.
288-I |Hadav) und deven Konsequenzes. FoIia FvinaloIogica
. I99I. TIe lvunI oJ lIe auslvaIopilIecines, in Oni-
gine|s) de Ia Iipedie cIez Ies Honinides. Ediled I Y. Coppens
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SCHMIBT-NIELSEN, KNUT. I984. ScaIing WI is aninaI size
so inpovlanl? CanIvidge CanIvidge Univevsil Fvess.
SCHOFIELB, C. I985. An annolaled IiIIiogvapI oJ souvce nale-
viaI Jov IasaI nelaIoIic vale dala. Hunan Nulvilion CIinicaI
Nulvilion 39C, suppI. I42-9I.
SCHOFIELB, W. N. I985. Fvedicling IasaI nelaIoIic vale Nev
slandavds and veviev oJ pvevious vovI. Hunan Nulvilion CIin-
icaI Nulvilion 39C, suppI. I5-4I.
SHIFMAN, F. I986. Scavenging ov Iunling in eavI Ioninids.
Anevican AnlIvopoIogisl 8827-43.
SHIFMAN, F., ANB A. WALKEB. I989. TIe cosls oJ Ieconing a
pvedalov. JouvnaI oJ Hunan EvoIulion i8373-92.
SILLEN, A. i992. Slvonliun-caIciun valios |Sv/Ca) oJ AuslvaIo-
pilIecus voIuslus and associaled Jauna Jvon SvavlIvans. Jouv-
naI oJ Hunan EvoIulion 23495-5I6.
SILLEN, A., B. ABMSTBONO, ANB O. HALL. n.d. Slvonliun-
caIciun valios |Sv/Ca) and 87Sv/86Sv oJ AuslvaIopilIecus vo-
Iuslus and Hono sp. Jvon SvavlIvans. JouvnaI oJ Hunan Evo-
Iulion. In pvess.
SFETH, J. B. I989. EavI Ioninid Iunling and scavenging TIe
voIe oJ neal as an enevg souvce. JouvnaI oJ Hunan EvoIulion
STAHL, A. B. I984. Honinid dielav seIeclion IeJove Jive. CUB-
STAHL, W. B. I965. Ovgan veigIls in pvinales and olIev nan-
naIs. Science I50I039-42.
ANB JANE OOOBALL. I994. Fallens oJ pvedalion I cIinpan-
zees on ved coIoIus nonIes in OonIe NalionaI FavI, i982-
I99 I. Anevican JouvnaI oJ FIsicaI AnlIvopoIog 942I3-28.
STEFHAN, H., H. FBAHM, ANB O. BABON. I98I. Nev and ve-
vised dala on voIune oJ Ivain slvucluves in inseclivoves and pvi-
nales. FoIia FvinaloIogica 35I-29.
SUSSMAN, B. W. I987. MovpIo-pIsioIogicaI anaIsis oJ diels,
in TIe evoIulion oJ Iunan IeIaviov Fvinale nodeIs. Ediled
I W. O. Kinze, pp. I5I-79. AIIan Slale Univevsil oJ Nev
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SNYBEB, W. S. I975. InlevnalionaI Connission on BadioIogicaI
Fvoleclion |ICBF) vepovl on lIe TasI Fovce on BeJevence Man.
OxJovd OxJovd Univevsil Fvess.
TAOUE, B. O., ANB C. 0. LOVEJOY. I986. TIe oIslelvic peIvis
oJ A.L. 288-I |Luc). JouvnaI oJ Hunan EvoIulion I5237-55.
TBINKAUS, E., ANB M. H. WOLFOFF. n.d. Bvain size in posl-
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