Group Competition, Reproductive Leveling, and the Evolution of Human Altruism

46 Pages·2006·0.92 MB·English

Group Competition, Reproductive Leveling, and the
Evolution of Human Altruism
Samuel Bowles, et al.
Science 314, 1569 (2006);
DOI: 10.1126/science.1134829
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RESEARCH ARTICLES
Group Competition, Reproductive variance.(E{}indicatesaweightedaverageover
demes.)Thecoefficientb istheeffectofvariation
G
inp ontheaveragefitnessofmembersofdemej
Leveling, and the Evolution of j
(w); b is the effect of variation in p (namely,
j i ij
switchingfromanNtoanA)onthefitnessofan
Human Altruism
individualindemej(w).Abehaviorisaltruisticif
ij
adopting it lowers one's expected fitness while
increasingtheaveragefitnessofone'sdeme(18).
Samuel Bowles Giventhisdefinition,weareinterestedinthecase
whereb isnegativeandb ispositive.
i G
Humans behavealtruistically innatural settingsandexperiments. Apossibleexplanation—that Using Eq. 1, we see that whether altruism
groups withmorealtruistssurvive whengroups compete—haslongbeenjudgeduntenableon evolves(Dp>0)dependsontheoutcomeofa
empiricalgroundsformostspecies.Buttherehavebeennoempiricaltestsofthisexplanationfor raceinwhichthebetween-selectionprocesspro-
humans.My empiricalestimatesshowthatgeneticdifferences between earlyhumangroupsare motingitsspread[var(p)b ]competeswiththe
j G
likelytohavebeen greatenoughsothatlethalintergroup competition couldaccountforthe within-selection processtending toeliminateit
evolutionofaltruism.Crucialtothisprocessweredistinctivehumanpracticessuchassharingfood (E{var(p )}b).Forthebetween-demeeffect to
ij i
beyond theimmediate family,monogamy,andotherformsof reproductiveleveling.These exceedthewithin-demeeffect(rearrangingEq.1),
culturallytransmitted practicespresupposeadvanced cognitiveand linguisticcapacities,possibly itmustbethat 6
accountingforthe distinctiveformsofaltruism foundinourspecies. 0
0
varðpÞ 2
Darwinthoughtthatthe“moralfaculties” Models(14),computersimulations(15),and Efvarðpj Þg>−bi=bG (2) 8,
had proliferated among early humans empiricalstudies(16)haveconfirmedthatinter- ij r
e
because a tribe of “courageous, sym- groupcompetitioncouldinfluencetheevolution b
m
pathetic and faithful members who were al- of culturally transmitted behavior. This study Theleft-handsideofthisconditionisameasure e
ways ready to…aid and defend each other… investigates whether, as an empirical matter, ofpositiveassortmentarisingfromthefactthat ec
D
would spread and be victorious over other intergroup competition and reproductive level- ifthefractionofA'sindemesdiffer[thatis,var(p)
tribes” (1, p. 134). Recent experiments have ing might have allowed the proliferation of a ispositive],thenA'saremorelikelythanN'stoj on
extensivelydocumentedaltruisticbehaviorsnot geneticallytransmittedpredispositiontobehave interactwithA's. g
r
only in laboratories but also among hunter- altruistically. To determine the facts necessary Becausethewithin-demebenefitsofaltruism o
gathererpopulations(2–4).Butinorderforthe for this inquiry, a model was developed that are randomly distributed, between-deme differ- ag.
m
survivalofmorealtruisticgroupsincompetition captures the main aspects of ancestral human encesintheprevalenceofA's[i.e.,var(p)>0]is
j e
withothergroupstoaccountfortheevolution geneticdifferentiation,between-groupcompeti- theonlyreasonwhyA'saremorelikelythanN'sto c
n
ofapredispositiontoactaltruistically,thegroup tion,andgroupsocialstructure. interactwithA'sandthustobenefitmutually.But e
extinction process would have to be strong Framework for the empirical analysis. ifA'sarelikelytobenefitforthisreason,theyare sci
enough to offset the lower fitness of altruists Consideralargemetapopulationofindividuals also more likely to compete over deme-specific w.
w
comparedtoothermembersoftheirgroup.For livinginpartiallyisolatedsubpopulations(called resources(19,20).Iassumethemoststringentform
w
thistobethecase,therewouldhavetobesub- demes).Altruists(A's)takeanactioncostingc of local density-dependent constraints on re- m
stantialdifferencesin thefractionofaltruists that confers a benefit b on an individual ran- productive output: Sites are saturated so that ter- o
r
in groups,which isthought tobeunlikely be- domlyselectedfromthenmembersofthedeme. ritorial expansion is required for deme growth. d f
cause migration among groups tends to limit (PayoffsaregiveninTable1,andthemodeland Thus, altruism can proliferate only by helping a e
d
between-group differences in group composi- notation are summarized in Table 2.) A's are demetoacquiremoreterritory,notbyanyofthe a
tion.Thus,manyhaveconcludedthatbetween- bearersofahypothetical“altruisticallele”;those otherwaysthatmembersofpredominantlyaltru- nlo
group genetic differences are too small for withouttheallele(N's)donotbehavealtruisti- isticdemesmightproducemoresurvivingoffspring. w
o
selective group extinction to offset the within- cally.Reproductionisasexual.Intheabsenceof Selective group extinction. Selective ex- D
group selective pressures that oppose the evo- reproductiveleveling,individualfitnessisiden- tinction may allow the evolution of altruism if
lution of a genetic predisposition to behave ticaltothepayoffsinTable1.Forexample,anA predominantly altruistic demes are more likely
altruistically[(5),butseealso(6)]. who interacts solely with A's will expect a than other demes to survive between-deme
However, early humans lived under con- number of offspring surviving to reproductive contestsandtocolonizeandrepopulatethesites
ditionssuchthatselectivegroupextinctionmight agethatisb−cgreaterthanthefitnessofanN vacatedbydemesthatfail(21).Thisprocessis
have been a powerful evolutionary force. Cul- whointeractsonlywithN's. captured by the term b , the size of which is
G
turally transmitted norms supporting resource Letp =1ifindividualiindemejisanA determined by the frequency of contests, the
ij
and information sharing, consensus decision- withp =0otherwise.Letp bethefractionof fitness effects of surviving a contest, and the
ij j
making, collective restraints on would-be ag- demej’smembershipthatareA’s;pandp'bethe contributionofaltruiststosurviving.
grandizers, monogamy, and other reproductive A-fractionofthemetapopulationinagivenand In every generation with probability k, each
leveling practices that reduced within-group subsequentgeneration,respectively;andDp≡ demeengagesina“contest.”(Acontestmaybea
differences in fitness may have attenuated the p'−p.Then,followingPrice(17)andassuming
selectivepressurestowhichaltruistsaresubject themetapopulationsizedoesnotchange,wecan
(7–11).Theimpactofintergroupcompetitionis express the possible evolution of altruism as Table 1. Payoffs to within-deme interactions.
heightened by the fact that although group ag- summarized by Dp as a between-deme effect Entries are the payoffs of the row individual
wheninteractingwithanindividualwhosetype
gression is not uniquely human (12), among plusawithin-demeeffect:
isgivenbythe column head.
humansitisextraordinarilylethal(13).
Dp=var(p)b +E{var(p )}b (1)
j G ij i Altruist Not
Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM Altruist(A) 1+b−c 1−c
Thetermsvar(p)andE{var(p)},are,respective-
87501, USA, and Universitá di Siena, 17 Piazza San j ij Not(N) 1+b 1
Francesco,Siena,Italy.E-mail:[email protected] ly, the between-deme and within-deme genetic
www.sciencemag.org SCIENCE VOL314 8DECEMBER 2006 1569
RESEARCH ARTICLES
hostile encounter or an environmental chal- To see how this works, suppose an N were Ifnislarge,thisisapproximatedby
lengewithoutdirectdemeinteraction.)Demes instead an A. In the absence of reproductive
that fail are eliminated, and surviving demes leveling,itsfitnesswouldbelessbyanamountc. F ð1(cid:1)tÞc
ST > (6)
repopulatethevacatedsites.Earlyhumandemes Buttheindividualwouldalsohavea1/nchanceof ð1(cid:1)F Þ k2l
ST A
probably faced frequent intergroup, environ- garneringthebenefitb,whichisdistributedran-
mental, and other challenges resulting in oc- domlytomembersofthegroup.Additionally,by Like Hamilton's rule for the evolution of al-
casional fatalities or territorial losses or gains increasingthechanceofsurvivalofthedeme(in truism by inclusive fitness, this model thus
[more closely resembling boundary skirmishes which case, like every member of the surviving yields a condition indicating the minimum de-
amongchimpanzees(22)thanthisall-or-nothing deme, it will be doubled), it also contributes gree of positive assortment necessary to allow
deme-extinction scenario]. I show (13) that es- directly to its own fitness an amount equal to altruismtoproliferate.Theleft-handterm, like
timatesoflong-termfitnesseffectsofcontinuous 1/n(i.e.,theeffectoftheswitchfromNtoAon Hamilton’s degreeof relatedness(r), is a mea-
low-level losses or gains are equivalent to a p)timesb (theeffectofvariationsinp onthe sureofpositiveassortment;buthereassortment
j G j
complete extinction-repopulation scenario oc- averagefitnessofthedeme).Thus arisessolelyfrombetween-demedifferencesin
curringinfrequently. theprevalenceofA's.Theright-handterminEq.
Demesarethesamesize(normalizedto1), bi≡dwij∕dpij=−c+b∕n+k2lA∕n (3) 6istheratioofindividualcoststogroup-level
exceptthatdemesthathaveoccupiedthesiteof benefits. We now ask if ancestral humans are
an eliminated deme are momentarily of size 2 Reproductive leveling can now be intro- likely to havelivedunder conditions such that
(and eliminated demes are of size zero). The duced by representing it as a convention, Eqs. 5 or 6 would be satisfied. Table 3 is a 6
surviving deme divides, forming two daughter conformity to which is in the interest of each summary of the main parameters and the 0
0
demesofequalsize.Lettheprobabilitythatthe deme member (25). Let some portion of the estimatedrangeofempiricallyplausiblevalues. 2
deme survives be l. The size of deme j in the payoffs initially acquired by an individual be Empirical estimates of FST. Wright [(27), 8,
next generation is thus 1, 2, or 0 with distributed equally among all deme members. p.203]speculatedthatanequilibriumF among r
ST e
probabilities (1 − k), kl, and k(1 − l), re- Reproductivelevelingthentakestheformofa human groups—namely, that which would b
m
spectively,sotheexpectedsizeiswj=1−k+ proportional deduction at rate t of each mem- balance the offsetting effects of migration and e
2kl.TheeffectoftheprevalenceofA'sonthe ber’s payoffs, the proceeds of which are drift—mightbeabout0.02,avaluethatwould ec
D
expectedsizeofthedemeinthenextgeneration distributedequallytoallmembersofthedeme. precludeinterdemiccompetitionasanimportant
(that is, bG ≡ dwj∕dpj) is the likelihood of a Theeffectistoreducewithin-demefitnessdif- evolutionaryforce.Butmostempiricalestimates on
contest (k), times the effect on deme size of ferencesbetweenA'sandN'sfrom−cto−(1−t)c, areconsiderablylarger.Themeasuresofgenetic g
r
surviving or not (2), times the effect of the sob =−(1−t)c+b∕n+k2l ∕n. differentiation in Table 4 are from recent for- o
i A g.
prevalenceofA'sontheprobabilityofademe Positive assortment and the evolution of aging populations whose population structure, a
survivingshouldacontestoccur(thatis,dl/dp ≡ altruism. Substituting these values for b and geographical and linguistic proximity, and m
j i e
l );sob =k2l .Thereisnowaytoestimate b inEq.1,wehave livelihoodmayresemblethoseofforagingbands c
A G A G n
l empirically, so I explore two alternative ofthelatePleistoceneandearlyHolocene(about e
vAalues(13):lA=1isderivedfromamodelin Dp=var(pj)k2lA 150,000 to 10,000 years before the present). sci
which all-A and all-N demes (respectively) These estimates are based on genetic material, w.
surviveandfailwithcertaintyshouldacontest −E{var(pij)}{(1−t)c− (b+k2lA)∕n} most of which was collected before the mid- w
w
occur; whereas if lA = ½, an all-A deme (4) 1970s, and in most cases are averages over a m
surviveswithprobability¾andanall-Ndeme large number of genetic systems and over F- o
r
surviveswithprobability¼. We will assess this condition with genetic data statistics among a large number of subpopula- d f
Reproductive leveling. Distinctive human fromrecenthunter-gathererpopulations,usinga tions.Anestedthree-levelhierarchyofmeasures e
d
practiceswithingroupsalsocreatedafavorable commonly measured statistic from population ofgeneticdifferentiationisestimated,depending a
o
nichefortheevolutionofaltruism.Individual genetics,thefractionofthetotalgeneticvariance onthesizeofthesubpopulationunits(13):FDG nl
differencesinsize,health,behavior,andother atalocusthatisbetweengroups,alsoknown measures genetic differentiation among demes w
influences on access to scarce resources are asWright'sinbreedingcoefficient(26):FST≡ (D) in the same ethno-linguistic group (G), Do
typically reflected in differences in reproduc- var(p)∕[var(p)+E{var(p)}].Usingthisdefini- whereas F and F , respectively, measure
j j ij GT DT
tive success. Among some primates (23, 24), tion,werewriteEqs.2and4andfindthattheA's differentiation among groups and demes in a
and especially among humans, reproductive shareofthemetapopulationwillincreaseif metapopulation (T). If most competition is
levelingattenuatesthisrelation.Becausealtru- betweendemesacrossethno-linguisticbounda-
ists receive lower payoffs than other deme FST >(cid:1)bi ¼ð1(cid:1)tÞc(cid:1)b=n(cid:1)1 ries,thenFDTistherelevantstatistic.
members (by the definition of altruism), they ð1(cid:1)F Þ b k2l n I think it is unlikely that Table 4 over-
ST G A
benefitfromreproductiveleveling,resultingin estimates the relevant degree of genetic differ-
areductionofthetermb. (5) entiation among early humans. First, extreme
i
Table 2. Summary of model and notation. b and c: benefits and costs to deme members; p: percent of deme k that are A’s; and p: percent of
k
metapopulation that are A’s.
Notation Eq.no. Equation Comment
GenericPriceequation(PE) 1 Dp=var(p)b +E{var(p )}b Dp=betweendeme+withindeme
j G ij i
GenericPEconditionforAtoincrease 2 var(p)∕E{var(p )}≡F ∕(1−F )>−b∕b F ≡between-demevar∕totalvar
j ij ST ST i G ST
EffectofAondeme-averagefitness(b ) b ≡dw∕dp =k(dw∕dl)(dl∕dp)=k2l k=probabilityofinterdemiccontest
G G j j j j A
EffectofAonindividualfitness(b) b ≡dw ∕dp =−(1−t)c+b∕n+k2l ∕n t=extentofreproductiveleveling
i i ij ij A
ConditionforA’stoincrease(Priceequation) 4 Dp=var(p)k2l −E{var(p )}{(1−t)c−(b+k2l )∕n} Dp=between–deme+within-demeeffect
j A ij A
ConditionforA’stoincrease 5 F ∕(1−F )>−b∕b ={(1−t)c−b/n}∕k2l −1/n LargerF favorsA’s.
ST ST i G A ST
ConditionforA’stoincrease(ifn=V) 6 F ∕(1−F )>(1−t)c∕k2l >individualcost∕demebenefit
ST ST A
1570 8DECEMBER 2006 VOL 314 SCIENCE www.sciencemag.org
RESEARCH ARTICLES
climate variability during the late Pleistocene an N can mimic the A's so as to evade their sus)sizeinthemostcomprehensivesurvey(13)
(fig. S3) probably induced frequent deme ex- choosiness is to adopt the altruistic behavior is19.Individualbandsmayhavecompetedfor
tinctions, population crashes, and subsequent itself and thus to bear its costs. Thus, the in- survival,but itislikelythat bands in coalition
growth,resultinginthecolonizationofnewsites stability arising in the case of assortation by alsoengagedincontests.Aplausiblebenchmark
bysmallpropagules.Naturalexperiments[e.g., “greenbeards”(34)doesnotarise. isthatademeisfivebands,givingn=32;Iwill
withtheplantSilenedioica(28)]suggestthatthe But there is nonetheless an impediment to alsoconsiderverylarge(strictly,infinite)demes.
effect may be a considerable elevation of selective assortment that is sometimes over- Plausiblevalues of c and b will depend on
between-groupgeneticvariance.Second,genet- looked:ExclusionofN'sislikelytobecostlyfor theparticularaltruisticbehaviorinquestion.For
ic differentiation among a subspecies of chim- the A's, whereas the associated benefits are example,awarningcallwouldhaveadifferentb
panzees(Pantroglodytesschweinfurthii)whose sharedbyalldememembers.However,itisnot and c than defending the community against
spatial distribution and demographic history implausiblethataltruistswouldundertakesome hostileneighbors.Tofacilitatetheexplorationof
may resemble those of early humans (29) is moderatelevelofN-exclusionasacontribution avarietyofaltruisticbehaviors,Ipresentresults
substantially higher than the median of the es- tothepublicgood.Thereisampleethnographic foragivenb=0.05andcvaryingfrom0to0.08.
timatesinTable4(F =0.102). evidence(11)thatforagerspracticeselectiveas- (Eqs. 5 and 6 make it clear that for sizable
ST
However,geneticdifferentiationatthelocus sortmentwhentheyostracizeorshunindividu- demes,bisoflittleimportance.)
ofanallelethatisexpressedinanaltruisticbe- als who violate behavioral norms. Models and Deme extinction. The extent of hostile
haviormaydifferfromthatestimatedforneutral simulations(35)confirmthatthesepracticescan group interactions during the late Pleistocene
loci(thosenotunderselection)suchasthosein proliferatewhenrareandpersistindefinitelyina and early Holocene may be suggested by cli- 6
Table4. First, an altruistic allele would be(by plausibleevolutionarydynamic.Moreover,itis matic data, hunter-gatherer demographics, ar- 0
0
definition) under directional selection. This readily shown (13) that a modest amount of chaeological evidence, and recent histories of 2
wouldbeexpectedtoreduceinterdemicgenetic selectiveassortmentgeneratessubstantiallevels foragingpeoples,andisamatterofsomedebate 8,
differentiationatleastintheverylongrun,be- ofbetween-demedifferences. [theevidenceisreviewedin(13)]. r
e
cause in the absence of offsetting effects, the Within-demeselection.Althoughtheeffects We know from ice and deep-sea cores that b
m
frequencyoftheA’sinthepopulationwilleven- ofmostformsofreproductivelevelingcannotbe average temperature during the late Pleistocene e
c
tually go tozero. However, thistendencymay estimated, the degree of within-deme resource variedbyasmuchas8°Coverperiodsoflessthan e
not work over time scales relevant to human sharing is known from empirical studies of the twocenturies—thedifferenceinaveragecontem- D
n
demes.Simulations(13)showthatevenforvery acquisition and consumption of nutrition among poraryannualtemperaturesbetweenCapeTown o
strong selection against the A’s and for plau- foragers(13).Onthisbasis,Itaket=⅔asaplau- and Mombasa, 4000 km to the north (fig. S3). g
r
sible initial distributions of A’s in demes, the siblebenchmarkwith⅓analternativevalue(13). Mortalchallengesresultingfromclimaticadversi- o
g.
FSTrisesfortensofgenerations.Formoderate Theappropriatevalueofnisthenumberof tymusthavebeenfrequent,aswellasfromhostile a
selectionagainsttheA’s,theF mayrisefor dememembersofabreedinggeneration(abouta interactions among groups migrating over un- m
ST e
morethanahundredgenerationsbeforefalling. thirdofthecensussize).Themedianband(cen- familiarterrainwithoutestablishedarrangements c
n
Becausefissionandextinctioneventsthaten- e
hofanmceaginntieturddeemmicovrearfiarenqcueeanrtetlhikaenlythtois,beitaanpopredaersr Table4.Geneticdifferentiationamong13hunter-gatherersubpopulations(13).Themedianand w.sci
thathighlevelsofF couldpersistindefinitely. mean values (respectively) are 0.076and 0.081. The median and meanfor the FDT estimates are w
ST 0.081and 0.093. w
Even with random fission (and relatively small m
demes), additional simulations (25) show that Population Index F o
r
exceptionally strong directional selection against IndigenouscircumpolarEurasianpopulations F 0.076 d f
theA's(c=0.1)iscompatiblewiththeindefinite DT e
NativeSiberianpopulations F 0.170 d
maintenanceofhighlevelsofFST. NativeSiberianpopulations FDT 0.114 oa
Second,altruistswillsometimesbeableex- !Kungdemes(SouthernAfrica) FDG 0.007 nl
cludenonaltruistsfromtheirdemes,resultingin DG w
whatEshelandCavalli-Sforzacalled“selective SouthernAfricangroups FGT 0.075 Do
assortment” (30, 31). This is particularly com- SouthernAfricandemes(from18groups) FDT 0.081
AboriginalAustralians F 0.042
mon when demes fission, a process Hamilton GT
(32)called“associativetribesplitting.”Directed Kaiadilt-Lardiilgroups(Australia) FDT 0.081
Asmat-Mappi(LowlandWesternNewGuinea): F 0.056
migration(33)willalsoenhancebetween-deme DT
Mbuti(CentralAfrica)–San(SouthernAfrica) F 0.149
variance and reduce within-deme variance. GT
Aka(CentralAfricabetween“villages”inthesamegroup) F 0.042
Here,selectiveassortmentiscontingentonpast DG
Aka (betweengroups) F 0.057
behaviorthatisitselfanobservableexpression GT
Aka(between“villages”inallgroups) F 0.097
ofthealtruisticallele.Asaresult,theonlyway DT
Table 3.Parameter estimates.Benchmark values are inbold.Entries not inbold are alternative values(d= 0.4 notused).
Determinant Rangeexplored Comment/methodofestimation(13)
Interdemicgeneticdifferentiation F 0.007–0.170;0.076 Geneticmarkers(recentforagers)
ST
Reproductiveleveling t 0.66,0.33 Foodsharing(recentforagers)
Gains−lossesfromcontestspergeneration d 0.30,(0.40) Archaeologicalandethnographicevidence
Per-generationprobabilityofadecisive(2,0)contest k =d∕2 Basedonestimatesofmortalityinongoingconflict
Effectofpercentaltruistsondemesurvival lA 1/2,1 Arbitrary(seeFig.1)
Effectivedemesize(one-thirdofcensussize) n 32,V Coalitionof5median-sizedbands
Costtoaltruist c 0.0to0.08 Dependsonbehaviorunderconsideration
Benefitstodememembers(withoutacontest) b 0.05 Asimmediatelyabove
www.sciencemag.org SCIENCE VOL314 8DECEMBER 2006 1571
RESEARCH ARTICLES
estimateincludesextinctionsinduceddirectlyby 5. G.C.Williams,AdaptationandNaturalSelection:
climatechangeorothereventsunrelatedtowar. ACritiqueofSomeCurrentEvolutionaryThought
(PrincetonUniv.Press,Princeton,NJ,1966).
I use the smaller estimate of the frequency of
6. D.S.Wilson,Ed.,Am.Nat.150(suppl.)(1997).
conflicts(k=1=7). 7. C.Boehm,J.Soc.Biol.Struct.5,413(1982).
Discussion.Theaboveestimatesaresubject 8. I.Eibl-Eibesfeldt,J.Comp.Ethol.60,177(1982).
tosubstantialerrorgiventhattheyareinferences 9. R.D.Alexander,TheBiologyofMoralSystems(Adinede
Gruyter,NewYork,1987).
aboutconditionsoccurringtensofthousandsof
10. H.Kaplan,M.Gurven,inMoralSentimentsandMaterial
yearsagoforwhichverylittledirectevidenceis
Interests:TheFoundationsofCooperationinEconomic
available. With this caveat in mind, suppose Life,H.Gintis,S.Bowles,R.Boyd,E.Fehr,Eds.(MIT
earlyhumans'demographicsandsocialpractices Press,Cambridge,MA,2005).
resultedingeneticdifferentiationatthelocusof 11. C.Boehm,HierarchyintheForest(HarvardUniv.Press,
Cambridge,MA,2000).
analtruisticallelethatwasthemagnitudeofthe
12. J.H.Manson,R.W.Wrangham,Curr.Anthropol.32,369
median in Table 4 (F = 0.076). For the (1991).
benchmarkvaluesoft,n,andl thesolidlines 13. SupportingmaterialsareavailableonScienceOnline.
A,
inFig.1givethecombinationsofcandksuch 14. R.Boyd,P.J.Richerson,J.Theor.Biol.145,331
(1990).
that Eq. 5 is satisfied as an equality. More fre-
15. R.Boyd,H.Gintis,S.Bowles,P.Richerson,Proc.Natl.
quent contests or less costly forms of altruism Acad.Sci.U.S.A.20,123(2003).
(pointsabovetheline)allowaltruismtoprolifer- 16. J.Soltis,R.Boyd,P.J.Richerson,Curr.Anthropol.36, 6
ate. Dashed lines do the same for more strin- 473(1995). 0
17. G.R.Price,Ann.Hum.Genet.35,485(1972). 0
gentalternativeparametervalues.Forexample, 2
for the estimated k, if c = 0.05, altruism pro- 18. B1.9K,e1r3r,5P(.2G0o0d4f)r.ey-Smith,M.Feldman,TrendsEcol.Evol. 8,
liferates (for both values of lA) under the 19. D.S.Wilson,G.B.Pollock,L.A.Dugatkin,Evol.Ecol.6, er
Fig. 1. Conditions for the evolution of altruism benchmarkassumptions,butnotforverylarge 331(1992). b
m
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ation.Basedonaveragesofthreelargesamples altruismareoflesserimportance.Theevidence T.Taylor,E.Szathmary,M.Tommaseo-Ponzetta,
from the ethnographic record (table S4), war doessuggestthatifsuchadispositionexists,it M.vanVeelen,J.Wilkins,D.SloanWilson,andE.Woodfor
was“rare”inonlyafifthofthehunter-gatherer may be the result of a gene-culture coevolu- theircontributionstothisresearch.
societiesand“continuous”inathird. tionaryprocessinwhich,asDarwinwrote,group
Ishow(13)thatthelevelofongoinghostility conflictplayedakeyrole. SupportingOnlineMaterial
www.sciencemag.org/cgi/content/full/314/5805/1569/DC1
indicated by these data would produce fitness
SOMText
effectsequivalenttotheextinction-repopulation ReferencesandNotes Figs.S1toS5
scenariomodeledaboveoccurringeveryfiveto 1. C.Darwin,TheDescentofMan(PrometheusBooks, TablesS1toS4
sevengenerations,thelatterfigureignoringwar Amherst,NY,1998). ReferencesandNotes
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1572 8DECEMBER 2006 VOL 314 SCIENCE www.sciencemag.org
Supporting online materials for
Group competition, reproductive leveling and the evolution of human altruism
Samuel Bowles, Santa Fe Institute and Universitá di Siena
Contents:
1. Background
2. Associative tribe-splitting
3. Inter-demic genetic differentiation
4. Deme extinction and survival
5. Selection within demes
6. Dynamics of an F at a locus under directional selection
st
7. Relaxing the carrying capacity constraint
8. Conditions for the evolution of altruism for forager-based estimates of F
st
9. Figures
S1. Hierarchical measures of genetic differentiation
S2. Survival probability for deme j if half of the paired deme are A's
S3. Pleistocene temperature variations
S4. Dynamics of an F at a locus under directional selection.
st
S5. Conditions for the evolution of altruism
10. Tables
S1. Associative tribe-splitting
S2. Sources of estimates in Table 4
S3. Fraction of deaths due to violence: archeological evidence
S4. Warfare in hunter-gatherer societies
11. Works cited
1. Background
The main features of this model – reproductive leveling and deme extinction – have
received considerable attention among biologists interested in social behavior. Haldane (1):210-
214 suggested that in a population of small endogamous “tribes,” an altruistic trait might evolve
because the “tribe splitting” that occurs when successful demes reach a certain size would by
chance create a few successor demes with a very high frequency of altruists. This would
enhance the force of selective extinction by increasing between-deme genetic differences.
Wright (2):114 similarly held that ‘isolation by distance’ would support “statistical differences
among local populations...[that] provide a possible basis for intergroup selection of genetic
systems, a process that provides a more effective mechanism for adaptive advance of the species
as a whole than does the mass selection that is all that can occur under panmixia.” Like Wright
and Haldane, Hamilton (8) remained skeptical that inter-demic competition would be a powerful
evolutionary force; but he noted that if the assignment of members to successor demes following
tribe-splitting was “associative” (p.137) rather than random, its importance would be enhanced.
From classic early works to recent contributions, phenotype-based models abstracting
from the details of diploid genetic transmission have played a central role in the literature on
inter-demic selection (3-5). Closest to the model here is the selective extinction model of Aoki
(6). Though based on an entirely different derivation (with an explicit analysis of the dynamics of
the between- and within-deme variances), the condition for altruism to evolve is the same in the
two models. His equation (6) is
(S1) f > s(cid:39)(s+ k)
2
where f = F , s = the selection coefficient measuring the cost of the altruistic behavior (that is, c
ST
in the notation of this paper) and k is a measure of “intensity of group selection” which (because
the average probability of survival is ½) is equal (cid:54)2(cid:56) . Using this equivalence and rearranging the
A
equation S1 we have
(S2) F (cid:39)(1-F ) > s/k = c(cid:39)(cid:54)2(cid:56)
ST ST A
which is my equation (6) in the absence of reproductive leveling.
By contrast to the selective extinction model used here, the selective emigration model (7)
works because the average fitness of members of predominantly altruistic demes is above the
meta-population average and thus they contribute disproportionately to the next generation. (This
is possible because sites are assumed not to be saturated and demes can either accommodate or
export increments to their population.) For simplicity of comparison with the selective extinction
model assume that n is sufficiently large so that we can ignore terms in 1/n and that (cid:74) = 0.. Then
(cid:36) = - c while the expected average fitness of members of deme j is w = 1 + p(b - c) so (cid:36) (cid:47)
i j j G
dw(cid:39)dp = b - c. Using these values and equation (1) the condition for the A trait to increase
j j
(analogous to equations 2 and 6) is
(S3) var(p)(cid:39)E{var(p )} > - (cid:36)(cid:39)(cid:36) = c(cid:39)(b - c)
j ij i G
or, upon rearranging,
(S4) var(p)(cid:39){E{var(p )} + var(p)} (cid:47) F > c(cid:39)b
j ij j ST
which reproduces Hamilton's rule for the evolution of altruism by inclusive fitness with r = F .
ST
Inspection of the estimates in table 4 shows that for this process to proliferate altruism, the
benefits of altruism relative to the costs would need to be over ten for most groups.
2. Associative tribe-splitting.
3
An examination of fission among Amazonian tribal peoples ((8):198) reports that
“fissioning ... keeps close kin together but separates them from more distant kin ... [T]he potential
line of cleavage is furnished by the division in patrilineages.” Among two pairs of Yanomamo
daughter villages formed by a fission resulting from hostile relations within the parent deme “the
net effect of lineal fission is to reduce the effective size of the village at the time of fission by a
factor of four, relative to expectation from random fission.” (9):179 (A reduction in effective size
of this magnitude increases the level of equilibrium genetic differentiation by a factor of almost
4.) The authors conclude: “The process of village fission is strongly nonrandom socially, and
results in pronounced genetic cohesion within, and great genetic differences between daughter
villages.” 194. About two-thirds of the genetic differentiation among South American tribes has
been estimated to be the effect of associative fission (10) rather than isolation and drift stressed
in the equilibrium F formulations due to Wright (11). In these cases, genetic differentiation of
ST
demes is an unintended byproduct of lineal fission, as the alleles in question are not expressed in
observable ways. For these alleles the between-deme genetic differentiation created by associative
tribe splitting is already captured by the data in Table 4. But in the case of a behavioral trait such
as altruism, one would expect deliberate associative fission and other forms of selective
assortment, as altruists seek to exclude non-altruists from their demes.
Because excluding an N may be costly to an A, and because the benefits of the exclusion
are shared with all members of the deme, selective assortment will frequently be a form of public
goods provision (that is, an n-person prisoners' dilemma). Gintis and I modeled the evolution of a
form of individually costly selective assortment behavior (12), in which substantial numbers of
individuals who behave altruistically and ostracize those who violate a norm of altruistic
4
behavior are sustained indefinitely, even when competing with cheaters who conform to the
norm so as to avoid ostracism but do not contribute to the public good by ostracizing norm
violators. The ethnographic literature suggests that selective assortment is common among some
groups of foragers (see the works cited in (13) as well as (14))
To assess the effects on between-deme genetic differentiation of non-random deme
fission we compare the expected between-deme variance resulting from associative fission and
infinite deme size with that resulting from random fission and small deme size. Suppose an
infinitely large “parent” deme splits into two “daughter” demes. We assume the secession is
organized by a single head who seeks to compose a deme made up of individuals like himself,
thereby setting aside the public goods aspect of selective assortment mentioned above and in the
text. Because information about the past behavior of the members (the only basis of his selection
of deme members) is noisy, with probability (1-r) he selects randomly from the parent deme and
with probability r he selects one of his own type. Thus r is the assortment coefficient for
associative fission. If the departing head is an A, and p is the fraction of A's in the parent deme,
the daughter deme will be composed of a fraction of A’s approximately equal to r + (1-r)p. The
fraction of A's among those remaining after the departure of the first daughter deme will be 2p - r-
(1-r)p. If the departing head is an N, the fraction of A's in his deme will be p - rp, and the
fraction of those remaining who are A's is 2p - p + rp. This process is summarized in Table S1
[Table S1 here]
If the departing head is drawn at random, he will be an A with probability p and the
variance between the daughter deme (1) and the remaining deme (2), denoted var(p; r, (cid:52)),
j
(meaning the variance of the deme means p (j (cid:48) [1,2] ) given r and assuming infinite deme
j
5