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Complex Colony Structure in Social Insects: I. Ecological Determinants and GeneticConsequencesAuthor(s): Valerie S. Banschbach and Joan M. HerbersSource: Evolution, Vol. 50, No. 1 (Feb., 1996), pp. 285-297Published by: Society for the Study of Evolution

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Evolution, 50(1), 1996, pp. 285-297

COMPLEX COLONY STRUCTURE IN SOCIAL INSECTS: I. ECOLOGICALDETERMINANTS AND GENETIC CONSEQUENCES

VALERIE S. BANSCHBACH1 AND JOAN M. HERBERS2

Department f Zoology, Universityf Vermont,urlington, ermont5405

Abstract.-For ocial nsect pecies, ntraspecificariationn colony ocial structurerovides n opportunityo relatethe evolution f social behavior oecologicalfactors. he species Myrmicaunctiventriss a cavity-dwellingorestant that xhibits erydifferentolony tructuresntwopopulationsnthenortheasternnited tates.Combined atafrom easonal ensuses, llozyme lectrophoresis,ndworker ostilityests howed hat population fM.punctiventrisin Vermont as strictly onogynousnd seasonally olydomous. he same procedures howed hat population fM. punctiventrisn New York was facultativelyolygynousnd predominantlyonodomous.Geneticrelatednessamong olony-mates as notdifferentrom amilton'sxpected alues ntheVermont opulation nd was consistentwith ittle xchange f antsbetween olonies ndsingle-matingfqueens. n contrast,elatedness as lower nNewYork, nd examination f nest-mateenotypes evealed xchange f antsbetween olonies,high ates fcolony ossand replacement f queens, or multiple-matingf queens. The genetic tructuref the Vermont opulationwasconsistent ith o nbreeding,ut nNewYork, hepopulation enetic tructureeflected icrogeographicubdivisionand nbreeding.revious tudy f the ntcommunitiest these ites mplicates est-siteimitationnNew York s aprimary onstraintn social structure.

Keywords.-Inbreeding, olydomy, ueennumber, elatedness,ocial insects.

ReceivedJuly 5, 1994. AcceptedJanuary , 1995.

Since Hamilton's (1964) developmentof inclusive fitnesstheory o explain the originof eusociality in the haplodiploidHymenoptera,much of the work addressing the evolution ofinsect societies has focused on the importance of geneticrelatedness and kin selection. Numerous studies have mea-sured the genetic relatedness of social insect colony-matesto understand he evolution of social behavior via kin selec-tion (reviewed in Breed and Page 1989). However,formanysocial insect species, colony structure oes not match Ham-ilton's assumption thatthere is only one queen which has

mated only once. Accordingly, observed relatedness amongsocial insect colony-mates has often been low (reviewed inHolldobler and Wilson 1990 for ants; Ross and Carpenter1991a for social wasps; and Kukuk 1989 for a primitivelysocial bee species). Thus, recentlysome studentsof socialinsects have suggested that the studyof genetic relatednesshas been overemphasized (Ito 1993), whereas theecologicaldeterminants f social behavior need to receive much moreattention Strassman and Queller 1989; Herbers 1993). Theimportance of ecological factors n promoting ociality haslong been stressed by workers studying a wide varietyofotheranimals (reviewed in Slobodchikoff 1988), includinglions (Scheel and Packer 1991), jays (Woolfendenand Fitz-patrick 1978; Marzluff nd Balda 1988), and spiders Rypstra

1993) but has been paid relatively ittlenotice bythosework-ing with the insect societies.Studyingdifferences n social structure etween popula-

tions of a species can reveal the selective pressuresthat acton sociality (Ross and Carpenter 1991b; Keller and Vargo1993). Ant species are excellent subjects for these compar-isons because even thoughthey xhibit thehighestdegreeof

1 Present ddress: epartmentfBiology, avidsonCollege,P.O.Box 1719, Davidson NC 28036-1719. E-mail: [email protected]

2 Present ddress:Department f Biology,Colorado State Uni-versity,Fort Collins, Colorado 80523. E-mail: [email protected]

social organization,usociality, hey lso exhibit reat ari-ability othbetween nd within pecies, n such specificsftheir ocial systemss queennumberHolldobler ndWilson1990; Ross and Carpenter 991b; Keller 1993). Here, wecompare ocialstructureor wopopulations fthe nt,Myr-mica punctiventris,elating cological factors o observedintraspecificifferences. e fully ocument ocial structurethathas two components:1) the genetic olonystructurethat epends pon uch haracteristicsf hebreedingystemas number f queens,number fmatings,nd level of in-

breeding Wade 1985; Ross 1993); and 2) other spectsofcolony tructurencluding ehaviors uch as polydomy ndexchange f workers etween olonies Holldobler nd Wil-son 1977;Herbers 984; PamiloandRosengren 984). In acompanion aper,we explorepatternsfreproductivello-cation Banschbach ndHerbers 996). Ourwork hus iffersfrom revious omparisons f populations ithin nt pecieswhichhave examined nly fewaspectsof social behavior(e.g., queen number nd/or elatedness; lmes and Wardlaw1982; PamiloandRosengren 984; Ross andFletcher 985;Herbers 986a; Elmes and Petal 1990; Ito 1990; Boomsmaet al. 1993;Herbers nd Stuart,npress).

We highlighthe mportancef differencesnqueennum-berbecause queennumbers a highly ariable omponent f

ant social structurehathas great mpact n relatednessfcolony-matesnd, hus, n their nclusive itness. olldoblerand Wilson 1977) first elineatedhe mportancef variablequeen number,nd their eminalpaper spurred large it-erature n theproblem,s evidenced y a recent ompilationof workKeller 1993). Keller ndVargo 1993) pointed utthat olygyny ay ctually e thepredominanttate fqueennumbernants.Why houldmultiple ueenscoexist ncol-onies,when his ituationmay oweroverallrelatednessfcolony-mates?nparticular,e must etermine hy queenaccepts ther ueen(s) ntoher stablishedolony secondarypolygyny), hichs themost ommonmechanismroducingpolygynyHolldoblerndWilson1990).The databasewhich

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286 V. S. BANSCHBACH AND J. M. HERBERS

we can use to answer his uestion s small, ut nsome asessecondary olygyny as been linkedto ecological factorssuch as predation nd nest-sitevailabilityHerbers 993).

We also focusuponpolydomy,n importanteature fmany nt pecies' social structurenwhich single nt olony

occupiesmultiple ests,usually n close proximityo oneanother.Workers, rood, nd queens maybe exchanged e-tween hese multiple ests of a colony.Polydomyndpo-lygyny ypically o-occur Holldobler nd Wilson 1977).Thus, tudyinghe ffects feither tate s made difficultytheconfoundingresence f theother tate.

Our study pecies, M. punctiventris,epresentshe onlywell-describedxample of polydomy inked o monogyny,incontrasto numerousxamples fpolygynous-polydomousant pecies e.g.,Pamilo nd Rosengren 984; Herbers 991;Herbers nd Grieco1994;Herbers nd Stuart,npress).Sny-der and Herbers1991) firsttudied population f theantM. punctiventrisn Vermont hichhas colonies thatfrac-tionatenspringndsummer utrecoalesce nfallfor ver-

wintering.n thispopulation,olonies are strictly onogy-nous (Snyder nd Herbers1991). This strictmonogynysunusualfor hegenusMyrmicacompare o Elmesand Kel-ler's (1993) reviewof studiesof queen number n severalEuropeanMyrmicapecies).Here,wecompare olony ocialstructuref thismonogynous,olydomous ntpopulationwith hat f a secondpopulationnNew York o discern heecologicalandgenetic actors hat elate o social behaviorofthis pecies.

MATERIALS AND METHODS

Our study rganism,M. punctiventris,nhabits emperateforestsnNewEngland ndranges outh o Tennessee nd

west to Iowa (Creighton 950). Preformedavities, uch ashollowed-outticks, corns, nd rolled eaves are thepre-ferred est ites f M.punctiventrisHerbers 989) and deadarthropodsrethepreferredood SnyderndHerbers 991).Despite taxonomic roblemswith he genus Myrmica s awhole,M. punctiventrisepresents well-definedpecies,morphologicallyuitedistinct rom tscongenersA. Fran-coeur, ers.comm.1988).

We studied opulationsfM.punctiventrisnVermontndin New York.Ourstudy ite nVermont as at Mallett's ayStatePark, nChittendenounty,t 93-foot levation. heforest t this site s mixed-hardwoodecondgrowth omi-natedby beech, maple,birch, nd oak trees.The antcom-munityt this itehas beendescribed yHerbers1989),and

the ocial structurefM.punctiventrisas been described ySnyder nd Herbers1991). Ourstudy ite nNew Yorkwasat theE. N. Huyck reserve,nAlbanyCounty,t 1500-footelevation. he forest t this ite s older econdgrowthom-inated ybeech,hemlock, nd oak trees. he ant ommunityat theNew York siteconsists f fewer peciesand is char-acterized y owernestdensities han he antcommunitytourVermontite Herbers 989).

To fully haracterize heseasonalstructuref bothpop-ulations f M.punctiventris,e collected ntnestsfrom hetwo ites t three imes uring 992:springmid-May),um-mer (mid-July),nd fall (mid-September).We excavatedthree 6-m2 lotsduring ach collection eriod t each site.

Differentocal areaswithin he iteswereused for ollectionin differenteasons such that ne collectiondid not affectsubsequent ollections.During these excavations,we in-spected very tem n the eaf itter n theplotsfor ntnests.Locations of nests were mapped and the nests themselves

werebaggedfor ransporto the aboratory. lthough hissampling erved o replicate he data collectedon the Ver-mont opulation y Snyder nd Herbers 1991), it was thefirst etailed xamination f the New York population. oaugment nformationn thisnew population,we made ad-ditional ollectionsn mid-August,993. At that ime,wecollected ntnests s we encounteredhem ather han romsystematicallyxcavatedplots n order o increase amplesizes.

In the aboratory, e putnests n plasticboxes and main-tained hem ccordingostandard racticeHerbers ndCun-ningham 983). We censusednests, ounting ueens,work-ers, arvae, pupae,and alates immediatelyfter ollectionandperiodically uring ach season,untilOctober.We alsochecked ests or hepresence f ocial parasites, hich avebeen observed or his pecies S. Cover, ers. omm.1991).All ants were frozen or gel electrophoresist the end ofOctober.

We performed orkerhostility ests to delimit olonyboundaries. ollowing nydernd Herbers1991), we intro-duced ntsfrom ifferentests nto neanother's estboxestodetect ggression. operformhese ests,wedustedwork-ers from ach nestwithfluorescent-coloredowder ndin-troducedhem,neworkert a time,nto ll other ests romtheir lot.Each pairof nestswithin plotwas testedwithreciprocalntroductionsnd all testswerereplicated tleastonce.Forplotswithmore han 0 nests, esting ll pairwisecombinations as impractical,nd thereforee employedsubsamplingcheme hat nsured hatwe could determine

all clusters ffriendlyests.During hetests,we scored nteractionsetween nts ona scalefrom to 3. The owest core, , representedo visibleaggression; scoreof1was given fantsopenedmandiblesat one another; scoreof2 was given fantsnipped t orbitoneanother;nd themaximumcore, ,wasgiven fantsdragged, arried, rpulledon one anotheras inSnyderndHerbers 991).Nestpairs hat ad a mean coreof 1weredeemed "amicable" and hencecon-colonial.

We determinedhenotypes orpolymorphic roteins oinfer enotypesf the ants nd estimateheir elatednessonest- ndcolony-mates.Weused cellulose-acetateels andstainedforthree oci: GPI (glucose-phosphatesomerase),MDH (malatedehydrogenase),ndPGD (phosphogluconate

dehydrogenase).We examinedallozyme patterns or allqueens, ll alates, ndupto 10 workers rom ach antnest.Theelectrophoreticata allowedus to calculate elatednessbetween ll pairings fworkers, ueens,males, nd femaleswithin ests, or ach seasonandsite,using heQueller ndGoodnight1989) algorithm. e also calculated -statistics(Wright 951) to lookfor videnceof inbreedingndpop-ulation ubdivisionntime ndspace.

RESULTS

CompositionofNests

Census data revealedmarked ifferencesn queendistri-butionmongnests f the wopopulations. ests nVermont







ECOLOGICAL DETERMINANTS OF COLONY STRUCTURE 287

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IRE2Queens

FIG. 1. Distributionsf queens n nestsduring ifferenteasonsforour 1992 samplesof (A) theVermont opulation nd (B) theNew Yorkpopulation.

always contained eitherone or no queens (Fig. IA), just asSnyderand Herbers 1991) foundduring heir1985 and 1986censuses. In contrast,New Yorknestshad up to four queens(Fig. iB). The distributions f queen number by season innestswere significantly ifferentt the two sites (X2 = 34.5,df = 2, P < 0.0001). Furthermore,he New York data didnotshow significantnnual variation summer1992 vs. sum-mer 1993, G = 0.28, df = 2, P = 0.87).

Our samplingcheme llowedus to ook for easonalvari-ation nqueennumber.n Vermont,ueen number id varyfrom pring ofall G = 13.9, df= 2, P < 0.001),with hesmallest roportionfqueenrightests ccurring uringhesummer,hepointof maximum olonyfractionationn the

seasonal ycle fpolydomyFig. lA). InNewYork, owever,thedistributionsfqueennumbers ere tatic hroughoutheyear (G = 3.7, df = 4, P = 0.45); that is, therewas noindication f seasonal polydomyn New York Fig. iB).

Differencesnabundance f other astes nd ife tages nnests t the two sites accompanied he differencen queennumber.Worker umbernVermont as significantlyowerthan nNew York Fig. 2; Mann-Whitney = 2,496,n, =64,n2 = 140,P < 0.0001),and numbers feggs, arvae, ndpupaewere often ower n Vermont s well (Table 1). WeperformedMANOVA on the og-transformedensus data(workers, ggs, arvae,pupae)with ite, eason,andqueennumber s independentariables. he wholemodel ndeacheffectwas signficant,s were all of the interactionerms

(wholemodelF = 36.4,df= 11,P < 0.00001).Wethereforescrutinizedhe ensusdata more ully or ffects fvariationin season and queen number. he results f two-wayAN-OVAs (Table 2) showthat ueennumber as a strongffecton nestdemographynNew Yorkbut not nVermont. heeffectsf season on workersnd mmaturesrecomparableatboth ites Table 2). Thus,variationn nestcontents e-tweenthe two sites is linked moststronglyo the corre-sponding ifferencesnqueendistribution.

Finally,nestdensitywas highernVermont han nNewYork Mann-Whitney = 12.5, n1 = 8,n2 =9, P = 0.02).Averagenestdensity as 18.1 ? 5.0 SE nests er36-M2plotin Vermont8 plots)as compared o 7.2 ? 2.4 SE nestsper36-M2plot nNewYork 9 plots)during 992.

Composition of Colonies

Nestswere ssigned o coloniesby ynthesizingehavioraland geneticdata. The worker ostilityestsallowedus todelimit6putativeolonies nourVermontamples. wenty-sevenofthese56 putative olonies consisted fmorethanone nest. Most interactions etweenVermont estswerescored s 0 (completely micable)or 3 (completely ostile).Table 3 shows that ntermediatecoreswere observed essthan20% of the time.These testswerevalidatedby self-introductions,hichwerenearly 00% amicablemeanhos-tilitycore= 0.03 + 0.01 SE, n = 66 tests), ndreplicationsof pairwisecombinations hichshowedhighcongruence

(85% of 612 testshad identical coreson all replicates).Furthermore,eciprocalnteractionsere tronglyorrelated.If workers rom estA attackedworkers rom estB, thelikelihoodwas veryhighthatworkers romnest B wouldalso attackworkers rom estA (Kendall'sTau = 0.37,n =

156,P < 0.0001).By contrast,nourNew York amplesfrom 992,we de-

limited 5 colonies,of whichonlynineconsisted fmorethan ne nest.That s, veryfewnests ppeared obelong olarger polydomouscolonies. Moreover,workerhostilityscoresweremore mbiguousn New York han nVermont;24.9% of the nteractions ere scored s 1's and 2's (inter-mediate evelsofaggression; able3). The distributionsf








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FIG. 2. Mean numberof workers + SE) in nests in (A) Vermontand (B) New Yorkduringdifferenteasons, grouped by queen num-ber in nests.

theworkerhostility cores at the two sites were differentG= 21.8, df= 3, P < 0.001). Although elf-introductions ereoften micable (mean hostility core = 0.27 ? 0.11 SE, n =51 tests), replicate introductions howed slightly ower fi-delitythan nVermont78% of217 tests had identical scoreson all replicates) and the correlationbetweenreciprocalnestpair test scores was weaker in New York (Kendall's Tau =

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TABLE 2. Effects f season ndqueennumber n nest ompositionof M. punctiventrisn New York and in Vermont.Two-way ANO-VAs to determineignificantreatmentffects ere calculated orlog-transformedariables or ach site separately. ueen numberwas categorized s 0, 1, or >1.

Vermont New York

E-ffectsf: Season Queen S. x Q. Season Queen S. X Q.

Workers*Eggs ** * ** ** **Larvae**Pupae ** ** ** **

* Bonferroni-corrected < 0.05; ** Bonferroni-corrected < 0.01.

0.18, n = 100, P < 0.006). We conclude thatcolony bound-aries in New York are more ambiguous thanin Vermont.

If a colony was more thanone meter from the edge of aplot and ifall M. punctiventris estswithin one-meter adiusof the colony had been collected and testedforaggression,

thenwe deemed the colony "complete" (following Snyder1988). In Vermont,16 of 56 colonies thatwe located werecomplete. Of these, eight = 50%) were queenless and pre-sumably orphaned. n New York, 17 of 45 colonies thatwecensused were complete; only five of these (= 29%) werequeenless and presumed orphaned.Because of the ow num-bers ofcomplete colonies, statistical nalyses used data fromall colonies unless noted.

We examinedourcolonydata for easonal changes innum-bers of nests comprisingcolonies at both sites. In Vermont,a seasonal patternof colony fission in springand summer,followed by fusion in fall was evident (Fig. 3). In spring,most colonies consisted of one or two nests, and in summermore colony fragmentswere found,followed by a return o

one nest per colony in fall. There was little suggestion ofcolony fractionation ccurring in New York, because themean number of nests per colony remained close to onethroughout he year (Fig. 3). Only nine out of 45 coloniesidentified n New York were polydomous, while 25 out of56 colonies identifiednVermontwerepolydomous. Overall,colonies consisted of more nests in Vermont than in NewYork (Fig. 3; Mann-WhitneyU = 915.5, n, = 56, n2 = 45,P = 0.003). Of the nine polydomous colonies in New York,five of these colonies contained multiple queens, and threeout of the five colonies with multiple queens had queensliving in different ests.

Like nests,colonies differed etween thetwosites nqueennumber. n Vermont,only two out of 56 colonies were po-

lygynous (both in spring and both containing just twoqueens), whereas in New York 15 out of 45 colonies werepolygynous.The sites differedn their rithmeticmeannum-berof queens per colony (Mann-WhitneyU = 911, n1 = 56,n2 = 45, P < 0.01) as well as the harmonicmean (Table 4),whichis themostrelevant tatistic orpredicting elatednessstructureWade 1985; Ross 1993). A major difference romthe nest-level demographics is thatcolonies did not differbetween sites in their verage numberofworkers, arvae, orpupae (Table 4; Mann-WhitneyU tests,n, = 56, n2 = 45, P> 0.05) whereas nests did (Table 1; Fig. 2).

Density of colonies on plots was not differentn 1992 forNew Yorkas comparedto VermontMann-WhitneyU = 47.5,

TABLE 3. Worker ostilitycoresforM.punctiventrisnVermontandNew York,1992. Values representounts f pairsofnests hathad the ndicatedmeanworker ostilitycore.Percentagesf nestswith he ndicatedmean core re n parentheses elow counts. hevertical inedenotes he utoff etween micable 0, 1) andhostile(2, 3) scores.

Worker ostility cores:N of

0 1 2 3 tests

Vermont 121 21 90 380 612(19.8%) (3.4%) (14.7%) (62.1%)

NewYork 26 16 58 197 297(8.8%) (5.4%) (19.5%) (66.3%)

MeanhostilitycoresVermont: 2.26 + 0.05 SE, n = 612New York: 2.52 + 0.05 SE, n = 297

n, = 8, n2 = 9, P = 0.27). In New York, the meannumberof colonies per plotwas 4.9 ? 1.5 SE (9 plots) as comparedto a mean of 7.0 ? 1.6 SE colonies per plot (8 plots) in

Vermont.In sum, many demographicfeatures f colonies are similar

in our two populations.The Vermont nd New York coloniesdiffered rimarily n how many queens theycontained andin how extensivelythey fragmented uringthe growingsea-son.

Geneticsof Colonies and Populations

We assayed ants by gel electrophoresisforallozyme vari-ation at three loci (Table 5). The frequencies of the mostcommon alleles at the three oci were not significantly if-ferent t the two sites (Wilcoxon's signed-rankstest, z =-1.07, n = 3 loci, P = 0.29). At both sites, polymorphism

was usually maximal in springsamples and minimal in fallsamples (Table 5); even so, therewas no measurablegeneticdifferentiation etweenthe seasons (Vermont:FST = -0.01? 0.08 SE; New York: FST = 0.10 ? 0.07 SE). We thereforepooled data across seasons forsubsequent analyses.

We synthesized hedata fromprotein lectrophoresiswiththeputativecolonyboundariesdrawnfrom esults ofworkerhostility ests.Figure 4 gives examples of plot diagramsforVermont and New York showing that synthesis.Nests thatwere amicable and thatwe thusdeemed partof one colonyusuallyhad been collected nearone another ndhad the samegenotypes,whereas those thatwere hostile and thus deemedseparate colonies usually were spatially separated and ge-neticallydistinct. An Appendixof genotypedata is available

from he authors upon request.)We inspectedour synthesis f behavioral and geneticdata

to findnests and colonies with any workerand/or late ge-notypesthat could notbe explained by the genotypesof thequeens present.We foundthat n Vermont, ne of 132 nestshad genotypes hat ould not be accounted forbythe colony'sresident queen; exactly one of 55 colonies and none of the16 complete colonies in Vermonthad genotypesthat couldnothave been producedbytheir ueen. However, nourNewYork 1992 sample, seven of 60 nests,six of43 colonies, andfourof 17 complete colonies had workerand/or alate ge-notypesthatcould not be explained by thequeen(s) present.Similarly,the New York 1993 sample contained fourof 41







290 V. S. BANSCHBACH AND J.M. HERBERS

3-9r NewYork

20.5- 1

2.5 S 5rin VermontC:

00

a)0- 3CD)CD

23

0

a)2ET

C:

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Spring Summer Falln=16 n=16 n=8 n=31 n=21 n=9colonies

FIG.3. Mean numberfnestspercolony ? SE) duringach season nthetwopopulations. hickhorizontalines ndicate hemodeandnumbers bovethebars ndicate hemaximum umber fnestspercolony.

nests with genotypes that could not be produced by thequeen(s) present.This indicates that n New York either u-pernumerary ueens were lost at a high rate throughout heseason (so there were ants in nests whose motherswere nolonger in the nest) or therewas frequent nest fission andfusionwithaccompanying worker exchanges.

We also investigatedthe genotype data for evidence ofmultiple-mating.We looked for nests and colonies that hadoffspringgenotypes all compatible with parentage by thequeen but requiringherto have been multiply-mated.Workerand alate genotypes n Vermontwere compatiblewithmon-andryfor all but threeof 132 nests, threeof 55 colonies,and none of 16 completecolonies. In contrast, he New York

TABLE 4. Seasonal changes n colonycomposition f M. puncti-ventrisnVermontndNewYork.Nrepresentsumbersf olonies.MeanH s theharmonicmean ueennumber,alculated y ncludingonly olonies hatwere ueenright.effs the ffectiveueennum-ber, stimated rom ata on colony-mateelatedness.

Queens Workers

Mean (SE) MeanH F,ff Mean (SE) N

VermontSpring 0.9 (0.1) 1.1 56.4 15.9) 16Summer 0.5 (0.1) 1.0 1.1 43.8 (7.8) 31Fall 0.7 (0.2) 1.0 J 24.9 (8.7) 9

New York1992Spring 1.4(0.3) 1.6 45.5 (12.3) 16Summer 0.9 (0.3) 1.3 1.8 33.8 14.8) 8Fall 1.1 0.2) 1.3 J 71.6(13.9) 21

NewYork 1993Summer 0.8 (0.3) 1.3 43.7 (27.7) 9

1992 data yielded ix of 60 nests, our f 43 colonies, ndtwo of 17 complete olonies whichhad genotypesnconsis-tentwithmonandry;n 1993, six of 41 nests n New Yorkhad genotypes nconsistent ith monandry. owever,be-cause of the imited esolution f our llozyme ata,missing

queens dead or migrated efore he colonywas collected)or workerxchanges annot e ruledout as alternativex-planations or hese nconsistencies.

We examined hegenetic atafor vidence fpopulationstructureia F-statistics, hichreveal theeffects fpopu-lation ubdivisionFST), inbreedingFIS),and the ombinedeffects f subdivision nd nbreedingnheterozygosityFIT)(Wright 951).Weused F-statisticsoquantifyhe xtent fgenetic ifferentiationetween oloniesrelative o thetotalpopulationFST,hereFCOLONY TOTAL) etween estsrela-tive o their olonies FIS, here NEST COLONY)nd betweennests elative o the otal opulationFIT,hereFNEST TOTAL).Forthese omputations,nly olonies hat onsisted fmorethan ne nest hereafteralled multinestolonies)andonly

genotype frequencydata fromworkers were used.For our Vermont ample, colony boundaries rawn ac-cording o the esults fworker ostilityestswere onfirmedby Wright's -statistics. oloniesweregenetically istinct:FCOLONY-TOTALwas significantly ifferentrom ero Table6; two-tailed = 3.00, df = 26, P < 0.01). Nests withincolonies were not differentiated:NEST COLONYwas signif-icantlyower han ero ndicatingnexcess of heterozygotesandsuggestingvoidance f ntranidal atingTable 6; one-tailed t = 3.00, df = 26, P < 0.005). Overall, the effects fpopulation ubdivision nd inbreeding n heterozygositywerenegligible: NEST-TOTALwas not significantly ifferentfrom ero Table 6; two-tailed = -0.71, df= 26,P > 0.4).








TABLE 5. Genetic variation in M. punctiventris samples for Vermont and New York. These are pooled data for queens, workers,andalates.

Vermont 992 New York 1992 1993

Spring Summer Fall All Spring Summer Fall All Summer

Number of nests 34 86 15 136 21 11 28 60 41

Number of individuals 379 1320 198 2022 307 156 399 862 577

Frequency of most common allelePGD: 0.73 0.79 0.77 0.77 0.67 0.79 0.85 0.78 0.82MDH: 0.94 0.92 1.00 0.93 0.68 0.88 0.91 0.82 0.92GPI: 0.99 0.99 0.98 0.99 0.80 1.00 0.99 0.93 0.98

Number of alleles foundPGD: 2 4 2 4 4 2 2 4 2MDH: 2 2 1 2 2 2 2 2 2GPI: 2 2 2 3 3 1 2 3 3

Finally,worker enotype requenciesmatched xpectationsforHardy-Weinbergquilibrium verthewholepopulation:theoverallF-statistic as not differentrom ero Table 6;two-tailed = 0.33, df= 130,P > 0.50).

For ourNewYork samplefrom 992, colonyboundariesdrawn p according o the esults ftheworker ostilityestswere also confirmedy F-statistics:COLONY - TOTAL wassignificantlyifferentrom ero Table 6; two-tailed= 3.28,df= 8, P < 0.02), indicating enetic ifferentiationfcol-onies.Within heseninepolydomous olonies,nestswerenotdifferentiated:NEST COLONY as significantlyess than ero(Table 6; one-tailed t = -5.14, df = 8, P < 0.0005), sug-gesting voidanceof intranidalmating. n these nine mul-tiple-nest olonies, he overalleffects f population ubdi-vision were negated y theavoidanceof inbreeding ithin

colonies: NEST-TOTALwas significantlyess than ero Table6; one-tailed = -2.76, df= 8, P < 0.05).Finally, urNew Yorkpopulation as not nHardy-Wein-

berg equilibrium.Overall, workergenotypefrequenciesstronglyndicatednbreeding.heoverall -statistic as sig-nificantlyreater han ero Table 6; one-tailed = 2.85, df= 58, P < 0.01). Thissuggestionf inbreedingntheNewYork populationwas confirmed y our 1993 sample fromNewYorkforwhich heoverallF-statistic as also greaterthan ero Table 6; one-tailed = 3.33,df= 40,P < 0.01).Positive F-values (i.e., a deficiency f heterozygotes)anderivefrom rue nbreedingmating etween elatives) rfrom opulation ubdivision. he atter,ermed heWahlundeffect,erives romnappropriatelyoolingdata across ub-

populations Wahlund 928). To distinguishetween hesepossibilities, e partitionedhegenetic ariation ntocom-ponents uetoseason,plotwithineason, nd colonywithinplot using data from ll colonies at each site. As ourF-statisticsrom hemultinestolonies howed Table 6), col-onieswerestronglyifferentiatedrom hetotalpopulationatboth ites Table7). Althougholonies tboth ites howedlittle easonal differentiation,ndividual lots were geneti-callydifferentiatednNew Yorkbut not nVermontTable7). True nbreedingeems to be a secondary ontributorothehigh verallF-value nNewYork, ince onlynineof 55nests deviated ndividually romHardy-WeinbergxpectedfrequenciesX2tests, < 0.05). Thus,we havestrongvi-

dence of colony tructurenbothpopulations ut also pop-ulation ubdivisionn a microgeographiccale n New York.

Genetic Relatedness of Nest- and Colony-Mates

Followingconfirmationf colony boundaries rawnupfrom he worker ostility ests,we next used our proteinelectrophoresisata to estimate est-matend colony-materelatednessn NewYork nd Vermont. ecause of the non-zeroF-value n New York,we appliedPamilo's 1984, 1985)correctionorpopulationubdivisiono thosedata.

Relatedness etween est-mate orkersn 1992 was sign-ficantlyower nNew Yorkthan nVermontTable 8; one-tailed t = 1.70, df = 185, P < 0.05). Worker-workerelat-ednesswas marginallyower hanHamilton's 1964) expec-

tation f 0.75 intheVermont opulationTable 8; two-tailedt = -2.00, df= 128,P = 0.05) andstronglyower n theNewYork 1992 population Table 8; two-tailed = -4.25,df = 57, P < 0.001).

Worker elatednessstimates or olony-matesere light-ly greater hanfornest-matesn both populationsn 1992(Table 8). The colony-levelelatednessstimate orVermontwas notdifferentrom amilton'sxpected alue ofr= 0.75forworker-workerelatednesstwo-tailed = -0.64, df =50, P > 0.50) but thecolony-level elatednessstimate orNew York was lower than hat xpectationtwo-tailed =

-3.25, df = 42, P < 0.01; Table 8).Weverifiedur estimate f worker est-mateelatedness

inNew York 1992 with ur1993 summer amplefrom ew

York Table 8C). Note that hese stimates gree n spiteofthefact hatwe wereunableto correct ur 1993New Yorkrelatedness stimates orpopulationubdivision ecausewehadno informationn subpopulationsfnests.

Relatednessestimatesforqueens, males, and femalesmatched amilton'sxpected alueswell n Vermontndbutnot n New York Table 8, two-tailed-tests).n New Yorkin both1992 and 1993, veryfew females lateswerepro-duced, nd thereforee havenorelatednessaluesfor latefemales here.

We were able to estimate elatedness f queensto othernest-matesnlyfor olygynousests n New York Table8).Thehighvalue ofnest-mateueen-to-queenelatednessor








a) Vermont lot V: Summer 992

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c1jbb Q: bbcc*bb 0: bb cc bb

obb

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0: bb ? bc

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FIG. 4. Plotdiagrams orA) a summerlot xcavatedn Vermontand B) a summer lotexcavatednNew York.Symbols epresentnestsofMyrmica unctiventrisithdifferentueennumbersn-dicated y symbol ype. llipsesenclosenests hatwere friendly"during ehavioral ests nd thuswere deemedpart fone colony.Nestsnot enclosedbyan ellipsewere considered ingle-nestol-onies.Three-partectangles eareach colony containworker e-notypes or he three ociMDH, GPI, andPGD. Genotypes f thequeen(s) of each colony realso listednear thecolony.

our New York 1992 sample (Table 8C) suggeststhat cohab-iting queens were sisters or mother-daughterairs. Our 1993New Yorksamplewas very small,but tshighvalue of queen-

queenrelatednessendsfurtherupportothe dea thatnest-matequeensarerelativesTable8). These queen-queen e-latedness alueswerenotcorrectedorpopulation ubdivi-sion/inbreedingecause a highF-value for queensresultsfromnbreedingn theprevious enerationndthus s not

valid correctionor xaminationf current opulationtruc-ture after eppa 1994). Queen relatedness o othernest-matesdoes not matchHamilton's xpectedvalues well inNew York Table 8C, two-tailed-tests).

We used ourrelatednessstimatesna furthernalysis fqueennumber t the two sites.We calculated he effectivenumberf queens Feff)nbothVermontndNew York c-cording o the method f Quelleret al. (1993), usingrelat-ednessestimates hatwerecorrected orpopulation ubdi-vision n NewYork. n Vermont,he ffectiveueennumber(1.1) matched heharmonicmean f observed ueennumber(1.1). But nNew York, he ffectiveueennumber as 1.8,whichwas somewhat igher han heharmonicmeanof ob-served ueennumber1.4).

DISCUSSION

OurtwopopulationsfM.punctiventrisiffertronglyntheir ocial structureTable9) yetretainmany imilarities.Colonieswerethe samesize andoccurred t the same den-sities n bothVermontndNewYork; ntsnestednthe ametypes fhollowplant avities ndweregeneralistcavengers(Herbers 989).Yet obligatemonogynyn Vermontontrastswith acultativeolygynyn NewYork; easonalpolydomystructuredolonies stronglyn Vermont utonlyweakly nNew York;therewas evidenceof microgeographiceneticstructurend possibly nbreedingn New York butnot nVermont;nd therewerepersistenttrong ifferencesn the

reproductiveiology fthe wopopulationss well Bansch-bach and Herbers 996). Because ourresults eplicatedhefindingsfSnyderndHerbers1991) for heVermontop-ulation nd becausewe wereable to detect hesame socialstructurenNew Yorkduringwo onsecutive ears,we con-cludethat hesedifferencesrebiologicallymeaningful.

TheantgenusMyrmicaas beencited s a group orwhichthestudy f intraspecificariationn queennumbern re-lation oecologicalfactorshould rovevaluablebecauseofthewiderange f variationhathas already eenfoundEl-mes andKeller1993).Myrmicapecieshavebeenespeciallywell-studiednEurope,wheremost refacultativelyolyg-ynous Elmes andKeller 1993); the distributionf queensamongnests andifferetween opulationsM.rubra, lmes

andPetal1990;M. ruginodis,eppa 1992) andcandiffernpopulations etweenyears M. sulcinodis, lmes 1987;M.rubra, lmesandPetal1990).Ourdata addto the mergingpicturefMyrmicapeciesby presentingnewsyndromefobligatemonogynyersusfacultativeolygynyndifferentpopulations. eppa (1992) has noted hat urVermontop-ulation ppears o be an aberrationn thegenusbecauseofthisobligatemonogyny.

A monogyny-polygynyichotomyas been described orseveral ther nt pecies, utfor llthose, olygynyslinkedtopolydomyH1lldobler ndWilson1977;Herbers 986a;Pamilo ndRosengren984,Pamilo1991,Ross and Fletcher1985, to 1990).Onewell-documentedase is thetransition








TABLE 6. F-statistics orM. punctiventrisorkers nmulti-nestolonies n Vermont nd New York.The Vermont alues are for90nests in 27 multi-nest colonies and the New York values are for 22 nests in nine multi-nest colonies. Standard errorsobtained byjackknifingver nests r colonies are isted.

Sources of variation: F-statistic:

X Y Fxy

Vermont New YorkNest Multi-Nest olony -0.43 + 0.04 -0.36 ? 0.07Nest Total -0.05 ? 0.07 -0.14 ? 0.05Multi-Nest olony Total 0.27 + 0.09 0.16 ? 0.05

Population values: 0.03 ? 0.09 1992: 0.37 ? 0.13n= 131 nests n = 59 nests

1993: 0.20 ? 0.06n = 41 nests

frommonogyny nd monodomy to polygyny nd polydomyin the imported fire nt, Solenopsis invicta. The queen stateof this species upon introduction n the southeasternUnitedStates is clearly monogyny,but polygyny appears to have

arisen spontaneously n many populations since the specieswas introduced Fletcher et al. 1980, Porter 1992). This tran-sition frommonogyny o polygynyhas been accompanied bychanges in the genetic and physical architecture f ant col-onies (Ross and Fletcher 1985, Keller and Ross 1993) thatinclude polydomy, inbreeding, owered relatedness amongnestmates, nd changes in reproductive iology. Furthermore,Keller and Ross (1993) found cultural transmission of themonogyne vs. polygyne behavior in S. invicta. Our studyspecies shares many of these distinguishingfeatures of themonogynous and polygynous forms,but our case differs nthat the monogynous population is polydomous. Thus, weview M. punctiventriss an important xceptionto thewidelyaccepted rule thatpolygyny nd polydomy re causally linked

(H6lldobler and Wilson 1977).What causes a populationto move frommonogyny o po-

lygyny, or vice versa, remains a mystery for most socialinsect species. A number of ecological variables have beenimplicated (reviewed by Herbers 1993), but direct experi-mental evidence is quite scarce. Herbers 1986b) was able toshow thatpolygyny n the tiny nt Leptothorax ongispinosusis a response to nest site shortage, and Hebers (1989) alsoproposed that this factor structured he entire communitiesof ants at her studysites. We have studied the populationsofM. punctiventrisn thosesame communities nd thus eval-uate our data in lightof thishypothesis.

TABLE 7. Hierarchical -statistics orM. punctiventrisorkerscollected n 1992 inVermontnd New York.The Vermontaluesare for 1 colonies on eight lots n three easons. TheNewYorkvalues are for43 colonies on sevenplots n three easons.

Sources of variation: F-statistic:

X Y Fxy

Vermont NewYorkColony Plot 0.34 0.30Colony Season 0.41 0.53Colony Total 0.39 0.48Plot Season 0.11 0.33Plot Total 0.07 0.26Season Total -0.04 0.11

Our study pecies nests n preformedlant avities, uchas hollow sticks, ickory uts, nd the ike.Myrmica unc-tiventrisppears ess discriminatinghan ther nts nthesehabitats, hough, ince we have foundnests n rolled-up

leaves, nvertebratexoskeletons,nd novelsites ikeshot-gun shells.The diversityf nest site use is higher orM.punctiventrisn Vermonthan n New York Herbers 989),and the pparentack of nest-sitehoosinessn Vermont aylead to the higher estdensityhere. ower nestdensitynNew York and a lower diversityftypes f occupiednestsitesmay ndicatehat est ites re imitinghere.fso,thennewly ertilizedueens mayopt toenter n established estrather han ry o find heir wn nestingite, eading o fac-ultative olygyny. ur evidence hat ueens iving ogetherin colonies n New Yorkare related o each other upportsthe return-homecenario.We know ittle bout thematingbehaviorof thisspecies,but thegeneticdata implicatingpopulationubdivision nd nbreedingreentirelyonsistentwith he stronglymale-biased ex ratioswe have observedin New York Banschbach nd Herbers 996).

Ourdata uggest hatnother actormay lso be important.InVermont,e nferredvery igh ate forphanedoloniesfrom ataon complete olonies, uggesting short ifespanofqueens, s hasbeenfoundn otherMyrmicapecies Seppa1994). New Yorkcolonieshad a lower nferredateof or-phaning, robably ue simply o greater umbersfqueenslivingncolonies nd thereforedecreased hance f endingup queenless.High ratesof queenmortality ay promoteworkers'willingness o acceptsupernumeraryueens intoestablished ests,with heconsequence f polygynouss-sociationsNonacs 1988). Presumably,n theVermontop-

ulation,whichdoes nothavethe ddedpressure f nest-sitelimitation,he ffects fhigh ueenmortalityrenot trongenough opromote olygyny.

Ifour hypothesiss correct, hatnest ites re imitingnNew York butnot n Vermont, e are left o explain whyseasonalpolydomyccurs n the Vermontite. One possi-bility s that ood s the imiting actor here, nd seasonalpolydomymayreflect strategyo increase oragingangeandcolonywideood ntakeSnyder 988).Thisview sbol-stered y a pilotfood-supplementationxperimentn Ver-mont,which roduced ramatichiftsn the ocial structureofM. punctiventrisests there.Withtheaddition f foodresources, olonieswentfrommonogynouso polygynous,







294 V. S. BANSCHBACHAND J.M. HERBERS

TABLE 8. Relatedness stimates orM. punctiventrisest- nd colony-mates.a) Relatedness alues expected n a colony withonesingly-matedueen Hamilton 964); b) Relatedness alues observed ornest-matesnVermont 992; c) Relatedness alues observedfornest-matesnNew York 1992 values are listedover1993 values); (d) Relatedness alues observedfor olony-matesn Vermont1992; e) Relatedness aluesfor olony-matesnNew York1992. All observed alues remeans+ standardrrors btained y ackknifingovernests.Numbers f nests ampled re istednparentheses.talicizedvalues were orrected or opulation ubdivisions perPamilo(1984). An asteriskndicates heobserved alue differsrom amilton's xpectation s determinedy a two-tailed-test, < 0.05. Nonests n Vermont ad more han ne queen and no femaleswereproduced y nests n our New York 1992 or 1993 samples;hence,noobservedvalues are istedfor hese ells.

(a) Hamilton's 1964) expectationsRelatedness f:

To: Queens Workers Males FemalesQueens 0.50 1.00 0.50Workers 0.50 0.75 0.50 0.75Males 0.50 0.25 0.50 0.25Females 0.50 0.75 0.50 0.75

(b) Nest-matesnVermont992Relatedness f:

To: Queens Workers Males FemalesQueensWorkers 0.61 + 0.07* 0.49 + 0.13 0.60 + 0.08

(129) (61) (47)Males 0.24 ? 0.07 0.49 + 0.09 0.31 ? 0.14

(61) (46) (23)Females 0.61 + 0.08 0.49 + 0.21 0.60 ? 0.08

(47) (23) (33)

1992(c) Nest-matesnNewYork1992

1993Relatedness f:

To: Queens Workers Males FemalesQueens 0.67 0.25 12) 0.06 0.13* 30) 0.56 + 0.06* 16) -

0.45+ 0.41 5) 0.30 + 0.14 17) 0.38 ? 0.22* 13)Workers 0.06 + 0.15* 30) 0.41 0.08* 58) -0.04 ? 0.13* 22) -

0.20 + 0.20 (17) 0.30 + 0.06 (40) -0.08 + 0.2* (25)

Males 0.16?

0.11* 16) -0.16?

0.07* 22) 0.17 0.12* 14)-

-0.02 + 0.13* 13) 0.05 ? 0.06* 25) 0.19+ 0.20 18)Females

(d) Colony-matesnVermont 992Relatedness f:

To: Queens Workers Males FemalesQueensWorkers 0.68 ? 0.11 0.52 + 0.15 0.75 ? 0.09

(51) (27) (19)Males 0.29 + 0.09 0.34 + 0.11 0.34 + 0.13

(27) (25) (15)Females 0.64 ? 0.11 0.50 ? 0.21 0.69 + 0.08

(19) (15) (17)

(e) Colony-matesnNew York1992Relatedness f:

To: Queens Workers Males FemalesQueens 0.64 + 0.19 0.20 ? 0.11 0.64 ? 0.06*

(14) (28) (14)Workers 0.20 + 0.13* 0.49 ?0.08* -0.10 + 0.12*

(28) (43) (19)Males 0.05?+0.10* 0 ?0.07* 0.17 ?0.11*-

(14) (19) (13)Females








TABLE 9. Social structuref two populations f M. punctiventris.

Vermont New York

Queen Number monogynous facultativelyolygynousColony Structure seasonally olydomous mainlymonodomousRelatedness f Nest- nd Colony-mates matchHamilton's xpected much owerthanHamilton's

values expected aluesNumber f Matings monandrous possibly olyandrousWorker xchange/Queen eplacement rarefornests nd colonies in at least 12% ofnests nd

12% ofcoloniesIncidence f Colony Orphaning 50% of "complete" colonies 29% of "complete"colonies

from olydomous o monodomous, nd from ight amilystructureo erodedrelatednessHerbers 993). We are cur-rently eplicatingnd expanding hat xperimento evaluatethe ood imitation ypothesisigorously.he food imitationidea is not supported y the fact hat roduction f sexualswas highern the Vermontopulation uring 992 than n

theNew York populationBanschbach nd Herbers1996),suggesting reater ood vailabilityn Vermonthan nNewYork.

Regardless f he elective ressuresmotivatinguch hiftsin social structure,he genetic onsequences re profound.Our Vermont opulation epresentshemost complete a-tabase of relatedness tructurehat s consistent ithHam-ilton's rules (1964). The colony-level elatedness mongworkers,fworkerso alates, f lates o workers,nd mongalates, re entirelyonsistent ith hevalues predictedorcolonyheadedby a single, nce-matedueen. Thus thepop-ulation fM. punctiventrisn Vermont epresents classiccase ofthe tructuredocial insect olony,withinwhichkinselection s presumed o be operational. hispresumptionsverified y data on sexual allocation Snyder nd Herbers1991; Banschbach ndHerbers 996), ince heVermontop-ulationhas produced exuals n a 3:1 female-biasednvest-ment attern or hree f thefouryearsforwhichwe havedata. That s, theVermont opulation onformserfectlyothe relatednesstructureositedbyHamilton s importantforkin election1964) and to workers inning ueen-work-er conflict ver sexual allocationratios Trivers nd Hare1976).

The genetic tructurefthe New Yorkpopulations af-fected y he resence fpolygynous ests,where elatednessvalues amongnestmates re significantlyrodedfrom heirHamiltonian xpectation nd from he values observed n

VermontTable 8). Population iscositys pronouncedhereas well.Suchviscosity as beenposited s a force romotingkin election Hamilton 964),but ecentmodelshaveshownthat hekin-selection alue of livingnear relatives an beoverriddeny the cost of competingwiththoserelatives(Queller 1992).Wecannot valuate he osts nd benefitsfthisviscosity or urstudy pecies,butpopulation iscosityhas been ssociatedwith olygynynother nt pecies Pam-ilo andVarvia-Aho 979;Sundstrom 993) andmaybe tiedto limiteddispersalby queens (Keller and Passera 1993).This limited ispersal f queens may then,n turn,ead tohighlymale-biased ex ratios, uch s thoseproduced yourspecies nNew York Banschbach ndHerbers 996),which

can serveas a meansof inbreedingvoidance, f males areable to dispersewidely Keller and Passera1992).

Another ossibleexplanation or hehighdegree f pop-ulation iscosityn New York s that ew olonies refound-ed via fissioning. eller 1991) found n association etweenpolygynynd foundingf newcoloniesvia fissioningor 4

ant species. f present,his typeof colonyfounding ouldresult n loweredmortalityf queens n theNew Yorkpop-ulation, ecause workersre able to defend hequeen(s) ofthebudding olonyfrom ts nception. he fewpolydomouscolonies we detectedn NewYork,via our behavioural ndgenetic ssays, ould have been newly issionednd soon tobe independentoloniesor colonies n theprocessof split-ting.

In conclusion, wopopulations fM. punctiventris iffermarkedlyn their olony ocial structureecauseof differentselective ressurest the wo ites.We propose hat est-sitelimitations of paramountmportanceo theNew Yorkpop-ulation, ut nest sitesare much more readily vailable inVermont. he Vermont opulation itsHamiltonianxpec-tations rom in-selectionheory lmostperfectly hereasthe New York population eviatesfrom heseexpectationssubstantially.urther xaminationf theecologicalforcesregulatingolony ocial structuretthe wo siteswillprovevaluable ndeterminingowkin election peratesnnaturalpopulations.

ACKNOWLEDGMENTS

Thanks o V. Backus,E. Choiniere,M. Freedman, . Sat-cowitz, . E. Snyder,nd D. Webbforhelping s to collectandcensus nts.We are also gratefuloH. Hobart, . Tolle,and J.Williams orhelp n the aboratory.uggestions romD. Queller idedouranalysis f thegenetic ata.This work

wassupported y grant oJ.M.H. rom heNational cienceFoundation.

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Correspondingditor:J. Carey

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