Putting the Altruism Back into Altruism: The Evolution of Empathy

25 Pages·2009·0.37 MB·English

ANRV331-PS59-11 ARI 4November2007 20:27
Putting the Altruism
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nnualrevie only. FLivrinagnLsinBks,.YMerk.esdNeatiWonalaParilmateResearchCenter,andPsychologyDepartment,
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als.al u EmoryUniversity,Atlanta,Georgia30322;email:[email protected]
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79-3F MI FirstpublishedonlineasaReviewinAdvanceon perception-action,perspective-taking,prosocialbehavior,
59:2Y O June5,2007 cooperation
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200RSI hTthtpe:/A/npnsyucahl.RanevniuewalroefvPiesywchs.oolorggyisonlineat Abstract
ol. VE
chNI Thisarticle’sdoi: Evolutionary theory postulates that altruistic behavior evolved for
ev. Psyby U 1C0o.p11yr4i6g/hatn(cid:2)ncur2e0v0.p8sybcyhA.5n9n.1u0al3R00e6v.i0e9w3s6.25 tahmeorettivuartnio-bneanlerfioltes,ithboewaervsethr,etpheeryfonremedert.oFboererxeptuerrnie-nbceendefibtystthoepolary-
u. R Allrightsreserved ganism.Motivationalanalysesshouldrestrictthemselves,therefore,
n
n 0066-4308/08/0203-0279$20.00 to the altruistic impulse and its knowable consequences. Empathy
A
is an ideal candidate mechanism to underlie so-called directed al-
truism,i.e.,altruisminresponsetoanother’spain,need,ordistress.
Evidenceisaccumulatingthatthismechanismisphylogeneticallyan-
cient,probablyasoldasmammalsandbirds.Perceptionoftheemo-
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
has yielded profound insights into the evo-
EmpathicPerspective-Taking..... 285
lutionofaltruism(e.g.,Dugatkin2006).Un-
UNDERLYINGMECHANISMS... 286
fortunately,however,theseinsightshavenot
PerceptionActionMechanism.... 286
come with a new terminology: Evolutionary
RussianDollModel.............. 287
biologypersistsinusingmotivationalterms.
ws.org FROALMTREUMIPSAMTH..Y..T..O............... 288 Thus, an action is called “selfish” regard-
e less of whether or not the actor deliberately
vi EmotionalContagion............. 288
nnualree only. SEymmppaaththicetPicerCspoenccteirvne-.T.a.k..in..g........... 228899 sceaellkesdb“eanlterfiutisstfiocr”iitfseiltf.bSeinmeifilatsrlay,raenciapciteinotnaist
m arjournals.aor personal us ECMOPDNPRIACROTLEXHUCIYMTSIAEAOSTDNEEAV.ML.O.TE.LR.CV.U.HE.I.DAS.MN..I..S..M......O....F.. 229912 anTstoihcntoegstshtpaertnooatioctnthttoyerrpuiadiccneattrloe—ranldsrtareeucgdriasitrfitodcilisebnseagsnhhoeeofifrntwleithyfhebeetethoeoetprthhreooarr-t.
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59:2Y O Altruism bridgingthegapbetweenegoismandaltru- helpfulforcommunicationaboutmotivation
ol. 2008.VERSIT (dbbeeihfioanlvoiitgoiiorcntah)l:at iasnmo,thsienrcpeeitrshoans’tshmeipsrfooprteurntyeoinfttroaonnsfeo’srmowinng ptoerdose.wThahteTwriavyertsodcildeawrhuepnthheedceocnifduesdiotnhaist
chNI increasesthe feelingofdistress. evolutionary analyses require that effects be
ev. Psyby U rceocsitptioentht’sefitnessata Hoffman(1981a,p.133) cvoernsseildye,rmedotsievpaatiroantealfraonmalymseostirveaqtuioirne. uCsonto-
R performers
u. keep motivation separate from evolutionary
n Ultimatecauseor INTRODUCTION
n considerations.Itisnotfornothingthatbiol-
A goal: thebenefitsan
Discussionsofaltruisticbehaviortendtosuf- ogistshammeronthedistinctionbetweenul-
organismoritsclose
kinderivefroma ferfromalackofdistinctionbetweenfunction timateandproximate(Mayr1961,Tinbergen
behavior,hencethe andmotivation.Thisisduetothecontrasting 1963). The ultimate cause refers to why a
probablereasonwhy emphasisofbiologistsandpsychologists,with behavior evolved over thousands of gener-
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,
pain,ordistress
Cooperation and altruistic behavior are truismcarriesaninitialcost,andpositivecon-
thoughttohaveevolvedtohelpfamilymem- sequencesoccuronlyafterasignificanttime Intentional
altruism: the
bers and those inclined to return the favor interval (e.g., the recipient reciprocates) or
altruistdeliberately
(Hamilton1964,Trivers1971).Regardlessof notatall(e.g.,carefordependentkin),making
seekstobenefit
g whetherthisisthewholeexplanationornot forratherpoorlearningconditions. eithertheother
s.or (see Sober & DS Wilson 1998, EO Wilson Intentionally selfish altruism would re- (intentionally
ew 2005), the point is that ultimate accounts quire the actor to explicitly expect others to altruisticaltruism)or
vi itself(intentionally
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m arjournals.aor personal us mhisfiodauwencryeh,vmtaehsore,rtyiehtepcislslaeouysb.neTelcynlheewiafisrhtbsawetmhcdoaarmtyivmebessoectdqlieivuraaeirttcieiotfendwdeaellaarlcytoorelnude--,, tat(eehr.neagta.t,shasenDuimomanwealdklys.inTtcrsauhrle1ey9coa7albm6tor,muuFitosetnaihcrcrelsap&irmeectiutFehrisans,ct-shhbibneuancmceehafianetlrssl aceaanmltroreptuahbitesohmrryn:wfhritoehmlpand
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chNI nect them with the original act. This ap- existsinmany
yU 3. Intentionalaltruism.Helpbasedonthe
ev. Psby prediction of behavioral effects. One pkilniegsdtoomm.ostreciprocalaltruismintheanimal a“nemimpaaltsh,yb”utinththeeterm
R prediction could be that the help will presentreview
nu. bereciprocated,hencethattheactwill Once evolved, behavior often assumes appliesevenifonly
n motivationalautonomy,i.e.,itsmotivationbe-
A produce a net benefit. Since the actor criterion(a)ismet
comesdisconnectedfromitsultimategoals.A
seeks to benefit itself, we may call this Motivational
goodexampleissexualbehavior,whicharose
autonomy:
intentionally selfish altruism. The sec-
toservereproduction.Sinceanimalsare,asfar independenceof
ondpossibilityishelpbasedonanap-
asweknow,unawareofthelinkbetweensex motivationfrom
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
representationsof
withinaltruismbyexploringtheroleofem- emotionalconnectednesslikelystartedinthe
statesinthesubject
pathyinthedirectedaltruismofhumansand context of parental care long before our
similartothose
perceivedinthe other animals. Some definitions of empathy speciesevolved(Eibl-Eibesfeldt1974[1971],
object stressthesharingofemotions,whereasother MacLean1985).Signalingtheirstatethrough
g Emotional definitions stress the capacity to put oneself smilingandcrying,humaninfantsurgetheir
s.or contagion: intotheother’s“shoes.”Thelatterdefinitions caregiver to come into action (Acebo &
ew emotional are so top-down, however, that they discon- Thoman 1995, Bowlby 1958). Equivalent
vi state-matchingofa
nnualree only. soubbjejeccttwithan nWeectfeomllopwathay bfrootmtomits-upposaspibplreoaacnhteciendsteenatds., mreepcrhoadnuicstmiosnorpeelireasteoninfeaeldlianngi,mcalelsaniningw,hainchd
nals.anal us acdluodpitnigngmtehreebermoaodtieosntaplossesnibslietivdietfiyntoitiootnh,eirns-. wpaarremnitnsgaolefrtthteoyoanudnga.fAfevciatendorbymathmemiraloifafn-
m arjouror perso Wineafinrismtcaolsnsainddertthheevuanridoeurslyleinvgelspoefrecmepptaiothny- swphroinrge’smnaieneeddsinlidkieflfyereonutt.-reproduced those
nloaded fro10/06/09. F aPecxrtpeilsootnorenmt&heecdhreaenlWaitsiamoanl (b(2Pe0At0wM2eae))n. Apefrmtoepproattshheydis,awnbdye caonudOldpnlbcaeye aatphrpeollieeedminopuatththseiidcweictdaheperarcneietaytrwineogxriksctooendft,seoxi-tt
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ol. 2008.VERSIT tphreeddiicrte?cStioo,netvheantethvooulugthiomnaortyivtahteioonrywwilolublde (tBhaotesacdhul1t9m92a)l,ewmhaicchaqisuesos cinrijutirceadlfdourrhineagliantg-
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R
u. butitstillneedstoproduce—onaverageand &Ratnayeke1989).
n
n inthelongrun—evolutionarilyadvantageous
A
outcomes. The central thesis to be argued
LEVELSOFEMPATHY
here,then,isthatempathyevolvedinanimals
asthemainproximatemechanismfordirected EmotionalContagion
altruism,andthatitcausesaltruismtobedis-
Thelowestcommondenominatorofallem-
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
(e.g.,consolation)
tween humans and apes is reflected in the rapidly than negatively conditioned stimuli.
similarityofemotionalcommunication(Parr Perhaps the most compelling evidence for Cognitiveempathy:
empathycombined
&Waller2007)aswellassimilarchangesin emotional contagion came from Wechkin
withcontextual
brainandperipheralskintemperatureinre- etal.(1964)andMassermanetal.(1964),who
appraisalandan
g sponse to emotionally charged images (Parr foundthatmonkeysrefusetopullachainthat understandingof
s.or 2001,Parr&Hopkins2001). deliversfoodtothemifdoingsodeliversan whatcausedthe
ew A flock of birds taking off all at once be- electricshocktoandtriggerspainreactionsin object’semotional
vi state
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nloaded from arjournals.a10/06/09. For personal us twwottphorurhheaotcsaetcsrtnceymrt(,sayHrstaiiehrgnyosoeggfrionefsembmroaeeitasddcfnoiauantunplh1vlste9oaieoou7lfivnotn5ehon—)it.mueiamaiAnanaltytamirwncetouhhasnnncpoeegdtrliweeecotorabnhosdro.reteiarmnSinnnogisdmfspoibtnitaafluhgarrdrttresi—elosstyde-sf, caSTtilvoyehonameirad,nlpahencaoxocttwehneeteovvaoftgeilariuco,vtaenCisorsiinoistvanmerccyoivegmsithcrebantprianioloescuodcsbuwaerrisoetwhxuphsaaleapln.ipnereamdisoaa-sl bwdoiistrthnreafsnrsoomtheerm’spathy
wn of another’s emotional state, i.e., emotional oftheother’ssituationandattemptstounder-
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59:Y affectthesubject,suchastheextremelynoisy contextualappraisal.
ol. 2008.VERSIT taermepbeerintagntrreujmecsteodf ydouurinnggapweesanwinhge.n Lthikeye symTphatehpysyfcrhoomlopgiecraslolnitaelradtiustrreedssi,stiwnhgiucihshiens
chNI human children (Potegal 2000), they ex- theirsocialconsequencesareeachother’sop-
yU
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u. mother to change her behavior to their or concern for a distressed or needy other
n
n advantage. (ratherthansharingtheemotionoftheother).
A
Emotional responses to displays of emo- Sympathy is believed to involve an other-
tion in others are so commonplace in ani- oriented, altruistic motivation” (Eisenberg
mals (de Waal 2003, Plutchik 1987, Preston 2000,p.677).Personaldistress,ontheother
&deWaal2002b)thatDarwin(1982[1871, hand, makes the affected party selfishly seek
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
aggression
sponsestofamilymembersinstructedtofeign thanrewardorthreatofpunishment)wasby
sadness (sobbing), pain (crying), or distress actingdistressed,hencebyinducingconcern
(choking), striking similarities emerged be- forherselfinhim.
tweenthereactionsofone-year-oldchildren Perhapsthebest-documentedexampleof
andpets,suchasdogsandcats.Thelatter,too, sympathetic concern is consolation, defined
g
s.or showedcomfortingattempts,suchasputting asreassuranceprovidedbyanuninvolvedby-
w
e theirheadinthelapofthe“distressed”person stander to one of the combatants in a pre-
vi
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nals.anal us bfoornhoibsosi,cPklryinccheimCphainmz,esehcoowmepdansuiochn,cPoannczeeren, ganoeasrmovaerrotuontdhehliossoerrhoefrashfioguhltdaenrds(gFeingtulyrepu1t)s.
m arjouror perso thatthescientificestablishmentmightreject De Waal & van Roosmalen (1979) analyzed
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Figure1
Consolationis
commonin
humansandapes,
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.,
understanding
receivedmildaggression. Afterseveralupsanddownsintheevidence,
another’sspecific
Subsequent studies have confirmed con- currentconsensusseemstobethatapes,but
situationandneeds
solation in captive apes (Cordoni et al. probably not monkeys, show some level of separatefromone’s
2004; Fuentes et al. 2002; Koski & Sterck perspective-takingbothintheirspontaneous own—combined
2006; Mallavarapu et al. 2006; Palagi et al. social behavior (de Waal 1996, 1998 [1982]) withvicarious
g
s.or 2004,2006),wildchimpanzees(Kutsukake& and under experimental conditions (Bra¨uer emotionalarousal
ew Castles2004,Wittig&Boesch2003),large- et al. 2005; Hare et al. 2001, 2006; Hirata Targetedhelping:
vi helpandcarebased
nnualree only. bchrailidnreednbi(rFdusji(sSaeweadeett aall..22000076),).anHdohwuemvearn, 200A6;Smhialljiotroetmaal.n2if0e0st5a)t.ion of empathic oapnpareccoigatniiotniveofthe
nals.anal us wthheesnamdeeWobasaelr&vaAtiuornelpir(o19to9c6o)lsteotoduettetoctacpopnly- pinegr,spwehcitcihvei-sthakeilnpgfiinses-otu-cnaeldletdotaanrgoethteedr’shseplpe-- ootrhseitru’sastpioencificneed
m arjouror perso sdoidlaotitohnerisn(mWoanttkseeytsa,lt.h2e0y0f0a)i.leTdhteocfionndsoalnatyi,oans cliitfiecrastiutureatioonnapnrdimgaotaelsb(edheaWvioarall1ea9v9e6s).lTitthlee
nloaded fro10/06/09. F g(oian.epe.,bshietutuwmateaieonnnsmawnohdnerkaeepyeossn)aenewxdtoetunhldedsHmevooemsntinetooxpidteheceat dpAoaltrurtbuictiusamlbaor,lubyteltionhwea)ep.xeAisstme(nsoecteehoeFfrrtoaamprgeeEwtemhdopharetelhtpuyinrntgos,
wn consolation to occur: Macaque mothers fail toawhimperingyoungstertohelpitfromone
oo
79-300. DF MIAMI t(tSoencchtoianmnoafoleyrtstiaslt.ho2ef0ihr0u4on)w.dnOre’odCfsfosonpfrnrieenlpgl’osar(ft1ts9ecr9o5an)fificrogmnh-st twtrhaeerendtotdhrteahpeoenneehxetthr—ebbyoyodusywngbasyettienwrgeieshnetrrabopowpthendttrrieneeeastn—od-
2O
59:Y that reassurance of distressed others is typi- goesbeyondmereconcernfortheother.Her
ol. 2008.VERSIT ctoalboefaepsteasbyliestheradr,ehionwmevoenrk,etyhsa.tItthsitsillbneheeadv-s r(ie.sep.,omnosethliekrealpyeisnovfotlevnesbreimefloytiwohniamlcpoenrttahgeimon-
chNI ioractuallydoesreducethedistressedparty’s selveswhentheyheartheiroffspringdoso),
yU
ev. Psby arousal. bthuetoadthdesra’sssdeisstsrmesesnatnodftthheeosptheceirfi’scgroeaalsso.nTrfoeer
R
u. bridgingisadailyoccurrenceinorangutans,
n EmpathicPerspective-Taking
n with mothers regularly anticipating their
A
Psychologists usually speak of empathy only offspring’sneeds(vanSchaik2004,p.104).
when it involves perspective-taking. They For an individual to move beyond being
emphasize understanding of the other, and sensitive to others toward an explicit other-
adoption of the other’s point of view. In orientation requires a shift in perspective.
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
mirror
1992). The relation between MSR and the cortex, at the temporo-parietal junction,
development of empathic perspective-taking underpins empathy by helping distinguish
holds even after the data have been sta- between self- and other-produced actions
tistically controlled for age (Bischof-Ko¨hler (Decety&Gre`zes2006).
1991).Gallup(1982)wasthefirsttopropose
g
s.or phylogeneticcoemergence,apredictionem-
ew pirically supported by the contrast between UNDERLYINGMECHANISMS
vi
nnualree only. mfoornMkeSyRs,ancodnaspoelas,tiwonit,hacnodmtpaerglleintegdevhiedlepnincge PerceptionActionMechanism
nals.anal us onlAypinaratpferso.mthegreatapes,theanimalsfor Pcorreestoofnth&edemeWpaatahlic(2c0a0p2aac)itpyrloiepsoasemtehcahtaantitshme
m arjouror perso wofhcicohnswoleatihoanveantdhetamrgoestetdsthreiklpininggaacrceoudnotl-s tahccaetspsrtoovitdheessaunbjoecbtsievrevestrat(ethoefsaunbojethcte)rw(tihthe
nloaded fro10/06/09. F pAphrletirnduisicstamend,dMbeeSlleoRpwhin)a.ndGtosalpl(lshueipens(F1arn9od8m3e)leEhpmahdapnaattlshr,eyaandtody obtebonjdediclsytt)ortehtphrroeeusogebnhjetatchtti’esonsstusa.btWjee,cthth’esenoswtuhbnejenscuetbu’sjrenacletuaarntad-l
wn these predictions have now been confirmed representationsofsimilarstatesareautomat-
oo
79-300. DF MIAMI btwoyittlhohoceuamtteaaramkmitrerasortrk,i(noPnlwohittnisciekhlfeattnhaialn.td2ii0tv0icd6au,naRnleonitessesed&es istchimaellieylaaarsinaednrduthnseococsuinabslcljyeiocctul’ssolsiydeeatcnwttioivfiaictnaedtdiio.vniTdhwueaitlmshaotrhreee,
2O
59:Y Marino2001).MSRisbelievedtobeabsent object, which enhances the subject’s match-
ol. 2008.VERSIT i&nGthaellruepst1o9f9t9h).eanimalkingdom(Anderson itnhgemsuobtjoerctangdetau“tuonndoemritchreesspkoinn”seos.fTthheisolebt-s
chNI Itshouldbeaddedthatself-representation ject, bodily sharing its emotions and needs,
yU
ev. Psby ifsewunllairkgeely-brtoainheadveanaipmpaelasr.edThdeefnraomvoewinorka winhgi.chPriensttounrn&madyefoWstaearl’ssym(2p00at2hay)aPnAdMhefilpt-s
R
u. ofdevelopmentalpsychologists,accordingto Damasio’s(1994)somaticmarkerhypothesis
n
n whichself-representationemergesinsmallin- of emotions as well as evidence for a link at
A
crementalsteps(Lewis&Brooks-Gunn1979, thecellularlevelbetweenperceptionandac-
Rochat 2003), may apply also to phylogeny. tion,suchasthemirrorneuronsdiscoveredin
Insteadofadheringtoanall-or-nothingdivi- macaquesbydiPellegrinoetal.(1992).
sionofself-representation,someanimalsmay Humandatasuggestthatasimilarphysio-
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,
representationsisanythingbutnew.Accord- Charman et al. 1997). Functional magnetic
ingly,empathyisarapidroutine,asconfirmed resonance imaging studies neurally connect
byelectromyographicstudiesofmusclecon- motormimicry,suchascontagiousyawning,
tractionsinthehumanfaceinresponsetopic- withempathicmodeling(Plateketal.2005).
tures of facial expressions, even if presented Other primates, too, yawn when they
g
s.or sobrieflythattheycannotbeconsciouslyper- seeconspecificsyawn(Andersonetal.2004,
w
e ceived(Dimbergetal.2000).Accountsofem- Paukner & Anderson 2006). In fact, behav-
vi
nnualree only. pauatthomyaastiaccroeganctiitoivnes,pwrohciecshsaorfetefnarnteogolercatpsiductho ioofratlhceoppyriimngat(e“sa.piSnogc”i)alisfapcriolintaotuionncedexipnerail-l
nals.anal us beundervoluntarycontrol. minegnatgsasihnowwhtehnattshaetyiatseedeportihmerasteesabte(gAidndeeasts-i
m arjouror perso RussianDollModel &scrVaticsahlbtheergmhsie2lv0e0s1w,hDeinndooth&ersdescWratacahl2th0e0m6)-,
nloaded fro10/06/09. F Eiwnmidthipvaisdtimhuyapll’cseoemvmeerocsthiaaolnnliastlmhsestaawtteaiytassffceioncrtsewaahnniodchtmheoornr’see, st(Baellaviremdsi2t(0aNt0ia6ok,naFyseiamrmraialrair2et0to0al4t.h)2,a0ta0no6fd).hNsuhmoovwaenlnibneefohananvat--s
wn complex mechanisms and perspective-taking ioriscopied,too,atleastbytheapes.Exam-
oo
79-300. DF MIAMI alsapbyeielairkteiedosfnaatsthuiertseRooufuststeiharenlcadaypoealrlcs.imtiBeoesdcieanlu,vsoienlvoewfdh,tihwcihes powlteehlselararsses(djuuecvcWeensasilfaeulsl1idm9o9i-8taas[t-1inI9-g8d2toh]e,exKppeo¨echruilmeliraer1nw9ts2a5wlk)itoahsf
2O
59:Y highercognitivelevelsofempathybuildupon humanmodels(Custanceetal.1995,Myowa-
ol. 2008.VERSIT a(defirWma,ahla2r0d0-w3)i.reTdhebacsliasi,msuicshnoatstthhaet PPAAMM YamBaokdoislyhis&imMilaartitsyu—zawsuach19a9s9w).ith members
chNI by itself explains sympathetic concern or of the same gender and species—likely en-
yU
ev. Psby pcoegrsnpieticvteivlye-mtaokriengad,bvuantcthedatfiotrumnsdeorfpeimnsptahtehsye, htiaonnc,ewshsihcahrehdasrbepeerensepnrotaptoiosnedaansdthideebnatsifiiscoa-f
R
u. and serves to motivate behavioral outcomes. trueimitation(deWaal1998,2001),suchas
n
n Without emotional engagement induced by seen in the apes (Horner & Whiten 2005).
A
state-matching, perspective-taking would be Thetendencyofnonhumanprimatestocopy
a cold phenomenon that could just as easily eachotherisasspontaneousastheempathic
lead to torture as to helping (Deacon 1997, response. Thus, mirror neurons fire auto-
deWaal2005). maticallytoobservedactions,evenintentions
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
sti
Di
r
e
h
Ot Sympathetic
- Coordination,
g elf shared goals concern,
or S consolation
s. d
w e
annualreviese only. Increas Motor mimicry PAM Ecomnotatigoinoanl
als.al u
nn
m arjouror perso
oF
d fr09. Figure2
wnloaden 10/06/ TtlahyheeesrusR,busjsuesccithanaansddosytllhmmepooabdthjeeelctoti,cfwecmoitnhpcaaettrhniytsaancndodrpeimetrhistepaetpiceotrinvc.eeE-pttmaikopinan-tgah,cybti(uorinilgdhmut)epcionhndaunthciseimssha(aPsriAdmM-iwl)ai.rrTeedmhseoodtcioioolnl-’aaslfofseutcattetiervein
oo
00. DAMI bthaesiPs.ASMhaurinndgetrhlieessammoetomremchimanicisrmy,,ctohoerddionlal’stioimn,itsahtiaornedsigdoea(llse,fat)ncdotrrrueelaitmesitwatitiohnt.hEeveemnptahtohuygshidteh.eHdeorlel’s,
79-3F MI oreumtearinlacyoernsndeecpteedndtoointspirnenferornctoarlef.unctioningandanincreasingself-otherdistinction,theseouterlayers
2O
59:Y
ol. 2008.VERSIT (pcl)ieasuttoomthaeticcoitryeamnedcshpaonnistman,enitoyt.nAelcleosfstahriislyapto- efimedpaptahiny.rAesgpooondseeoxafmmpicleesseeeeminsgtohtehienrtemniscie-
chNI themorecomplexouterlayersoftheRussian inpain(Langfordetal.2006).Emotionalcon-
v. Psyby U dthoellemnvoidreoln,mwhenicth. developininteractionwith taalagrimonomfaoythleearsdtiondhiivdieduoarlsflfereig,hatmenoetdhebrydtihse-
e
R
u. tressedbyheroffspring’sdistresstoreassure
nn bothherselfandheroffspringbywarmingor
A FROMEMPATHYTOALTRUISM
nursing them, or inhibit an individual from
Not all altruistic behavior requires empa- inflictingpainuponanotherbecauseofthevi-
thy. When animals alert others to an out- cariousnegativearousalinducedbytheother’s
sidethreat,worktogetherforimmediateself- distresscalls.Thus,simpleempathicreactions
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