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Kin Recognition Mechanisms: Phenotypic Matching or Recognition Alleles? Author(s): Andrew R. Blaustein Source: The American Naturalist, Vol. 121, No. 5 (May, 1983), pp. 749-754 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/2460878 . Accessed: 11/04/2011 14:32 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at . http://www.jstor.org/action/showPublisher?publisherCode=ucpress. . Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press and The American Society of Naturalists are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org NOTES AND COMMENTS 749 KIN RECOGNITION MECHANISMS: PHENOTYPIC MATCHING OR RECOGNITION ALLELES? Kin recognitionin the absence of obvious opportunitiesto learnone's kinis an importantbiological phenomenonand elucidatingthe mechanismby which the recognitionis achieved is a major challenge. Such recognitionis importantbeacts to kin ifotherfactorssuch as proximityto cause it can facilitatepreferential withotherindividualsare not correlatedwithkinshipand if nepoor familiarity tismhas been selected for. But preciselyhow is kin recognitionachieved? It is criticalto keep in mind that the essence of Hamilton's (1964) inclusive fitness model is that,all otherthingsbeing equal, individualsshould behave differently towardone anotherbased on geneticrelatedness,regardlessof the mechanismby whichindividualsdeterminethe degreeof geneticrelatednessamongthemselves. There are fourpossible mechanismsproposed forkin recognition(reviewedby Alexander 1979; Bekoff1983; Dawkins 1982; Holmes and Sherman 1982). 1. Recognitioncan be based on spatial distribution.-Ifrelativesare distributed predictablyin space, altruisticacts mightbe selected forif the acts are directed toward those individualsin a particularlocation. Such a location preferentially may be a home site or territory. 2. Recognitioncan be based on familiarityand priorassociation.-If relatives predictablyoccur in appropriatesocial circumstances,recognitioncould occur throughsocial learning(Alexander 1979). Thus, individualsof the same litter withinthesamenestor thosefromone clutchmaylearnto recognize"familiar" and individuals(see Bekoff1981, 1983fora detaileddiscussionof familiarity meet Relativesmightalso recognizeone anotheriftheypredictably recognition). in the presence of a thirdindividualwho is familiarto each of them.One example of this may be two maternallyrelated half siblingsfrom differentlittersthat interactwiththeircommon mother(Holmes and Sherman 1982). 3. Recognition could occur throughphenotypic matching.-In phenotypic matchingan individuallearns and recalls the phenotypesof relativesor of itself The is correlatedwithgenotypicsimilarity). (assumingphenotypicsimilarity betweenits ownphenotype individual thenassesses similarities and differences andunfamiliar Thus,forexample,ifchemicalsorodorsareinvolved conspecifics. butmustbe learnedfor in kinrecognition, theymayhave a geneticcomponent, kinrecognition to occur. 4. Recognition could be achieved by the action of recognitionalleles.Phenotypescould be used in recognitionindependentof learningif recognition alleles existed. In this system,the phenotypicmarker(e.g., a particularchemical or odor) and the knowledgeof thatmarkerhave geneticbases. Mechanisms 1 and 2 are actually indirectmeans by which kin could be aided because kinper se are notactuallyrecognized,ratherthoseindividualsmostlikely to be kin are the ones most likelyto be aided and thus recognitionerrorsmay Am. Nat. 1983. Vol. 121, pp. 749-754. ? 1983 by The Universityof Chicago. 0003-0147/83/2105-0012$02.00. All rightsreserved. 750 THE AMERICANNATURALIST occurifthesearetheprimary meansofrecognition. Recognition errorscouldalso 3 wereutilizedifindividuals occurifmechanism havea similar phenotypic marker but such a markeris coded by different genesor ifthe same genescoded for similarmarkersbut the individualswere unrelated.The selectivebasis for whereasformechanism 4 itis 1 and 2 is overallgeneticrelatedness, mechanisms whowillbe thesharing ofa particular gene(orsmallsetofgenes)thatdetermines or theparticular aided. Mechanism3 can dependon overallgeneticrelatedness gene(s) involvedin producingthe marker.Mechanisms3 and 4 are the ones theoretical discussedin mostdetailwhenconsidering aspectsofkinrecognition (see discussioninDawkins1982).The problemis, thehypothesis invoking recognitionalleles has generallybeen revokedin favorof the phenotypic matching oftherecognition allelehypothesis is basedprimarily The refutation hypothesis. on theoryalthoughempiricalevidenceexiststhatis consistentwithboththe and recognition allelehypotheses. phenotypic matching THEORETICAL ARGUMENTS CONCERNING THE EXISTENCE OF RECOGNITION ALLELES Alexanderand Borgia(1978)suggestthattheexistenceofrecognition allelesis fortwobasicreasons.First,as pointedoutoriginally unlikely byHamilton(1964, p. 25), theactionsofrecognition alleleswouldbe complex.Suchallelesmust(1) be expressedphenotypically, (2) cause therecognition ofthephenotypic marker, and (3) enablethoseindividualscarrying copies of theseallelesto favorother individuals also carrying thealleles(fordetaileddiscussionssee Alexander1979; AlexanderandBorgia1978;HolmesandSherman1982).Thissystemis similarto the "greenbeard" altruistic systemsuggestedby Dawkins(1976)in whichhe stated,forillustrative purposes,thatone suchphenotypic marker might be a green beard. Secondly,recognition alleles may be "outlaw" alleles (Alexanderand Borgia1978).Outlawsare allelesthatfavorthemselves at theexpenseofall other allelesin thegenome(including thoseat othergeneloci) (Alexanderand Borgia 1978). Segregationdistorters or meioticdrivegenes are examplesof outlaws becausesuchgenesarefavoredat theirownlocusandappearinmorethan50%of thegametesproduced. The theoretical of recognition alleles theimprobability arguments concerning havebeengenerally accepted(examplesare HolmesandSherman1982;Kurland 1980;Sherman1980;butsee Rothstein 1980).Thisis interesting becauseHamilton (1964, p. 25) was not so positivethatrecognition alleles are impossible.He thatthesamea prioriobjectionsmaybe arguedagainsttheexistenceof suggested assortative mating whichhas evolved"despiteitsobscureadvantages."It is even questionablethatrecognition alleles wouldbe outlaws(see Ridleyand Grafen and Barash1982).Acceptanceofthetheoretical 1981;Rothstein arguments may lead to premature rejectionofthepossibility ofrecognition alleles. Phenotypic matching seemsto be thefavoredmechanism forkinrecognition even thoughempiricalevidenceconsistent withbothphenotypic matching and recognition allelesexists.The problemis, itis probablyimpossibleto falsify the phenotypic matching hypothesis. 751 NOTESAND COMMENTS EMPIRICAL EVIDENCE CONSISTENT WITH BOTH PHENOTYPIC RECOGNITION MATCHING AND ALLELES matching To illustrate theproblemof differentiating betweenthephenotypic and recognition allele hypothesesI willdescribetheresultsof threerecentkin recognition studies. In theirextremely Holmesand Sherman important workon groundsquirrels, (1982)reported thatBelding'sgroundsquirrels (Spermophilus beldingi)thatwere electrophoretically identified as fullsistersand maternalhalfsisters(withinthe same litter)seemedto treateach otherdifferently whenaggressive as yearlings and amicablebehaviorwas quantified. Full sistersfoughtsignificantly less often thanhalfsistersandchasedeachothersignificantly than lessoftenfromterritories didhalfsisters.Bothtypesofsiblingsshareda commonnestandevena common uterus.Holmesand Sherman(1982,p. 506) suggestthedata imply". . sibling inadditionto simple recognition inS. beldingiis augmented bysomemechanism matching may associationinthenatalburrow."Theyalso suggestthatphenotypic be involvedin differentiating betweenmaternal halfsiblingsandfullsiblings(see p. 512). Individualscould learntheirown phenotypic traitsuchas an odorand thenassess thesimilarities anddifferences betweenthemselves andotherindividuals theycontact.Thus, fullsiblingsmay smellmoresimilarthanhalf-sibling groundsquirrels. Wu et al. (1980)showedthatunfamiliar macaques infantpaternalhalf-sibling nonrelawerepreferred (Macaca nemestrina) inassociationtestsoverunfamiliar tives.This studyis particularly powerfulbecause maternallearningeffectsare absentsinceonlypaternaland notmaternalhalfsiblingswereused. Therefore maternal"labeling"or "imprinting" is unlikely (see Blausteinand O'Hara 1982 fordiscussion). Phenotypic matching was invokedsubtlybyWu et al. (1980)as themechanism ofitself formacaquekinrecognition. experience Theysuggestthatan individual's couldbe thebasisforlatersocialpreferences. Dawkins(1982,p. 150)states"my betis thatthemonkeys ofrelativesto perceivedfeatures recognizeresemblances of themselves"(i.e., phenotypic Bekoff(1983) correctly pointsout matching). with thatthemonkeysin theexperiments of Wu et al. wereallowedto interact nonrelatives forrelativesmaybe based priorto testingand thatlaterpreference on a modelsimilarto theone proposedby Bateson(1978,1980,1982)to explain from different mateselection,wherebyindividuals choosemateswhoare slightly the individuals withwhomtheywerereared.UnderBekoff's(1983)interpretation and a be an artifact kinpreference observedby Wu et al. (1980)may preference fornonkinmayhaveoccurredhadthemacaquesbeenrearedwiththeirhalfsibs. relevantto Studieson Cascades frog(Rana cascadae) tadpolesareparticularly thisdiscussionbecause of thevariousrearingregimesemployed(Blausteinand O'Hara 1981,1982;O'Hara andBlaustein1981).In thefirst seriesofexperiments animalsrearedwithsiblingsand thoserearedin a mixedgroupof siblingsand (O'lHara.and nonsiblings preferred to associate withsiblingsover nonsiblings Blaustein1981). In the second experimental seriesindividualsrearedin total isolationfroman earlyembryonic stagepreferred to associatewithunfamiliar 752 THE AMERICANNATURALIST siblingsover unfamiliar nonsiblings (Blausteinand O'Hara 1981).In the third experimental series,tadpolesrearedwithsiblingsor in isolationpreferred to associate withfullsiblingsover halfsiblings(eithermaternalhalfsiblingsor paternalhalfsiblings)and halfsiblingsovernonsiblings (eithermaternal or paternal; Blausteinand O'Hara 1982).Furthermore, inthelatterseriesofexperiments thejellymassthatsurrounds eachclutchandis producedbyfemaleswas removed fromtwoclutches.One clutchwas rearedwithnojellymassand tadpolesfrom thisgrouppreferred to associatewithunfamilar fullsiblingsover paternalhalf siblings.Tadpolesfroma secondclutchwererearedwithjelly froma paternal half-sibling clutchandtadpolesrearedwiththisforeign jellypreferred toassociate withunfamiliar fullsiblingsoverpaternalhalfsiblingsfromwhichtheirforeign jellycame. Thesejellytransplant experiments are important becauseithas been proposedthatfemalesmay"label" theirclutchesthrough thejellycoatsandthus tadpolescouldlearntoassociatewithindividuals fromthesameclutchbylearning containedwithinthejellyand "absorbed"bythetadpolesduring characteristics development (see discussionin Blausteinand O'Hara 1982). Resultsof these tadpoleexperiments reveal thattadpolescan differentiate betweenindividuals ofvarying degreesofrelatedness, eveniftheyare rearedin mixtures ofsiblings andnonsiblings, inisolation,orwithfullsiblings.Holmesand Sherman(1982)interpret theresultsofthefirst twoseriesofexperiments (Blausteinand O'Hara 1981; O'Hara and Blaustein1981)as a possibleexampleof phenotypic matching. According to proponents ofphenotypic matching, tadpoles rearedin isolationcouldlearntheirowncues and latermatchtheirownphenotypeswithotherindividuals, even totallyunfamiliar ones, and thenmaketheir associationchoice. How does one explainthe resultsof tadpoleschoosingto associatewithunfamiliar siblingsoverunfamiliar nonsiblings afterthesetadpoles wererearedin mixedrearingregimes?It wouldbe easy to invokephenotypic matching foreventheseresults.One couldsaythattadpolesrearedwithnonsiblingsand siblingsare still"closer to themselves,"and thusan individual'sown odoris themostpervasiveone, so itschoicecouldstillbe madeby matching its ownphenotype withotherphenotypes. willobvior thoseusingpaternalhalfsiblings, Actually,isolationexperiments, betweenthe phenotypic ously yieldequivocalresultsas faras differentiating to allelehypotheses is concerned.It maybe impossible andrecognition matching thephenotypic For example,ifsingletadpolesfrom falsify matching hypothesis. one clutchwererearedwithnumerousnonsiblings (as in O'Hara and Blaustein to associatewithsiblingsin associationtests,one could 1982)and stillpreferred was themostpervasive stillarguethattheindividual'sown odoror phenotype alleles could be invokedbut recognition one. Therefore, phenotypic matching thoseindividualsthey cannotbe ruledout. If, however,the tadpolepreferred allelehypothesis thentherecognition wererearedwith,in thiscase, nonsiblings, and would not be supported(see Buckle Greenberg1981; Greenberg1979). couldonlybe achieved allelehypothesis Unequivocalsupportfortherecognition an individual to the of byexperimentally masking ability perceivethephenotypic difficult. This seems markerin questionthroughout ontogeny. Theresultsconcerning groundsquirrels (HolmesandSherman1982),macaques NOTES AND COMMENTS 753 (Wu et al. 1980), and tadpoles (Blaustein and O'Hara 1981, 1982; O'Hara and Blaustein 1981) are consistentwith both phenotypicmatchingand recognition allele explanations. In fact, there may be essentiallyno differencebetween the two mechanisms. Phenotypic matchingmerely specifies a learned component whereby geneticallyencoded informationis manifested.If the members of a populationhave identicalgenes enablingthemto learntheirindividualphenotypic markersand to aid otherswiththe same marker,thenthe differencebetween the two mechanismsis trivial.Proponentsof phenotypicmatchingseem to require that there be no learningbefore recognitionalleles are considered. However, virtuallyno complicatedbehavior is totallyimperviousto learning. AlthoughI do not necessarilyendorse theirexistence, I recommendthat we keep an open mind as to the existence of recognitionalleles. Certainlythe empiricalevidence presentedis consistentwitheitherexplanation.Both mechanisms functionsimilarlyand lead to the same evolutionarypredictions. Both mechanismsallow an individualto recognizeotherstheyhave neverhad contact with. Perhaps parsimony should prevail in the final consideration.Given the theoreticalargumentsagainst the existence of recognitionalleles it may be suggestedthatphenotypicmatchingis themoreparsimoniousexplanation.However, according to the empiricalevidence, recognitionalleles provide an explanation that is at least as parsimoniousand perhaps more so. Should theoryoutweigh empiricalevidence when parsimonyis to be invoked? It is importantto evaluate such questions carefully. ACKNOWLEDGMENTS I wish to thankKathy Lumas, Rick O'Hara, and especially Steve Rothsteinfor criticallyreviewingthe manuscriptand providingmanyvaluable suggestionsfor improvingit. Kathy Moore provided valuable discussion. Two anonymous reviewers offeredextremelyvaluable suggestionsfor improvingthe manuscript. Financial support was provided by NIH Biomedical Research Support Grant RR07079, the O.S.U. Research Council, and NSF grantBNS 8120203. LITERATURE CITED Alexander,R. D. 1979. 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An investigationof siblingrecognitionin Rana cascadae tadpoles. Anim. Behav. 29:1121-1126. 1982. Kin preferencebehavior in Bufo boreas tadpoles. Behav. Ecol. Sociobiol. 11:43-49. Ridley, M., and A. Grafen. 1981. Are greenbeard genes outlaws? Anim. Behav. 29:954-955. Rothstein,S. I. 1980. Reciprocal altruismand kin selectionare not clearlyseparable phenomena.J. Theor. Biol. 87:255-261. Rothstein,S. I., and D. P. Barash. 1982. Gene conflictsand the conceptsof outlaw and sheriff alleles. J. Social Biol. Struct.(in press). Sherman,P. W. 1980. The limitsof groundsquirrelnepotism.Pages 505-544 in G. W. Barlow and J. Silverberg,eds. Sociobiology: beyond nature/nurture? Westview Press, Boulder, Colo. Wu, H. M. H., W. G. Holmes, S. R. Medina, and G. P. Sackett. 1980. Kin preferencein infantMacaca nemestrina.Nature 285:225-227. ANDREW R. BLAUSTEIN DEPARTMENT OF ZOOLOGY OREGON STATE UNIVERSITY CORVALLIS, OREGON 97331 SubmittedMay 27, 1982; Revised October 5, 1982; Accepted October 22, 1982