In the Light of Evolution V: Cooperation and Conflict issue Proceedings of the National Academy of Sciebces of

142 Pages·2011·7.58 MB·English

by  Joan E. Strassmann

Supplement to
June 28, 2011 u vol. 108 u suppl. 2 u 10787–10926
Coverimage:PicturedisaBatikpaintinginwoad,aplant-deriveddye,oncotton.Thetwo
ants illustrate the phenomenon of cooperation, the focus of many of the articles in this
supplementarisingfromtheArthurM.SacklerColloquium,“IntheLightofEvolutionV:
CooperationandConflict.”Thesupplementexploresrecentdevelopmentsinthestudyofthe
evolutionof cooperationamongallorganismsfromthelevelofgenestothatofsocieties;
frombacteriatohumans.SeetheintroductoryarticlebyJoanE.Strassmanetal.onpages
10787–10791.ImagecourtesyofRobinParis,www.robinparis.co.uk.
Abouttheartist:Fromayoungage,BatikartistRobinParishasfoundantsfascinatingto
watchandstudy.ThiswasreinforcedonherAustralianandSouthEastAsiantravelswhen
she encountered ants of many different sizes, habits, and ferociousness—but always in
active, orderly societies. Here, a pair of ants facing in opposite directions ensures safety
foreachother.
Supplement to the Proceedings of the National Academy of Sciences of the United States of
America, which includes articles from the Arthur M. Sackler Colloquium of the National
Academy of Sciences In the Light of Evolution V: Cooperation and Conflict. The complete
programisavailableontheNASWebsiteatwww.nasonline.org/SACKLER_cooperation.
Contents
10831 Evolutionofrestraintinastructured
rock–paper–scissorscommunity
JoshuaR.Nahum,BrittanyN.Harding,
andBenjaminKerr
INTRODUCTION 10839 Socialevolutioninmultispeciesbiofilms
SaraMitri,JoãoB.Xavier,andKevinR.Foster
10787 InthelightofevolutionV:Cooperationandconflict
JoanE.Strassmann,DavidC.Queller,JohnC.Avise, 10847 Molecularevolutionaryanalysesofinsectsocieties
andFranciscoJ.Ayala BrielleJ.Fischman,S.HollisWoodard,
andGeneE.Robinson
10855 Evolutionofcooperationandcontrolofcheatingin
COLLOQUIUM PAPERS
asocialmicrobe
JoanE.StrassmannandDavidC.Queller
10792 ExpandedsocialfitnessandHamilton’sruleforkin,
kith,andkind 10863 Selfishgeneticelements,geneticconflict,and
DavidC.Queller evolutionaryinnovation
JohnH.Werren
10800 Evolutionarytransitionsinbacterialsymbiosis
JoelL.Sachs,RyanG.Skophammer,andJohnU.Regus
10871 Theevolutionofdrugresistanceandthecurious
10808 Kinship,greenbeards,andrunawaysocialselectionin orthodoxyofaggressivechemotherapy
theevolutionofsocialinsectcooperation AndrewF.Read,TroyDay,andSilvieHuijben
PeterNonacs
10878 Genomicimprintingandtheevolutionarypsychology
10816 Spatiotemporalenvironmentalvariation,riskaversion,
ofhumankinship
andtheevolutionofcooperativebreedingasa
DavidHaig
bet-hedgingstrategy
DustinR.Rubenstein
10886 Pathologyfromevolutionaryconflict,withatheoryof
10823 Endemicsocialdiversitywithinnaturalkingroupsofa Xchromosomeversusautosomeconflictover
cooperativebacterium sexuallyantagonistictraits
SusanneA.KraemerandGregoryJ.Velicer StevenA.FrankandBernardJ.Crespi
PNAS u June28,2011 u vol.108 u suppl.2 u iii–iv
10894 Cooperationandcompetitionina 10910 Evolutionaryfoundationsofhumanprosocialsentiments
cliff-dwellingpeople JoanB.SilkandBaileyR.House
BeverlyI.Strassmann
10918 Theculturalniche:Whysociallearningisessential
10902 Extentandlimitsofcooperationinanimals forhumanadaptation
DorothyL.Cheney RobertBoyd,PeterJ.Richerson,andJosephHenrich
iv u www.pnas.org
F
R
O
fl
In the light of evolution V: Cooperation and con ict M
T
H
JoanE.Strassmanna,DavidC.Quellera,JohnC.Aviseb,andFranciscoJ.Ayalab,1
E
aDepartmentofEcologyandEvolutionaryBiology,RiceUniversity,Houston,TX77004;andbDepartmentofEcologyandEvolutionary
BTiology,UniversityofCalifornia,Irvine,CA92697 A
C
hispaperservesasanintro- interpreting sexualselection andmany useful, andit istheframeworkusedby
A
duction tothe fifthinaseriesof other phenomenaintermsofindividual manyworksinthisvolume. Queller(16)
D
Colloquiaunderthegeneraltitle advantage, andunderstanding frequency- revisitswhyinclusive fitnesshasbeenso
“IntheLightofEvolution”(ILE; dependent effects throughgametheory, usefulandsuggestswaystoexpanditto E
seeBox1).Papersfromthefirstfour effortsthat continuetothepresent. speakmoredirectlytointeractionsbesides M
colloquiainthe “Inthe LightofEvolu- Thepuzzleofcooperation wasthe kinselection.Hedelimits twoother kinds Y
tion”series, titled“Adaptation and dominant themeofresearchintheearly ofsocialselection thatcan betreated :
ComplexDesign,”“Biodiversity and years, whereasrecentworkhasempha- moreexplicitly inHamilton’srule (6,7). C
Extinction,”“TwoCenturiesofDarwin,” sizedits importanceandubiquity. Far Kindselection,whichinvolves synergisms O
and“TheHumanCondition,”are refs. frombeingararetraitshownbysocial betweenindividuals expressingthe same
L
1–4,respectively. Thecurrentvolume insectsandafewothers,cooperationis traits, groupstogether greenbeards L
exploresrecent developmentsinthe bothwidespreadtaxonomically and (genesthat,ineffect,can identify the O
studyofcooperation andconflict,ranging essential tolife.Majortransitions inthe presenceofcopies ofthemselves in
fromthe levelofthegene tosocieties hierarchyoflife haveofteninvolved co- otherindividuals) andmanycasesof Q
andsymbioses. operation amonglower-level units tothe frequency-dependent games.Theyshare U
Anystudentofhistoryknowsthathu- pointwhere theyevolveinto higher-level thefeature thatindividuals expressing I
manscanbeaviciouslot,but paradox- organisms(8,9).Examplesinclude the U
thetraithave differenteffects onother
ically,wearealsoamongnature’sgreat assembly oftheeukaryoticcell withits M
expresserscomparedwithnonexpressers,
cooperators.Whichofus,asanindividual, symbioticorganelles, theevolution of
andtheyalso sharemanydifferences
canmanufactureacellphone oranair- multicellular organisms,andtheorganis- I
frompurekinselection.Kith selection N
plane?Evenourgreatconflicts—wars— malcolonies ofsomesocialinsects. Or-
requiresneither kinnorkind, butinstead T
areextremelycooperative endeavors on ganismsare,atmultiplelevels,thoseunits
involvesactors affectingpartnersinways R
ebaecsthusniddee.rsStoomodecouflttuhrisalclyo,obpuetrawtieonaries tbhoautnhdaavreiees,voexlvteredmtoe choaovpe,erwaittihoinnathnedir thatfeedbacktotheactor’sfitness.Mu- O
alsoproducts ofevolution, withbodies, minimal conflict (10,11).Thedepth of tualism andmanipulation areincludedin D
brains,andbehaviors moldedbynatural researchoncooperation andconflicthas tHhaismcialttoengo’sryru.lTehweitehxpkainn,dekdithv,earsnidonkionfd U
selection.Howcooperation evolveshas increased greatly,mostnotablyinthedi-
couldbringthe advantagesofHamilton’s C
beenoneofthe bigquestionsinevolu- rection ofthe smallorganisms.Microbes
methodstoabroaderrangeofsocialin- T
tionarybiology,andhowitpaysor does turnout tohavehighlydeveloped co-
teractions(6,7). I
notpay isagreat intellectual puzzle. operation (12),andthey,along with O
Interactions betweenindividuals of
Ifnothingmakessenseinbiologyexcept other modelorganisms,have provenin-
different speciesareamajortypeofkith N
inthe lightofevolution (5),thenforthe strumental inbeginningtounderstand
firstcenturyafterDarwin,cooperationand sociality atthe geneticandmolecular selection,whereindividuals areselected
altruismdidnotmake muchsense.We levels, thestudyofrealselfishgenes(13). toaffecttheir partnersinwaysthatulti-
couldseethatindividual organismssome- Thesocial evolutionapproach hasgiven mately benefitthemselves (ortheir kin).
timeshelpedothers,evenatacosttotheir usinsights ondiseasesoftencausedby Suchinteractionsneednotbecooperative,
ownfitness.Itwasclearthatsuchbehavior microbes (14).Attheotherendofthe butwhen theyare,theytypically involve
couldbenefitthegroup,population, spe- spectrum,wearegetting amuchbetter exchangeofdifferentservicesthatone
partnerneedsandthe othercaneasily
cies,oreven otherspeciesandwhole understanding ofthe cooperationand
communities.However,itwasnotobvious conflictthatmatters mosttoourspecies provide;therefore,partners canbevery
different.Accordingly,Sachs etal.(17)
howsucheffects wouldbeheritable. All (15).Cooperation hasbeencentralto
ourmathematical models—thehard work humanity’sspectacularsuccessandwillbe explore associationsorsymbiosis among
ofthe modernsynthesis—wereaboutin- centraltoourshort-andlong-termfates. partnersthat areverydifferentindeed,
onebeingeukaryotic andtheotherbeing
dividualswithonealleleout-reproducing
Fundamentalsof Evolutionary prokaryotic. Suchsymbioses,byleading
thosewithanalternative. Thisprocess
Cooperation tomitochondriaandchloroplasts, were
wouldfavorindividuals withhigherre-
productionbutwould notbeexpectedto Althoughmostofthisvolumeisaboutthe
produceself-sacrifice. However,apparent newtopicsthatarebeing treatedaspart
cooperationwasroutinelyattributedtothe ofsocial evolution,suchasgenes,mi- ThispaperintroducesthePNASsupplementthatresulted
fromtheArthurM.SacklerColloquium“IntheLightof
goodofthegroup,species,orcommunity. crobes,andmedicine,the oldfunda- EvolutionV:CooperationandConflict,”whichwasspon-
Thissituation changedinthe firstdecade mentaltopicsstillmatterandremainthe soredbytheNationalAcademyofSciencesonJanuary7–8,
ofDarwinism’ssecondcentury.Hamilton subjectofvigorousresearch.Thefirstfour 2011,attheAcademy’sArnoldandMabelBeckmanCenter
(6,7)argued thatcooperation wasim- papersintheseproceedingsrevisit some inIrvine,CA.Thecompleteprogramandaudiofilesof
mostpresentationsareavailableontheNASWebsiteat
portantinnatureandthatsocialevolution ofthesestandard arenas,includingso- www.nasonline.org/SACKLER_cooperation.
couldbeunderstoodintermsofdirect cial insects,cooperatively breeding
Authorcontributions:J.E.S.,D.C.Q.,J.C.A.,andF.J.A.wrote
gainstotheactor’sownfitnessorindirect birds,mutualisms, andmodelsofsocial thepaper.
benefitstothefitnessofothers whoshare evolution. Theauthorsdeclarenoconflictofinterest.
thecooperation allele.Therefollowedan Therearemanywaystothinkabout
ThisarticleisaPNASDirectSubmission.
intenseperiod ofexploringtheindirect andmodelsocial evolution.Inclusivefit-
1Towhomcorrespondenceshouldbeaddressed.E-mail:
effectsofcooperation andaltruism,re- nessisoneofthemostvenerableandmost [email protected].
www.pnas.org/cgi/doi/10.1073/pnas.1100289108 PNAS | June28,2011 | vol.108 | suppl.2 | 10787–10791
responsiblefor theevolution oftheeu-
Box1. IntheLightof Evolution evolutionary principles andprocessesis
karyoticcell itself.However,additional
In1973,Dobzhansky(5)pennedashort importantinothersocietal arenasas
symbiosesarewidespreadandsometimes
commentarytitled“NothinginBiology well,suchaseducation,medicine, soci-
ancient.Sachs etal.(17)useacombina-
MakesSenseExceptintheLightof ology,andotherappliedfieldsincluding
tionofbroad-scale phylogeneticanalyses
Evolution.”Most scientistsagreethat agriculture,pharmacology, andbio-
andcasehistoriesofparticular systemsto
exploreseveral transitions. Theyfind,for evolution provides theunifying frame- technology. Theramificationsofevolu-
workfor interpreting biologicalphe- tionarythought extend intolearned
example,thatthereislittle phylogenetic
nomena thatotherwisecan oftenseem realmstraditionally reservedforphilos-
signaltoindicate thatsomebacterial
unrelated andperhapsunintelligible. ophyandreligion.Thecentralgoalof
groupsarepreadapted foreukaryotic
Giventhecentralposition ofevolution- the“IntheLightofEvolution”seriesis
symbiosis(17).Instead,thegenesrequired
arythought inbiology,itissadlyironic topromotethe evolutionarysciences
seemtobequitewidely availablethrough
that evolutionaryperspectives outside throughstateofthe artcolloquiaand
horizontaltransmission. Mutualistic inter-
thesciences haveoftenbeenneglected, their publishedproceedings. Eachin-
actionsseemtoarisefrombothparasitic
misunderstood,or purposefullymis- stallmentwillexplore evolutionary per-
andfree-living ancestors.Onceacquired,
represented.Biodiversity—the genetic spectivesonaparticularbiologicaltopic
thesemutualisticinteractions seemtobe
varietyoflife—is anexuberant product thatis scientifically intriguingbut also
quitestable,withfewreversionstonon-
oftheevolutionary past,avasthuman- hasspecialrelevance tocontemporary
mutualisticforms. Giventhe tendencyof
supportive resource(aesthetic,in- societalissuesorchallenges.Individually
vertically transmittedsymbiontstode-
tellectual, andmaterial) ofthepresent, andcollectively, the“IntheLightof
gradeandthe propensityofhorizontally
andarichlegacytocherishandpreserve Evolution”serieswillaimtointerpret
transmittedonestocheat,this stability is
forthefuture.Twochallenges(aswellas phenomenainvariousareasofbiology
somewhatsurprising.
opportunities) for21stcentury science throughthelens ofevolution,address
Thesocialinsectshave longbeen
aretogaindeeperinsights intothe someofthemostintellectuallyengaging
viewedasthe pinnacleofcooperation.
evolutionary processesthat fosterbiotic aswell aspragmaticallyimportant
Thisviewismosttenableifoneignoresthe
diversity andtotranslate thatunder- societal issuesofourtimes,andfoster
cooperationthat goesonintransitions
standing intoworkablesolutionsfor agreaterappreciation ofevolutionary
thatarealready complete,suchasmulti-
theregionalandglobalcrisesthatbio- biologyasaconsolidatingfoundationfor
cellularanimalsorthe eukaryoticcell.
diversity currentlyfaces. Agraspof thelife sciences.
However,somesocialinsect coloniesare
socooperativeandintegratedthattheyare
viewedassuperorganisms(organisms evolvefrommonogamousones,anddis- found,becausemicrobes performmany
madeupofotherorganisms).Themotive criminationevolvesinsystemsthatshow functions(likedigestion) extracellularly
forcebehind theevolution ofthesesocie- variationinrelatedness(20).However, thatanimalsperforminside. Oneofthe
ties,whichconsistofcloserelatives,is thestoryismorecomplicatedfortworea- recenttransformative elements ofthe
kinselection(6).Nonacs(18)points out sons.First,althoughsomehelpersgain studyofmicrobes hasbeenanapprecia-
thatpredictions fromkin selectiontheory kin-selectedbenefitsthroughhelpingclose tionofthe importanceoftheir socialin-
havebeenbothsuccessfulandalsodisap- kin,othersmaygaindirectbenefits.Com- teractions. Manyofthetypesofsocial
pointing.Thedifference, hesuggests, is paredwiththesocialinsects,morere- interactionsfoundinanimalshave their
notbecauseofchance.Thesuccessful searchonbirdshasaddressedtheparti- counterparts inmicrobes. Someco-
predictionsfromsexratiotheory and cularbenefitsofremainingathomeand operative interactionsare muchmore
worker-policingtheoryoccur whenthe theecologicalconstraintsthatmaylimit easilystudied inmicrobes,particularly
predictedbehaviorscanbeachievedusing
independentbreeding.Varianceinre- ifthegoalis toilluminate thegenetic
simpleenvironmental cuesthat correlate
productivesuccesshasplayedarolein basisofbehavior orusethepowerof
withkinship.Itiseasytotreat malesdif-
thesediscussions,butRubenstein(21) experimental evolution.
ferentlyfromfemalesor workersdiffer-
movesittoamorecentralposition.He Perhapsthebest-studied social bacte-
entlyfromqueens.Thelesssuccessfulkin
suggeststhatcooperativebreedersmay riumis Myxococcus xanthus,aspeciesof
selectionpredictions,suchaspartsofskew bebethedgers,gainingadvantagefroma δ-proteobacteriathatspendsitsentirelife
theory,mayfailbecausethey requirege-
netickinrecognitionmechanismssuffi- moreuniformreproductiveoutputincoop- insocialgroups (23).Itis apredatory
erativegroups.Rubenstein(21)drawson bacterium thathunts otherbacteriainso-
cienttodetectcloserfrommoredistant
manyyearsofhisfielddataonstarlingsin cialpacks,dissolving its preyinpoolsof
relativeswithin colonies.Thismaynot
Africa,wherethereismuchvariationin cooperatively producedenzymesbefore
explaineverything, becausegenetic kin
bothtimeandspace,andhefindssupport ingestingthem.Movementusuallyisbased
recognitionsystemsdoexist, atleastfor
forseveralpredictionsofthishypothesis. onType IVpili andisfundamentallyso-
distinguishingcolony membersfromnon-
cial.Whenfoodisscarce, individualbac-
colonymembers.Theinteraction between
CooperationWrit Small:Microbes teriaaggregateintoafruitingbody.Inthis
environmental andgeneticrecognition
Perhapsnotaxaareaspromising foren- stalklessfruiting body,mostornearlyall
systemshasscarcelybeenexplored, and
Nonacs(18)runscomputer simulations hancing bothourunderstanding ofco- cellslyse,perhaps tothebenefitofthe
showinghowgreenbeardlocican perturb operation andourunderstanding ofthe remainingfew,whichformhardyspores.
theoutcomesexpected underpedigree mechanismsasmicrobes.Earlyworkon Experimental evolution hasshownus
relatednessalone. microbes concentrated onpurifyingand muchaboutthe natureofsociality in
Afterthesocialinsects,cooperative isolating themforgrowthinpure culture. M.xanthus.Forexample,when foodwas
birdsandmammalshaveattractedthe ThepostulatesbyKoch(22)requiredthis patchily distributed, thespeciesevolved
mostattention.Manybirdspecieshave andwereimportantfordetermining ex- moreefficientgrouphunting techniques
helpersatthenest,usuallyoffspringfrom actlywhichmicrobes causedaparticular (24).Underothercircumstances, social
previousbroodswhohaveremainedat disease.However,innature,microbeslive cheaterscandrive population crashes
theirnatalsite(19).Kinshipisimportant incomplexmultispecies structuredenvi- (23,25).Inonefascinatingcase,anewco-
hereaswell.Helpingsystemsusually ronments.Social interactions arepro- operator evolvedfromthesocial cheater.
10788 | www.pnas.org/cgi/doi/10.1073/pnas.1100289108 Strassmannetal.
However,thisworkdoesnot tellushow ronment.Forexample,microorganisms talcarbohydrate metabolism. Again,this
naturaltheseeventsare;forthat ex- growingonsubstratesaremorelikelytobe fitswithanutritional basisforcaste,but
planation,wemustturntonaturalvaria- incontactwithclonematesthanthoseliv- itseemssurprisingthatchanges arecom-
tioninwildfruitingbodies.Kraemerand inginamorefluidenvironment.Another moninsuchbasicpathways. Theseissues
Velicer(26)explorenatural phenotypic possibility,andoneinvestigatedinthe shouldbeclarifiedwithadditionalgenome
variationinsocial traitsofdistinct clones modelspresentedbyMitrietal.(29),isthat sequencesandfunctional studiesofin-
withinafruitingbody. Theytook10 otherspeciescangeneratestructurethat dividual species.
fruitingbodiesfromnature,andfrom favorswithin-speciesclonality.Thispaper StrassmannandQueller(32)explore
them,theyisolated 48individualclones usesamodelingapproachtounderstand amicrobialsocialsystemwhereitispossi-
andexamined theirsocialphenotypes howadditionalspeciescanchangeinter- bletomanipulategenes.Inthesocial
(26).Theseclonesvaried withinfruiting actionswithinspeciesforthecaseofa amoebaDictyosteliumdiscoideum,starved
bodiesinswarmingandsporeproduction, growth-promotingsecretion(29).This cellscometogetherinlargegroupsinwhich
genetictraitslikelytohavearisenrecently, agent-basedmodelingapproachusesone 20%ofthecellssacrificethemselvesto
becausethe clonesfromthesamefruit- otherspeciestostandinforallcompeting makeastalkthataidsindispersalofthe
ingbodywerenearlygeneticallyidentical. species.Themodelsindicatethatother othersasspores(33).Besidesthisimpres-
Thisfascinating workwillshedlighton speciescaninsulatesecretorsfromselfish sivealtruism,thisspecieshasbeenshownto
thenature ofsociality intheabsenceof nonsecretors,evenwhentheotherspecies havecheating,kinrecognition,andeven
asinglecell bottleneck, wherevariations canusethesecretionsthemselves.Other primitivefarmingoftheirbacterialfood.
thatbenefitsinglecloneswithinthegroup factorssuchastheroleofdispersaland Numerousgenesofmanyfunctionaltypes
canspread,even atthecostofother nutrientlevelsarealsoaddressedinthese canbemutatedtocheaters.Somecheaters
groupmembers. models,whichrepresentabeginningtothe coulddestroycooperation,butcoopera-
Oneadvantage tostudyingmicrobial importanttaskofconsideringmicrobial tionismaintainedforavarietyofreasons,
socialsystemsisthat attributesthat are socialityandecologysimultaneously,be- onebeingtheratherhighgeneticre-
strongbut sometimeshardtomeasurein causethesefactorsmustinfluencehowse- latednessinthefield,partofwhichis
animalsareeasilyexaminedinexperi- lectionoperateonthesesystemsinnature. causedbykinrecognitionmediatedby
mentalsystems.Onesuchattribute can highlypolymorphicadhesiongenes.Other
becalledrestraint.Itmaynotbeeasyto Real Selfish(andCooperative)Genes controlsoncheatingthathavebeenshown
determinewhetheracowinaherd is Itisremarkablethatafieldfoundedonthe includetheevolutionofresistorgenes,
eatingallthatitcouldorisholdingbackso conceptofselfishgenes(30)gotsofarfor powerasymmetries,andlottery-likemech-
thatothersmay eat.Ifitwereholding solongwithout paying muchattention to anisms.StudiesofthedimAandcsaAgenes
back,thiswouldbeasocialtraitthat specifiablegenes.Thisfactisprobably haveshownthatcheatingcanalsobecon-
wouldbenefitothers andthus,would be becausewelearnedhowphenotypic strat- trolledbyidiosyncraticpleiotropiesofpar-
expectedtoevolveunderkinselection egiesofcooperationandconflictcouldbe ticulargenes.Thecheatingallelewouldbe
onlyifthegenesforthat traitarealso understoodasthe resultsofgenesmaxi- favoredbyselection,butotherdeleterious
presentinothers (andtheybenefitac- mizing inclusivefitness.However,studies effectsofthesameallelekeepitfrom
cordingly).Inanexperiment,Nahumetal. atthegenetic levelare nowbecoming spreading,suggestingthatcheat-proofco-
(27)lookattheevolution ofrestraint in commonandshouldshedlightbothonthe operationoftenmaybebuiltusingelements
anontransitive hierarchyoftendescribed mechanismsandthemannerinwhichso- thatareessentialforotherreasons.Con-
bythe rock–paper–scissorsgame inwhich cial selectionoperates. sistentwithongoingsocialconflictsand
noonetypeconsistently dominates.They Fischmanetal.(31)reviewandextend armsraces,socialgenesevolverapidly.
usedEscherichiacoli clonesandthe whatisknownaboutthemoleculargenetic Dawkins(30)argued thatallgenesare
colicinsystem(28).Colicins arecostly to mechanismsofeusociality. Someofthe selfish,but theonesthat showthetrait
produceandresist,butsensitivestrainsare information comesfromstudiesofpartic- mostdistinctivelyare selfishgeneticele-
killedwhenproducers releasethem.The ulargenesandpathways,butmuchisnow ments.Theseare therenegadesofthe
researchersengineereddouble colicin comingfromevolutionaryanalyses ofge- genome,chunksofDNAthatreplicate,in
producersandresisterssothat produc- nome-scale data.Tothesevensequenced partatleast,throughdifferent pathways
tionandresistancewouldnot belostor genomesofsocialinsects, Fischmanetal. thanmostgenesandthus,canbeselected
gainedintheir system,andthen,they (31)addtheir owntranscriptome-based toconflict withotherloci.Transposons,
askedhowthethreetypesofclonewould protein-codingsequencesfor10socialand forexample,increase theirrepresentation
fareunderdifferentmigration schemes nonsocial beespecies,representing three byjumpingfromoneplacetoanother,
comparedwithhowtheresistorperformed origins ofsociality. Someofthepatterns oftenatsomecosttotheorganism.Other
onitsown. Theyfoundthatthe resistor are idiosyncratic.For example,earlyre- examplesincludemeiotic driveelements,
strainexhibited themostrestraintwith sults fromthe honeybee genomepointed variousmodificationrescuesystems,
restrictedmigrationinthepresence totheimportance ofodorant receptors imprintedgenes,B chromosomes,and
ofall threestrains,just theconditions andimmunitygenes, butthisimportance organellar genes.Werren(34)tacklesthe
wheretheirmodels expectcooperation doesnot holdupinthebroader analyses. issuesofthefunction andadaptation of
toevolve (28). Findingsinclude increasedratesofevolu- theseelements.Hesurveysthe evidence,
Cooperationamongclonematesarises tion ofbrain-relatedgenesintheprimi- sometimesstrongandsometimessugges-
easily,becausethegenesunderlyingco- tively eusocialbees,conceivably because tive,thatsuchelements havehadimpor-
operationarepresentinbothpartners.In oftheincreased cognitivedemandsof tantfunctional consequencesfor their
microbes,cooperationoftentakestheform their competitivesocial environment. genomes.For example,partsoftrans-
ofextracellularsecretions,includingthose Juvenile hormoneandinsulinareoften posonssometimesevolve intoregulatory
usedforquorumsensing,ironscavenging, important incaste.Thisisnot surprising regions,anddefenses againstselfishele-
andfruitingbodyformation.Therefore, ifcaste isnutritionally based,although mentsmayhave ledtotheeukaryotic in-
akeyquestioninvolveswhatfavorsthe the effectsofjuvenile hormonearequite tron-splicingapparatus.However,contrary
formationofclonalpatchessuchthatco- different fromtheeffects innonsocial tosomerecentsuggestions,Werren (34)
operationcanbefavored.Oneanswer insects. Thereis alsoarapidevolutionary arguesthatthereis asyetlittle evidence
involvesthephysicalstructureoftheenvi- change inproteinsinvolved infundamen- thatthesearetheadaptivereasonsforthe
Strassmannetal. PNAS | June28,2011 | vol.108 | suppl.2 | 10789
maintenanceoftheseelements.Instead, nancy whenthereisanupset inthe pre- operation istolookatwhathumans do
selfishgeneticelementsaremaintainedby carious resolutionofembryo–maternal andwhattheoutcomesare,just asone
theirselfishbehavior,butthe newchunks conflict.Taking aradical stepfurther,he- mightdofor othersocialanimals. This
ofDNAthatthey sprinklethroughout haspointedoutthat theoptimalstrategy techniquecanbeparticularly informative
genomessometimes getco-opted,domes- ofanembryo’sgenediffers according whenthe humangrouplivesinwayscon-
ticated,orotherwisemodifiedtocause towhetheritcamefromthedamorthe sistent withhumansover mostoftheir
somebeneficialeffect tothe organism. sire,withmaternallocibeinglessselected evolutionary past.TheDogonofMali,
totakeresourcesfromthe mother.Re- reportedonbyStrassmann(40),aremillet
SocialityandMedicine markably,imprintedgenesseemtobehave andonionfarming agriculturalists whodo
Mostbiologists probablyworkinbio- inaccordwith thistheory.Haig(38)ex- not usecontraception,adherelargelyto
medicalfields.Ifnothinginbiologymakes tends thisthinkinginseveraldirections. indigenous religions,practicepolygyny,
senseexceptinthelightofevolution, Henotes thatmostofourkin belongto andhavehighmortality rates. Ina25-y
thenmedicineshouldhave muchtolearn categories thathave asymmetrical re- longitudinal study, Strassmann(40)ad-
fromevolutionary reasoning. Therapidly latednesstoourmaternal andpaternal dressesthehypothesis thatthe Dogon
growingfield ofDarwinian medicine (35) genes, andtherefore,mostofourpsycho- arecooperative breeders,wheresome
isbasedonthispremiseandseeksto logical adaptationsfordealing withkin, individuals helprearnondescendentkin
provideinsightontopicsliketheevolution andperhapspathologies,mayreflectthese ratherthantheir ownprogeny.Shedoes
ofvirulence anddiseasesofaltered evo- kinds ofconflicts.Inparticular,he shows not findthat thedatasupportthishy-
lutionaryenvironments. Asubfield,re- howthisperspectivemay illuminate un- pothesis. First,neitherwomennormen
centlycalled Hamiltonianmedicine (14), solvedproblemssurroundingtheevolution delay reproductioninordertoraisesib-
investigatestheimpactofsocialevolution, ofadolescenceandthe timingofsexual lings.Althoughparentsforcedaughtersto
cooperation,andconflictondisease. maturation inhumans(38). careforextrasiblings,thisisbetterviewed
Readetal.(36)treat thevitalproblem Frank andCrespi(39)extendandgen- asparentalmanipulation. asthe presence
ofhowtominimizethe evolution of eralizethesametheme:that conflictcan ofsiblingsreducessurvivorship. Similarly,
pathogenresistanceandthereby extend lead topathologieswhenopposing inter- grandmothers donot appeartobeeffec-
theusefullivesofourarsenalofantibiotic eststhatareprecariouslybalancedbecome tivealloparents.Rather thanincreasing
drugs.Thisinvolvesacomplexsetofin- unbalanced.FrankandCrespi(39)suggest survivorship, thepresence ofpaternal
teractingcauses,someofwhichhaveaso- that theconflict betweenmaternaland grandmothersdoestheopposite,doubling
cialelementandothersdonot.Readetal. paternalgenesinoffspring,throughits thehazardofdeath forachild.What
(36)challenge thedogmathat wemini- showneffects onthe regulationandpa- mattersmostforsurvivalisthepresenceof
mizetheevolutionofresistancebyradical thologies ofgrowth, mayberesponsible themother, andother relativesare not
pathogencure: usingenoughofadrugto forsomecancers. Theythendiscussthe adequatereplacements. Taskcooperation
trytoeliminate the pathogenfromthe excitingidea thatthissamebalanceis occurswithin thegroups thatworkand
patient’sbody.Thereasonable rationale partly responsible forawidespectrum eattogether,butconflictisalwayspresent
behindthispractice istolowerthepath- ofpsychiatric disorders,suchasautism, inwaysthatare carefullyexplainedby
ogenpopulation size andminimizethe that mayresultfroman overexpression Strassmann(40).
occurrenceofnovelresistancemutations. ofpaternalinterests inoffspring self- Inan overviewofvertebrate inter-
However,Readetal.(36)arguethatthis ishness.Similarly,other disorderssuchas actions, Cheney(41)showsthatanimals
ignorestheselectivephase, whichmay schizophreniamightresultfromanover- ranging fromchickadees tochimpanzees
bemoreimportantindetermining the expressionofgenesunderlyingthemater- areawareoftheir ownstatusandtheir
timetodrugimpotence,particularlywhen nalgoalofgreatersocialintegration. companions,andtheybehaveaccordingly.
resistancemutationsarisewithrelatively Finally, FrankandCrespi(39)present Eavesdroppingonhowindividualsinteract
ease.Inthisselectivephase, theradical atheoryofconflictbetweenautosomal withothers canchangebehaviors. Rela-
pathogencureprovides thestrongest pos- andXchromosomes.Xchromosomes tednesses areoftenknownandimpact
sibleselection forresistance. According spendtwo-thirdsoftheir timeinfemales interactions. Invervetmonkeys,for
toReadetal.(36),the socialstructureof andtherefore,shouldbeselectedtogive example,anindividual whohasbeen
thepathogencanpowerfullyaugmentthis greaterweighttofemale thanmaleadap- attackedmayturnandsubsequentlyattack
selection.Whenahostisinfected by tation. Autosomesshouldgiveequal arelativeofheropponent.Dominance
multiplestrains ofthe pathogen(asis weight.Itwillbefascinatingtoseeifem- hierarchiesalso impact suchinteractions.
oftentrueofmalaria)andthetotaldensity piricaltests supportthe authors’pre- However,someanimal interactions are
ofthe pathogenis regulated,thenwiping dictionthat suchconflictwillunderlie moresubtle.Ravensare morelikelyto
outsusceptiblestrainswithantibiotics pathologiesofexpressionalongthemale– cachefoodinhiddensiteswhencom-
cangreatlyincrease thefrequencyoffor- female axis. petitorsare present,forexample. How-
merlyrareresistantstrains. Thisraises ever,thecalculations ofgain,cost,and
thepossibilitythatthemedicalcommunity Are HumansDifferent? punishmentnecessary forreciprocal al-
isignoringan importanthumansocial Evolutionary principles forcooperation truism(herecalled contingent altruism)
dilemma:thatthebest treatmentfora that havebeendeveloped fromstudiesof seemlargelylackingoutside ofhumans.
patientmaynot bethebestoutcomefor diversesocial organismsshouldapplyto Instead,thereis agreat dealoftolerance
societyasawhole. humans.Themoreimmediate rootsto ininteractionsandalackofdirectpayback
Somehumandisorders canspringnot humancooperation andconflict alsomay amongclose relativesandlong-time
fromafailure ofadaptation persebut beseeninprimates.However,thereare partners.However,itisintheserelation-
fromdisagreement andconflict over challenges instudyinghumansandtheir shipswherecooperation overwhelmingly
whatis thecorrectadaptation. Thisis close relatives.Objectivity isessential. occurs.Acommon featureofcooperative
particularlyso intherealmofhuman Therearemanypossibilities forstudy actsisthat theyare notnecessarilytran-
interpersonalrelations,starting withfun- techniques (suchasthequestionnaireor sitive.Someindividuals consistentlytake
damentalconflicts betweenparentand survey)inhumans,butthesealso offer onthe riskyjobs,beitmale chimpspa-
offspring.Haig(37)hasarguedthatsuch manyopportunities forconfusion. One trollingtheirterritorial edgesor female
conflicts canleadtopathologies inpreg- powerfulapproach tostudying humanco- lionsleading thehunt.Thisisalso true
10790 | www.pnas.org/cgi/doi/10.1073/pnas.1100289108 Strassmannetal.
inorganisms(suchaswasps)withmuch outsiders,andthey willsuffercoststo andacquiringofinformationfromothers.
simplerbrains,wherecooperation flows punishcheaters. Asdescribed bySilk These cultural learners have an advan-
fromworkerstothe queen. andHouse(42),versions ofsocialgames tage,becausetheycangraspthebestfrom
Observationsofhumansandprimates involving foodor toolsthat likewise the past even if they innovate personally
innatural situations canteachusmuch have beenusedwithprimates produce only occasionally. Tools and customs
aboutbehavior,butenvironmental com- complex results.Cooperation clearly certainly make life for humans easier
plexitycanmake causationdifficultto occurs andtrackslevelsofsociality in or possible.
discern.Analternativeistoexamine the groups,butsomeresultsarecontro- Thestudyofcooperation andconflict
choicesmadeunderhighlyregulated cir- versialandremain opentoalternative hascomeaverylongwayfromthetime,
cumstances.Toaddresssocialactssuchas interpretations. 50yearsago,whenHamilton (6,7)first
generosity,trust,fairness,andpunishment, In themodernworld, mostofa pondered howtoexplainthe evolution
manypurportedly relevantgameshave person’smaterialpossessions areitems ofworkerbehaviorinsocialinsectswith
beenappliedtohumans,onesimple ex- that noindividualcould possiblymakeby astrangegeneticsystem. Ithasspread
amplebeingtheDictator Gamethatal- herself. Insteadtheywereproducedwith out taxonomically, extendingeven tomi-
lowsasubjecttodecidewhethertoshare the learnedandspecialized expertise crobes.Ithasdeepenedmechanisticallyas
aquantifiableresource withanunseen ofothers.Inthe finalpaperofthesepro- weprobe itsmolecular andgeneticbasis.
other(thisgametypicallyyieldsdonations ceedings,Boydetal.(43)arguethat Itisbeginningtoshowpracticalapplica-
of20–30%oftheresource). Although learningfromothers(andnotintelligence tions,asinmedicine.Additionally,it
suchgameshaveweaknesses,theyseemto alone) isthekeytohumansuccess,the hasprovenessential forunderstanding
indicatethathumansarewillingtodonate characteristic thathasmade ussoadapt- thestructureoflife fromcellstomulti-
butonlyatlevelsindicating thatthey able. Initially in human history, these cellular organismstosocieties. Finally,
consistentlyvaluethemselves mosthighly. adaptations involved direct protection itsstudyhelpsus tounderstand the mix
Theseandotherexperiments further in- from the climate, food acquisition, and ofcooperationandconflictthatmakes
dicatethat humansfavorrelatives, long- food storage.Thus,it isa particularkind thehumananimal bothordinaryand
termpartners,andgroupmembersover of intelligence that involves the sharing remarkable.
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Strassmannetal. PNAS | June28,2011 | vol.108 | suppl.2 | 10791
fi ’
Expanded social tness and Hamilton s rule for kin,
kith, and kind
DavidC.Queller1
DepartmentofEcologyandEvolutionaryBiology,RiceUniversity,Houston,TX77005
EditedbyJohnC.Avise,UniversityofCalifornia,Irvine,CA,andapprovedApril22,2011(receivedforreviewFebruary11,2011)
Inclusivefitnesstheoryhasacombinationofsimplicity,generality, of social causation covered explicitly, while trying to maintain
and accuracy that has made it an extremely successful way of reasonable simplicity. For example, I will show how to specify
thinkingabout and modeling effects on kin. However, there are mutualistic social effects in a category that I call kith selection,
types of social interactions that, although covered, are not namedafterthelargelyarchaicwordforacquaintances,friends,
illuminated.Here,Iexpandtheinclusivefitnessapproachandthe andneighbors.
correspondingneighbor-modulatedapproachtospecifytwoother Iwillalsoarguethatitisoftenworthdistinguishingkinandkith
kinds of social selection. Kind selection, which includes green- selectionfromwhatIcallkindselection,partlytoproperlycapture
beardsandmanynonadditivegames,iswhereselectiondepends socialcausalityandpartlybecausetheseformsofsocialselection
onanactor’straithavingdifferenteffectsonothersdependingon actinverydifferentways.Inclusivefitness,developedbyHamilton
whethertheysharethetrait.Kithselectionincludessocialeffects (1),iscloselyassociatedwiththeprocessofkinselection,namedby
thatdonotrequireeitherkinorkind,suchasmutualismandma- Maynard Smith (4). However, they are not the same thing. In-
nipulation.Itinvolvessocialeffectsofatraitthataffectapartner, clusive fitness is an accounting method and maximand. Kin
withfeedbacktotheactor’sfitness.Ideriveexpandedversionsof selection is a process, and it can be described by other kinds of
Hamilton’sruleforkithandkindselection,generalizingHamilton’s accounting. Theobviousexampleistheneighbor-modulated ap-
insightthatwecanmodelsocialselectionthroughasumoffitness proachthatusesthesamefitnesspartitionasinclusivefitnessbut
effects,eachmultipliedbyanappropriateassociationcoefficient. groupsbyeffectsreceivedratherthaneffectsgiven(5).However,
Kinshipis,thus,onlyoneoftheimportanttypesofassociation,but models with other fitness partitions, such as multilevel selection
allcanbeincorporatedwithinanexpandedinclusivefitness. models,alsooftendescribekinselection(6–9).Anotherreasonis
thatinclusivefitnessincludesstandardselectionwherethereare
| |
cooperation kinselection altruism no kin effects at all. Finally, kin selection, when interpreted as
resulting from genome-wide genealogical relatedness, does not
Hamilton’s rule and the associated concept of inclusive fit- coverallindirecteffects.Themostcommonlycitedexamplesare
ness (1) have provided an extremely successful way of greenbeard genes (10), which act based on their own identities
thinking about and modeling social evolution (2). There are a ratherthanpedigreekinship.Thesearecommonlygroupedunder
number of reasons why this is true. It is simple, and therefore, kin selection, but I will arguethat greenbeards are oneexample
userscanapplyitslogicwithease;nevertheless,itisquitegeneral. ofthedistinctphenomenonthatIwillcallkindselection.
Insomeversions,itisexact,andevenlessexactversionsarenot Specifically, I derive an expanded Hamilton’s rule (1) or in-
necessarily a strong concern for field or comparative studies, clusivefitnesseffect(andneighbor-modulatedfitnesseffect)as
wherewecanonlymeasurecrudelyanyway.Crucially,itisoften X X X
sufficientlyindependentofthegeneticdetails,suchasdominance (cid:1)c+ b(cid:3)r+ d(cid:3)s+ m(cid:3)f>0: [1]
andrecessiveness,thenumberofgenes,andtheirallelefrequen-
cies.Thisallowsittobecomeanimportanttoolofthephenotypic ThefirsttwotermslooklikethestandardHamilton’srulebutare
gambit (3) and optimality approaches. It can be used for traits notexactlythesame,becausesomesocialeffectshavebeensplit
wherewedonotunderstandtheunderlyinggenetics,and,infact, offintoadditionalterms.Here,−cisnonsocialdirectfitnessbut
weneverfullyunderstandthegenetics.Italsoconvenientlysep- doesnotincludesomesocialcomponentsofdirectfitness.These
aratesselectionintotwokindsofsummaryterms:effectsonfit- fitnesseffects,m(formutualismormanipulation),aremultiplied
ness(costsandbenefits)andpopulationstructure(relatedness). byafeedbackcoefficient ftogive thekith selection term.Also,
This separation makes the process easy to think about and the kind effects d (deviation from additivity) multiplied by a kind
equations easy to apply. Inclusive fitness points to cause–effect coefficient s(synergism)are splitoff. Theseincludegreenbeard
relations,specificallytothevariouseffectscausedbytheactor’s effectsthatarenormallyinindirectfitnessandsomefrequency-
behavior.Thisfocusonwhattheactorcancontrolallowsustotie dependenteffectsthatareusuallyplacedindirectfitness.Thisis
an expanded form in two senses. First, it covers more kinds of
into the long biological tradition of thinking of actors, or their
social selection or at least, it covers more in a causal manner.
genes,asagents.Additionally,ittellsusthattheseagentsshould
appeartobetryingtomaximizeinclusivefitness. Second, it expands out into the number of terms needed to de-
Inclusive fitness is not perfect. It does not provide the most scribe this causation with two kinds of distinct terms: selection
terms relating social actions to fitness components and associa-
natural way to handle explicit dynamics. It usually takes pop-
ulationstructureasagiven,andwhenitdoesthis,itmaynotyield
insight into how population structure emerges. Although, in
principle, it covers everything, its summary parameters may ThispaperresultsfromtheArthurM.SacklerColloquiumoftheNationalAcademyof
sometimesconcealinterestingcomplexity.Evenitstreatmentof Sciences,“IntheLightofEvolutionV:CooperationandConflict,”heldJanuary7–8,2011,
attheArnoldandMabelBeckmanCenteroftheNationalAcademiesofSciencesand
social causation is incomplete. For example, although it would EngineeringinIrvine,CA.Thecompleteprogramandaudiofilesofmostpresentations
includeanybenefitsfrommutualisminwithothereffectsonthe areavailableontheNASWebsiteatwww.nasonline.org/SACKLER_cooperation.
actor’sdirectfitness,itdoesnotusuallyseparateouttheseeffects Authorcontributions:D.C.Q.designedresearch,performedresearch,andwrotethe
orprovideacausaltreatmentofthem.Manyorallofthesedef- paper.
icits are fixable, although sometimes at the cost of making the Theauthordeclaresnoconflictofinterest.
models more complex and therefore, losing some of the advan- ThisarticleisaPNASDirectSubmission.
tagesoftheapproach.Inthispaper,Iwilltrytoexpandthetypes 1E-mail:[email protected].
10792–10799 | PNAS | June28,2011 | vol.108 | suppl.2 www.pnas.org/cgi/doi/10.1073/pnas.1100298108
toifonthcooseeffiecffieecnttss.tIhactonetsisneunetiatollycdalelscthriibseathveerrseiolantiovef Hhearmitailbtoilnit’ys βWG:G′+βWG′:GβGG′>0: [6]
rulebecauseofthiskeysimilarity. This is Hamilton’s rule, with the direct effect on fitness βWG.G′,
In introducing kith and kind selection, I am not claiming to theindirecteffectofapartnerβWG′.G,andaregressioncoefficient
have discovered new forms of social selection. All of the social of relatedness βGG′. It is a neighbor-modulated fitness form of
situations that I discuss have been explored in other ways. Nor Hamilton’srule,whichtotes upeffectoneachindividual, butit
shouldthistreatmentbeviewed asinvalidating thestandard in- canberearrangedunderquitegeneralconditionstoaninclusive
clusive fitness approach; it can be viewed as a more detailed fitnessformthatswitchesalloftheprimesandnonprimesinthe
version of that approach. My goal here is to present a useful secondtermandthus,totesuptheeffectsofeachindividual(17).
classificationofsocialbehaviorsandderiveacommontheoretical Becauseweassumedweknewthegenes,thisformisextremely
frameworkthatpartakesofthemanyadvantagesoftheinclusive general. It belies the claim that is occasionally made that in-
fitnessapproach. clusivefitnessrequiresmanyassumptions(18).Thoseclaimsare
usually made about phenotypic versions that are used when we
ModelingSocial Effects
do not assume that we know the genetic basis of the traits, and
Inthissection,IillustratethemethodIusetopartitiondifferent thesamelimitationswouldgenerallyapplytoalternativemodels
kindsofselectionusingthemethodsofQueller(6,11).Theap- faced with that assumption. Therefore, proponents of inclusive
proachcloselyparallelsthecausalmodelingapproachpioneered fitness can rightly refute the claim of limited generality. How-
byLandeandArnold(12),whichisfurtherdevelopedforsocial ever, one of the main appeals of inclusive fitness is that it can
traits in the indirect genetics effects approach (13–15). I begin oftenbeusedwithoutknowledgeofthegenes,andtherefore,we
withPrice’s(16)equation9forthechangeintheaveragesome willconsiderthephenotypic gambitshortly.
quantity—here, the average breeding value for a trait, G(cid:1), which Ihavedwelledabitonalreadypublishedmath(6,11),because
canbeforasinglegeneormultiplelociaffectingatrait.Price’s(16) every subsequent derivation in this paper, for which I will not
equationisanidentitythatalwaysholds,butadditionalassump- show the math, follows an exactly parallel procedure consisting
tionsareoftenmade.Here,Ifollowthecommonpracticeofig- ofthefollowing steps:
noringitssecondterm,whichcanincorporateeffectslikemeiotic
i)Writearegressionmodelforthe actor’sfitness.
driveorchangeinenvironment,tofocusonorganismalselection
andadaptation.Price’s(1)equationcanthenbewrittenas ii) Substitute that expression for fitness into the abbreviated
Price’s(16)equation.
— — iii) Divide the covariance into separate terms, one for each
WΔG¼CovðW;GÞ; [2]
term oftheregression.
iv)Dropoutthe α(intercept) term.
showingthatbreedingvalueisexpectedtoincreaseifitcovaries
positively with fitness. Now, consider a social trait where an v) Dropouttheε(residual)termprovidedthatCov(G,ε)=0.
individual’sfitnessisaffectedbybothhisowntraitandthetrait vviii))EAxstkrawchtetnheΔrG(cid:1)eg>res0s.ioncoefficientsfromthecovariances.
ofapartner.Forthemoment,wewillassumethatweknoweach
individual’sgenesforthetrait,withabreedingvalueofGforthe viii)Divide through by the covariance associated with actor’s
focalindividualandG′foritspartner.Fitnesscanbewrittenin fitness.
theformofaregression Wecouldstopatstepvitopreserveamoregeneralequation
(cid:1)
thatpredictsactualchangeinG,butIwillfollowthecustomary
W ¼α+βWG′:GG+βWG′:GG′+ε: [3] step in inclusive fitness analysis of asking the more restricted
(cid:1)
The α is the intercept, and it can be conceived of as the base questionofwhenGincreases.Eitherway,thecrucialstepturns
fitness before any social actions. The β symbols are partial re- outtobestepv.Thisistheonlystepthatinvokesanassumption,
gressioncoefficientsfortheeffectofthefocalindividual’sgenes whichisCov(G,ε)=0.Thisconditionwill,therefore,determine
and the partner’s genes on the focal individual’s fitness, each whether an exact Hamilton-type (1) result can legitimately be
holding the effect of the other individual constant. The ε is the obtained.Whenitdoesdropout,weendupwithanequationwith
thedesiredneatseparationbetweenfitnessandstructureterms,
residual or remainder, including the effects of any other causes
andtherefore,Ihavecalledthistheseparationcondition(6).
and any truly random effects. The regression equation might
makeitseemthatweareinterestedpurelyinestimation,butitis
Causality
also gives us a model of fitness which, depending on the pre-
There is nothing preordained about the predictors used in the
dictors,can beuseful,useless,oreven misleading.
Substituting Eq.2into expression 1yields derivation above. We could attempt to get a result from any
equation predicting or describing fitness. Indeed, it was techni-
— — cally unnecessary to include the partner’s breeding value. If we
WΔG¼C+oCvoðαv;ðGβWÞG+′:GCGov′;ðGβWÞG+:GC′Gov;ðGε;ÞGÞ: [4] aunsedofnollylotwhestfeopcsaliii–nvdiiiviiadbuoavle’s,bwreeesdhionwgvthaaluteG(cid:1)(W>=0wαh+enβWβGWGG+>ε0).
This does not take us far from Price’s (16) equation, but it has
The first covariance drops out, because a constant has zero co- exactly the same level of validity and accuracy as the inclusive
variance.Thelasttermdropsout,becausetheresidualsofare- fitnessresultderivedabove.Whythendoweprefertheinclusive
gressionareuncorrelatedwiththepredictorvariables.Ifweare fitnessresult?Thefirstreason,tobetreatedshortly,isthatleaving
thinking in terms of a model, we assume that ε and G are un- outthepartnerdoesnotworkwhenwetrytoplaythephenotypic
correlated. Next, we can pull the constant β outside of the co- gambit.Theotherreasonisthatincludingthepartnercanprovide
variancetermstogive someadditionalcausalexplanation.Wearenolongerjustsaying
certain genes are associated with fitness; we are giving a break-
— —
WΔG¼βWG:G′CovðG;GÞ+βWG′:GCovðG;G′Þ: [5] down of how that association is caused. It is this causal feature
— thatIwanttoexpandtoincludemorethankineffects.
Average breeding value ΔG will increase when βWG.G′Cov(G, Toillustratethepointaboutcausality,consideranothermodel
G) + βWG′.GCov(G′,G) > 0. Dividing through by the first co- of fitness based on the individual’s breeding value G and the
variance gives βWG.G′ + βWG′.GCov(G′,G)/Cov(G,G) > 0 or phaseofthemoon,representedbyM.IfwesubstituteW=α+
Queller PNAS | June28,2011 | vol.108 | suppl.2 | 10793