Complex Colony Structure in Social Insects: I. Ecological Determinants and Genetic Consequences Author(s): Valerie S.

Banschbach and Joan M. Herbers Source: Evolution, Vol. 50, No. 1 (Feb., 1996), pp. 285-297 Published by: Society for the Study of Evolution Stable URL: http://www.jstor.org/stable/2410800 . Accessed: 08/06/2013 00:11
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Evolution, 50(1), 1996, pp. 285-297

COMPLEX COLONY STRUCTURE IN SOCIAL INSECTS: I. ECOLOGICAL DETERMINANTS AND GENETIC CONSEQUENCES
Department of Zoology, University 05405 of Vermont, Burlington, Vermont Abstract.-Forsocial insectspecies,intraspecific in colonysocial structure variation provides an opportunity to relate theevolution of social behaviorto ecological factors. The species Myrmica is a cavity-dwelling forest punctiventris antthat exhibits in twopopulations in thenortheastern verydifferent colonystructures UnitedStates.Combined data from seasonalcensuses, allozyme electrophoresis, andworker hostility tests a population showedthat ofM. punctiventris in Vermont was strictly monogynous and seasonallypolydomous. The same procedures showedthata population of in New York was facultatively M. punctiventris and predominantly monodomous. polygynous Geneticrelatedness was notdifferent from Hamilton's amongcolony-mates expected valuesin theVermont and was consistent population withlittle coloniesand single-mating of queens.In contrast, exchangeof antsbetween relatedness was lowerin New York,and examination of nest-mate genotypes revealedexchangeof antsbetween colonies,highratesof colonyloss and replacement of queens, or multiple-mating of queens. The geneticstructure of the Vermont populationwas consistent with no inbreeding, butin New York,thepopulation structure genetic reflected subdivision microgeographic and inbreeding. Previousstudy of theantcommunities at thesesitesimplicates in New Yorkas a nest-site limitation on social structure. primary constraint Key words.-Inbreeding, polydomy, queen number, social insects. relatedness, ReceivedJuly 25, 1994. AcceptedJanuary 5, 1995. Since Hamilton's (1964) development of inclusive fitness theoryto explain the originof eusociality in the haplodiploid Hymenoptera,much of the work addressing the evolution of insect societies has focused on the importance of genetic relatedness and kin selection. Numerous studies have measured the genetic relatedness of social insect colony-mates to understandthe evolution of social behavior via kin selection (reviewed in Breed and Page 1989). However, formany social insect species, colony structure does not match Hamilton's assumption that there is only one queen which has mated only once. Accordingly,observed relatedness among social insect colony-mates has often been low (reviewed in Holldobler and Wilson 1990 for ants; Ross and Carpenter 1991a for social wasps; and Kukuk 1989 for a primitively social bee species). Thus, recently some students of social insects have suggested that the study of genetic relatedness has been overemphasized (Ito 1993), whereas the ecological determinants of social behavior need to receive much more attention(Strassman and Queller 1989; Herbers 1993). The importance of ecological factors in promotingsociality has long been stressed by workers studying a wide variety of other animals (reviewed in Slobodchikoff 1988), including lions (Scheel and Packer 1991), jays (Woolfenden and Fitzpatrick1978; Marzluffand Balda 1988), and spiders (Rypstra 1993) but has been paid relativelylittlenotice by those working with the insect societies. Studying differencesin social structurebetween populations of a species can reveal the selective pressures that act on sociality (Ross and Carpenter 1991b; Keller and Vargo 1993). Ant species are excellent subjects for these comparisons because even thoughtheyexhibitthe highestdegree of
1 Present address: Department ofBiology, DavidsonCollege,P.O. Box 1719, Davidson NC 28036-1719. E-mail: vabanschbach@ davidson.edu 2 Present address:Department of Biology,Colorado State University, Fort Collins, Colorado 80523. E-mail: herbers@ lamar.colostate .edu

VALERIE

S.

BANSCHBACH1

AND JOAN

M.

HERBERS2

eusociality, theyalso exhibit greatvarisocial organization, of and within species,in such specifics ability bothbetween (Holldobler andWilson as queennumber their social systems 1991b; Keller 1993). Here, we 1990; Ross and Carpenter oftheant,Myrfortwopopulations compare social structure to observed relating ecological factors mica punctiventris, document social structure We fully intraspecific differences. (1) the geneticcolony structure thathas two components: system ofthebreeding that depends uponsuchcharacteristics of queens,number of matings, and level of inas number breeding (Wade 1985; Ross 1993); and (2) otheraspectsof and such as polydomy including behaviors colonystructure and Wilbetween colonies(Holldobler exchangeof workers 1984). In a son 1977; Herbers1984; Pamilo and Rosengren of reproductive allocompanion paper,we explorepatterns thusdiffers 1996). Ourwork cation(Banschbach andHerbers within antspecies comparisons ofpopulations from previous whichhave examined onlya fewaspectsof social behavior Elmes and Wardlaw and/or relatedness; (e.g., queen number 1985; 1984; Ross and Fletcher 1982; Pamilo and Rosengren Herbers1986a; Elmes and Petal 1990; Ito 1990; Boomsma in press). et al. 1993; Herbers and Stuart, in queennumtheimportance of differences We highlight of variablecomponent is a highly berbecausequeennumber of ant social structure thathas greatimpacton relatedness fitness. Holldobler on their inclusive and,thus, colony-mates theimportance ofvariable and Wilson(1977) first delineated a large litand theirseminalpaper spurred queen number, erature on theproblem, as evidenced compilation by a recent out of work(Keller 1993). Kellerand Vargo(1993) pointed ofqueen be thepredominant state mayactually that polygyny in ants.Whyshouldmultiple queens coexistin colnumber of may loweroverallrelatedness onies,whenthissituation In particular, we mustdetermine whya queen colony-mates? colony(secondary acceptsother queen(s) intoherestablished mechanism whichis themostcommon producing polygyny), and Wilson1990). The databasewhich polygyny (Holldobler

285
C) 1996 The Society forthe Study of Evolution. All rightsreserved.

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286

V. S. BANSCHBACH AND J. M. HERBERS

local areaswithin thesiteswereused forcollection we can use to answer thisquestion is small,butin somecases Different seasons such thatone collectiondid not affect has been linkedto ecological factors in different secondary polygyny such as predation and nest-site availability (Herbers1993). subsequentcollections.During these excavations,we ineveryitemin theleaflitter on theplotsforantnests. We also focus upon polydomy, an important of spected feature many antspecies' socialstructure inwhich a singleantcolony Locations of nests were mappedand the nests themselves to the laboratory. Although this occupies multiple nests,usually in close proximity to one were bagged fortransport servedto replicate the data collectedon the Veranother. Workers, brood,and queens maybe exchanged be- sampling by Snyderand Herbers(1991), it was the tweenthesemultiple nestsof a colony.Polydomy and po- montpopulation detailedexamination of the New York population. To lygyny typically co-occur (Holldoblerand Wilson 1977). first information on thisnew population, we made adThus,studying theeffects of either stateis madedifficult by augment 1993. At thattime,we ditionalcollectionsin mid-August, theconfounding presenceof theother state. them rather thanfrom Our studyspecies,M. punctiventris, represents the only collectedantnestsas we encountered in to systematically excavated plots order increase sample well-described exampleof polydomy linkedto monogyny, sizes. incontrast tonumerous examples ofpolygynous-polydomous In thelaboratory, we putnestsin plasticboxes and mainantspecies(e.g., Pamiloand Rosengren 1984; Herbers 1991; to standard tained them according practice (Herbers andCunHerbers and Grieco1994; Herbers and Stuart, in press).Snyningham 1983). We censused nests, counting queens, workder and Herbers (1991) first studieda population of theant aftercollection in Vermont M. punctiventris whichhas colonies thatfrac- ers, larvae, pupae, and alates immediately each season,untilOctober. We also during in spring tionate and summer butrecoalescein fallforover- and periodically for of checked nests the social have presence parasites, which In thispopulation, wintering. colonies are strictly monogybeen observed forthisspecies(S. Cover, pers.comm.1991). nous (Snyderand Herbers1991). This strict is monogyny All ants were frozenforgel electrophoresis at the end of unusualforthegenusMyrmica to Elmes and Kel- October. (compare ler's (1993) reviewof studiesof queen number in several We performed workerhostility tests to delimitcolony European Myrmica species).Here,we compare colonysocial boundaries. and Herbers FollowingSnyder (1991), we introstructure of this monogynous, polydomousant population ducedantsfrom different nestsintoone another's nestboxes withthatof a secondpopulation in New Yorkto discern the to detect we dusted To perform thesetests, workaggression. thatrelateto social behavior ers from ecological and geneticfactors each nestwithfluorescent-colored powderand inof thisspecies. one worker at a time, intoall other nestsfrom troduced them, a plot was testedwith their plot. Each pair of nestswithin MATERIALS AND METHODS introductions and all testswerereplicated reciprocal at least once. For plotswithmorethan20 nests,testing all pairwise Our studyorganism, M. punctiventris, inhabits temperate combinations and therefore a was impractical, we employed in New Englandand rangessouthto Tennesseeand subsampling forests schemethatensuredthatwe could determine westto Iowa (Creighton 1950). Preformed cavities,such as all clusters of friendly nests. hollowed-out sticks,acorns,and rolled leaves are the prebetweenantson Duringthetests,we scoredinteractions ferred nestsitesofM. punctiventris (Herbers 1989) and dead a scale from 0 to 3. Thelowestscore, no visible 0, represented arethepreferred andHerbers arthropods food(Snyder 1991). aggression; a scoreof 1 was givenif antsopenedmandibles Despite taxonomic withthe genus Myrmica problems as a at one another; a score of 2 was givenif antsnippedat or whole, M. punctiventris represents a well-defined species, bitone another; andthemaximum score,3, was givenifants from its congeners morphologically quitedistinct (A. Fran- dragged, and or pulledon one another carried, (as in Snyder coeur,pers.comm.1988). had a meanscoreof ? 1 were Herbers 1991). Nestpairsthat We studied ofM. punctiventris in Vermont and deemed"amicable" and hencecon-colonial. populations in New York.Our study for polymorphic to sitein Vermont We determined was at Mallett's Bay phenotypes proteins their to of theantsand estimate relatedness StatePark,in Chittenden genotypes at 93-foot elevation.The infer County, We used cellulose-acetate gels and forest at this site is mixed-hardwood domi- nest-and colony-mates. second growth isomerase), natedby beech,maple,birch,and oak trees.The ant com- stainedforthreeloci: GPI (glucose-phosphate and PGD (phosphogluconate at thissitehas beendescribed munity byHerbers (1989), and MDH (malatedehydrogenase), We examined allozyme patternsfor all thesocial structure ofM. punctiventris has beendescribed by dehydrogenase). from each antnest. and Herbers sitein New Yorkwas queens,all alates,and up to 10 workers Snyder (1991). Our study data allowed us to calculaterelatedness at theE. N. HuyckPreserve, in AlbanyCounty, at 1500-foot The electrophoretic of workers, all pairings queens,males,and females elevation. The forest at thissiteis oldersecondgrowth dom- between for and within each season nests, site,usingtheQuellerand inatedby beech,hemlock, and oak trees. The antcommunity We also calculatedF-statistics (1989) algorithm. at theNew Yorksite consistsof fewerspecies and is char- Goodnight and pop1951) to look forevidenceof inbreeding acterized thantheantcommunity at (Wright by lowernestdensities in and ulation subdivision time space. site (Herbers1989). our Vermont To fullycharacterize the seasonal structure of bothpopRESULTS ulationsof M. punctiventris, the we collectedantnestsfrom of Nests Composition twositesat three times 1992: spring sumduring (mid-May), mer (mid-July), and fall (mid-September). We excavated in queen distridifferences Census data revealedmarked three 36-m2 each collection plotsduring periodat each site. bution Nestsin Vermont amongnestsofthetwopopulations.

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ECOLOGICAL DETERMINANTS OF COLONY STRUCTURE

287

a)
0.9 0.8 (07-

0.7 0c
a) 1 0.6(00
0

schemeallowedus to look forseasonalvariOur sampling In Vermont, queen number did vary ationin queen number. from spring to fall (G = 13.9, df = 2, P < 0.001), withthe nestsoccurring the during of queenright smallest proportion in the the pointof maximum colonyfractionation summer, however, (Fig. lA). In New York, seasonalcycleofpolydomy the werestatic throughout ofqueennumbers thedistributions
year (G = 3.7, df = 4, P = 0.45); that is, there was no

t: EL

a 0.4_
0.2

0.2 0 Spring 1992

b)
0.9 0.8 C)0.70

38 nests

Summer 1992
n 88 nests

FaIl 1992
n

= nests 14

09 C'

'E 0.64

0.5-

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in New York(Fig. iB). indication of seasonalpolydomy castesand lifestagesin of other Differences in abundance in queen the difference nestsat the two sites accompanied in Vermont was significantly lower Worker number number. U = 2,496, n, = thanin New York(Fig. 2; Mann-Whitney ofeggs,larvae,and 64, n2 = 140,P < 0.0001), and numbers as well (Table 1). We pupae were oftenlower in Vermont census data a MANOVA on thelog-transformed performed (workers, eggs, larvae,pupae) withsite,season, and queen The wholemodeland each variables. number as independent as were all of the interaction terms effect was signficant, (wholemodelF = 36.4, df= 11,P < 0.00001). We therefore foreffects ofvariation thecensusdatamorefully scrutinized ANin season and queen number. The resultsof two-way has a strong effect OVAs (Table 2) showthatqueen number in New Yorkbut not in Vermont. The on nestdemography and immatures are comparable of season on workers effects in nestcontents beat bothsites (Table 2). Thus,variation to the corretweenthe two sites is linkedmost strongly in queen distribution. differences sponding in Vermont thanin New was higher Finally,nestdensity U = 12.5, n1 = 8, n2 =9, P = 0.02). York(Mann-Whitney was 18.1 ? 5.0 SE nestsper36-M2 plot Averagenestdensity to 7.2 ? 2.4 SE nestsper in Vermont (8 plots) as compared 1992. 36-M2 plot in New York(9 plots) during
Composition of Colonies

&03
0.2

A n

to coloniesbysynthesizing behavioral Nestswereassigned testsallowed us to and geneticdata. The worker hostility 56 putative delimit coloniesinourVermont Twentysamples. 0 of morethan colonies consisted seven of these56 putative Summer 1993 1992 Summer 1992 FaIl 1992 Spring betweenVermont nests were one nest. Most interactions n =ll nests n =32 nests n= 4lnests n =2l nests scoredas 0 (completely hostile). amicable)or 3 (completely scores were observedless Table 3 shows thatintermediate than20% of the time.These testswere validatedby self3 Queens FL 0 Queens whichwerenearly100% amicable(meanhosintroductions, * 1 Queen El 4 Queens = 0.03 + 0.01 SE, n = 66 tests), andreplications score tility IRE 2 Queens of pairwise combinations which showed high congruence seasons (85% of 612 tests had identicalscores on all replicates). different FIG. 1. Distributions of queens in nestsduring and (B) the Furthermore, forour 1992 samplesof (A) the Vermont werestrongly population interactions correlated. reciprocal New Yorkpopulation. workers fromnest B, the If workers fromnest A attacked fromnest B would likelihoodwas veryhigh thatworkers workers from nestA (Kendall's Tau = 0.37, n = also attack always contained either one or no queens (Fig. IA), just as 156, P < 0.0001). in ourNew Yorksamplesfrom1992,we deBy contrast, Snyderand Herbers (1991) foundduringtheir1985 and 1986 45 colonies,of whichonly nine consistedof more censuses. In contrast,New York nests had up to fourqueens limited (Fig. iB). The distributionsof queen number by season in thanone nest.Thatis, veryfewnestsappearedto belongto at the two sites (X2 = 34.5, larger polydomous colonies. Moreover,workerhostility nests were significantly different in New Yorkthanin Vermont; df = 2, P < 0.0001). Furthermore, the New York data did scoresweremoreambiguous were scoredas 1's and 2's (internot show significant annual variation(summer 1992 vs. sum- 24.9% of theinteractions of mer 1993, G = 0.28, df = 2, P = 0.87). mediatelevels of aggression; Table 3). The distributions
0.1

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288

V. S. BANSCHBACH AND J. M. HERBERS

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n = 41 nests

m m m 00

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3 Queens 4 Queens

9 2 Queens

~~~~~

FIG. 2. Mean number of workers (+ SE) in nests in (A) Vermont and (B) New York duringdifferent seasons, grouped by queen number in nests.

0R~6 C 566

fA-6

the workerhostilityscores at the two sites were different (G = 21.8, df = 3, P < 0.001). Althoughself-introductions were oftenamicable (mean hostilityscore = 0.27 ? 0.11 SE, n = 51 tests), replicate introductionsshowed slightly lower fidelitythanin Vermont(78% of 217 testshad identical scores on all replicates) and the correlationbetween reciprocal nest pair test scores was weaker in New York (Kendall's Tau =

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ECOLOGICAL DETERMINANTS OF COLONY STRUCTURE

TABLE

289

in Vermont scoresforM. punctiventris hostility 3. Worker countsof pairsof neststhat and New York,1992. Values represent of nests score.Percentages hostility meanworker effects werecalculatedfor had theindicated VAs to determine significant treatment The belowcounts. Queen number withtheindicated meanscoreare in parentheses log-transformed variablesforeach site separately. amicable(0, 1) and hostile between was categorized as 0, 1, or >1. vertical line denotesthecutoff (2, 3) scores.
of M. punctiventris in New York and in Vermont.Two-way ANO-

on nestcomposition 2. Effects of seasonandqueennumber

TABLE

Vermont E-ffects of: Season Queen S. x Q. Season

New York Queen S. X Q. 0

scores: Workerhostility 1 2 3

Workers* Eggs Larvae** Pupae

N of tests

**
**

**
**

**
**

**
**

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

0.18, n = 100, P < 0.006). We conclude thatcolony boundaries in New York are more ambiguous than in Vermont. If a colony was more than one meter fromthe edge of a nests withina one-meter radius plot and if all M. punctiventris of the colony had been collected and tested for aggression, then we deemed the colony "complete" (following Snyder 1988). In Vermont,16 of 56 colonies that we located were complete. Of these, eight (= 50%) were queenless and presumably orphaned. In New York, 17 of 45 colonies that we censused were complete; only five of these (= 29%) were queenless and presumed orphaned. Because of the low numbers of complete colonies, statisticalanalyses used data from all colonies unless noted. We examined our colony data forseasonal changes in numbers of nests comprisingcolonies at both sites. In Vermont, a seasonal patternof colony fission in spring and summer, followed by fusion in fall was evident (Fig. 3). In spring, most colonies consisted of one or two nests, and in summer more colony fragments were found, followed by a returnto one nest per colony in fall. There was little suggestion of colony fractionationoccurring in New York, because the mean number of nests per colony remained close to one throughoutthe year (Fig. 3). Only nine out of 45 colonies identifiedin New York were polydomous, while 25 out of in Vermontwere polydomous. Overall, 56 colonies identified colonies consisted of more nests in Vermont than in New York (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 three out of the five colonies with multiple queens had queens nests. living in different between the two sites in queen Like nests,colonies differed number.In Vermont,only two out of 56 colonies were polygynous (both in spring and both containing just two queens), whereas in New York 15 out of 45 colonies were in theirarithmetic mean numpolygynous. The sites differed ber of queens per colony (Mann-WhitneyU = 911, n1 = 56, n2 = 45, P < 0.01) as well as the harmonic mean (Table 4), which is the most relevantstatisticforpredictingrelatedness structure (Wade 1985; Ross 1993). A major differencefrom the nest-level demographics is that colonies did not differ between sites in theiraverage numberof workers,larvae, or pupae (Table 4; Mann-WhitneyU tests,n, = 56, n2 = 45, P > 0.05) whereas nests did (Table 1; Fig. 2). in 1992 for Density of colonies on plots was not different New York as compared to Vermont (Mann-WhitneyU = 47.5,

121 21 90 (3.4%) (14.7%) (19.8%) 58 26 16 New York (8.8%) (5.4%) (19.5%) scores Mean hostility 2.26 + 0.05 SE, n = 612 Vermont: 2.52 + 0.05 SE, n = 297 New York: Vermont

380 (62.1%) 197 (66.3%)

612 297

n, = 8, n2 = 9, P = 0.27). In New York, the mean number of colonies per plot was 4.9 ? 1.5 SE (9 plots) as compared to a mean of 7.0 ? 1.6 SE colonies per plot (8 plots) in Vermont. In sum, many demographicfeaturesof colonies are similar in our two populations. The Vermontand New York colonies differedprimarilyin how many queens they contained and duringthe growing seain how extensivelytheyfragmented son. Genetics of Colonies and Populations We assayed ants by gel electrophoresisfor allozyme variation at three loci (Table 5). The frequencies of the most difcommon alleles at the three loci were not significantly ferentat the two sites (Wilcoxon's signed-ranks test, z = -1.07, n = 3 loci, P = 0.29). At both sites, polymorphism was usually maximal in spring samples and minimal in fall samples (Table 5); even so, therewas no measurable genetic differentiation between the seasons (Vermont: FST = -0.01 ? 0.08 SE; New York: FST = 0.10 ? 0.07 SE). We therefore pooled data across seasons for subsequent analyses. We synthesizedthe data fromproteinelectrophoresiswith the putativecolony boundaries drawn fromresultsof worker hostilitytests. Figure 4 gives examples of plot diagrams for Vermont and New York showing that synthesis. Nests that were amicable and that we thus deemed part of one colony usually had been collected near one anotherand had the same genotypes,whereas those thatwere hostile and thus deemed separate colonies usually were spatially separated and geneticallydistinct.(An Appendix of genotypedata is available fromthe authors upon request.) We inspected our synthesisof behavioral and genetic data to findnests and colonies with any worker and/oralate genotypes that could not be explained by the genotypes of the queens present.We found that in Vermont,one of 132 nests had genotypesthatcould not be accounted forby the colony's resident queen; exactly one of 55 colonies and none of the 16 complete colonies in Vermonthad genotypes that could not have been produced by theirqueen. However, in our New York 1992 sample, seven of 60 nests, six of 43 colonies, and four of 17 complete colonies had worker and/or alate genotypes thatcould not be explained by the queen(s) present. Similarly, the New York 1993 sample contained four of 41

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290 3-

V. S. BANSCHBACH AND J. M. HERBERS

r
S 5rin

NewYork Vermont

C:

2.5

0 0

0-

a)

CD)

CD
0

a)2
ET
C:

20.5- 5 1
0.5-\X

23

ca

a)

n=16

Spring

n=16

n=8

Summer

n=31

n=21

Fall

n=9colonies

FIG. 3. Mean number Thickhorizontal of nestsper colony(? SE) during each season in thetwo populations. lines indicate themode and numbers number of nestsper colony. above thebars indicatethemaximum

1992 data yieldedsix of 60 nests,fourof 43 colonies,and two of 17 complete colonieswhichhad genotypes inconsistentwithmonandry; in 1993, six of 41 nestsin New York had genotypes inconsistent with monandry. However,because of thelimited of ourallozymedata,missing resolution queens (dead or migrated beforethe colonywas collected) exor worker exchangescannotbe ruledout as alternative planations fortheseinconsistencies. We examined thegeneticdata forevidenceof population of popustructure via F-statistics, whichrevealthe effects lationsubdivision (FIS), and thecombined (FST), inbreeding on heterozygosity effects of subdivision andinbreeding (FIT) to quantify theextent of (Wright 1951). We used F-statistics geneticdifferentiation between coloniesrelative to thetotal between nestsrela- TOTAL) (FST,hereFCOLONY TABLE 4. Seasonal changesin colonycomposition of M. puncti- population tive between to their here and colonies FNEST - COLONY) (FIS, ventrisinVermont andNew York.N represents numbers ofcolonies. here nests relative to the total population (FIT, FNEST TOTAL). MeanHis theharmonic meanqueennumber, calculated byincluding of more onlycoloniesthat onlycoloniesthat consisted werequeenright. Feff is theeffective queen num- For thesecomputations, from data on colony-mate ber,estimated relatedness. thanone nest(hereafter called multinest colonies) and only
nests with genotypes that could not be produced by the queen(s) present.This indicates that in New York eithersupernumerary queens were lost at a high rate throughout the season (so there were ants in nests whose motherswere no longer in the nest) or there was frequent nest fission and fusion with accompanying workerexchanges. We also investigated the genotype data for evidence of multiple-mating. We looked for nests and colonies that had offspringgenotypes all compatible with parentage by the queen but requiringher to have been multiply-mated. Worker and alate genotypes in Vermontwere compatible with monandry for all but three of 132 nests, three of 55 colonies, and none of 16 complete colonies. In contrast, the New York
Queens Mean (SE) MeanH F,ff Workers Mean (SE) N

Vermont Spring 0.9 (0.1) Summer 0.5 (0.1) Fall 0.7 (0.2) New York 1992 Spring 1.4(0.3) Summer 0.9 (0.3) Fall 1.1 (0.2) New York 1993
Summer 0.8 (0.3)

1.1 1.0 1.0 1.6 1.3 1.3

1.3

1.1

43.8 (7.8)

56.4 (15.9)

24.9 (8.7)

31

16 9

For our Vermont sample, colony boundariesdrawnacofworker tests wereconfirmed cording to theresults hostility distinct: by Wright's F-statistics. Colonies weregenetically different from zero (Table FCOLONY-TOTALwas significantly t = 3.00, df = 26, P < 0.01). Nests within 6; two-tailed
was signifcolonies were not differentiated: FNEST- COLONY

genotype frequencydata fromworkers were used.

1.8

45.5 (12.3) 33.8 (14.8) 71.6(13.9)

43.7 (27.7)

16 8 21
9

on heterozygosity populationsubdivisionand inbreeding werenegligible: different FNEST-TOTALwas not significantly t = -0.71, df = 26, P > 0.4). from zero (Table 6; two-tailed

tailed t = 3.00, df = 26, P < 0.005). Overall, the effectsof

an excess ofheterozygotes icantly lowerthanzeroindicating and suggesting avoidanceof intranidal mating (Table 6; one-

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ECOLOGICAL DETERMINANTS OF COLONY STRUCTURE

TABLE 5.

291

alates.

Genetic variation in M. punctiventris samples for Vermont and New York. These are pooled data for queens, workers, and
Vermont1992 Spring Summer Fall All Spring New York 1992 Summer Fall All 1993 Summer

Number of nests Number of individuals

34 379

86 1320 0.79 0.92 0.99 4 2 2

15 198 0.77 1.00 0.98 2 1 2

136 2022 0.77 0.93 0.99 4 2 3

21 307 0.67 0.68 0.80 4 2 3

11 156 0.79 0.88 1.00 2 2 1

28 399 0.85 0.91 0.99 2 2 2

60 862 0.78 0.82 0.93 4 2 3

41 577 0.82 0.92 0.98 2 2 3

Frequency of most common allele PGD: 0.73 MDH: 0.94 GPI: 0.99 Number of alleles found PGD: MDH: GPI: 2 2 2

of colony boundariesdrawnup Followingconfirmation hostility tests,we next used our protein fromthe worker and colony-mate data to estimate nest-mate electrophoresis Because of thenonrelatedness in New Yorkand Vermont. zeroF-valuein New York,we appliedPamilo's(1984, 1985) to thosedata. forpopulation subdivision FNEST- COLONY was significantly differentiated: less thanzero correction in 1992 was signnest-mate workers Relatedness between (Table 6; one-tailed t = -5.14, df = 8, P < 0.0005), sug(Table 8; onelowerin New Yorkthanin Vermont gestingavoidanceof intranidal In these nine mul- ficantly mating. relattiple-nest colonies,the overalleffects of population subdi- tailed t = 1.70, df = 185, P < 0.05). Worker-worker (1964) expeclowerthanHamilton's vision were negatedby the avoidanceof inbreeding within ednesswas marginally (Table 8; two-tailed population of 0.75 in theVermont colonies:FNEST-TOTAL was significantly less thanzero (Table tation lowerin the t = -2.00, df = 128, P = 0.05) and strongly 6; one-tailed t = -2.76, df = 8, P < 0.05). t = -4.25, (Table 8; two-tailed Finally, ourNew Yorkpopulation was notin Hardy-Wein- New York 1992 population berg equilibrium.Overall, workergenotypefrequencies df = 57, P < 0.001). wereslightestimates for colony-mates Worker relatedness The overallF-statistic strongly indicated was siginbreeding. in bothpopulations in 1992 thanfornest-mates nificantly greater thanzero (Table 6; one-tailed t = 2.85, df ly greater = 58, P < 0.01). This suggestion estimate forVermont relatedness in theNew (Table 8). The colony-level of inbreeding expected valueof r = 0.75 from Hamilton's York populationwas confirmed by our 1993 sample from was notdifferent relatedness t = -0.64, df = (two-tailed New YorkforwhichtheoverallF-statistic was also greater forworker-worker estimate for relatedness thanzero (Table 6; one-tailed t = 3.33, df = 40, P < 0.01). 50, P > 0.50) but thecolony-level t= (two-tailed PositiveF-values (i.e., a deficiency of heterozygotes) can New York was lowerthanthatexpectation derivefromtrueinbreeding (matingbetweenrelatives)or -3.25, df = 42, P < 0.01; Table 8). relatedness We verified of worker nest-mate our estimate from The latter, population subdivision. termed theWahlund New samplefrom derivesfrom effect, inappropriately poolingdata acrosssub- in New York1992 withour 1993 summer agreein spiteof betweenthese York(Table 8C). Note thattheseestimates populations (Wahlund1928). To distinguish our 1993 New York we partitioned the geneticvariation intocom- thefactthatwe wereunableto correct possibilities, because we forpopulation subdivision estimates ponents due to season,plotwithin season,and colonywithin relatedness of nests. on subpopulations plot using data fromall colonies at each site. As our F- had no information Relatednessestimatesfor queens, males, and females from themultinest statistics coloniesshowed(Table 6), colandbut expected valueswell in Vermont Hamilton's onies were strongly differentiated thetotalpopulation matched from In New York t-tests). atbothsites(Table7). Although coloniesatbothsitesshowed not in New York(Table 8, two-tailed littleseasonal differentiation, individual plots were geneti- in both 1992 and 1993, veryfew femalesalates were provalues foralate we have no relatedness in New Yorkbut not in Vermont cally differentiated (Table duced,and therefore seems to be a secondary to femalesthere. contributor 7). Trueinbreeding relatedness of queens to other We were able to estimate thehighoverallF-valuein New York,sinceonlynineof 55 nestsin New York(Table 8). onlyforpolygynous nestsdeviatedindividually fromHardy-Weinberg expected nest-mates for relatedness P < 0.05). Thus,we have strong evi- The highvalue of nest-mate queen-to-queen frequencies (X2tests,

Finally,worker genotype frequencies matched expectations forHardy-Weinberg equilibrium overthewholepopulation: the overallF-statistic was notdifferent from zero (Table 6; two-tailed t = 0.33, df = 130, P > 0.50). For our New Yorksamplefrom1992, colonyboundaries to theresults oftheworker drawn up according hostility tests were also confirmed by F-statistics: FCOLONY - TOTAL was from zero(Table6; two-tailed significantly different t = 3.28, df = 8, P < 0.02), indicating of colgeneticdifferentiation onies.Within theseninepolydomous werenot colonies,nests

in bothpopulations but also popdence of colonystructure scale in New York. on a microgeographic ulation subdivision
Genetic Relatedness of Nest- and Colony-Mates

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292
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to theidea thatnestsupport lendsfurther queen relatedness re(Table 8). These queen-queen matequeens are relatives subdiviforpopulation latednessvalues werenotcorrected because a high F-value forqueens results sion/inbreeding and thusis nota generation in theprevious inbreeding from strucpopulation of current forexamination valid correction to othernestture (afterSeppa 1994). Queen relatedness mates does not matchHamilton'sexpectedvalues well in t-tests). New York(Table 8C, two-tailed analysisof in a further estimates We used ourrelatedness at the two sites.We calculatedthe effective queen number and New Yorkacin bothVermont of queens (Feff) number of Quelleret al. (1993), usingrelatto themethod cording forpopulationsubdithatwere corrected edness estimates queen number theeffective visionin New York.In Vermont, queennumber meanof observed theharmonic (1.1) matched was 1.8, queen number (1.1). But in New York,theeffective meanof obthantheharmonic higher whichwas somewhat (1.4). servedqueen number
DISCUSSION

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4. Plotdiagrams for(A) a summer plotexcavatedin Vermont and (B) a summer plotexcavatedin New York.Symbolsrepresent inwithdifferent nests of Myrmica punctiventris queen numbers dicatedby symbol were"friendly" type. Ellipsesencloseneststhat testsand thusweredeemedpartof one colony. behavioral during colsingle-nest Nests notenclosedby an ellipse were considered genear each colonycontainworker onies. Three-part rectangles of the forthethree loci MDH, GPI, and PGD. Genotypes notypes queen(s) of each colonyare also listednearthecolony.
FIG.

our New York 1992 sample (Table 8C) suggests that cohabpairs. Our 1993 itingqueens were sistersor mother-daughter New York sample was very small, but its high value of queen-

in differ strongly of M. punctiventris Our twopopulations (Table 9) yetretainmanysimilarities. theirsocial structure at thesame denColonies werethesame size and occurred inthesame andNew York;antsnested sitiesin bothVermont scavengers ofhollowplantcavitiesandweregeneralist types in Vermont contrasts monogyny 1989). Yet obligate (Herbers in New York;seasonal polydomy withfacultative polygyny in Vermont but onlyweaklyin colonies strongly structured genetic New York; therewas evidenceof microgeographic in New York but not in and possiblyinbreeding structure in the differences werepersistent strong and there Vermont; as well (Banschbiologyofthetwopopulations reproductive the replicated bach and Herbers1996). Because our results popand Herbers (1991) fortheVermont of Snyder findings ulationand because we wereable to detectthesame social we conin New Yorkduring twoconsecutive years, structure meaningful. are biologically clude thatthesedifferences forwhich has beencitedas a group The antgenusMyrmica in rein queen number variation the studyof intraspecific shouldprovevaluablebecause of lationto ecologicalfactors been found(Elthathas already thewide rangeof variation specieshavebeenespecially mes and Keller 1993). Myrmica polygin Europe,wheremostare facultatively well-studied of queens ynous(Elmes and Keller 1993); the distribution Elmes between (M. rubra, populations amongnestscan differ in Seppa 1992) and can differ and Petal 1990; M. ruginodis, Elmes 1987; M. betweenyears(M. sulcinodis, populations Elmes and Petal 1990). Our data add to theemerging rubra, of a new syndrome ofMyrmica speciesby presenting picture in different versusfacultative polygyny obligatemonogyny popSeppa (1992) has notedthatour Vermont populations. in thegenusbecause of ulationappearsto be an aberration thisobligatemonogyny. for has been described A monogyny-polygyny dichotomy is linked antspecies,butforall those, polygyny severalother to polydomy (H1lldoblerand Wilson 1977; Herbers1986a; PamiloandRosengren 1984,Pamilo 1991,Ross andFletcher case is thetransition 1985,Ito 1990). One well-documented

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ECOLOGICAL DETERMINANTS OF COLONY STRUCTURE

TABLE

293

jackknifing overnestsor coloniesare listed.

Sources of variation: X

nests in 27 multi-nestcolonies and the New York values are for 22 nests in nine multi-nestcolonies. Standard errors obtained by
F-statistic: Y Fxy

6. F-statistics forM. punctiventris workers in multi-nest colonies in Vermont and New York.The Vermont values are for90

Nest Nest Multi-Nest Colony Population F values:

Multi-Nest Colony Total Total

n= 131 nests

-0.43 + 0.04 -0.05 ? 0.07 0.27 + 0.09 0.03 ? 0.09

Vermont

-0.36 ? 0.07 -0.14 ? 0.05 0.16 ? 0.05 1992: 0.37 ? 0.13 1993: 0.20 ? 0.06
n = 41 nests n = 59 nests

New York

frommonogynyand monodomy to polygynyand polydomy in the importedfireant, Solenopsis invicta. The queen state of this species upon introduction in the southeasternUnited States is clearly monogyny,but polygyny appears to have arisen spontaneously in many populations since the species was introduced(Fletcher et al. 1980, Porter 1992). This transition frommonogynyto polygynyhas been accompanied by changes in the genetic and physical architecture of ant colonies (Ross and Fletcher 1985, Keller and Ross 1993) that include polydomy, inbreeding, lowered relatedness among nestmates,and changes in reproductive biology. Furthermore, Keller and Ross (1993) found cultural transmission of the monogyne vs. polygyne behavior in S. invicta. Our study species shares many of these distinguishingfeaturesof the monogynous and polygynous forms,but our case differsin that the monogynous population is polydomous. Thus, we view M. punctiventris as an important exception to the widely accepted rule thatpolygynyand polydomyare causally linked (H6lldobler and Wilson 1977). What causes a population to move frommonogynyto polygyny, or vice versa, remains a mysteryfor most social insect species. A number of ecological variables have been implicated (reviewed by Herbers 1993), but direct experimental evidence is quite scarce. Herbers (1986b) was able to show thatpolygynyin the tinyant Leptothoraxlongispinosus is a response to nest site shortage, and Hebers (1989) also proposed that this factor structured the entire communities of ants at her study sites. We have studied the populations of M. punctiventris in those same communitiesand thus evaluate our data in light of this hypothesis.

plantcavities,such Our study species nestsin preformed puncnuts,and thelike. Myrmica hickory as hollowsticks, antsin these thanother appearsless discriminating tiventris though,since we have foundnests in rolled-up habitats, and novel siteslike shotexoskeletons, leaves, invertebrate of nest site use is higher forM. gun shells. The diversity in Vermont thanin New York(Herbers1989), punctiventris may in Vermont choosiness lack ofnest-site andtheapparent in Lower nestdensity there. nestdensity lead to thehigher of typesof occupied nest New York and a lower diversity If so, then there. nestsitesarelimiting that sitesmayindicate nest an established queens mayopt to enter newlyfertilized site,leadingto facown nesting their thantryto find rather Our evidencethatqueens livingtogether ultative polygyny. in colonies in New Yorkare relatedto each othersupports scenario.We know littleaboutthe mating the return-home behaviorof this species, but the geneticdata implicating consistent areentirely subdivision and inbreeding population male-biasedsex ratioswe have observed withthe strongly in New York(Banschbachand Herbers1996). factor mayalso be important. another Ourdatasuggest that colonies highrateoforphaned In Vermont, we inferred a very lifespan a short colonies,suggesting from data on complete in other species(Seppa Myrmica ofqueens,as has beenfound rateof or1994). New Yorkcolonies had a lower inferred of queens numbers to greater due simply probably phaning, chanceofending a decreased livingin coloniesandtherefore may promote up queenless.High ratesof queen mortality queens into to accept supernumerary workers'willingness asestablished nests,withthe consequenceof polygynous in theVermont popsociations(Nonacs 1988). Presumably, TABLE 7. Hierarchical of nest-site F-statistics for M. punctiventris workers ulation, whichdoes nothave theaddedpressure and New York.The Vermont values limitation, collectedin 1992 in Vermont are notstrong theeffects of highqueen mortality are for51 colonieson eightplotsin three seasons.The New York polygyny. enoughto promote values are for43 colonies on seven plotsin threeseasons. in If our hypothesis is correct, thatnestsitesare limiting are left to why not in we explain New York but Vermont, Sources of variation: F-statistic: site. One possioccurs in the Vermont seasonal polydomy X Y Fxy and seasonal factor there, bilityis thatfood is the limiting Vermont New York a strategy range to increaseforaging mayreflect polydomy Plot 0.34 0.30 Colony foodintake and colonywide (Snyder1988). This viewis bol0.41 0.53 Season Colony in Verexperiment steredby a pilot food-supplementation Total 0.39 0.48 Colony 0.33 Plot 0.11 Season in thesocial structure shifts dramatic whichproduced mont, 0.07 0.26 Plot Total nests there.Withthe additionof food of M. punctiventris Total -0.04 0.11 Season to polygynous, monogynous colonies wentfrom resources,

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294
TABLE

V. S. BANSCHBACHAND J.M. HERBERS

nest-and colony-mates. (a) Relatednessvalues expectedin a colony withone 8. Relatednessestimates forM. punctiventris in Vermont valuesobserved valuesobservedfornest-mates 1992; (c) Relatedness singly-mated queen (Hamilton1964); (b) Relatedness in New York(1992 values are listedover 1993 values); (d) Relatedness in Vermont values observedforcolony-mates fornest-mates byjackknifing inNew York1992.All observed valuesaremeans+ standard errors obtained 1992; (e) Relatedness valuesfor colony-mates as perPamilo Italicizedvalueswerecorrected forpopulation subdivision overnests.Numbers of nestssampledare listedin parentheses. t-test, P < 0.05. No from Hamilton's expectation as determined by a two-tailed (1984). An asterisk indicates theobservedvalue differs by nestsin our New York 1992 or 1993 samples;hence,no nestsin Vermont had morethanone queen and no femaleswereproduced observedvalues are listedforthesecells. (a) Hamilton's (1964) expectations Relatedness of: Queens To: Queens Workers 0.50 Males 0.50 Females 0.50 in Nest-mates 1992 (b) Vermont Relatedness of: To: Queens Workers Males Females Queens Workers 0.50 0.75 0.25 0.75 Males 1.00 0.50 0.50 0.50 Females 0.50 0.75 0.25 0.75

Workers 0.61 + 0.07* (129) 0.24 ? 0.07 (61) 0.61 + 0.08 (47)

Males 0.49 + 0.13 (61) 0.49 + 0.09 (46) 0.49 + 0.21 (23)

Females 0.60 + 0.08 (47) 0.31 ? 0.14 (23) 0.60 ? 0.08 (33)

1992 in New York 1992 (c) Nest-mates 1993 of: Relatedness To: Queens Workers Males Females Queens 0.67 ? 0.25 (12) 0.45 + 0.41 (5) 0.06 + 0.15* (30) 0.16 ? 0.11* (16) -0.02 + 0.13* (13)
0.20 + 0.20 (17)

Workers 0.06 ? 0.13* (30) 0.30 + 0.14 (17) 0.41 ? 0.08* (58) -0.16 ? 0.07* (22) 0.05 ? 0.06* (25)
0.30 + 0.06 (40)

Males 0.56 + 0.06* (16) 0.38 ? 0.22* (13) -0.04 ? 0.13* (22)
-0.08 + 0.2* (25)

Females
-

0.17 ? 0.12* (14) 0.19 + 0.20 (18)

in Vermont 1992 (d) Colony-mates of: Relatedness To: Queens Workers Males Females in New York 1992 (e) Colony-mates Relatedness of: To: Queens Workers Males Females Queens 0.64 + 0.19 (14) 0.20 + 0.13* (28) 0.05?+0.10* (14) Workers 0.20 ? 0.11* (28) 0.49 ?0.08* (43) 0 ?0.07* (19) Males 0.64 ? 0.06* (14) -0.10 + 0.12* (19) 0.17 ?0.11*(13) Females Queens Workers 0.68 ? 0.11 (51) 0.29 + 0.09 (27) 0.64 ? 0.11 (19) Males 0.52 + 0.15 (27) 0.34 + 0.11 (25) 0.50 ? 0.21 (15) Females 0.75 ? 0.09 (19) 0.34 + 0.13 (15) 0.69 + 0.08 (17)

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ECOLOGICAL DETERMINANTS OF COLONY STRUCTURE

TABLE 9.

295

Social structure of two populations of M. punctiventris.

Vermont New York

Queen Number ColonyStructure Relatedness of Nest-and Colony-mates Number of Matings Worker Exchange/Queen Replacement Incidenceof ColonyOrphaning

monogynous seasonallypolydomous matchHamilton's expected values monandrous rarefornestsand colonies 50% of "complete"colonies

facultatively polygynous mainly monodomous muchlowerthanHamilton's expectedvalues possiblypolyandrous in at least 12% of nestsand 12% of colonies 29% of "complete" colonies

frompolydomous to monodomous, and fromtightfamily can serveas a meansof inbreeding avoidance,if males are structure to erodedrelatedness (Herbers1993). We are cur- able to dispersewidely(Keller and Passera 1992). forthehighdegreeof popAnother possible explanation rently replicating and expanding thatexperiment to evaluate newcoloniesarefoundviscosity in New Yorkis that thefoodlimitation hypothesis rigorously. The foodlimitation ulation between an association Keller(1991) found idea is not supported by thefactthatproduction of sexuals ed via fissioning. for24 of newcoloniesvia fissioning and founding in the Vermont was higher population during1992 thanin polygyny could thistypeof colonyfounding the New Yorkpopulation (Banschbachand Herbers1996), ant species. If present, of queens in theNew Yorkpopsuggesting greater foodavailability in Vermont thanin New resultin loweredmortality thequeen(s) of are able to defend ulation, because workers York. The fewpolydomous its inception. colonyfrom Regardless oftheselective pressures motivating suchshifts thebudding in New York,via our behavioural and in social structure, the geneticconsequencesare profound. colonieswe detected and soon to assays,could have been newlyfissioned Our Vermont the most completeda- genetic population represents coloniesor coloniesin theprocessof splitwithHam- be independent tabase of relatedness structure thatis consistent ting. ilton's rules (1964). The colony-levelrelatednessamong differ In conclusion, of M. punctiventris two populations ofworkers workers, to alates,ofalatestoworkers, andamong becauseof different in their colonysocial structure withthevalues predicted fora markedly alates,are entirely consistent nest-site at thetwosites.We proposethat pressures colonyheadedby a single,once-mated queen.Thusthepop- selective New York popimportance to the limitation is of paramount in Vermont a classic ulationof M. punctiventris represents case of thestructured whichkin ulation,but nest sites are much morereadilyavailable in social insectcolony, within fitsHamiltonian The Vermont expecpopulation selection is presumed This presumption is Vermont. to be operational. whereas almostperfectly theory verified by data on sexual allocation(Snyderand Herbers tationsfromkin-selection theseexpectations deviatesfrom 1991;Banschbach andHerbers 1996),sincetheVermont pop- the New Yorkpopulation of the Further examination ecological forces substantially. ulationhas produced investsexuals in a 3:1 female-biased at thetwo siteswill prove colonysocial structure mentpattern forthreeof the fouryearsforwhichwe have regulating in natural howkinselection operates data. Thatis, theVermont to valuablein determining population conforms perfectly populations. the relatedness structure positedby Hamiltonas important forkinselection (1964) andto workers winning queen-workACKNOWLEDGMENTS er conflict over sexual allocationratios(Triversand Hare 1976). L. SatM. Freedman, Thanksto V. Backus,E. Choiniere, is af- cowitz,L. E. Snyder, The geneticstructure of the New Yorkpopulation us to collect and D. Webbforhelping where relatedness and censusants.We are also grateful fected ofpolygynous bythepresence nests, T. Tolle, to H. Hobart, their and J.Williamsforhelpin thelaboratory. values amongnestmates erodedfrom are significantly from Suggestions Hamiltonian expectation and fromthe values observedin D. Quelleraided ouranalysisof thegenetic data.This work is pronounced there was supported Vermont (Table 8). Population viscosity theNational Science toJ.M.H.from bya grant as well. Such viscosity has beenpositedas a force promoting Foundation. kinselection (Hamilton 1964),butrecent modelshaveshown thatthe kin-selection value of livingnear relativescan be LITERATURE CITED overridden with those relatives by the cost of competing V. S., andJ.M. Herbers.1996. Complexcolonysocial of Banschbach, (Queller 1992). We cannot evaluatethecostsand benefits conqueen-worker structure in social insects: II. Reproduction, thisviscosity forour study species,butpopulation viscosity Evolution50:298-307. and levels of selection. flict, in other has beenassociatedwith antspecies(Pam- Boomsma,J. J., P. J. Wright, polygyny and A. H. Brouwer. 1993. Social nestsor multistructure in the ant Lasius flavus: Multi-queen ilo and Varvia-Aho 1979; Sundstrom 1993) and maybe tied 18:47-53. Ecological Entomology nestmounds? to limiteddispersalby queens (Keller and Passera 1993). M. S., and R. E. Page Jr. 1989. The geneticsof social This limiteddispersalof queens may then,in turn, lead to Breed, CO. Press,Boulder, Westview evolution. highly male-biased sex ratios, suchas thoseproduced by our Creighton, America.The Cosmos W. S. 1950. The antsof North Press,Cambridge, MA. speciesin New York(Banschbach and Herbers1996),which

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296

V. S. BANSCHBACH AND J. M. HERBERS

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