Table Of Content

REVIEW Hamilton’sgeneralpointwasthatnaturalse- lectionleadsorganismstoappeardesignedasif Altruism, Spite, and Greenbeards tomaximizetheirinclusivefitness,whichisthe sum of fitness gained through producing off- spring (direct fitness) and through affecting the Stuart A. West* andAndy Gardner* fitnessofrelatedindividuals(indirectfitness).The Hamilton’stheoryofinclusivefitnessshowedhownaturalselectioncouldleadtobehaviorsthat easiestwayinwhichindirectfitnesscanbeob- decreasetherelativefitnessoftheactorandalsoeitherbenefit(altruism)orharm(spite)other tained is through interactions with close kin, in individuals.However,severalfundamentalissuesintheevolutionofaltruismandspitehaveremained whichcasegenesareidenticalbydescent(froma contentious.Here,weshowhowrecentworkhasresolvedthreekeydebates,helpingclarifyhow commonancestor),andsothisisusuallyreferred Hamilton’stheoreticaloverviewlinkstoreal-worldexamples,inorganismsrangingfrombacteriato toas“kinselection.”However,inclusivefitness humans:Istheevolutionofextremealtruism,representedbythesterileworkersofsocialinsects, isnotsimplyaconceptthatrelatestointeractions drivenbygeneticsorecology?Doesspitereallyexistinnature?And,canaltruismbefavoredbetween betweenrelatives;itisourmoderninterpretation individualswhoarenotclosekinbutsharea“greenbeard”geneforaltruism? ofDarwinianfitness,providingageneraltheory ofadaptation(6,7). Darwin’s (1) theory of natural selection altruisticorspitefultraits,whicharecostlytothe explains both the process and the pur- individuals that perform them. The paragon of ExtremeAltruismandthe poseofadaptation(Fig.1).Theprocess altruism is thesterileworker caste within social- HaplodiploidyHypothesis 0 1 isthatheritablecharactersassociatedwithgreater insect colonies, which help rear the offspring of Thesterileworkersofthesocialinsectsareex- 0 rceupmroudlautcetiivnensautuccraelsspowpiulllabtieonsesl.eTctheidslfeoardasntdoathce- tmheoilrdquceeellns.Athnateqaultarulliysteicxatlrleymgeievxeamupplethaeriersoliwmne tpreenmdeenatltrruepisrtosd,uwchtioongiivneourpdearnytochhealnpceotohferisn.dIen- 1, 2 1 apparentpurposeofadaptation:charactersappear- survivaltobecomethenonviablestalkofafruiting theHymenoptera(ants,bees,andwasps)andter- h c ing as if designed to maximize the individual’s body,helpingothercellstodisperseintheformof mites,thisextremealtruismhasledtoadivision r a reproductivesuccess(fitness). spores (5). The problem is that such altruism oflaborbetweenindividualsandtheevolution M ofthehighestlevelofsocialorganization,termed n o A Dynamics B Design eusociality. Depending upon how eusociality is g defined,ithasevolved3to11timesintheHy- or menoptera,aswellasintermites,thrips,aphids, g. a spiders,beetles,shrimps,andmolerats(8,9). m A major topic of debate has been whether e c eusociality has evolved multiple times in hy- n e menopterans because of their haplodiploid ge- ci s netics or their ecology. Under haplodiploidy, w. fertilized eggs develop into (diploid) females, w sg= cov(v,g) p pm a Px v(p) aHnadmuinltfoenrtili(z3e)desguggsgedsetveedlopthianttob(ehcaapulosied)hmaaplleos-. wm o diploidyleadstoafemalebeingmorerelatedto r Fig. 1. Darwinian adaptation—dynamics and design. (A) Natural selection is the genetic change in the her sisters (r = 0.75, assuming an outbred d f populationowingtodifferentialreproductivesuccessofindividualorganisms.Forexample,amongancestral e population in which females mate once) than d Arcticfoxes,individualswithpalefurleftmoredescendantsthanindividualswithdarkfursothatgenesforpale a pfuorrtaicocnuomfualnatyecdhianrathcteerpoapscurliabtaiobnle.tPorincea’tsu(r3a5l)seelqeuctaitoinon(Dforgm)aisliezeqsutahlitso,stthaetincogvtahraiatntcheebcehtawnegeeninanthinedhiveirdituaabll’es hfoerrHowamnioltfofnsp’srirnugle(rto=be0.s5a)t,istfhiiesdm(Faikge.s3iAte).asier wnlo S genetic(“breeding”)valueforthetrait(g)anditsrelativefitness(v).(B)Asaconsequenceofpastnatural However, haplodiploidy also leads to a fe- o D selection,today’sArcticfoxeslook“designed”tofittheirenvironment.Thisiscapturedbyanoptimization male being less related to a brother (r = 0.25), program,whichstatesthatthephenotype(p)oftheorganismisfunctioningasiftomaximizetheindividual’s exactlycancelingthebenefitofincreasedrelated- relativefitness(v;moregenerally,itsinclusivefitness)(6,7).[Credit:Biosphoto/CordierSylvain/PeterArnoldInc.] nesstosisters(10).Thehaplodiploidyhypothesis isnotrescuedifthepopulationsexratioisbiased Fisher(2)unitedDarwinismwithMendelian reducesthereproductivesuccessofthealtruist—so towardfemalesbecausethisbiasalsoreducesthe geneticsbydescribingnaturalselectioninterms whyisitnotweededoutbynaturalselection? relative reproductive value of females, exactly ofchangesingenefrequencies.Genesassociated Hamilton (3) showed that genes can spread cancelinganyrelatednessbenefits(11).Numer- withgreaterindividualfitnessarepredictedtoin- notonlythroughtheirdirectimpactontheirown ous studies have examined whether certain life creaseinfrequency,leadingtoanincreaseinmean transmission but also through their indirect im- historiescouldrescueHamilton’shaplodiploidy fitness.This“fundamentaltheoremofnaturalse- pactonthetransmissionofcopiespresentinother hypothesisbymakingtheaveragerelatednessto lection”wasintendedtocapturetheprocess(nat- individuals.Consequently,altruisticbehaviorscan siblings r > 0.5, but none appears generally uralselection)andthepurpose(maximizationof befavoredifthebenefitsaredirectedtowardother applicable (SOM text). In contrast, others have individualfitness)ofadaptation. individualswhosharegenesforaltruism(Fig.2). arguedthatwhatisspecialaboutthehymenop- ThisisencapsulatedbyHamilton’srule(3),which terans is that their natural history leads to a Altruism, Spite,and Inclusive Fitness statesthatatraitwillbefavoredbyselectionwhen relativelyhighbenefitofhelping(highb/cratio), Inthe1960s,Hamilton(3,4)realizedthatmaxi- rb–c>0,wherecisthefitnesscosttotheactor,b such as advanced parental care and a powerful mization of individual fitness could not explain isthefitnessbenefittotherecipient,andristheir stingthatfacilitatesgroupdefense(12). geneticrelatedness.ThisformofHamilton’srule DepartmentofZoology,OxfordUniversity,SouthParksRoad, emphasizesinteractionsbetweentwoindividuals, TheMonogamy Hypothesis OxfordOX13PS,UK. but it can be extended to allow for interactions Recent work (8, 13) has suggested a possible *To whom correspondence should be addressed. E-mail: withmultipleindividuals[supportingonlinemate- resolutiontothisdebate,arguingthatstrictlife- [email protected] (S.A.W); [email protected]. ac.uk(A.G.) rial(SOM)textandtableS1]. timemonogamy,inwhichfemalesonlymatewith www.sciencemag.org SCIENCE VOL327 12 MARCH 2010 1341 REVIEW tosiblings(r>0.5)hasbeenaredherring;whatis A Altruism B Reciprocity keyisthataveragerelatednessstaysat0.5.Other redherringsincludethepossibilityforeusociality Relative to have evolved via cooperation between sisters Help Help Relative (theparasocialroute)becausethatwouldleadto Actor or non- Actor Help relative r<0.5(8)andthesuggestionthathighrelat- edness is a consequence rather than a cause of eusociality(15),inwhichcasetheobservedcor- Nonrelative Not altruism! relationwithmonogamywouldnotbepredicted (9). Finally, the monogamy hypothesis suggests C Spite D Greenbeard thatfactorsthatfacilitatemonogamy,suchaslife- timestorageofspermbyfemales,arealsoimpor- tantinexplainingthedistributionofeusociality. Relative Bearded Help GettheRight Spite Benefit Actor or Benefit Actor Inclusive-fitness theory explains altruism but Harm Harm alsohasadarkerside.Spitefultraits,whichare harmful to both actor and recipient, may be Nonrelative Nonbearded favored (4). Considering the classic two-party 0 1 versionofHamilton’srule,ifcispositive(which 0 dFiirge.ct2ed.Mtoewcahradnrisemlastifvoers.a(lBtr)uRisemci,psrpoictiet,yainsdfarveocriepdrowcihtey.n(Ait)mAaltkreusistmhecaacntobremfaovroerleikdeilfyittoisrepcreeifveerehnetlipalilny icsosctolysttloytthoertheceipaicetnotr)),,thanendrbb–iscn>e0gactaivnebe(wsahtiicsfhieids 1, 2 1 thefuture.Reciprocityreliesuponafuturedirectfitnessbenefitforcooperationandsoisnotaltruistic.(C) ifrelatedness(r)isnegative. Negative relatedness h Spitecanbe favoredif it is preferentiallydirectedtowardrelativelyunrelatedindividuals,whoseloss c mayseemabizarreconcept,butitsimplymeans r improves the fitness of relatives. (D) Greenbeards are favored by directing altruism toward fellow a thattherecipientislessrelatedtotheactorthanisan M greenbeardindividualsorspitetowardnonbeardedindividuals. averagememberofthepopulation(SOMtext). n o Another way to think about spite is to dis- g onemaleintheirentirelife,iscrucialfortheevo- already lost the ability to mate and realize full tinguish between the primary recipient of the or lution of eusociality. Monogamy leads to a reproductive potential (9). Furthermore, these harming behavior (the individual physically g. a potential worker being equally related (r = 0.5) specieshavehadthetimetoevolvedivisionof attacked) and those secondarily influenced as a m toherownoffspringandtotheoffspringofher labor and specialized helping behaviors, giving byproduct of this (those experiencing reduced e c mother(siblings).Inthiscase,anysmallefficiency asubstantialb/c. competitionfromtheharmedindividual)(16,17). n e benefit for rearing siblings over their own off- Thebeautyofthemonogamyhypothesisisthat Fromthisperspective,spitecanbefavoredifthe ci s spring(b/c>1)willfavoreusociality(Fig.3B). itsimplifiesourunderstandingofhoweusociality actorismorerelatedtothesecondaryrecipients w. Incontrast,evenalowprobabilityofmultiple evolved,emphasizingthattheinteractionbetween (whobenefit)thantotheprimaryrecipients(who w mating means that potential workers would be kinshipandecologyisfundamentalandthatthey areharmed).Spitecanthereforebethoughtofas w morerelatedtotheirownoffspring.Inthiscase, are not competing explanations (8, 13). For altruismtowardthesecondaryrecipients:Harm- m o costly helping would require a significant effi- example,thesearchforhowtoincreaserelatedness inganindividualcanbefavoredifthisprovidesa r ciency advantage to rearing siblings over own d f e offspring(Fig.3C).Untilgrouplivingisestab- d A B C a lished,allowingtheevolutionofspecializedco- Haplodiploidy Monogamy Polyandry o operativebehavioranddivisionoflabor,theratio hypothesis nl Offspring Siblings Offspring Siblings Offspring Siblings w b/ccannotbeexpectedtogreatlyexceed1.For r= 0.5 r> 0.5 r= 0.5 r= 0.5 r= 0.5 r < 0.5 o D example,feedingasiblingisunlikelytobehugely morebeneficialthanfeedinganoffspringbythe same amount. Consequently, in the absence of strictmonogamythepopulationcannotevenget startedontheroadtoeusociality. In support of this hypothesis, comparative studieshavefoundmonogamytobetheancestral D E F stateinalltheindependentoriginsofeusociality studied(9,14).Monogamyoriginatedfirst,giving ahighrelatedness,andthenwhenecologicalcon- ditionsledtoahighenoughb/c,eusocialityevolved (SOMtext).Importantecologicalconditionsin- clude“lifeinsurance”benefitsofallowinghelpers to complete parental care after the death of the Fig. 3. Monogamypavesthewaytoeusociality.(A)Thehaplodiploidyhypothesisreliesonindividuals mother(forexample,ants,bees,andwasps),and beingmorerelatedtosiblingsthanoffspring,makingsiblingsworthmorethanoffspring.Asoriginally “fortressdefense”benefitsofremainingtohelpuse envisioned,thisappearstohavebeenaredherring.(B)Themonogamyhypothesisemphasizesthatifan or defend a food source, when opportunities for individualisequallyrelatedtoitssiblingsanditsoffspring,evenaveryslightefficiencybenefitforraising successfulmigrationarelow(forexample,aphids, siblingstranslatesintoaselectiveadvantageforhelping.(C)Withoutstrictmonogamy,individualsaremore beetles,termites,thrips,andshrimps)(12,14). relatedtotheiroffspringthantheyaretotheirsiblingssothatalargeefficiencybenefitisrequiredinorder There are some eusocial species in which forsibling-rearingtobefavored.(D)SterileworkerscaringforbroodintheantCamponotusherculeanus. queensmatemultiply.However,thisisaderived (E)AlifetimemonogamouspairfromthetermiteReticulitermesflavipes.(F)Nonbreedingworkersinthe condition that has evolved after workers have shrimpSynalpheusregalis.[PhotosprovidedbyDavidNash,BarbaraThorne,andEmmettDuffy] 1342 12MARCH 2010 VOL327 SCIENCE www.sciencemag.org REVIEW benefittocloserrelatives(Fig.2C). toconspecificsthatlackanimmu- Table1.Notspite:examplesoftraitsthathavebeensuggestedasspiteful Thesetwodifferentencapsulations nitygene(22).Insomecases,cell but actually provide a direct benefit to the actor and hence are selfish ofspitearedifferentwaysoflook- death is required to release the (table S2). ingatthesamething,usingeithera bacteriocins into the environment, two-orthree-partyHamilton’srule Taxa Suggestedspitefultraits Whyselfish,notspiteful and so it is clearly a costly trait (SOMtext)(16,17).Iftheactoris (positive c). In addition, there is Birds Protectionofterritories, Decreasedcompetitionfor morecloselyrelatedtothesecond- geneticlinkagebetweenthebacte- siblicideatneighboring resources,forselfor aryrecipientsthantheprimaryre- riocin production and immunity nests. offspring cipients in a three-party rule, then genes so that close relatives both Fish Eggcannibalism Decreasedcompetitionfor thisleadstoanegativerelatedness produce and are immune to a resources,foroffspring inthetwo-partyrule. particular bacteriocin (22). Conse- Humans Punishmentandrejectionof Leadstoincreased Althoughmanybehaviorshave quently,thereleaseofbacteriocins lowoffersineconomic cooperationinthelongterm beensuggestedasspiteful,theyare killsnonrelatives,freeingupresources games usuallyexplainedasselfishbehav- forclone-mates.Experimentalwork Mammals Infanticide,harassmentof Decreasedcompetition,for iorsthatarecostlytotherecipient onbacteriocins has alsosupported nondescendantjuveniles offspringormates butprovideabenefittotheactor(c< the prediction that the relative ad- andinjuredmales 0)(Table1).Thisbenefitisoftena vantageofspiteisgreaterwhenvar- reductioninfuturecompetitionfor ianceinrelatednessishigher(giving resources, for the actor or their offspring, with sterilesoldiercasteinpolyembryonicparasitoid anintermediatemeanrelatedness)becausethis 0 1 confusion arising because the direct fitness waspssatisfiesalltheseconditions(17).Females leads to interactions with both close relatives 0 cteornmseaqnudenncoetsowveerrethoenlilfyetcimonesiodfetrheedainctothre(SsOhoMrt laafyterthweihricehggthseownathspeeeggggssdoifvimdeotahsecxautearlplyillaanrsd, alantdednnoenssretloatitvhees,seaclloonwdianrgyaberenleaftiicviealryiehsig(Fhiegr.r4e)- 1, 2 1 text)(18).Whatmattersfornaturalselectionare consumethegrowingcaterpillarfromtheinside (21,23). h c fitnessconsequencesovertheentirelifetimeand (20). Although most larvae develop normally, a r a notsomearbitraryperiod.Forexample,herring fractionbecomeasoldiermorph.Developingasa Spiteful Words M gullskillthechicksatneighboringnests,butthis soldieriscostlytotheactor,becausethesoldiersare As discussed above, spite can be considered a n o reducesthefuturecompetitionoverresourcesfor sterile, and costly to the recipient, because the formofaltruism.Consequently,itisusefultoask g both themselves and their offspring. Further- soldiers seek out and kill other larvae within the whetherwegainanythingbydistinguishingspite or more, there is no evidence that such examples host. Finally, soldiers preferentially kill larvae to from altruism. At one level, it can be useful to g. a involveasufficientsecondarybenefittorelatives. which they are less related (those that have emphasizethesimilarities,thatbotharefavored m Indeed, it has even been suggested that the developedfromothereggs),freeingupresources becausetheyleadtoanincreaseintheinclusive e c conditions required are so restrictive that spite fortheirclone-mates. fitnessoftheactorthroughindirectfitnesscon- n e wouldberareornonexistent(11,12). Another example of spite is provided by sequences.Thiswillalsohelpavoiddebatesover ci s However, recent theory has shown that a the production of antimicrobial bacteriocins by whether certain traits should be classed as al- w. positive relatedness to secondary recipients can manybacteria(21).Thesecompoundsarelethal truismor spite because the mathematics of any w beobtainedmoreeasilythanpreviouslythought, w suggesting that at least from a theoretical m o perspective spite is plausible (19) if there is (i) A B 4.0 r lpbaeerhtgiateovrisov;rasr(iiaia)nimckeeindindaitsrceirlniamdteiivdninadetuisoasnls,btweotiwthweehhnoamrcmoitmnhge- efficient Spite Altruism efficient 23..00 oaded f actor is relatively unrelated (making the actor n co n co 1.0 wnl relatively more related to the secondary recip- o o o ients); or (iii) strong local competition so that ecti ecti 0.0 D harming the primary recipient provides appre- Sel Sel ciable benefits to secondary recipients. When -1.0 0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0 theseconditionsaremet,spitefulbehaviorscan Kinship Kinship be favored so as to reduce competition for rel- C D atives. Consider the extreme example of when twogeneticallyidentical(clonal)individualsare competingwithanonrelativetowhomtheyare unrelated. One of the clone-mates could be selected to harm the nonrelative, at a cost to itself, if this harming reduces the nonrelative’s ability to compete for resources and hence benefitstheotherclone-mate. RealSpite Todemonstratespite,itmustbeshownthatatrait Fig. 4. Populationstructure,altruism,andspite.(A)Theorypredictsthatasrelatednesswithinapatch iscostlytotheactor(positivec)andcostlytothe increases,thereisanincreaseinaltruistictraitsandadomedrelationshipwithspitefultraits(3,15).(B)As recipient (negative b). In addition, for spite to predicted, the relative benefit of bacteriocin production inPseudomonas aeruginosa shows a domed haveevolvedbymeansofnaturalselection,the relationshipwithrelatedness(23)(C)Altruism:afruitingbodyoftheslimemoldDictyosteliumdiscoideum. actor must be more closely related to the sec- (D)Spite:Apieceoffilterpapersoakedwithabacteriocin(leftspot)causesaninhibitionzonewherebacteria ondary recipients (beneficiaries) than to the cannotgrow,inthesamewayasatraditionalantibiotic(rightspot;bottomspotshowsbothincombination). primaryrecipientthattheyharm(Fig.2C).The [PhotosprovidedbyOwenGilbert,MargaretRiley,andSaraCody] www.sciencemag.org SCIENCE VOL327 12 MARCH 2010 1343 REVIEW casecanberearrangedsoastomakeaspitefulor wouldnotoccurinnaturebecausetheycouldbe biology. Theoretical work on spite and green- altruistictwo-partyrule(16,17). easily invaded by “falsebeards” (cheats) that beards was spurred by biological examples but However,therearealsoanumberofreasons displayedthebeardwithoutalsoperformingthe thenledtoaunifyingframeworkthatilluminated whyitisusefultodistinguishspitefromaltruism behavior(27). detectionproblemsandsuggestedwheretolook (17). From a behavioral perspective, there is a Thisassumptionhasbeenoverturnedbythe forfurtherexamples.Alloftheseexamplesillus- clear difference between helping and harming. discoveryofanumberofaltruisticgreenbeards. tratethatthedistinctionbetweengenetics(r)and Additionally, there are biologically interesting In the slime mold Dictyostelium discoideum, ecology (b/c) is both artificial and unhelpful. differences between altruism and spite. For ex- individuals with the csa gene adhere to each What really matters is how they interact, as has ample,localcompetitionforresourcestypically other in aggregation streams and cooperatively alwaysbeenemphasizedbyHamilton’srule. selects for spite and against altruism (21); formfruitingbodieswhileexcludingnoncarriers altruistic traits are predicted to show a positive of the gene (5). Other examples have been ReferencesandNotes relationshipwithrelatedness(3),whereasspite- foundinyeast,abacterialplantpathogen,anda 1. C.Darwin,OntheOriginofSpeciesbyMeansofNatural Selection,or,thePreservationofFavouredRacesinthe fultraitsarepredictedtoshowadomedrelation- lizard (SOM text). In addition, spiteful green- StruggleforLife(JohnMurray,London,UK,1859). ship(Fig.4)(19,21);andkindiscriminationis beardshavebeendiscovered,includingtheGp-9 2. R.A.Fisher,TheGeneticalTheoryofNaturalSelection key in the examples of spite, whereas altruism gene of the fire ant Solenopsis invicta (29). 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D.Giron,D.W.Dunn,I.C.W.Hardy,M.R.Strand, w Greenbeards place to look for new greenbeards may be in Nature430,676(2004). m Hamilton(3,26)pointedoutthatindirect-fitness microbes, in which asexual growth can lead to 21. A.Gardner,S.A.West,A.Buckling,Proc.Biol.Sci.271, ro benefits require genetic relatedness per se and extreme population structuring; the relatively 1529(2004). d f 22. M.A.Riley,J.E.Wertz,Annu.Rev.Microbiol.56,117(2002). e not kinship. Imagine a gene (or cluster of simple link between genotype and phenotype 23. R.F.Inglis,A.Gardner,P.Cornelis,A.Buckling,Proc. d a tightly-linked genes) that gives rise to a con- may prevent a decoupling of beard and social Natl.Acad.Sci.U.S.A.106,5703(2009). o spicuous phenotype, uses this phenotype to trait (falsebeards), and genetic knockouts facil- 24. M.Hauser,K.McAuliffe,P.R.Blake,Philos.Trans.R.Soc. nl w Lond.BBiol.Sci.364,3255(2009). discriminate between carriers and noncarriers itatethedetectionofgreenbeards(30). o 25. K.Jensen,J.Call,M.Tomasello,Proc.Natl.Acad.Sci.U.S.A. D ofthegene,andleadstocostlyhelpingtoward Somemodelsforaltruisminhumans(31–34) 104,13046(2007). other carriers of the gene (Fig. 2D). This gene and social insects (15) implicitly invoke green- 26. W.D.Hamilton,inBiosocialAnthropology,R.Fox,Ed. could be favored by natural selection, even if beard mechanisms without realizing this, such (Wiley,NewYork,1975),pp.133–155. 27. R.Dawkins,TheSelfishGene(OxfordUniv.Press,Oxford, carrierssharenoothergenesincommon.Thus, asthesuggestionthataltruisticindividualsdiffer 1976). the crucial requirement for altruism is genetic from individuals whoare not altruisticinsome 28. L.Lehmann,L.Keller,J.Evol.Biol.19,1365(2006). relatednessatthealtruismlocusandnotgenea- observable characteristic [such as being more 29. L.Keller,K.G.Ross,Nature394,573(1998). logicalrelationshipoverthewholegenome. likelytosmileandlaugh(31,32)]ormodelsof 30. A.Gardner,S.A.West,Evolution64,25(2010). Dawkinsproposedthehypotheticalexample “strongreciprocity”thatassumepunishmentand 31. R.H.Frank,Am.Econ.Rev.77,593(1987). 32. M.J.Owren,J.-A.Bachorowski,inEmotions:Current ofagenethatgivesrisetoagreenbeardwhile altruismtobegeneticallylinked(33,34).How- IssuesandFutureDirections,T.J.Mayne,G.A.Bonanno, simultaneously prompting individuals with ever,thereisnoreasontosuspectthattraitssuch Eds.(Guilford,NewYork,2001),pp.152–191. greenbeardstodirectcooperationtowardother assmilingorpunishmentwillbeencodedbythe 33. H.Gintis,J.Theor.Biol.206,169(2000). green-bearded individuals (27). However, this samegeneorcloselylinkedgenesasthosethat 34. S.Bowles,H.Gintis,Theor.Popul.Biol.65,17(2004). 35. G.R.Price,Nature227,520(1970). “greenbeard”mechanismcanalsooccurwithout leadtoaltruism.Consequently,falsebeardscould 36. WethankJ.Alpedrinha,K.Boomsma,A.Griffin, avisibletag.Whatisrequiredmoregenerallyis arise,andtheseproposedexplanationsforaltruism M.Hauser,K.Jensen,L.KellerandP.Taylorfor a single gene (or a number of tightly-linked wouldnotbeevolutionarilystable(30). commentsandtheRoyalSociety,EuropeanResearch genes) encoding both the cooperative behavior Council,andLeverhulmeTrustforfunding. and causing cooperators to associate (26, 28). Conclusions SupportingOnlineMaterial Greenbeards are oneof the twoways in which Aunifyingthemeinalltheissuesthatwehave www.sciencemag.org/cgi/content/full/327/5971/1341/DC1 natural selection can favor altruistic behavior, discussedhereistheimportanceoftheinterplay SOMText withtheotherbeinginteractionswithgenealog- between theory and data. The monogamy hy- TablesS1andS2 ical kin (3). However, despite this fundamental pothesiscutsthroughthesuperfluousdetailsby References position it has been assumed that greenbeards focusing on a key aspect of the underlying 10.1126/science.1178332 1344 12MARCH 2010 VOL327 SCIENCE www.sciencemag.org www.sciencemag.org/cgi/content/full/327/5971/1341/DC1 Supporting Online Material for Altruism, Spite, and Greenbeards Stuart A. West* and Andy Gardner* *To whom correspondence should be addressed. E-mail: [email protected] (S.A.W); [email protected] (A.G.) Published 12 March 2010, Science 327, 1341 (2010) DOI: 10.1126/science.1178332 This PDF file includes: SOM Text Tables S1 and S2 References Supporting Online Material for ‘Altruism, Spite and Greenbeards’, by Stuart A. West & Andy Gardner ! #$!%&’(!()*%’+$!,)!)-./$0!’$!12)/%)2!0)%/’3!4.+$!()5)2/3!’((4)(!,)!/002)((!’$!%&)!6/’$! %)-%7!*3/2’89’$1!3’$:(!,’%&!%&)!)-’(%’$1!3’%)2/%42)!6+2)!1)$)2/339;! ! Hamilton’s rule! </6’3%+$=(!243)!>1, 2?!’(!4(4/339!,2’%%)$!/(!rb @!c!A!B7!+2!’$!(+6)!)C4’5/3)$%!8+267! ,&’*&!)6.&/(’D)(!/!8’%$)((!’$%)2/*%’+$!E)%,))$!/!(’$13)!/*%+2!>,&+!(488)2(!/!8’%$)((! 0)*2)6)$%!c?!/$0!/!(’$13)!2)*’.’)$%!>,&+!1/’$(!/!8’%$)((!’$*2)6)$%!b?;!<+,)5)27!/*%’+$(! ,’33!%9.’*/339!&/5)!8’%$)((!*+$()C4)$*)(!8+2!6+2)!%&/$!+$)!2)*’.’)$%7!(+!6+2)!1)$)2/339! ,)!*/$!,2’%)!! !r b!@!c!A!B7!,&)2)!I!’(!%&)!()%!+8!/33!’$0’5’04/3(!>)-*340’$1!%&)!/*%+2?! i!I i i ,&+()!8’%$)((!’(!/88)*%)0!E9!%&)!/*%’+$!>b!"!B?!/$0!,&+!/2)!.+(’%’5)39!+2!$)1/%’5)39! i 2)3/%)0!%+!%&)!/*%+2!>r!"!B?7!/$0!r!/$0!b!/2)!%&)!2)3/%)0$)((!/$0!8’%$)((!’$*2)6)$%7! i i i 2)(.)*%’5)397!*+22)(.+$0’$1!%+!%&)!i%&!2)*’.’)$%;!F9.’*/3397!*+(%(!/$0!E)$)8’%(!/2)!82/6)0!’$! /E(+34%)! >(425’5’$1! +88(.2’$1?! +2! 2)3/%’5)! >(&/2)! +8! .+.43/%’+$! 2).2+04*%’5)! (4**)((?! %)26(;!#$!(*)$/2’+(!,&)2)!’$0’5’04/3(!E)3+$1!%+!()./2/%)!*3/(()(7!(4*&!/(!()-!+2!/1)! *3/(()(7!8’%$)((!)88)*%(!64(%!E)!)-.2)(()0!’$!%)26(!+8!2).2+04*%’5)!5/34)!>3-5?;!G+%)!%&/%! %&’(!(466/%’+$!8+26!’(!(%’33!</6’3%+$=(!243)7!/$0!’%!,+430!E)!.+’$%3)((!%+!/214)7!8+2! )-/6.3)7!%&/%!</6’3%+$=(!243)!’(!’$5/3’0/%)0!,&)$!%&)2)!’(!6+2)!%&/$!+$)!2)*’.’)$%;! H/%&)27!%&)!:)9!)3)6)$%(!+8!</6’3%+$=(!243)!/2)I!>"?!%&)!$+%’+$!%&/%!/!.+(’%’5)!’$*34(’5)! 8’%$)((!)88)*%!’(!%&)!43%’6/%)!*2’%)2’+$!8+2!/$!/*%’+$!%+!E)!8/5+42)0!E9!$/%42/3!()3)*%’+$J!>K?! %&/%!’$*34(’5)!8’%$)((!’(!1’5)$!E9!%&)!(46!+8!0’2)*%!8’%$)((!/$0!’$0’2)*%!8’%$)((J!/$0!>L?!%&/%! 8’%$)((!)88)*%(!8+2!2)*’.’)$%(!/2)!%2/$(3/%)0!’$%+!’$0’2)*%!8’%$)((!)88)*%(!8+2!%&)!/*%+2!’$! .2+.+2%’+$!%+!%&)!1)$)%’*!2)3/%)0$)((!+8!/*%+2!/$0!2)*’.’)$%;!! G)5)2%&)3)((7!’%!’(!,+2%&,&’3)!%+!/(:I!,&)$!0+)(!%&)!(’6.3)2!%,+M./2%9!243)!rb @!c! 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Social behaviours and intentional language! V2+6!/$!)5+34%’+$/29!.)2(.)*%’5)!/!%2/’%!+2!E)&/5’+2!’(!(+*’/3!’8!’%!&/(!8’%$)((! *+$()C4)$*)(!8+2!E+%&!%&)!’$0’5’04/3!%&/%!.)28+26(!%&/%!E)&/5’+2!>%&)!/*%+2?!/$0!/$+%&)2! ’$0’5’04/3!>%&)!2)*’.’)$%?;!</6’3%+$!>2?!*3/((’8’)0!(+*’/3!E)&/5’+2(!/**+20’$1!%+!,&)%&)2! %&)!*+$()C4)$*)(!%&)9!)$%/’3!8+2!%&)!/*%+2!/$0!2)*’.’)$%!/2)!E)$)8’*’/3!>’$*2)/()!0’2)*%! 8’%$)((?!+2!*+(%39!>0)*2)/()!0’2)*%!8’%$)((?!>F/E3)!]‘W"?;! ! L F&)! /0/.%/%’+$’(%! /..2+/*&! .2+5’0)(! %&)! 8+26/3! ^4(%’8’*/%’+$! 8+2! %&)! 4()! +8! ’$%)$%’+$/3! 3/$14/1)7! (4*&! /(! /3%24’(6! /$0! (.’%)! >32?;! ].)*’8’*/3397! %&)! 09$/6’*(! +8! $/%42/3!()3)*%’+$!3)/0(!%+!’$0’5’04/3!+21/$’(6(!%&/%!E)&/5)!/(!8’%$)((!6/-’6’D’$1!/1)$%(7! /$0!&)$*)!E)&/5)!/(!’8!%&)9!&/5)!’$%)$%’+$!+2!.42.+()!/%!%&)!’$0’5’04/3!3)5)3;!#$%)$%’+$/3! %)26(!0+!$+%!.2+5’0)!/!(4.)28’*’/3!13+((7!E4%!2/%&)2!*+$5)9!’6.+2%/$%!’$8+26/%’+$!/E+4%! 1)$)! 82)C4)$*9! 09$/6’*(;! #$! ./2%’*43/27! %&)! 6/-’6’D’$1! /1)$%! /$/3+19! &/(! 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H)*’.2+*/3!/3%24’(6!’(!$+%!/*%4/339!/3%24’(%’*!>V’1;!K?7!/$0!(+!E)%%)2!%)26)0!2)*’.2+*’%9=! >33?;!F+!1’5)!/$+%&)2!)-/6.3)7!%&)!12+4.!()3)*%’+$!3’%)2/%42)!0)8’$)(!/3%24’(6!2)3/%’5)!%+! %&)!8’%$)((!+8!+%&)2!’$0’5’04/3(!’$!%&)!12+4.!>34?;!<+,)5)27!$/%42/3!()3)*%’+$!+.)2/%)(!+$! 8’%$)((!2)3/%’5)!%+!%&)!.+.43/%’+$7!$+%!(+6)!/2E’%2/29!82/*%’+$!+8!’%;!F&)()!/$0!+%&)2! )-/6.3)(!/2)!0’(*4(()0!’$!12)/%)2!0)%/’3!’$!%&)!8+33+,’$1!()*%’+$;! O88)*%!+$!/*%+2! O88)*%!+$!2)*’.’)$%! ! b! M! b! W4%4/339!E)$)8’*’/3! ])38’(&! M! U3%24’(%’*! ].’%)843! Table SOM1. Social Behaviors. U$! )5+34%’+$/29! *3/((’8’*/%’+$! (*&)6)! 8+2! (+*’/3! E)&/5’+2(!%&/%!&/5)!E))$!()3)*%)0!8+2!E9!$/%42/3!()3)*%’+$!>2, 33?;!O88)*%(!/2)!6)/(42)0!’$! %)26(!+8!3’8)%’6)!)88)*%(!+$!0’2)*%!8’%$)((;!<)3.’$1!E)&/5’+2(!/2)!b!%+!%&)!2)*’.’)$%7!/$0! */$!E)!64%4/339!E)$)8’*’/3!+2!/3%24’(%’*;!</26’$1!E)&/5’+2(!/2)!@!%+!%&)!2)*’.’)$%!/$0!*/$! E)!()38’(&!+2!(.’%)843;!T++.)2/%’+$!’(!0)8’$)0!/(!/!&)3.’$1!E)&/5’+2!%&/%!&/(!)5+35)0!/%! 3)/(%!./2%’/339!04)!%+!%&)!)88)*%!+$!%&)!2)*’.’)$%!@!%&’(!’$*340)(!/33!/3%24’(%’*!E)&/5’+2(!/$0! (+6)! 64%4/339! E)$)8’*’/3! E)&/5’+2(! >33?;! W+(%! (+*’/3! E)&/5’+2(! ,’33! &/5)! 8’%$)((! *+$()C4)$*)(!8+2!%&2))!+2!6+2)!’$0’5’04/3(7!(+!,)!6/9!(/9!%&/%!/!E)&/5’+2!’(!/3%24’(%’*!’$! 2)3/%’+$!%+!’6./*%!4.+$!+$)!2)*’.’)$%7!/$0!(.’%)843!’$!2)3/%’+$!%+!’%(!’6./*%!4.+$!/$+%&)2! 2)*’.’)$%;!#%!’(!2)/(+$/E3)!%+!%)26!(4*&!/!E)&/5’+2!/(!/3%24’(6!’8!%&)!.2’6/29!2)*’.’)$%!’(! %&)!E)$)8’*’/297!/$0!(.’%)!’8!%&)!.2’6/29!2)*’.’)$%!’(!%&)!5’*%’6; Not altruism F)26(! (4*&! /(! /3%24’(6! &/5)! 5)29! (.)*’8’*! 6)/$’$1(7! ,&’*&! *+$5)9! 4()843! ’$8+26/%’+$;!#8!%&)()!%)26(!/2)!6’(4()07!+2!2)0)8’$)07!%&)!2)(43%!’(!*+$84(’+$!>33?;!F&’(! &/(!E))$!/!./2%’*43/239!3/21)!.2+E3)6!,’%&!%&)!%)26!/3%24’(6!>33?7!.;!a"cMaKL?7!,&’*&!&/(! E))$! 2)0)8’$)0! ’$! 6/$9! ,/9(7! ’$*340’$1I! >/?! 2)*’.2+*/3! /3%24’(67! ,&)2)! &)3.’$1! ’(! 8/5+42)0!E)*/4()!’%!,’33!3)/0!%+!%&)!/*%+2!E)’$1!&)3.)0!E/*:!/%!/!3/%)2!0/%)!>35?J!>E?!/! 0)*2)/()!’$!%&)!8’%$)((!+8!%&)!8+*/3!’$0’5’04/37!2)3/%’5)!%+!%&)!+%&)2!6)6E)2(!+8!’%(!12+4.! >2)3/%’5)39! *+(%39! %+! ’$0’5’04/37! 2)3/%’5)39! E)$)8’*’/3! %+! %&)! 12+4.J! (+6)%’6)(! %)26)0! \,)/:!/3%24’(6=?!>34, 36-41?J!>*?!/!0)*2)/()!’$!8’%$)((!+5)2!%&)!(&+2%!%)26!>42, 43?J!>0?! .3/9’$1!*++.)2/%)!’$!/!.2’(+$)2(=!0’3)66/!1/6)!>44?J!>)?!/!8/’342)!%+!&/26!+%&)2(!>45?J!>8?! %&)!6)*&/$’(6!E9!,&’*&!+$)!’$0’5’04/3!’(!6+%’5/%)0!%+!&)3.!+%&)2(!>46?;! ! a F&)!.2+E3)6!,’%&!/33!+8!%&)()!2)0)8’$’%’+$(!’(!%&/%!%&)9!’$*340)!(’%4/%’+$(!,&)2)! *++.)2/%’+$! *+430! .2+5’0)! /! 0’2)*%! 8’%$)((! E)$)8’%7! /$0! &)$*)! *+430! E)! 64%4/339! E)$)8’*’/3;!T+$()C4)$%397!%&’(!3)/0(!%+!/!E)&/5’+2!E)’$1!3/E)3)0!/(!/3%24’(%’*!,&)$!’%!’($=%! *+(%39! /$0! /*%4/339! E)$)8’%(! %&)! /*%+2;! V+2! )-/6.3)7! *+$(’0)2’$1! 2)*’.2+*/3! &)3.’$1! >)-/6.3)!/!/E+5)?7!*++.)2/%’+$!’(!+$39!8/5+2)0!>E)%,))$!$+$M2)3/%’5)(?!’8!’%!3)/0(!%+!/$! +5)2/33!E)$)8’%!>%&2+41&!’$*2)/()0!3’:)3’&++0!+8!E)’$1!&)3.)0!’$!%&)!84%42)?7!’$!,&’*&!*/()! ’%!’(!64%4/339!E)$)8’*’/37!/$0!(+!2)*’.2+*/3!/3%24’(6!’(!$+%!/3%24’(%’*;!#$!%&)!+%&)2!*/()(! >)-/6.3)(!EM8?!&)3.’$1!*/$!E)!64%4/339!E)$)8’*’/3!+2!/3%24’(%’*!>M_b?7!0).)$0’$1!4.+$! 6+0)3! 0)%/’3(! /$0! ./2/6)%)2! 5/34)(! /((46)0;! O3(),&)2)7! ,)! 0’(*4((! ’$! 0)%/’3! %&)! *+$84(’+$! %&/%! %&’(! */$! 3)/0! %+! >33?;! ]4*&! 2)0)8’$’%’+$(! +E(*42)! %&)! 84$0/6)$%/3! 0’(%’$*%’+$!E)%,))$!,&)$!0’2)*%!+2!’$0’2)*%!8’%$)((!E)$)8’%(!/2)!2)C4’2)0!%+!)-.3/’$!%&)! +E()25)0!*++.)2/%’+$!>33, 47, 48?;!F&’(!*/$!3)/0!%+!%&)!(’%4/%’+$!,&)2)!/!E)&/5’+2!’(! 0)(*2’E)0! /(! /3%24’(%’*7! E4%! */$! E)! )-.3/’$)0! E9! 0’2)*%! 8’%$)((! E)$)8’%(! >’;);! E9! ()38M ’$%)2)(%)0!+2!()38M2)1/20’$1!E)&/5’+2(?;!W+2)!8+26/3397!%&)()!2)0)8’$’%’+$(!/2)!6’(3)/0’$1! 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Description:
decrease the relative fitness of the actor and also either benefit (altruism) or harm (spite) other individuals who share genes for altruism (Fig. 2).
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Altruism, Spite, and Greenbeards REVIEW PDF

18 Pages·2010·0.55 MB·English
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Preview Altruism, Spite, and Greenbeards REVIEW

REVIEW Hamilton’sgeneralpointwasthatnaturalse- lectionleadsorganismstoappeardesignedasif Altruism, Spite, and Greenbeards tomaximizetheirinclusivefitness,whichisthe sum of fitness gained through producing off- spring (direct fitness) and through affecting the Stuart A. West* andAndy Gardner* fitnessofrelatedindividuals(indirectfitness).The Hamilton’stheoryofinclusivefitnessshowedhownaturalselectioncouldleadtobehaviorsthat easiestwayinwhichindirectfitnesscanbeob- decreasetherelativefitnessoftheactorandalsoeitherbenefit(altruism)orharm(spite)other tained is through interactions with close kin, in individuals.However,severalfundamentalissuesintheevolutionofaltruismandspitehaveremained whichcasegenesareidenticalbydescent(froma contentious.Here,weshowhowrecentworkhasresolvedthreekeydebates,helpingclarifyhow commonancestor),andsothisisusuallyreferred Hamilton’stheoreticaloverviewlinkstoreal-worldexamples,inorganismsrangingfrombacteriato toas“kinselection.”However,inclusivefitness humans:Istheevolutionofextremealtruism,representedbythesterileworkersofsocialinsects, isnotsimplyaconceptthatrelatestointeractions drivenbygeneticsorecology?Doesspitereallyexistinnature?And,canaltruismbefavoredbetween betweenrelatives;itisourmoderninterpretation individualswhoarenotclosekinbutsharea“greenbeard”geneforaltruism? ofDarwinianfitness,providingageneraltheory ofadaptation(6,7). Darwin’s (1) theory of natural selection altruisticorspitefultraits,whicharecostlytothe explains both the process and the pur- individuals that perform them. The paragon of ExtremeAltruismandthe poseofadaptation(Fig.1).Theprocess altruism is thesterileworker caste within social- HaplodiploidyHypothesis 0 1 isthatheritablecharactersassociatedwithgreater insect colonies, which help rear the offspring of Thesterileworkersofthesocialinsectsareex- 0 rceupmroudlautcetiivnensautuccraelsspowpiulllabtieonsesl.eTctheidslfeoardasntdoathce- tmheoilrdquceeellns.Athnateqaultarulliysteicxatlrleymgeievxeamupplethaeriersoliwmne tpreenmdeenatltrruepisrtosd,uwchtioongiivneourpdearnytochhealnpceotohferisn.dIen- 1, 2 1 apparentpurposeofadaptation:charactersappear- survivaltobecomethenonviablestalkofafruiting theHymenoptera(ants,bees,andwasps)andter- h c ing as if designed to maximize the individual’s body,helpingothercellstodisperseintheformof mites,thisextremealtruismhasledtoadivision r a reproductivesuccess(fitness). spores (5). The problem is that such altruism oflaborbetweenindividualsandtheevolution M ofthehighestlevelofsocialorganization,termed n o A Dynamics B Design eusociality. Depending upon how eusociality is g defined,ithasevolved3to11timesintheHy- or menoptera,aswellasintermites,thrips,aphids, g. a spiders,beetles,shrimps,andmolerats(8,9). m A major topic of debate has been whether e c eusociality has evolved multiple times in hy- n e menopterans because of their haplodiploid ge- ci s netics or their ecology. Under haplodiploidy, w. fertilized eggs develop into (diploid) females, w sg= cov(v,g) p pm a Px v(p) aHnadmuinltfoenrtili(z3e)desguggsgedsetveedlopthianttob(ehcaapulosied)hmaaplleos-. wm o diploidyleadstoafemalebeingmorerelatedto r Fig. 1. Darwinian adaptation—dynamics and design. (A) Natural selection is the genetic change in the her sisters (r = 0.75, assuming an outbred d f populationowingtodifferentialreproductivesuccessofindividualorganisms.Forexample,amongancestral e population in which females mate once) than d Arcticfoxes,individualswithpalefurleftmoredescendantsthanindividualswithdarkfursothatgenesforpale a pfuorrtaicocnuomfualnatyecdhianrathcteerpoapscurliabtaiobnle.tPorincea’tsu(r3a5l)seelqeuctaitoinon(Dforgm)aisliezeqsutahlitso,stthaetincogvtahraiatntcheebcehtawnegeeninanthinedhiveirdituaabll’es hfoerrHowamnioltfofnsp’srirnugle(rto=be0.s5a)t,istfhiiesdm(Faikge.s3iAte).asier wnlo S genetic(“breeding”)valueforthetrait(g)anditsrelativefitness(v).(B)Asaconsequenceofpastnatural However, haplodiploidy also leads to a fe- o D selection,today’sArcticfoxeslook“designed”tofittheirenvironment.Thisiscapturedbyanoptimization male being less related to a brother (r = 0.25), program,whichstatesthatthephenotype(p)oftheorganismisfunctioningasiftomaximizetheindividual’s exactlycancelingthebenefitofincreasedrelated- relativefitness(v;moregenerally,itsinclusivefitness)(6,7).[Credit:Biosphoto/CordierSylvain/PeterArnoldInc.] nesstosisters(10).Thehaplodiploidyhypothesis isnotrescuedifthepopulationsexratioisbiased Fisher(2)unitedDarwinismwithMendelian reducesthereproductivesuccessofthealtruist—so towardfemalesbecausethisbiasalsoreducesthe geneticsbydescribingnaturalselectioninterms whyisitnotweededoutbynaturalselection? relative reproductive value of females, exactly ofchangesingenefrequencies.Genesassociated Hamilton (3) showed that genes can spread cancelinganyrelatednessbenefits(11).Numer- withgreaterindividualfitnessarepredictedtoin- notonlythroughtheirdirectimpactontheirown ous studies have examined whether certain life creaseinfrequency,leadingtoanincreaseinmean transmission but also through their indirect im- historiescouldrescueHamilton’shaplodiploidy fitness.This“fundamentaltheoremofnaturalse- pactonthetransmissionofcopiespresentinother hypothesisbymakingtheaveragerelatednessto lection”wasintendedtocapturetheprocess(nat- individuals.Consequently,altruisticbehaviorscan siblings r > 0.5, but none appears generally uralselection)andthepurpose(maximizationof befavoredifthebenefitsaredirectedtowardother applicable (SOM text). In contrast, others have individualfitness)ofadaptation. individualswhosharegenesforaltruism(Fig.2). arguedthatwhatisspecialaboutthehymenop- ThisisencapsulatedbyHamilton’srule(3),which terans is that their natural history leads to a Altruism, Spite,and Inclusive Fitness statesthatatraitwillbefavoredbyselectionwhen relativelyhighbenefitofhelping(highb/cratio), Inthe1960s,Hamilton(3,4)realizedthatmaxi- rb–c>0,wherecisthefitnesscosttotheactor,b such as advanced parental care and a powerful mization of individual fitness could not explain isthefitnessbenefittotherecipient,andristheir stingthatfacilitatesgroupdefense(12). geneticrelatedness.ThisformofHamilton’srule DepartmentofZoology,OxfordUniversity,SouthParksRoad, emphasizesinteractionsbetweentwoindividuals, TheMonogamy Hypothesis OxfordOX13PS,UK. but it can be extended to allow for interactions Recent work (8, 13) has suggested a possible *To whom correspondence should be addressed. E-mail: withmultipleindividuals[supportingonlinemate- resolutiontothisdebate,arguingthatstrictlife- [email protected] (S.A.W); [email protected]. ac.uk(A.G.) rial(SOM)textandtableS1]. timemonogamy,inwhichfemalesonlymatewith www.sciencemag.org SCIENCE VOL327 12 MARCH 2010 1341 REVIEW tosiblings(r>0.5)hasbeenaredherring;whatis A Altruism B Reciprocity keyisthataveragerelatednessstaysat0.5.Other redherringsincludethepossibilityforeusociality Relative to have evolved via cooperation between sisters Help Help Relative (theparasocialroute)becausethatwouldleadto Actor or non- Actor Help relative r<0.5(8)andthesuggestionthathighrelat- edness is a consequence rather than a cause of eusociality(15),inwhichcasetheobservedcor- Nonrelative Not altruism! relationwithmonogamywouldnotbepredicted (9). Finally, the monogamy hypothesis suggests C Spite D Greenbeard thatfactorsthatfacilitatemonogamy,suchaslife- timestorageofspermbyfemales,arealsoimpor- tantinexplainingthedistributionofeusociality. Relative Bearded Help GettheRight Spite Benefit Actor or Benefit Actor Inclusive-fitness theory explains altruism but Harm Harm alsohasadarkerside.Spitefultraits,whichare harmful to both actor and recipient, may be Nonrelative Nonbearded favored (4). Considering the classic two-party 0 1 versionofHamilton’srule,ifcispositive(which 0 dFiirge.ct2ed.Mtoewcahradnrisemlastifvoers.a(lBtr)uRisemci,psrpoictiet,yainsdfarveocriepdrowcihtey.n(Ait)mAaltkreusistmhecaacntobremfaovroerleikdeilfyittoisrepcreeifveerehnetlipalilny icsosctolysttloytthoertheceipaicetnotr)),,thanendrbb–iscn>e0gactaivnebe(wsahtiicsfhieids 1, 2 1 thefuture.Reciprocityreliesuponafuturedirectfitnessbenefitforcooperationandsoisnotaltruistic.(C) ifrelatedness(r)isnegative. Negative relatedness h Spitecanbe favoredif it is preferentiallydirectedtowardrelativelyunrelatedindividuals,whoseloss c mayseemabizarreconcept,butitsimplymeans r improves the fitness of relatives. (D) Greenbeards are favored by directing altruism toward fellow a thattherecipientislessrelatedtotheactorthanisan M greenbeardindividualsorspitetowardnonbeardedindividuals. averagememberofthepopulation(SOMtext). n o Another way to think about spite is to dis- g onemaleintheirentirelife,iscrucialfortheevo- already lost the ability to mate and realize full tinguish between the primary recipient of the or lution of eusociality. Monogamy leads to a reproductive potential (9). Furthermore, these harming behavior (the individual physically g. a potential worker being equally related (r = 0.5) specieshavehadthetimetoevolvedivisionof attacked) and those secondarily influenced as a m toherownoffspringandtotheoffspringofher labor and specialized helping behaviors, giving byproduct of this (those experiencing reduced e c mother(siblings).Inthiscase,anysmallefficiency asubstantialb/c. competitionfromtheharmedindividual)(16,17). n e benefit for rearing siblings over their own off- Thebeautyofthemonogamyhypothesisisthat Fromthisperspective,spitecanbefavoredifthe ci s spring(b/c>1)willfavoreusociality(Fig.3B). itsimplifiesourunderstandingofhoweusociality actorismorerelatedtothesecondaryrecipients w. Incontrast,evenalowprobabilityofmultiple evolved,emphasizingthattheinteractionbetween (whobenefit)thantotheprimaryrecipients(who w mating means that potential workers would be kinshipandecologyisfundamentalandthatthey areharmed).Spitecanthereforebethoughtofas w morerelatedtotheirownoffspring.Inthiscase, are not competing explanations (8, 13). For altruismtowardthesecondaryrecipients:Harm- m o costly helping would require a significant effi- example,thesearchforhowtoincreaserelatedness inganindividualcanbefavoredifthisprovidesa r ciency advantage to rearing siblings over own d f e offspring(Fig.3C).Untilgrouplivingisestab- d A B C a lished,allowingtheevolutionofspecializedco- Haplodiploidy Monogamy Polyandry o operativebehavioranddivisionoflabor,theratio hypothesis nl Offspring Siblings Offspring Siblings Offspring Siblings w b/ccannotbeexpectedtogreatlyexceed1.For r= 0.5 r> 0.5 r= 0.5 r= 0.5 r= 0.5 r < 0.5 o D example,feedingasiblingisunlikelytobehugely morebeneficialthanfeedinganoffspringbythe same amount. Consequently, in the absence of strictmonogamythepopulationcannotevenget startedontheroadtoeusociality. In support of this hypothesis, comparative studieshavefoundmonogamytobetheancestral D E F stateinalltheindependentoriginsofeusociality studied(9,14).Monogamyoriginatedfirst,giving ahighrelatedness,andthenwhenecologicalcon- ditionsledtoahighenoughb/c,eusocialityevolved (SOMtext).Importantecologicalconditionsin- clude“lifeinsurance”benefitsofallowinghelpers to complete parental care after the death of the Fig. 3. Monogamypavesthewaytoeusociality.(A)Thehaplodiploidyhypothesisreliesonindividuals mother(forexample,ants,bees,andwasps),and beingmorerelatedtosiblingsthanoffspring,makingsiblingsworthmorethanoffspring.Asoriginally “fortressdefense”benefitsofremainingtohelpuse envisioned,thisappearstohavebeenaredherring.(B)Themonogamyhypothesisemphasizesthatifan or defend a food source, when opportunities for individualisequallyrelatedtoitssiblingsanditsoffspring,evenaveryslightefficiencybenefitforraising successfulmigrationarelow(forexample,aphids, siblingstranslatesintoaselectiveadvantageforhelping.(C)Withoutstrictmonogamy,individualsaremore beetles,termites,thrips,andshrimps)(12,14). relatedtotheiroffspringthantheyaretotheirsiblingssothatalargeefficiencybenefitisrequiredinorder There are some eusocial species in which forsibling-rearingtobefavored.(D)SterileworkerscaringforbroodintheantCamponotusherculeanus. queensmatemultiply.However,thisisaderived (E)AlifetimemonogamouspairfromthetermiteReticulitermesflavipes.(F)Nonbreedingworkersinthe condition that has evolved after workers have shrimpSynalpheusregalis.[PhotosprovidedbyDavidNash,BarbaraThorne,andEmmettDuffy] 1342 12MARCH 2010 VOL327 SCIENCE www.sciencemag.org REVIEW benefittocloserrelatives(Fig.2C). toconspecificsthatlackanimmu- Table1.Notspite:examplesoftraitsthathavebeensuggestedasspiteful Thesetwodifferentencapsulations nitygene(22).Insomecases,cell but actually provide a direct benefit to the actor and hence are selfish ofspitearedifferentwaysoflook- death is required to release the (table S2). ingatthesamething,usingeithera bacteriocins into the environment, two-orthree-partyHamilton’srule Taxa Suggestedspitefultraits Whyselfish,notspiteful and so it is clearly a costly trait (SOMtext)(16,17).Iftheactoris (positive c). In addition, there is Birds Protectionofterritories, Decreasedcompetitionfor morecloselyrelatedtothesecond- geneticlinkagebetweenthebacte- siblicideatneighboring resources,forselfor aryrecipientsthantheprimaryre- riocin production and immunity nests. offspring cipients in a three-party rule, then genes so that close relatives both Fish Eggcannibalism Decreasedcompetitionfor thisleadstoanegativerelatedness produce and are immune to a resources,foroffspring inthetwo-partyrule. particular bacteriocin (22). Conse- Humans Punishmentandrejectionof Leadstoincreased Althoughmanybehaviorshave quently,thereleaseofbacteriocins lowoffersineconomic cooperationinthelongterm beensuggestedasspiteful,theyare killsnonrelatives,freeingupresources games usuallyexplainedasselfishbehav- forclone-mates.Experimentalwork Mammals Infanticide,harassmentof Decreasedcompetition,for iorsthatarecostlytotherecipient onbacteriocins has alsosupported nondescendantjuveniles offspringormates butprovideabenefittotheactor(c< the prediction that the relative ad- andinjuredmales 0)(Table1).Thisbenefitisoftena vantageofspiteisgreaterwhenvar- reductioninfuturecompetitionfor ianceinrelatednessishigher(giving resources, for the actor or their offspring, with sterilesoldiercasteinpolyembryonicparasitoid anintermediatemeanrelatedness)becausethis 0 1 confusion arising because the direct fitness waspssatisfiesalltheseconditions(17).Females leads to interactions with both close relatives 0 cteornmseaqnudenncoetsowveerrethoenlilfyetcimonesiodfetrheedainctothre(SsOhoMrt laafyterthweihricehggthseownathspeeeggggssdoifvimdeotahsecxautearlplyillaanrsd, alantdednnoenssretloatitvhees,seaclloonwdianrgyaberenleaftiicviealryiehsig(Fhiegr.r4e)- 1, 2 1 text)(18).Whatmattersfornaturalselectionare consumethegrowingcaterpillarfromtheinside (21,23). h c fitnessconsequencesovertheentirelifetimeand (20). Although most larvae develop normally, a r a notsomearbitraryperiod.Forexample,herring fractionbecomeasoldiermorph.Developingasa Spiteful Words M gullskillthechicksatneighboringnests,butthis soldieriscostlytotheactor,becausethesoldiersare As discussed above, spite can be considered a n o reducesthefuturecompetitionoverresourcesfor sterile, and costly to the recipient, because the formofaltruism.Consequently,itisusefultoask g both themselves and their offspring. Further- soldiers seek out and kill other larvae within the whetherwegainanythingbydistinguishingspite or more, there is no evidence that such examples host. Finally, soldiers preferentially kill larvae to from altruism. At one level, it can be useful to g. a involveasufficientsecondarybenefittorelatives. which they are less related (those that have emphasizethesimilarities,thatbotharefavored m Indeed, it has even been suggested that the developedfromothereggs),freeingupresources becausetheyleadtoanincreaseintheinclusive e c conditions required are so restrictive that spite fortheirclone-mates. fitnessoftheactorthroughindirectfitnesscon- n e wouldberareornonexistent(11,12). Another example of spite is provided by sequences.Thiswillalsohelpavoiddebatesover ci s However, recent theory has shown that a the production of antimicrobial bacteriocins by whether certain traits should be classed as al- w. positive relatedness to secondary recipients can manybacteria(21).Thesecompoundsarelethal truismor spite because the mathematics of any w beobtainedmoreeasilythanpreviouslythought, w suggesting that at least from a theoretical m o perspective spite is plausible (19) if there is (i) A B 4.0 r lpbaeerhtgiateovrisov;rasr(iiaia)nimckeeindindaitsrceirlniamdteiivdninadetuisoasnls,btweotiwthweehhnoamrcmoitmnhge- efficient Spite Altruism efficient 23..00 oaded f actor is relatively unrelated (making the actor n co n co 1.0 wnl relatively more related to the secondary recip- o o o ients); or (iii) strong local competition so that ecti ecti 0.0 D harming the primary recipient provides appre- Sel Sel ciable benefits to secondary recipients. When -1.0 0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0 theseconditionsaremet,spitefulbehaviorscan Kinship Kinship be favored so as to reduce competition for rel- C D atives. Consider the extreme example of when twogeneticallyidentical(clonal)individualsare competingwithanonrelativetowhomtheyare unrelated. One of the clone-mates could be selected to harm the nonrelative, at a cost to itself, if this harming reduces the nonrelative’s ability to compete for resources and hence benefitstheotherclone-mate. RealSpite Todemonstratespite,itmustbeshownthatatrait Fig. 4. Populationstructure,altruism,andspite.(A)Theorypredictsthatasrelatednesswithinapatch iscostlytotheactor(positivec)andcostlytothe increases,thereisanincreaseinaltruistictraitsandadomedrelationshipwithspitefultraits(3,15).(B)As recipient (negative b). In addition, for spite to predicted, the relative benefit of bacteriocin production inPseudomonas aeruginosa shows a domed haveevolvedbymeansofnaturalselection,the relationshipwithrelatedness(23)(C)Altruism:afruitingbodyoftheslimemoldDictyosteliumdiscoideum. actor must be more closely related to the sec- (D)Spite:Apieceoffilterpapersoakedwithabacteriocin(leftspot)causesaninhibitionzonewherebacteria ondary recipients (beneficiaries) than to the cannotgrow,inthesamewayasatraditionalantibiotic(rightspot;bottomspotshowsbothincombination). primaryrecipientthattheyharm(Fig.2C).The [PhotosprovidedbyOwenGilbert,MargaretRiley,andSaraCody] www.sciencemag.org SCIENCE VOL327 12 MARCH 2010 1343 REVIEW casecanberearrangedsoastomakeaspitefulor wouldnotoccurinnaturebecausetheycouldbe biology. Theoretical work on spite and green- altruistictwo-partyrule(16,17). easily invaded by “falsebeards” (cheats) that beards was spurred by biological examples but However,therearealsoanumberofreasons displayedthebeardwithoutalsoperformingthe thenledtoaunifyingframeworkthatilluminated whyitisusefultodistinguishspitefromaltruism behavior(27). detectionproblemsandsuggestedwheretolook (17). From a behavioral perspective, there is a Thisassumptionhasbeenoverturnedbythe forfurtherexamples.Alloftheseexamplesillus- clear difference between helping and harming. discoveryofanumberofaltruisticgreenbeards. tratethatthedistinctionbetweengenetics(r)and Additionally, there are biologically interesting In the slime mold Dictyostelium discoideum, ecology (b/c) is both artificial and unhelpful. differences between altruism and spite. For ex- individuals with the csa gene adhere to each What really matters is how they interact, as has ample,localcompetitionforresourcestypically other in aggregation streams and cooperatively alwaysbeenemphasizedbyHamilton’srule. selects for spite and against altruism (21); formfruitingbodieswhileexcludingnoncarriers altruistic traits are predicted to show a positive of the gene (5). Other examples have been ReferencesandNotes relationshipwithrelatedness(3),whereasspite- foundinyeast,abacterialplantpathogen,anda 1. C.Darwin,OntheOriginofSpeciesbyMeansofNatural Selection,or,thePreservationofFavouredRacesinthe fultraitsarepredictedtoshowadomedrelation- lizard (SOM text). In addition, spiteful green- StruggleforLife(JohnMurray,London,UK,1859). ship(Fig.4)(19,21);andkindiscriminationis beardshavebeendiscovered,includingtheGp-9 2. R.A.Fisher,TheGeneticalTheoryofNaturalSelection key in the examples of spite, whereas altruism gene of the fire ant Solenopsis invicta (29). (Clarendon,Oxford,1930). canoftenevolvewithoutkindiscriminationwhen Workerswiththeballeleatthislocususeodor 3. W.D.Hamilton,J.Theor.Biol.7,1(1964). limiteddispersalkeepsrelativestogether(3). todeterminewhetherprospectivequeensalsocarry 4. W.D.Hamilton,Nature228,1218(1970). 5. D.C.Queller,E.Ponte,S.Bozzaro,J.E.Strassmann, Spitecanalsobedefinedfromamechanistic this allele, dismembering them if they do not. Science299,105(2003). or psychological perspective in primates and Another example is provided by bacteriocin 6. A.Grafen,J.Evol.Biol.20,1243(2007). 0 humansasabehaviorthatharmsanotherorarises production,inwhichthebacteriocin-encodinggene 7. A.Gardner,Biol.Lett.5,861(2009). 01 cfraosmes,ahdaermsirinegtoishlaikrmelyatnoobtheefra(v2o4r,ed25b)e.cIanutsheeosen andTthheeoirmetmicuanlitwyogreknehaarsetcilgahrtilfyiedlinkwehden(22w).e 8. J3.6J4.,B3o1om91sm(2a0,0P9h)i.los.Trans.R.Soc.Lond.BBiol.Sci. 1, 2 9. W.O.H.Hughes,B.P.Oldroyd,M.Beekman, 1 averageit providesadirectbenefittotheactor wouldexpectgreenbeardstooccur(30).Green- F.L.W.Ratnieks,Science320,1213(2008). h c (c<0)andisselfish,notspiteful.Itiscrucialnot beardscanbecategorizedintofourgroups,with 10. R.L.Trivers,H.Hare,Science191,249(1976). r a tomixdefinitionsofspitebyraisingtheproblem different evolutionary dynamics, according to 11. R.Craig,Evolution33,319(1979). M andrarityofevolutionaryspitethengoingonto whether they are altruistic (helping) or spiteful 12. J.E.Strassmann,D.C.Queller,Proc.Natl.Acad.Sci.U.S.A. n 104(suppl1),8619(2007). o examineaharmingbehaviorthatprovidesadirect (harming) and always expressed (obligate; for 13. J.J.Boomsma,Curr.Biol.17,R673(2007). g benefit to the actor, and therefore is not evolu- example, bacteriocins) or only expressed in 14. J.E.Duffy,K.S.Macdonald,Proc.Biol.Sci.277,575(2010). or tionaryspiteful.Thespecificconditionsrequired response to the presence of the greenbeard in 15. E.O.Wilson,B.Hölldobler,Proc.Natl.Acad.Sci.U.S.A. g. 102,13367(2005). a to favor evolutionary spite might make it rela- others (facultative; for example,Gp-9). For all m 16. L.Lehmann,K.Bargum,M.Reuter,J.Evol.Biol.19, tivelyunlikelyinhumansandotherprimates.In- casesexceptthefacultativealtruisticgreenbeard, e 1507(2006). c deed, spite may be rare in general because it is the greenbeard is selected against at low 17. A.Gardner,I.C.W.Hardy,P.D.Taylor,S.A.West,Am. n e hardtoobtainsituationsinwhichpopulationsare frequencies and only favored when it has Nat.169,519(2007). ci structuredsothatharmingnonrelativesisanef- establisheditselftoacertainfrequency.Popula- 18. FKe.nRn..F3o8st,e2r,2T9.(W20en0s1e)l.eers,F.L.W.Ratnieks,Ann.Zool. w.s ficientwayofhelpingrelatives. tionstructurecansolvethisproblembykeeping 19. A.Gardner,S.A.West,J.Evol.Biol.17,1195(2004). w individuals with greenbeards together. The best 20. D.Giron,D.W.Dunn,I.C.W.Hardy,M.R.Strand, w Greenbeards place to look for new greenbeards may be in Nature430,676(2004). m Hamilton(3,26)pointedoutthatindirect-fitness microbes, in which asexual growth can lead to 21. A.Gardner,S.A.West,A.Buckling,Proc.Biol.Sci.271, ro benefits require genetic relatedness per se and extreme population structuring; the relatively 1529(2004). d f 22. M.A.Riley,J.E.Wertz,Annu.Rev.Microbiol.56,117(2002). e not kinship. Imagine a gene (or cluster of simple link between genotype and phenotype 23. R.F.Inglis,A.Gardner,P.Cornelis,A.Buckling,Proc. d a tightly-linked genes) that gives rise to a con- may prevent a decoupling of beard and social Natl.Acad.Sci.U.S.A.106,5703(2009). o spicuous phenotype, uses this phenotype to trait (falsebeards), and genetic knockouts facil- 24. M.Hauser,K.McAuliffe,P.R.Blake,Philos.Trans.R.Soc. nl w Lond.BBiol.Sci.364,3255(2009). discriminate between carriers and noncarriers itatethedetectionofgreenbeards(30). o 25. K.Jensen,J.Call,M.Tomasello,Proc.Natl.Acad.Sci.U.S.A. D ofthegene,andleadstocostlyhelpingtoward Somemodelsforaltruisminhumans(31–34) 104,13046(2007). other carriers of the gene (Fig. 2D). This gene and social insects (15) implicitly invoke green- 26. W.D.Hamilton,inBiosocialAnthropology,R.Fox,Ed. could be favored by natural selection, even if beard mechanisms without realizing this, such (Wiley,NewYork,1975),pp.133–155. 27. R.Dawkins,TheSelfishGene(OxfordUniv.Press,Oxford, carrierssharenoothergenesincommon.Thus, asthesuggestionthataltruisticindividualsdiffer 1976). the crucial requirement for altruism is genetic from individuals whoare not altruisticinsome 28. L.Lehmann,L.Keller,J.Evol.Biol.19,1365(2006). relatednessatthealtruismlocusandnotgenea- observable characteristic [such as being more 29. L.Keller,K.G.Ross,Nature394,573(1998). logicalrelationshipoverthewholegenome. likelytosmileandlaugh(31,32)]ormodelsof 30. A.Gardner,S.A.West,Evolution64,25(2010). Dawkinsproposedthehypotheticalexample “strongreciprocity”thatassumepunishmentand 31. R.H.Frank,Am.Econ.Rev.77,593(1987). 32. M.J.Owren,J.-A.Bachorowski,inEmotions:Current ofagenethatgivesrisetoagreenbeardwhile altruismtobegeneticallylinked(33,34).How- IssuesandFutureDirections,T.J.Mayne,G.A.Bonanno, simultaneously prompting individuals with ever,thereisnoreasontosuspectthattraitssuch Eds.(Guilford,NewYork,2001),pp.152–191. greenbeardstodirectcooperationtowardother assmilingorpunishmentwillbeencodedbythe 33. H.Gintis,J.Theor.Biol.206,169(2000). green-bearded individuals (27). However, this samegeneorcloselylinkedgenesasthosethat 34. S.Bowles,H.Gintis,Theor.Popul.Biol.65,17(2004). 35. G.R.Price,Nature227,520(1970). “greenbeard”mechanismcanalsooccurwithout leadtoaltruism.Consequently,falsebeardscould 36. WethankJ.Alpedrinha,K.Boomsma,A.Griffin, avisibletag.Whatisrequiredmoregenerallyis arise,andtheseproposedexplanationsforaltruism M.Hauser,K.Jensen,L.KellerandP.Taylorfor a single gene (or a number of tightly-linked wouldnotbeevolutionarilystable(30). commentsandtheRoyalSociety,EuropeanResearch genes) encoding both the cooperative behavior Council,andLeverhulmeTrustforfunding. and causing cooperators to associate (26, 28). Conclusions SupportingOnlineMaterial Greenbeards are oneof the twoways in which Aunifyingthemeinalltheissuesthatwehave www.sciencemag.org/cgi/content/full/327/5971/1341/DC1 natural selection can favor altruistic behavior, discussedhereistheimportanceoftheinterplay SOMText withtheotherbeinginteractionswithgenealog- between theory and data. The monogamy hy- TablesS1andS2 ical kin (3). However, despite this fundamental pothesiscutsthroughthesuperfluousdetailsby References position it has been assumed that greenbeards focusing on a key aspect of the underlying 10.1126/science.1178332 1344 12MARCH 2010 VOL327 SCIENCE www.sciencemag.org www.sciencemag.org/cgi/content/full/327/5971/1341/DC1 Supporting Online Material for Altruism, Spite, and Greenbeards Stuart A. West* and Andy Gardner* *To whom correspondence should be addressed. E-mail: [email protected] (S.A.W); [email protected] (A.G.) Published 12 March 2010, Science 327, 1341 (2010) DOI: 10.1126/science.1178332 This PDF file includes: SOM Text Tables S1 and S2 References Supporting Online Material for ‘Altruism, Spite and Greenbeards’, by Stuart A. West & Andy Gardner ! #$!%&’(!()*%’+$!,)!)-./$0!’$!12)/%)2!0)%/’3!4.+$!()5)2/3!’((4)(!,)!/002)((!’$!%&)!6/’$! %)-%7!*3/2’89’$1!3’$:(!,’%&!%&)!)-’(%’$1!3’%)2/%42)!6+2)!1)$)2/339;! ! Hamilton’s rule! </6’3%+$=(!243)!>1, 2?!’(!4(4/339!,2’%%)$!/(!rb @!c!A!B7!+2!’$!(+6)!)C4’5/3)$%!8+267! ,&’*&!)6.&/(’D)(!/!8’%$)((!’$%)2/*%’+$!E)%,))$!/!(’$13)!/*%+2!>,&+!(488)2(!/!8’%$)((! 0)*2)6)$%!c?!/$0!/!(’$13)!2)*’.’)$%!>,&+!1/’$(!/!8’%$)((!’$*2)6)$%!b?;!<+,)5)27!/*%’+$(! ,’33!%9.’*/339!&/5)!8’%$)((!*+$()C4)$*)(!8+2!6+2)!%&/$!+$)!2)*’.’)$%7!(+!6+2)!1)$)2/339! ,)!*/$!,2’%)!! !r b!@!c!A!B7!,&)2)!I!’(!%&)!()%!+8!/33!’$0’5’04/3(!>)-*340’$1!%&)!/*%+2?! i!I i i ,&+()!8’%$)((!’(!/88)*%)0!E9!%&)!/*%’+$!>b!"!B?!/$0!,&+!/2)!.+(’%’5)39!+2!$)1/%’5)39! i 2)3/%)0!%+!%&)!/*%+2!>r!"!B?7!/$0!r!/$0!b!/2)!%&)!2)3/%)0$)((!/$0!8’%$)((!’$*2)6)$%7! i i i 2)(.)*%’5)397!*+22)(.+$0’$1!%+!%&)!i%&!2)*’.’)$%;!F9.’*/3397!*+(%(!/$0!E)$)8’%(!/2)!82/6)0!’$! /E(+34%)! >(425’5’$1! +88(.2’$1?! +2! 2)3/%’5)! >(&/2)! +8! .+.43/%’+$! 2).2+04*%’5)! 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A!B!)-/*%39!.2)0’*%!%&)!0’2)*%’+$!+8!*&/$1)!’$!1)$)!82)C4)$*’)(N!#%!0+)(!(+!,&)$!%&)! /*%’+$!&/(!/!(’$13)!.2’6/29!2)*’.’)$%!%+!,&’*&!%&)!/*%+2!’(!.+(’%’5)39!+2!$)1/%’5)39!2)3/%)07! /$0!,&)$!()*+$0/29!2)*’.’)$%(!/2)!)’%&)2!/E()$%!+2!4$2)3/%)0!%+!%&)!/*%+2;!#$!/$!’$8’$’%)! .+.43/%’+$7!,’%&!)’%&)2!$+!+2!13+E/3!2)143/%’+$!+8!0)$(’%9!in response to the social action7! ()*+$0/29!8’%$)((!*+$()C4)$*)(!/2)!)’%&)2!/E()$%!+2!(&/2)0!/6+$1!’$0’5’04/3(!,&+()! 2)3/%)0$)((!%+!%&)!/*%+2!’(!D)2+;!#$!/!8’$’%)!.+.43/%’+$7!%&)!(+*’/3!/*%’+$!+$39!1’5)(!/!$)%! ()*+$0/29!’$0’2)*%!8’%$)((!)88)*%!+8!D)2+!’8!%&)2)!’(!$+!0)$(’%9!2)143/%’+$!)88)*%!8+2!+%&)2! ’$0’5’04/3(;!F&’(!’(!E)*/4()!%&)!()*+$0/29!2)*’.’)$%(!,’33!1)$)2/339!$+%!&/5)!/$!/5)2/1)! 2)3/%)0$)((! +8! D)2+! %+! %&)! /*%+2;! O-*).%’+$/3! */()(! )-’(%! ’$! .2’$*’.3)I! ,&)2)! 0)$(’%9! 2)143/%’+$!8/33(!4$)5)$39!+$!%&)!+%&)2!’$0’5’04/3(!’$!%&)!.+.43/%’+$7!/$0!’$!/!*+$%2’5)0! ,/9!’$!2)3/%’+$!%+!%&)’2!2)3/%)0$)((!%+!%&)!/*%+27!(+!/(!%+!1’5)!/!()*+$0/29!’$0’2)*%!8’%$)((! )88)*%!+8!)-/*%39!D)2+J!+2!)3()7!(3’1&%39!6+2)!.3/4(’E397!,&)2)!%&)!2)*’.’)$%!’(!2)3/%)0!%+!%&)! /*%+2!E9!r!P!M"7!(+!%&)!2)6/’$0)2!+8!%&)!.+.43/%’+$!’(!2)3/%)0!%+!%&)!/*%+27!+$!/5)2/1)7!E9! D)2+;! G+%)! %&/%7! ’8! ,)! *&++()! %+! 6)/(42)! *+(%(! /$0! E)$)8’%(! ’$! 2)3/%’5)M8’%$)((! +2! 2).2+04*%’5)M5/34)!%)26(7!%&)$!0)$(’%9!2)143/%’+$!’(!4$/5+’0/E3)!/(7!8+2!+$)!’$0’5’04/3!%+! 1/’$7!+%&)2!’$0’5’04/3(!64(%!3+()7!/$0!vice versa;!F&)()!*+$(’0)2/%’+$(!2)5)/3!%&/%7!’$!5)29! 6/$9! */()(7! %&)! ’$0’2)*%! 8’%$)((! )88)*%(! +8! (+*’/3! /*%’+$(! +,’$1! %+! %&)’2! ’6./*%! +$! ()*+$0/29! 2)*’.’)$%(! */$$+%! E)! ’1$+2)07! /$0! %,+M./2%9! </6’3%+$=(! 243)(! ,’33! E)! %&)! )-*).%’+$!2/%&)2!%&/$!%&)!243);! ! " ! 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The monogamy hypothesis Y++6(6/!>19, 20?!,/(!$+%!%&)!8’2(%!%+!&’1&3’1&%!%&)!(’1$’8’*/$*)!+8!6+$+1/697! E4%! %&)! 6)2’%! +8! &’(! 2)8+2643/%’+$! +8! %&’(! ’0)/! ,’%&! )-.3’*’%! )6.&/(’(! +$! 3’8)M%’6)! 6+$+1/69!’(!%&/%!’%!*/$!E)!)-.3/’$(!%&)!)5+34%’+$!+8!.)26/$)$%!)4(+*’/3’%9!’$!5)29!(’6.3)! %)26(;!<’(%+2’*/3!0)%/’3(!*/$!E)!8+4$0!’$!Y++6(6/=(!>19, 20?!./.)2(;! ! The ecological correlates of cooperation and eusociality ! U!$46E)2!+8!(%40’)(!&/5)!)-/6’$)0!%&)!)*+3+1’*/3!*+22)3/%)(!+8!*++.)2/%’+$!/$0! )4(+*’/3’%9;! ! K #$! %&)! )4(+*’/3! ’$()*%(! ’%! &/(! E))$! (411)(%)0! %&/%! )*+3+1’*/3! /05/$%/1)(! +8! *++.)2/%’+$! /$0! )4(+*’/3’%9! /2’()! 82+6! %,+! 8/*%+2(! >21, 22?;! V’2(%7! %&)2)! */$! E)! /! (4E(%/$%’/3!E)$)8’%!%+!(%/9’$1!/%!%&)!$/%/3!$)(%!/$0!&)3.’$1!0)8)$0!/!5/34/E3)!2)(+42*);! 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Social behaviours and intentional language! V2+6!/$!)5+34%’+$/29!.)2(.)*%’5)!/!%2/’%!+2!E)&/5’+2!’(!(+*’/3!’8!’%!&/(!8’%$)((! *+$()C4)$*)(!8+2!E+%&!%&)!’$0’5’04/3!%&/%!.)28+26(!%&/%!E)&/5’+2!>%&)!/*%+2?!/$0!/$+%&)2! ’$0’5’04/3!>%&)!2)*’.’)$%?;!</6’3%+$!>2?!*3/((’8’)0!(+*’/3!E)&/5’+2(!/**+20’$1!%+!,&)%&)2! %&)!*+$()C4)$*)(!%&)9!)$%/’3!8+2!%&)!/*%+2!/$0!2)*’.’)$%!/2)!E)$)8’*’/3!>’$*2)/()!0’2)*%! 8’%$)((?!+2!*+(%39!>0)*2)/()!0’2)*%!8’%$)((?!>F/E3)!]‘W"?;! ! L F&)! /0/.%/%’+$’(%! /..2+/*&! .2+5’0)(! %&)! 8+26/3! ^4(%’8’*/%’+$! 8+2! %&)! 4()! +8! ’$%)$%’+$/3! 3/$14/1)7! (4*&! /(! /3%24’(6! /$0! (.’%)! >32?;! ].)*’8’*/3397! %&)! 09$/6’*(! +8! $/%42/3!()3)*%’+$!3)/0(!%+!’$0’5’04/3!+21/$’(6(!%&/%!E)&/5)!/(!8’%$)((!6/-’6’D’$1!/1)$%(7! /$0!&)$*)!E)&/5)!/(!’8!%&)9!&/5)!’$%)$%’+$!+2!.42.+()!/%!%&)!’$0’5’04/3!3)5)3;!#$%)$%’+$/3! %)26(!0+!$+%!.2+5’0)!/!(4.)28’*’/3!13+((7!E4%!2/%&)2!*+$5)9!’6.+2%/$%!’$8+26/%’+$!/E+4%! 1)$)! 82)C4)$*9! 09$/6’*(;! #$! ./2%’*43/27! %&)! 6/-’6’D’$1! /1)$%! /$/3+19! &/(! E))$! 8+26/3’D)0!,’%&!2)(.)*%!%+!/$!’$0’5’04/3=(!3’8)%’6)!2).2+04*%’5)!(4**)((!@!$+%!8+2!^4(%! (+6)!/(.)*%!+8!8’%$)((!>);1;!8)*4$0’%9?!+2!+5)2!(+6)!3’6’%)0!%’6)!(*/3)!+2!2)3/%’5)!%+!(+6)! (4E()%!+2!12+4.!+8!%&)!.+.43/%’+$;! U3%)2$/%’5)! )5+34%’+$/29! 0)8’$’%’+$(! +8! %)26(! (4*&! /(! /3%24’(6! E+%&! */4()! *+$84(’+$! /$0! 3/*:! /! 8+26/3! ^4(%’8’*/%’+$! >33?;! V+2! )-/6.3)7! %&)! 4()! +8! \2)*’.2+*/3! /3%24’(6=!0)8’$)(!/3%24’(6!+5)2!%&)!(&+2%M%)26!8’%$)((!*+$()C4)$*)(;!<+,)5)27!$/%42/3! ()3)*%’+$!+.)2/%)(!+$!3’8)%’6)!8’%$)((!*+$()C4)$*)(7!$+%!+5)2!(+6)!/2E’%2/29!(&+2%M%)26;! H)*’.2+*/3!/3%24’(6!’(!$+%!/*%4/339!/3%24’(%’*!>V’1;!K?7!/$0!(+!E)%%)2!%)26)0!2)*’.2+*’%9=! >33?;!F+!1’5)!/$+%&)2!)-/6.3)7!%&)!12+4.!()3)*%’+$!3’%)2/%42)!0)8’$)(!/3%24’(6!2)3/%’5)!%+! %&)!8’%$)((!+8!+%&)2!’$0’5’04/3(!’$!%&)!12+4.!>34?;!<+,)5)27!$/%42/3!()3)*%’+$!+.)2/%)(!+$! 8’%$)((!2)3/%’5)!%+!%&)!.+.43/%’+$7!$+%!(+6)!/2E’%2/29!82/*%’+$!+8!’%;!F&)()!/$0!+%&)2! )-/6.3)(!/2)!0’(*4(()0!’$!12)/%)2!0)%/’3!’$!%&)!8+33+,’$1!()*%’+$;! O88)*%!+$!/*%+2! O88)*%!+$!2)*’.’)$%! ! b! M! b! W4%4/339!E)$)8’*’/3! ])38’(&! M! U3%24’(%’*! ].’%)843! Table SOM1. Social Behaviors. U$! )5+34%’+$/29! *3/((’8’*/%’+$! (*&)6)! 8+2! (+*’/3! E)&/5’+2(!%&/%!&/5)!E))$!()3)*%)0!8+2!E9!$/%42/3!()3)*%’+$!>2, 33?;!O88)*%(!/2)!6)/(42)0!’$! %)26(!+8!3’8)%’6)!)88)*%(!+$!0’2)*%!8’%$)((;!<)3.’$1!E)&/5’+2(!/2)!b!%+!%&)!2)*’.’)$%7!/$0! */$!E)!64%4/339!E)$)8’*’/3!+2!/3%24’(%’*;!</26’$1!E)&/5’+2(!/2)!@!%+!%&)!2)*’.’)$%!/$0!*/$! E)!()38’(&!+2!(.’%)843;!T++.)2/%’+$!’(!0)8’$)0!/(!/!&)3.’$1!E)&/5’+2!%&/%!&/(!)5+35)0!/%! 3)/(%!./2%’/339!04)!%+!%&)!)88)*%!+$!%&)!2)*’.’)$%!@!%&’(!’$*340)(!/33!/3%24’(%’*!E)&/5’+2(!/$0! (+6)! 64%4/339! E)$)8’*’/3! E)&/5’+2(! >33?;! W+(%! (+*’/3! E)&/5’+2(! ,’33! &/5)! 8’%$)((! *+$()C4)$*)(!8+2!%&2))!+2!6+2)!’$0’5’04/3(7!(+!,)!6/9!(/9!%&/%!/!E)&/5’+2!’(!/3%24’(%’*!’$! 2)3/%’+$!%+!’6./*%!4.+$!+$)!2)*’.’)$%7!/$0!(.’%)843!’$!2)3/%’+$!%+!’%(!’6./*%!4.+$!/$+%&)2! 2)*’.’)$%;!#%!’(!2)/(+$/E3)!%+!%)26!(4*&!/!E)&/5’+2!/(!/3%24’(6!’8!%&)!.2’6/29!2)*’.’)$%!’(! %&)!E)$)8’*’/297!/$0!(.’%)!’8!%&)!.2’6/29!2)*’.’)$%!’(!%&)!5’*%’6; Not altruism F)26(! (4*&! /(! /3%24’(6! &/5)! 5)29! (.)*’8’*! 6)/$’$1(7! ,&’*&! *+$5)9! 4()843! ’$8+26/%’+$;!#8!%&)()!%)26(!/2)!6’(4()07!+2!2)0)8’$)07!%&)!2)(43%!’(!*+$84(’+$!>33?;!F&’(! &/(!E))$!/!./2%’*43/239!3/21)!.2+E3)6!,’%&!%&)!%)26!/3%24’(6!>33?7!.;!a"cMaKL?7!,&’*&!&/(! E))$! 2)0)8’$)0! ’$! 6/$9! ,/9(7! ’$*340’$1I! >/?! 2)*’.2+*/3! /3%24’(67! ,&)2)! &)3.’$1! ’(! 8/5+42)0!E)*/4()!’%!,’33!3)/0!%+!%&)!/*%+2!E)’$1!&)3.)0!E/*:!/%!/!3/%)2!0/%)!>35?J!>E?!/! 0)*2)/()!’$!%&)!8’%$)((!+8!%&)!8+*/3!’$0’5’04/37!2)3/%’5)!%+!%&)!+%&)2!6)6E)2(!+8!’%(!12+4.! >2)3/%’5)39! *+(%39! %+! ’$0’5’04/37! 2)3/%’5)39! E)$)8’*’/3! %+! %&)! 12+4.J! (+6)%’6)(! %)26)0! \,)/:!/3%24’(6=?!>34, 36-41?J!>*?!/!0)*2)/()!’$!8’%$)((!+5)2!%&)!(&+2%!%)26!>42, 43?J!>0?! .3/9’$1!*++.)2/%)!’$!/!.2’(+$)2(=!0’3)66/!1/6)!>44?J!>)?!/!8/’342)!%+!&/26!+%&)2(!>45?J!>8?! %&)!6)*&/$’(6!E9!,&’*&!+$)!’$0’5’04/3!’(!6+%’5/%)0!%+!&)3.!+%&)2(!>46?;! ! a F&)!.2+E3)6!,’%&!/33!+8!%&)()!2)0)8’$’%’+$(!’(!%&/%!%&)9!’$*340)!(’%4/%’+$(!,&)2)! *++.)2/%’+$! *+430! .2+5’0)! /! 0’2)*%! 8’%$)((! E)$)8’%7! /$0! &)$*)! *+430! E)! 64%4/339! E)$)8’*’/3;!T+$()C4)$%397!%&’(!3)/0(!%+!/!E)&/5’+2!E)’$1!3/E)3)0!/(!/3%24’(%’*!,&)$!’%!’($=%! *+(%39! /$0! /*%4/339! E)$)8’%(! %&)! /*%+2;! V+2! )-/6.3)7! *+$(’0)2’$1! 2)*’.2+*/3! &)3.’$1! >)-/6.3)!/!/E+5)?7!*++.)2/%’+$!’(!+$39!8/5+2)0!>E)%,))$!$+$M2)3/%’5)(?!’8!’%!3)/0(!%+!/$! +5)2/33!E)$)8’%!>%&2+41&!’$*2)/()0!3’:)3’&++0!+8!E)’$1!&)3.)0!’$!%&)!84%42)?7!’$!,&’*&!*/()! ’%!’(!64%4/339!E)$)8’*’/37!/$0!(+!2)*’.2+*/3!/3%24’(6!’(!$+%!/3%24’(%’*;!#$!%&)!+%&)2!*/()(! >)-/6.3)(!EM8?!&)3.’$1!*/$!E)!64%4/339!E)$)8’*’/3!+2!/3%24’(%’*!>M_b?7!0).)$0’$1!4.+$! 6+0)3! 0)%/’3(! /$0! ./2/6)%)2! 5/34)(! /((46)0;! O3(),&)2)7! ,)! 0’(*4((! ’$! 0)%/’3! %&)! *+$84(’+$! %&/%! %&’(! */$! 3)/0! %+! >33?;! ]4*&! 2)0)8’$’%’+$(! +E(*42)! %&)! 84$0/6)$%/3! 0’(%’$*%’+$!E)%,))$!,&)$!0’2)*%!+2!’$0’2)*%!8’%$)((!E)$)8’%(!/2)!2)C4’2)0!%+!)-.3/’$!%&)! +E()25)0!*++.)2/%’+$!>33, 47, 48?;!F&’(!*/$!3)/0!%+!%&)!(’%4/%’+$!,&)2)!/!E)&/5’+2!’(! 0)(*2’E)0! /(! /3%24’(%’*7! E4%! */$! E)! )-.3/’$)0! E9! 0’2)*%! 8’%$)((! E)$)8’%(! >’;);! E9! ()38M ’$%)2)(%)0!+2!()38M2)1/20’$1!E)&/5’+2(?;!W+2)!8+26/3397!%&)()!2)0)8’$’%’+$(!/2)!6’(3)/0’$1! E)*/4()!%&)!(.2)/0!+8!/!1)$)!’(!0)%)26’$)0!E9!’%(!+5)2/33!>3’8)%’6)?!8’%$)((!*+$()C4)$*)(7! 2)3/%’5)! %+! +%&)2(! ’$! %&)! E2))0’$1! .+.43/%’+$7! /$0! $+%! ’%(! *+$()C4)$*)(! +5)2! (+6)! /2E’%2/2’39!0)8’$)0!\(&+2%M%)26=7!+2!2)3/%’5)!%+!(+6)!(4E()%!+8!%&)!.+.43/%’+$7!(4*&!/(!,’%&! ,&+6!%&)9!&/..)$!%+!’$%)2/*%!>4, 33, 49, 50?;! #%! ’(! /3(+! ,+2%&! *+6./2’$1! %&)! 0’(%’$*%’+$! E)%,))$! /3%24’(6! /$0! %&)! 5/2’+4(! 2)0)8’$’%’+$(!,’%&!Y++6(6/=(!>19, 20?!)6.&/(’(!+8!%&)!’6.+2%/$*)!+8!%&)!0’(%’$*%’+$! E)%,))$!+E3’1/%)!/$0!8/*43%/%’5)!)4(+*’/3’%9!>51?;!U(!3+$1!/(!)4(+*’/3’%9!’(!$+%!+E3’1/%)! >’;);!)5)29!6)6E)2!+8!/!&)3.)2!*/(%)!’(!/88)*%)0?!%&)2)!’(!(%’33!/!>/3E)’%!+8%)$!8/’$%39!6’$+2?! 0’2)*%!8’%$)((!’$%)2)(%!%+!E)!&/0!’$!%&)!84%42)!82+6!(,’%*&’$1!0)5)3+.6)$%/3!./%&,/9!%+! .)2(+$/3! E2))0’$1;! F&’(! ’(! ,&9! Y++6(6/! */%)1+2’D)(! 8/*43%/%’5)! )4(+*’/3’%9! 4$0)2! *++.)2/%’5)!E2))0’$1; Spiteful or selfish? F&)2)! /2)! $46)2+4(! )-/6.3)(! +8! &/26’$1! %2/’%(! ,&’*&! &/5)! E))$! /214)0! %+! 2).2)()$%!)5+34%’+$/29!>+2!</6’3%+$’/$?!(.’%)7!E4%!,&’*&!*/$!E)!)-.3/’$)0!E9!0’2)*%! E)$)8’%(!%+!%&)!/*%+27!/$0!,&’*&!%&)2)8+2)!2).2)()$%!()38’(&!$+%!(.’%)843!%2/’%(!>52, 53?;!#$! %/E3)!]‘WK!,)!(466/2’D)!/!$46E)2!+8!)-/6.3)(7!1+’$1!’$%+!12)/%)2!0)%/’3!%&/$!’$!%/E3)! ";!V+2!6/$9!+8!%&)()!*/()(7!%&)!8/*%!%&/%!%&)!%2/’%!*/$!E)!)-.3/’$)0!E9!0’2)*%!E)$)8’%(!&/(! /32)/09!E))$!.+’$%)0!+4%;!X)!,+430!3’:)!%+!)6.&/(’D)!%&)!/00’%’+$/3!.+’$%7!%&/%!’$!/33!+8! %&)()!*/()(7!%&)2)!’(!$+!)5’0)$*)!%&/%!%&)!&/26!*/4()0!E9!%&)()!%2/’%(!.2+5’0)(!/!E)$)8’%!%+! 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E)*/4()!%&)!*3/((’8’*/%’+$!’(!E/()0!4.+$!8’%$)((!*+$()C4)$*)(7!/$0!$/%42/3!()3)*%’+$!/*%(! +$!%&)!/5)2/1)!8’%$)((!*+$()C4)$*)(!+8!/!%2/’%;!V+2!)-/6.3)7!(4..+()!%&/%!/112)((’+$!,/(! ! R

Description:
decrease the relative fitness of the actor and also either benefit (altruism) or harm (spite) other individuals who share genes for altruism (Fig. 2).
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