Putting the Altruism Back into Altruism: The Evolution of Empathy

25 Pages·2010·0.37 MB·English

ANRV331-PS59-11 ARI 4November2007 20:27
Putting the Altruism
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ews.org0. For pers •••• TTOAooRtpph’s e dccrioot aewmrdtnpi calrolreetahiscd eilenends st hiavirest ivsceolealusrcmhe The Evolution of Empathy
ualrevi4/29/1 Frans B.M. de Waal
nals.annRY on 0 LEimvionrgyLUinnkivse,rYseitryk,eAstNlanattiao,nGalePorrgimiaa3te03R2e2s;eeamrcahilC:deenwteara,[email protected],
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00. AR Annu.Rev.Psychol.2008.59:279–300 KeyWords
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79-GE FirstpublishedonlineasaReviewinAdvanceon perception-action,perspective-taking,prosocialbehavior,
hol. 2008.59:2ND - COLLE hTJTuthhtnpiees:/A5a/r,npt2nsiyc0ulc0aehl7’s.Radneovniiu:ewalroefvPiesywchs.oolorggyisonlineat cAEovboospltuertraiaoctnitoanry theory postulates that altruistic behavior evolved for
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PsyYL 10.1146/annurev.psych.59.103006.093625 thereturn-benefitsitbearstheperformer.Forreturn-benefitstoplay
ev. AR Copyright(cid:2)c 2008byAnnualReviews. amotivationalrole,however,theyneedtobeexperiencedbytheor-
u. RF M Allrightsreserved ganism.Motivationalanalysesshouldrestrictthemselves,therefore,
AnnY O 0066-4308/08/0203-0279$20.00 to the altruistic impulse and its knowable consequences. Empathy
T is an ideal candidate mechanism to underlie so-called directed al-
SI
R truism,i.e.,altruisminresponsetoanother’spain,need,ordistress.
E
V
NI Evidenceisaccumulatingthatthismechanismisphylogeneticallyan-
U cient,probablyasoldasmammalsandbirds.Perceptionoftheemo-
y
b tionalstateofanotherautomaticallyactivatessharedrepresentations
causingamatchingemotionalstateintheobserver.Withincreasing
cognition,state-matchingevolvedintomorecomplexforms,includ-
ingconcernfortheotherandperspective-taking.Empathy-induced
altruismderivesitsstrengthfromtheemotionalstakeitoffersthe
selfintheother’swelfare.Thedynamicsoftheempathymechanism
agree with predictions from kin selection and reciprocal altruism
theory.
279
ANRV331-PS59-11 ARI 4November2007 20:27
“Youbeginwiththeeffectofbehavioronac-
Contents torsandrecipients;youdealwiththeproblem
of internal motivation, which is a secondary
INTRODUCTION................. 280
problem,afterward....[I]fyoustartwithmo-
ORIGINOFEMPATHY............ 282
tivation, you have given up the evolutionary
LEVELSOFEMPATHY........... 282
analysisattheoutset.”
EmotionalContagion............. 282
Thisisaperfectlylegitimatestrategythat
SympatheticConcern............. 283
y. has yielded profound insights into the evo-
nl EmpathicPerspective-Taking..... 285
o lutionofaltruism(e.g.,Dugatkin2006).Un-
e UNDERLYINGMECHANISMS... 286
s
u fortunately,however,theseinsightshavenot
al PerceptionActionMechanism.... 286
n come with a new terminology: Evolutionary
so RussianDollModel.............. 287
nals.annualreviews.orgRY on 04/29/10. For per FERMOAESEPyLmmMAmTToppREtaHiatoUMhtYhniIcPeaSAltAPMiSCTcerEoCH.sn.VpoY.tenOa.ccgT.tLe.iiOorvV.nne.E.-..T.D...a...k.....i.n....g........................ 222288889898 bTlscaneeaioshoceltslokuleosstosdhgt,fbye“tewaoannpalhteceterfithrautosctehiirstsseiattfoirisocncntrot”ioneririnitsfsnudresoieecltiftgdna.blagtSlehtreoidnmedmleeboaifi“slectastsitnservooellaaryfifift,isdtrowaheennt”hclhaiieabeplrcteiehtteoregienaotrarhttmnreeodalisryr-st..
ourRA PROXIMATEMECHANISMOF The prototypical altruist is a honeybee that
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79-GE Empathy may be uniquely well suited for ogy by evolutionary biologists has been un-
008.59:2COLLE A(dbelitfiornuloiitgsimiocna)l: bisrmid,gsiinngcetihtehgasapthbeeptwroepeenrteygoofistmranasnfdoramltirnug- hpeerlpsfeu.lTfohrecowmaymtuoncicleaatirounpabthoeutcomnofutisviaotnioins
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PsyYL recipient’sfitnessata Hoffman(1981a,p.133) considered separate from motivation. Con-
ev. AR costtothe versely, motivational analyses require us to
RM performers
Annu. Y OF Ugoltailm: athteebcaeunesefitosran INTRODUCTION kcoeenpsidmeroattiivoantiso.nItsiespnaortatfeorfnroomthienvgotlhuatitobniaorly-
T Discussionsofaltruisticbehaviortendtosuf- ogistshammeronthedistinctionbetweenul-
SI organismoritsclose
ER kinderivefroma ferfromalackofdistinctionbetweenfunction timateandproximate(Mayr1961,Tinbergen
V
NI behavior,hencethe andmotivation.Thisisduetothecontrasting 1963). The ultimate cause refers to why a
U probablereasonwhy emphasisofbiologistsandpsychologists,with behavior evolved over thousands of gener-
by thebehaviorwas theformerfocusingonwhataparticularbe- ations, which depends on its fitness conse-
favoredbynatural
havior is good for, and the latter on how it quences. The proximate cause, on the other
selection
comesabout. hand, refers to the immediate situation that
Proximatecause:
Evolutionaryexplanationsarebuiltaround triggers behavior, and the role of learning,
situationthat
triggersbehaviorand theprinciplethatallthatnaturalselectioncan physiology, and neural processes—typically
themechanism workwitharetheeffectsofbehavior—notthe thedomainofpsychologists.
(psychological, motivationbehindit.Thismeansthereisonly Proximateandultimateviewpointsdoin-
neural,physiological)
onelogicalstartingpointforevolutionaryac- form each other, yet are not to be con-
thatenablesit
counts, as explained by Trivers (2002, p. 6): flated. For example, primate cooperation is
280 deWaal
ANRV331-PS59-11 ARI 4November2007 20:27
promotedbysocialtolerance.Throughitsef- trinsically rewarding qualities in that it of-
fectonfood-sharing,toleranceevensoutpay- fers the actor an emotional stake in the re-
offdistributions(deWaal&Davis2003,Melis cipient’swell-being,i.e.,ifhelpingtheother
Directedaltruism:
et al. 2006). Tolerance likely is a proximate ameliorates the helper’s internal state (see
helpingor
mechanismthatevolvedtoservetheultimate Empathy as Evolved Proximate Mechanism, comfortingbehavior
goalofcooperation,whichistoyieldbenefits below).Extrinsicrewards,ontheotherhand, directedatan
forallcontributors. arelesslikelytoplayarole.Bydefinition,al- individualinneed,
y. Cooperation and altruistic behavior are truismcarriesaninitialcost,andpositivecon- pain,ordistress
nl
o thoughttohaveevolvedtohelpfamilymem- sequencesoccuronlyafterasignificanttime Intentional
e
s altruism: the
u bers and those inclined to return the favor interval (e.g., the recipient reciprocates) or
al altruistdeliberately
n (Hamilton1964,Trivers1971).Regardlessof notatall(e.g.,carefordependentkin),making
o seekstobenefit
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gper whetherthisisthewholeexplanationornot forratherpoorlearningconditions. eithertheother
ews.or0. For (2s0e0e5S),obthere&poDinSt Wis itlhsoant u19lt9im8,atEeOacWcoiulsnotns quiIrnettehnetioacntaolrlytoseelxfipslhiciatlltyrueixspmectwootuhledrsrteo- (ailntrtuenisttiiocnaalltlryuism)or
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PsyYL 3. Intentionalaltruism.Helpbasedonthe pliestomostreciprocalaltruismintheanimal animals,buttheterm
ev. AR prediction of behavioral effects. One kingdom. “empathy”inthe
RM prediction could be that the help will presentreview
Annu. TY OF bperordeucciperoacnaetetdb,ehneenficte.tShiantcethtehaectacwtoilrl mcoomOtievnsacdteiioscneoavnloanluvetecodtne,dombfreyoh,mai.veii.to,srituslotmifmtoetanitveaagtsioosaunlmsb.eeA-s acpriptelireisonev(ean)iisfmonelty
RSI seeks to benefit itself, we may call this goodexampleissexualbehavior,whicharose Motivational
E autonomy:
V intentionally selfish altruism. The sec-
NI ondpossibilityishelpbasedonanap- toservereproduction.Sinceanimalsare,asfar independenceof
U asweknow,unawareofthelinkbetweensex motivationfrom
by preciation of how one’s own behavior and reproduction, they must be engaging in ultimategoals
willhelptheother.Sincetheactorseeks
sex(asdohumansmuchofthetime)without
tobenefittheother,wemaycallthisin-
progenyinmind.Justassexcannotbemoti-
tentionallyaltruisticaltruism.
vated by unforeseen consequences, altruistic
Some directed altruistic behavior is pro- behaviorcannotbemotivatedbyunforeseen
moted by built-in rewards, such as the payoffs.
oxytocin release during suckling that may Thealtruisticimpulseistobetakenvery
underpin maternal care (Panksepp 1998). seriously, therefore, because even if altruis-
Empathy-basedaltruismmayhavesimilarin- tic behavior were partially learned based on
www.annualreviews.org • TheEvolutionofEmpathy 281
ANRV331-PS59-11 ARI 4November2007 20:27
short-termintrinsicrewardsorlong-termex- cognition is often critical, it is a secondary
trinsicrewards,thisbynomeansrulesoutthe development. As noted by Hoffman (1981b,
altruisticimpulse.Infact,itpresupposesthis p.79),“[H]umansmustbeequippedbiologi-
Perception-action
impulsegiventhatabehavior’sconsequences callytofunctioneffectivelyinmanysocialsit-
mechanism(PAM):
automaticallyand cannotbelearnedwithoutspontaneouslyen- uations without undue reliance on cognitive
unconsciously gaginginitinthefirstplace. processes.”
activatedneural This review seeks to restore the altruism The selection pressure to evolve rapid
y. representationsof withinaltruismbyexploringtheroleofem- emotionalconnectednesslikelystartedinthe
nl statesinthesubject
o pathyinthedirectedaltruismofhumansand context of parental care long before our
e similartothose
s
al u perceivedinthe other animals. Some definitions of empathy speciesevolved(Eibl-Eibesfeldt1974[1971],
n object stressthesharingofemotions,whereasother MacLean1985).Signalingtheirstatethrough
o
s
gper Emotional definitions stress the capacity to put oneself smilingandcrying,humaninfantsurgetheir
ews.or0. For cemonottaiognioanl: ianretostohetoopt-hdeor’ws“ns,hhooews.e”vTerh,ethlaatttetrhdeeyfidniistcioonn-s cTahreogmivaenr 1to995c,omBeowilnbtyo 1a9c5ti8o)n. E(Aqcueibvaolen&t
nals.annualreviRY on 04/29/1 ssotubabjtejeec-ctmtawticthhinangofa nWacdleuoecdtpiftneoigmnllgompwtaehtrheeayberbfmroooaotmdttoieomsintts-apulpopsosessniasbpsiblipetlirevdoieaatfiycnhntteoitciienoodstnhte,eneairtndss-.., mrwpeaaeprrcermhonaditnsnugicsatmolieofsrnttohrtpeeoelyireoaasntueodnngina.ffeAfaeelvdlciaitanenndgio,mrbcalymelsaatnhimnienmigwr,ahloaiinfacfnhd-
ourRA Wefirstconsiderthevariouslevelsofempathy spring’s needs likely out-reproduced those
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PsyYL considerations,intheendthetwowillmeet. ily return to their native group, where they
ev. AR Empathymaybemotivationallyautonomous, aremorelikelytoreceivethisservice(Dittus
RM
u. F butitstillneedstoproduce—onaverageand &Ratnayeke1989).
AnnY O inthelongrun—evolutionarilyadvantageous
T outcomes. The central thesis to be argued
SI LEVELSOFEMPATHY
R here,then,isthatempathyevolvedinanimals
E
V
NI asthemainproximatemechanismfordirected EmotionalContagion
U altruism,andthatitcausesaltruismtobedis-
y Thelowestcommondenominatorofallem-
b pensed in accordance with predictions from
pathic processes is that one party is affected
kinselectionandreciprocalaltruismtheory.
byanother’semotionalorarousalstate.This
broad perspective on empathy, which goes
ORIGINOFEMPATHY
backasfarasLipps(1903),leadsonetorec-
Empathyallowsonetoquicklyandautomat- ognizecontinuitybetweenhumansandother
icallyrelatetotheemotionalstatesofothers, animals as well as between human adults
whichisessentialfortheregulationofsocial and young children. Emotional connected-
interactions, coordinated activity, and coop- nessinhumansissocommon,startssoearly
eration toward shared goals. Even though in life (e.g., Hoffman 1975, Zahn-Waxler &
282 deWaal
ANRV331-PS59-11 ARI 4November2007 20:27
Radke-Yarrow 1990), and shows neural and their own response to pain (Langford et al.
physiological correlates (e.g., Adolphs et al. 2006).
1994, Decety & Chaminade 2003a, Rimm- Miller et al. (1959) published the first of
Sympathetic
Kaufman&Kagan1996)aswellasagenetic a series of pioneering studies on the trans-
concern: concern
substrate (Plomin et al. 1993), that it would mission of affect in rhesus macaques. These aboutanother’sstate
bestrangeindeedifnocontinuitywithother monkeystendtoterminateprojectedpictures andattemptsto
species existed. Evolutionary continuity be- of conspecifics in a fearful pose even more amelioratethisstate
y. tween humans and apes is reflected in the rapidly than negatively conditioned stimuli. (e.g.,consolation)
nl
o similarityofemotionalcommunication(Parr Perhaps the most compelling evidence for Cognitiveempathy:
e
s empathycombined
u &Waller2007)aswellassimilarchangesin emotional contagion came from Wechkin
al withcontextual
n brainandperipheralskintemperatureinre- etal.(1964)andMassermanetal.(1964),who
o appraisalandan
s
gper sponse to emotionally charged images (Parr foundthatmonkeysrefusetopullachainthat understandingof
ews.or0. For 200A1,flPoacrkr&ofHbiordpskitnaski2n0g01o)f.f all at once be- deleelcivtreircssfhooocdkttooathnedmtriigfgdeorisnpgaisnordeealcitvieornssainn wobhjaetctc’sauesmedottihoenal
nualrevi04/29/1 creafluseex-loinkee,ahmigohnlygatdhaepmtiviesssptarertaldeidngshoofwfesaar acocnocmerpnanfoiornth.Weohthetehre(rsetehebierlosawc)rirfiecmearienflseucnt-s sPteatresonaldistress:
ded from arjournals.anELDIN LIBRARY on twwotthoruhheatcsaetsrtncymrt(,ayHrtaiihrgnyooeggfronefembmroeeitasdcfniauantunlh1vlse9oaeou7lfivotn5ehon)it.mueiamaAnaaltytamirncetouhasnnncpeegdtriweecotorabnhsdro.eteiarmnSnnogisdmfsoibtnitafluhgardrtresielosstyde-sf, caSTlvyehoameird,npahenaoxcttweheeeovvofteilaruc,vtaeCisorsinoitvanmercyivegsithcreantpraioloscuocsbuaerrsoewxuphsalealn.ineemdoa-s sbwdeoiisltrfth-nrceaefsnrnsootmethreeedrm’sdpiastthreyss
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hol. 2ND - ahruemabneincghilrderjeencte(dPodteugrainlg20w0e0a)n,inthge.yLeikxe- sthymeirpasothcyialfcroomnsepqeuresnocneasladreisetraecshs,otwhheirc’shopin-
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PsyYL ploit emotional contagion to induce mater- posites. Sympathy is defined as “an affective
ev. AR nal distress, which in turn may lead the response that consists of feelings of sorrow
RM
u. F mother to change her behavior to their or concern for a distressed or needy other
AnnY O advantage. (ratherthansharingtheemotionoftheother).
T Emotional responses to displays of emo- Sympathy is believed to involve an other-
SI
R tion in others are so commonplace in ani- oriented, altruistic motivation” (Eisenberg
E
V
NI mals (de Waal 2003, Plutchik 1987, Preston 2000,p.677).Personaldistress,ontheother
U &deWaal2002b)thatDarwin(1982[1871, hand, makes the affected party selfishly seek
y
b p.77])alreadynotedthat“manyanimalscer- to alleviate its own distress, which mimics
tainlysympathizewitheachother’sdistressor that of the object. Personal distress is not
danger.” For example, rats and pigeons dis- concerned,therefore,withtheother(Batson
playdistressinresponsetoperceiveddistress 1991).Astrikingnonhumanprimateexample
inaconspecific,andtemporarilyinhibitcon- is how the continued screams of a punished
ditioned behavior if it causes pain responses infantrhesusmonkeywillcauseotherinfants
in others (Church 1959, Watanabe & Ono to embrace, mount, or even pile on top of
1986).Arecentexperimentdemonstratedthat thevictim.Thus,oneinfant’sdistressspreads
mice perceiving other mice in pain intensify quicklytoitspeers,whichthenseektoreduce
www.annualreviews.org • TheEvolutionofEmpathy 283
ANRV331-PS59-11 ARI 4November2007 20:27
their own negative arousal (de Waal 1996, his claims: “If I were to tell of his altruistic
p.46). and obviously sympathetic behavior towards
Concern for others is different in that it PanzeeIshouldbesuspectedofidealizingan
Consolation:
reliesonaseparationbetweeninternallyand ape.” Ladygina-Kohts (2001 [1935]) noticed
comfortingbehavior
directedata externally generated emotions. This separa- similartendenciesinheryounghome-reared
distressedparty,such tion is observable in many mammals. In a chimpanzee.Shediscoveredthattheonlyway
asarecentvictimof studythatsoughttodocumentchildren’sre- to get him off the roof of her house (better
y. aggression sponsestofamilymembersinstructedtofeign thanrewardorthreatofpunishment)wasby
nl
o sadness (sobbing), pain (crying), or distress actingdistressed,hencebyinducingconcern
e
s
u (choking), striking similarities emerged be- forherselfinhim.
al
n tweenthereactionsofone-year-oldchildren Perhapsthebest-documentedexampleof
o
s
gper andpets,suchasdogsandcats.Thelatter,too, sympathetic concern is consolation, defined
ews.or0. For sthheoiwrehdeacdoimnftohretilnagpoatfttehmep“tdsi,stsruecshseads”ppuetrtsionng astsarnedaesrsutroanocneeproofvtidheedcboymabnatuannitnsvoinlveadpbrye--
nualrevi04/29/1 (ZaYhenr-kWesax(l1e9r2e5t,apl..1294864)).reported how his vRioooussmaaglgenre1ss9i7ve9).inFcoirdeenxatm(dpele,Waathalird&pavratny
nals.anRY on bfoornhoibsosi,cPklryinccheimCphainmz,esehcoowmepdansuiochn,cPoannczeeren, ganoeasrmovaerrotuontdhehliossoerrhoefrashfioguhltdaenrds(gFeingtulyrepu1t)s.
ourRA thatthescientificestablishmentmightreject De Waal & van Roosmalen (1979) analyzed
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V Consolationis
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U commonin
y humansandapes,
b
butvirtuallyabsent
inmonkeys.Herea
juvenile
chimpanzeeputs
anarmarounda
screamingadult
male,whohasjust
beendefeatedina
fight.Photograph
bytheauthor.
284 deWaal
ANRV331-PS59-11 ARI 4November2007 20:27
hundredsofconsolationsinchimpanzees,and and best-known definitions by Smith (1759,
de Waal & Aureli (1996) included an even p. 10) “changing places in fancy with the
larger sample. These studies show that by- sufferer.”
Empathic
standers contact victims of aggression more Menzel(1974)wasthefirsttoinvestigate
perspective-taking:
often than they contact aggressors, and by- whetherchimpanzeesunderstandwhatothers thecapacitytotake
standerscontactvictimsofseriousaggression know,settingthestageforstudiesofnonhu- another’s
moreoftenthantheycontactthosewhohad man theory-of-mind and perspective-taking. perspective—e.g.,
y. receivedmildaggression. Afterseveralupsanddownsintheevidence, understanding
nl another’sspecific
o Subsequent studies have confirmed con- currentconsensusseemstobethatapes,but
e situationandneeds
s
al u solation in captive apes (Cordoni et al. probably not monkeys, show some level of separatefromone’s
n 2004; Fuentes et al. 2002; Koski & Sterck perspective-takingbothintheirspontaneous own—combined
o
gpers 2006; Mallavarapu et al. 2006; Palagi et al. social behavior (de Waal 1996, 1998 [1982]) withvicarious
ews.or0. For 2C0a0s4tl,e2s020060)4,,wWilditcthigim&paBnozeesecsh(K20u0ts3u),kalakrege&- aentdal.un2d0e0r5;exHpaerreimeetnatla.l2c0o0n1d,it2io0n0s6;(BHria¨ruaetar eTmarogtieotneadlhareolpuisnalg:
nals.annualreviRY on 04/29/1 bcwthhrheaielidsnnaremdedneebWoi(rFbadusaseljir&(svSaaewAteiaudorneeelttpir(aao1ll.9t.o29c206o00)l0s7te6)ot,).oaduneHtdtetoochwtuaecpmvopeanlrny-, 2pin0egr0A,s6pw;ehScmihtciihvallejioi-tsrtohakeeitlmnpagalfi.nin2isfe0es-0ostt5u-ac)nt.aieoldlnetdotaoanfrgoethetemedrp’shasetphlpeic-- hoaoopntrehplspaeritrecau’csonaigsadtpitnoiceionatcnirivfieeocbfantsheeeedd
ourRA solationinmonkeys,theyfailedtofindany,as cificsituationandgoals(deWaal1996).The
ded from arjELDIN LIB dg(iai.dep.o,bthheutewmrsea(enWnsamatntosdnetkaaeplye.ss2)0a0nex0dt)e.tnThdehseHecvooemnnsiontlooaitditohenea ldpioaterurtbiacttuualrbaeorluyotntinhperaeipmxeissattee(nsecbeeeohFfarvtoaimorgreEtleemadvpheaestlhplyiitnttgloe,
aK
nloMC one situation where one would most expect Altruism,below).Amotherapewhoreturns
300. DowPARK - ct(Soocnchsoionmloaftoieortntaltt.ho2e0ior0c4oc)uw.rnO: M’oCffaoscnparnqienulegl’sma(f1to9etr9h5ea)rsficogfanhi-tl ttworaearedwtothhitmeheopnnereeixntthg—eybyoyouunswnggsatsyetirenrtgoishheterrlapopwiptenfrdtorimeneoatnnode-
9-E
7G tentanalysisofhundredsofreportsconfirms then drape her body between both trees—
008.59:2COLLE tchalatofreaapsesusryaentcrearoefidnismtroensskeedyso.tIhtesrtsililsnteyepdi-s greosepsobnesyeolnikdemlyeirnevocolvnecseernmfootriotnhaeloctohnetra.gHioenr
hol. 2ND - tioorbaecteusatlalybldisoheesdr,ehdouwceevthere,dtihsatrtetshseisdbpeahrtayv’-s (sie.lev.,emswothheenrathpeeysohfeteanrbthreieirflyowffshpimrinpgerdtohesmo)-,
cA
PsyYL arousal. butaddsassessmentofthespecificreasonfor
ev. AR theother’sdistressandtheother’sgoals.Tree
RM
Annu. Y OF EmpathicPerspective-Taking bwriitdhginmgoitsheardsairlyegouclcaurlryrenacneticinipoatriannggutthaneisr,
T Psychologists usually speak of empathy only offspring’sneeds(vanSchaik2004,p.104).
SI
R when it involves perspective-taking. They For an individual to move beyond being
E
V
NI emphasize understanding of the other, and sensitive to others toward an explicit other-
U adoption of the other’s point of view. In orientation requires a shift in perspective.
y
b this view, then, empathy is a cognitive affair The emotional state induced in oneself by
dependent on imagination and mental state the other now needs to be attributed to the
attribution, which may explain the skepti- other instead of the self. A heightened self-
cismaboutnonhumanempathy(Hauser2000, identityallowsasubjecttorelatetotheobject’s
Povinelli1998).Perspective-takingbyitselfis, emotionalstatewithoutlosingsightoftheac-
ofcourse,hardlyempathy:Itissoonlyincom- tualsourceofthisstate(Hoffman1982,Lewis
bination with emotional engagement. The 2002). The required self-representation is
latter here is called “empathic perspective- hardtoestablishindependently,butonecom-
taking,” such as in one of the oldest monavenueistogaugereactionstoamirror.
www.annualreviews.org • TheEvolutionofEmpathy 285
ANRV331-PS59-11 ARI 4November2007 20:27
The coemergence hypothesis predicts that 2005,Emery&Clayton2001).Thesereports
mirrorself-recognition(MSR)andadvanced concern the finding or hiding of food, how-
expressions of empathy appear together in ever,hencenotempathicperspective-taking.
Mirror
bothdevelopmentandphylogeny. Inthefuture,wemaybeabletoaddressthe
self-recognition
(MSR): recognizing Ontogenetically, the coemergence hy- self-other distinction more directly through
thatone’sownbody pothesis is well-supported (Bischof-Ko¨hler neural investigation (Decety & Chaminade
isreflectedinthe 1988, Johnson 1992, Zahn-Waxler et al. 2003b).Inhumans,therightinferiorparietal
y. mirror 1992). The relation between MSR and the cortex, at the temporo-parietal junction,
nl
o development of empathic perspective-taking underpins empathy by helping distinguish
e
s
u holds even after the data have been sta- between self- and other-produced actions
al
n tistically controlled for age (Bischof-Ko¨hler (Decety&Gre`zes2006).
o
s
gper 1991).Gallup(1982)wasthefirsttopropose
ews.or0. For pphiryicloalgleynseutipcpcoorteemdebrgyenthcee,caonprtreadsitctbioentweemen- UNDERLYINGMECHANISMS
nualrevi04/29/1 mfoornMkeSyRs,ancodnaspoelas,tiwonit,hacnodmtpaerglleintegdevhiedlepnincge PerceptionActionMechanism
nals.anRY on onlAypinaratpferso.mthegreatapes,theanimalsfor Pcorreestoofnth&edemeWpaatahlic(2c0a0p2aac)itpyrloiepsoasemtehcahtaantitshme
ourRA which we have the most striking accounts that provides an observer (the subject) with
ded from arjELDIN LIB opAfhlticrnousnisasmonl,dabteieollenopwha)na.ndGttsaalr(lsgueepete(Fd1r9oh8me3lp)Eihnmagdpaaartlehreydaodtloy- aobcbocjdeeisclsyt)trtoehptrrhoeeusgesnhutbatjhteiecotnsiuvs.ebWjsetcahtt’esenoowtfhnaennsouetbuhjreearclt(atanhtde-
aK
nloMC predictedMSRindolphinsandelephants,and tendstotheobject’sstate,thesubject’sneural
300. DowPARK - tbthoyetlsoheceapmtreeadrakicmtteiaosrtnk,sinohnwavhietiscenhlofawtnhibantedeiintvicdcaounnanlfionrtmeeseeddes risciemaplrliyleasarennadntadutinsoocnocsinaoslcflyisoicmulsoillsyaeratcswttiaovtaeitnsedadir.veiTdahuueatolmsmaoarrete-,
9-E
7G withoutamirror(Plotniketal.2006,Reiss& theeasierthesubject’sidentificationwiththe
008.59:2COLLE Minatrhienore2st00o1f)t.hMeSanRimisablekliinegvdedomto(Abendaebrsseonnt oinbgjemcto,tworhaicnhdaeunthoannocmesicthreespsuobnjseecst.’sTmhiastlceht-s
hol. 2ND - &GItaslhluopul1d9b9e9)a.ddedthatself-representation tjehcet,subbojdeiclyt gshetar“inugndietsrethmeotsikoinns”aonfdthneeeodbs-,
cA
PsyYL is unlikely to have appeared de novo in a whichinturnmayfostersympathyandhelp-
ev. AR few large-brained animals. The framework ing. Preston & de Waal’s (2002a) PAM fits
RM
u. F ofdevelopmentalpsychologists,accordingto Damasio’s(1994)somaticmarkerhypothesis
AnnY O whichself-representationemergesinsmallin- of emotions as well as evidence for a link at
T crementalsteps(Lewis&Brooks-Gunn1979, thecellularlevelbetweenperceptionandac-
SI
R Rochat 2003), may apply also to phylogeny. tion,suchasthemirrorneuronsdiscoveredin
E
V
NI Insteadofadheringtoanall-or-nothingdivi- macaquesbydiPellegrinoetal.(1992).
U sionofself-representation,someanimalsmay Humandatasuggestthatasimilarphysio-
y
b reach an intermediate stage similar to that logicalsubstrateunderliesbothobservingand
of pre-MSR human infants (de Waal et al. experiencinganemotion(Adolphsetal.1997,
2005). 2000), and that affect communication cre-
Possibly, the link between MSR and ates matching physiological states in subject
perspective-taking is relatively loose. and object (Dimberg 1982, 1990; Levenson
Perspective-takinghasrecentlybeenreported & Reuf 1992). Recent investigations of the
for species that appear to lack MSR, both neural basis of human empathy confirm the
mammals (Kuroshima et al. 2003, Vira´nyi PAMinthattheyreportneuralsimilaritybe-
et al. 2005) and birds (Bugnyar & Heinrich tweenself-generatedandvicariousemotions
286 deWaal
ANRV331-PS59-11 ARI 4November2007 20:27
(Carretal.2003,Decety&Chaminade2003a, involvedinbothimitationandempathy,one
Decety&Jackson2006,deGelderetal.2004, expectscorrelationsbetweenbothcapacities.
Singer et al. 2004), such as activation of the Highlyempathicpersonsareindeedmorein-
anteriorventralinsulabothwhenwearedis- clinedtounconsciousmimicry(Chartrand&
gusted and when we see another person ex- Bargh 1999) and humans with autism spec-
pressingdisgust(Wickeretal.2003). trum disorder are not only deficient in em-
Theideathatperceptionandactionshare pathy but also imitation (Charman 2002,
y. representationsisanythingbutnew.Accord- Charman et al. 1997). Functional magnetic
nl
o ingly,empathyisarapidroutine,asconfirmed resonance imaging studies neurally connect
e
s
u byelectromyographicstudiesofmusclecon- motormimicry,suchascontagiousyawning,
al
n tractionsinthehumanfaceinresponsetopic- withempathicmodeling(Plateketal.2005).
o
s
gper tures of facial expressions, even if presented Other primates, too, yawn when they
ews.or0. For scoeibvreidefl(Dyitmhabtetrhgeeytcaaln.2n0o0t0b)e.Acocncoscuinotussolyfpemer-- sPeaeukconnersp&eciAfincsdeyraswonn(2A0n0d6e).rsIonnfeatcta,l.b2eh00av4-,
nualrevi04/29/1 pauatthomyaastiaccroeganctiitoivnes,pwrohciecshsaorfetefnarnteogolercatpsiductho ioofratlhceoppyriimngat(e“sa.piSnogc”i)alisfapcriolintaotuionncedexipnerail-l
nals.anRY on beundervoluntarycontrol. minegnatgsasihnowwhtehnattshaetyiatseedeportihmerasteesabte(gAidndeeasts-i
ourRA &Visalberghi2001,Dindo&deWaal2006),
ded from arjELDIN LIB REinmudispvsaiditahunyal’DcsoeovmellrosMtiaolonldatlehsletawteayasffeinctswahniochtheorn’se, sstacelrlvaiemtcshit(atNhtieaomknasyseiamlmveialsawr2ht0oe0n4th)o,atthanoerfdshssuchmroawatcnhnintehfoaennmat--s
aK
nloMC withsimplemechanismsatitscoreandmore (Bard2006,Ferrarietal.2006).Novelbehav-
300. DowPARK - calaobymielirpteiledesxnamasteuicrtsheaoonfuisttmehreslcaaanypdearcsp.ietirBesespceiancutvisovelev-oetfadk,tihwniges ipooltrehseisarrsceo(djpueiveWedn,aitlaeolso1i,m9a9ti8tlae[t1ains9tg8b2thy],etKhpeoe¨chaulpelierasr1.w9E2ax5lak)moa-sf
9-E
7G speak of the Russian doll model, in which wellassuccessfuldo-as-I-doexperimentswith
008.59:2COLLE haigfihrmer,cohgarndit-iwveirleedveblsaosifs,emsupcahthaysbtuhiledPupAoMn hYuammaaknomshoid&elsM(Catussutzaanwceae1t9a9l9.)1.995,Myowa-
hol. 2ND - (bdye iWtsealafl 2e0xp03la)i.nTshseymclpaiamtheisticnoctotnhcaetrPnAMor of tBhoedislaymseimgielanrditeyr—asnudchspaesciwesit—hlmikeelmybeenr-s
cA
PsyYL perspective-taking,butthatitunderpinsthese hances shared representation and identifica-
ev. AR cognitivelymoreadvancedformsofempathy, tion,whichhasbeenproposedasthebasisof
RM
u. F and serves to motivate behavioral outcomes. trueimitation(deWaal1998,2001),suchas
AnnY O Without emotional engagement induced by seen in the apes (Horner & Whiten 2005).
T state-matching, perspective-taking would be Thetendencyofnonhumanprimatestocopy
SI
R a cold phenomenon that could just as easily eachotherisasspontaneousastheempathic
E
V
NI lead to torture as to helping (Deacon 1997, response. Thus, mirror neurons fire auto-
U deWaal2005). maticallytoobservedactions,evenintentions
y
b Perception-action mechanisms are well (Fogassietal.2005),andmonkeysrequireno
known for motor perception (Prinz & extrinsicrewardstocopyeachother’sbehav-
Hommel2002,Wolpertetal.2001),sothat ior(Bonnie&deWaal2006).
we may assume PAM to underlie not only In accordance with the PAM (Preston &
emotional state matching but also motor de Waal 2002a), the motivational structure
mimicry. This means that the Russian Doll ofbothimitationandempathythereforein-
also relates to doing as others do, including cludes(a)sharedrepresentations;(b)identifi-
bodily synchronization, coordination, imita- cationwithothersbasedonphysicalsimilarity,
tion, and emulation (Figure 2). If PAM is shared experience, and social closeness; and
www.annualreviews.org • TheEvolutionofEmpathy 287
ANRV331-PS59-11 ARI 4November2007 20:27
Imitation Empathy
n True imitation, Perspective-
o
cti emulation taking, targeted
n helping
y. sti
nl Di
se o er
nal u Oth Sympathetic
nals.annualreviews.orgRY on 04/29/10. For perso Increased Self- MCshooaotroredrd imn gaiomtiaoiclnsr,y PAM Ecccooomnnnoctsateoigolraninot,ainoln
ourRA
om arjN LIB
ded frELDI FTihgeuRreus2siandollmodelofempathyandimitation.Empathy(right)inducesasimilaremotionalstatein
wnloaMCK tlahyeesrus,bsjueccthaansdsythmepoabthjeectti,cwcoitnhcaetrnitsancdorpeetrhsepepcetrivcee-pttaikoinn-ga,cbtiuoinldmuepcohnanthisimsh(aPrAdM-w)i.rTedhseodcoioll-’asfofeuctteirve
DoK - basis.Sharingthesamemechanism,thedoll’simitationside(left)correlateswiththeempathyside.Here,
00. AR thePAMunderliesmotormimicry,coordination,sharedgoals,andtrueimitation.Eventhoughthedoll’s
9-3E P outerlayersdependonprefrontalfunctioningandanincreasingself-otherdistinction,theseouterlayers
7G remainconnectedtoitsinnercore.
008.59:2COLLE (c)automaticityandspontaneity.Allofthisap- empathy.Agoodexampleseemstheintensi-
hol. 2ND - pthlieesmtoortehecocmorpelmexeochutaenrislmay,enrostonfetcheessRaurislsyiatno fiinepdapinai(nLraensgpfoonrdseetoaflm.2i0c0e6s)e.eEinmgootitohnearlmcoince-
cA
syL dollmodel,whichdevelopininteractionwith tagionmayleadindividualsfrightenedbythe
PY
ev. AR theenvironment. alarmofotherstohideorflee,amotherdis-
RM
u. F tressedbyheroffspring’sdistresstoreassure
AnnY O FROMEMPATHYTOALTRUISM bothherselfandheroffspringbywarmingor
T nursing them, or inhibit an individual from
SI
R Not all altruistic behavior requires empa- inflictingpainuponanotherbecauseofthevi-
E
V thy. When animals alert others to an out- cariousnegativearousalinducedbytheother’s
NI
U sidethreat,worktogetherforimmediateself- distresscalls.Thus,simpleempathicreactions
y
b reward,orvocallyattractotherstodiscovered may benefit both the actor and individuals
food,biologistsmayspeakofaltruismorco- closetothem.
operation,butthisbehaviorisunlikelytobe Behavioral copying, too, often produces
motivatedbyempathywiththebeneficiary. adaptive outcomes. Imagine a group of ani-
malsinwhicheverymemberwastoeat,sleep,
forage,orplayindependently:Thiswouldbe
EmotionalContagion
impossiblefornomadicanimals,suchaspri-
Self-centeredvicariousarousal,knownasper- mates.Beinginsyncisoftenamatteroflife
sonal distress, represents the oldest kind of ordeath(Boinski&Garber2000).
288 deWaal