Download Kin Recognition Mechanisms: Phenotypic Matching or Recognition

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
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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.
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ANDREW R. BLAUSTEIN
DEPARTMENT OF ZOOLOGY
OREGON STATE UNIVERSITY
CORVALLIS, OREGON 97331
SubmittedMay 27, 1982; Revised October 5, 1982; Accepted October 22, 1982