SUPPL.NO.25 SOUTHWESTERNENTOMOLOGIST SEPT.2OO2

THE KILLING OF NESTMATEQUEENS IN COLONIES

RichardJ. Deslippe

Departmentof BiologicalSciences, Texas Tech University Lubbock,TX 79409-3131USA

ABSTRACT

I review the literature on the killing of queensby conspecific nestmatesin ant colonies,with specialemphasis on the red importedfire ant, Solenopsisinvicta Buren (:Formicidae.) Killings in pleometroticassociations and incipientcolonies aredistinguished from thoseoccurring in secondarilyformed polygynous colonies. In the former,queen mortality follows a typicalpattern where all queensexcept one are killed or abandonedfollowing worker emergence.In the latter,queen eliminations serve partly to counterbalanceincreases in queenabundance that may resultfrom adoptionsofrelated or unrelatedqueens. Pheromones produced by queensapparently trigger workers to execute queens,but the compoundshave never been identified. Characterizationof the "execution"pheromone of S. invictahas been a major objectiveof my researchover the pastseveral years, and I commenton progresstowards this goal.

INTRODUCTION

Within coloniesof social ,queens are often killed, and I herereview the literature and comment on recent research on such killings in (Hymenoptera: Formicidae).The discussionis restrictedto executionsby workersor otherqueens ofthe samespecies. Emphasis is placed on the red imported fire ant, Solenopsisinvicta Buren, themyrmecine featured in this supplementalissue. The number of wingless queensharbored by an ant colony rangeswidely, from zero to over a hundred(Htilldobler and Wilson 1990,Elmes and Keller 1993).A single queen(monogyny) is typical of most species,but multiple queens(polygyny) can be cornmonespecially in socialparasites, and in speciesspecializing on short-livednest sites or long-lived patchily distributedhabitats (Hiilldobler and Wilson 1977).Polygyny is either primary or secondary.In the former, foundressesform a group to start a new nest (pleometrosis),and they and their workers continueto tolerateeach other through colony maturation(H

lll and culminatesin eliminationmay occur when direct conflict betweenqueens escalates (Bartz Hdlldobler death(Heinze 1993),or when workers attackand executethem and by iSgZ, Fig. 1). Such killing of queensby nestmateshas garneredmodest attention researchersfrom both Uaiic and practical perspectives.Rationales for studieshave includedclarifying proximate and ultimatecauses of the behavior,and uncoveringtraits linked to gr"ut"r-rist of mortality. My own efforts over the past severalyears have involvedeiploring the pheromonalbasis of workerexecution of queensin S. invicta,with theultimate goal of exploitingthe behavior to induceself-destruction of colonies.

FIG. 1. Workers(5. invicta)attacking and dismembering one of their queens.An executed queenoften ends up with her head,limbs andgaster severed from the thorax.

PLEOMETROSISAND QUEENELIMINATION

Pleometrosisis one of severalsuccessful strategies employed by antsto navigate the challengingfounding stage, and foundressespartaking in it experiencevarious advantagesover those initiating colonies independently.Pleometrotic queens, for instance,tend to havereduced mortality, raise more brood,produce'larger minims, and ,,raiseboth workers and sexualssooner (Stumper 1962,Taki 1976, Mintzer 1979,1987, 1990,Hdlldobler and Carlin 1985,Rissing and Pollock 1987,Vargo 1988,Peeters and Andersen1989, Sommerand Hdlldobler 1995, Cahanand Julian 1999,Kenne et al. 2000).In S. invicta, pleometrosisduring the clauskalphase of nest foundingincreases total offspring output (Tschinkel and Howard 1983, Tschinkel 1993), but does not improvemortality rqtes of foundresseslike in Lasiusflavus Fabicius (Waloff 1957). Maximuminitial proddctionof workersis achievedby queensin groupsof intermediate size(Tschinkel and Howard 1983),as is the casewith Myrmecocystusmimicu.s Wheeler (Barz andHdlldobler 1982) and Formica podzolica Francoevr (Deslippe and Savolainen 1995).

n2 Queensin pleometroticassociations often die from both natural causeslike starvationand aggressive social interactions during colony development. Their deathrates tend to increasedramatically once workers begin eclosing,for frghting among queen escalatesas in Aztecaxanthacroa Roger (Choe and Perman 1997) or workersharass some queensbut not others as in M. mimicus(Bartz and H

ll3 Who becomesvictorious is also likely influencedby whetherit is the queens Oemselvesor tlte workers who do the killing. When the former are involved, selection should favor improvedfighting ability of queens.Investigators typically assumesuch ability is associatedwith larger size or weight (Nonacs1992, Balas and Adams 1996a; BEmasconiand Keller 1999),but the link may be weakerthan presumed.For instance, sotnetimesqueens are heaviestbecause they becomephysogastric sooner, and their cumbersome gasters then inhibit rather than promote fighting ability (personal obeervationson F. podzolica).Likewise, smallerqueens can be superiorfighters and readilykill largerones, as illustrated in dynamicsbetween parasitic and larger host queens duringusurpation of colonies(Htilldobler and Wilson 1990).When workers eliminite the supehumcraryqueens, they may do so on the basisof pheromoneproduction by queens. If suchproduction is linked to ovariandevelopment as in s. invieti (yugo lgdz,'lggg), then selectionshould favor greaterbrood production. Greaterproduction should also be favorcd when workers can distinguish their mothersfrom other queens,because a queen shouldhave a better chanceof surviving when most of the offspring are her own. Survivorshipofincipient coloniesdepends critically uponthe initial invesrnentrn 1or!ers, as a larger or more able force can better withstand tbreats to the colony (Techinkeland Howard 1983,Jerome et al. 1998).One suchthreat is intraspecificbrood raidingresulting from intensecompetition among young colonies (Bartz and Hdlldobler 1982,Rissing and Pollock 1987,1991, Nonacs ts-9j, edamsand tschinkel 1995).During rai&, worken transporteggs, larvae and pupae between nests until they accumulatein the witming colonies. Workers from the losing coloniesthen join the victors, leaving behind thcir qucerrs.Generally, neither raiding nor raided workers attempt to recruit the raided quc€n, but sometimesthe abandonedqueens try to join the strengthenedcolonies and successfullydisplace the original queens(Stamps and vinson 1991,Tschinkel 1992a,b, Balasand Adams 1997). The abandonmentof nestmatequeens can be adaptive when colony takeover is porsiblc.In essence,workers make the bestofa bad situationby hopingtheir queencan ulurp the colony to which they have relocated (i.e., the "hopeful co-ernigration" hytpothesis)(Pollock and Rissing 1989).Support for this notion comesfrom the most sttldicd of the brood raiding species,S. invicta. In this ant, attemptsat usurpationsucceed more often when the migrating queenpenetrates a colony with familiar workers (Adams and rschinkel 1995,Balas and Adams 1996b,1997). They are also more successfulwhen &bandoneesenter a colony within a few hours following conclusionof brood raiding @alasmd Adarns 1997).Presumably, the challengeris desperate,for failure to takeovera colony slsurcs her imminent death.

SECONDARY POLYGYNY AND QUEEN EXECUTIONS

Following a queenright(i.e., one queenper nest)period, queenabundance can increasebecause workers sometimes adopt either related or unrelatedqueens into their nests, or becausealate queensshed their wings despite not being fertilized. Although workers of monogyne forms normally adopt only when their colonies are queenless (Fletcherand Blum 1983,Sorensen and Fletcher 1985), workers ofpolygyne formsadopt morereadily evenwhen their colonieshouse fertilized queens @letcher and Blum 1983, Brian 1988,Glancey and Lofgren 1988,Fortelius et al. 1993, Sundstrdm1997). The reulting increasein nestmatequeens can be substantial,and may be counterbalancedby th€ir executions.This combinationof adoptionsand executionsenables the critical ability to fegulatequeen abundance. When queens are killed in polygynous colonies, workers usually perform the deedsrather than other queens,especially when populouscolonies are formed and queens

ll4 arepoorly equippedfor fighting as in S. invicta (Wllson 1966,Fletcher and Blum 1983, Lipski et al. 1992,Heinze 1993).In such colonies,workers are larger, and are more numerousand aggressivethan those in incipient colonies.These traits facilitate the processof workers overcomingtheir nestmatequeens, which are normally larger and, understandably,resistant to their own execution.Further, at least someof the dealated queensin polygytous coloniesare older than thosein incipientcolonies, thus probably making them better pheromoneproducers. Elevated pheromoneproduction may enable queensto control worker behaviorbetter, including control over worker executionof otherqueens (Fletcher and Blum 1983,Flether and Ross1985, Fletcher 1986). In this way, queenscan indirectly kill other nestmatequeens. A remarkablepulse of queen executionsoccurs at the beginning of the reproductiveseason in the fugentine anI,Linepithema humile Mayr. Every spring,about 90% of nestmatequeens are killed by workers,resulting in a lossof about8% of the tptal biomassof the colony (Markin 1970, Keller et al. 1989).Markin (1970) not€d that workers attackedqueens as they would large prey, and describedan event where many queensjoined workerson the foragingtrails. Workers attacked about l0% of thesequwns and eventuallysevered the gastersand headsof their victims. Further study of the phenomenonrevealed that the age,weight and fecundityofqueens played no substantial role in which individualsthat workersselected for execution(Keller et al. 1989).The drasticreduction in queensenables female larvae to developas new queens,apparently a result of being releasedfrom the inhibitory effect of a queenprimer pheromone(Vargo 1998).

n iVOLVEMENT OF PHEROMONES

The fertility of a queenis positively associatedwith her pheromonalinfluence (Fletcherand Blum 1983,Willer andFletcher 1986, Carious-Etienne and Passera1993). In S. invicta,the sheddingofwings correspondsto rapid changesin the endocrinesystem of queens,and these changesstimulate pheromoneproduction and ovary development (Vargo 1999).As a result,wingless queens are superiorover winged onesin conholling nestmatesvia pheromones(Vargo and Fletcher1986, 1987). Less than 50% of wingless queensmay be fertilized in S. invicta colonies,and althoughthey tend to be more fecund thantheir unfertilizednestmates (Vargo and Fletcher 1989), dealate queens, regardless of reproductivestatus, are more effectivethan alatequeens at pheromonalcontrol. The rate ofworker executionofsexual larvae,for example,was significantlygreater in queenright than in queenlesscolonies, but did not differ betweenqueenright colonies containing eithera fertilizedor unfertilizedqueen (Klobuchar and Deslippe unpublished). With respect to the regulation of queen numbers, it is thought pheromone concentrationin coloniesplays a key role. Fletcherand Blum (1983) proposedthat deviations from an optimal range in the amount of queenpheromones circulating in a colony stimulatesworkers to restorethe concentrationwithin the optimal rangeby either adoptingnew queensor executingsupemumerary queens, as appropriate.Working with the monogyne form of S. invicta, they inhoduced pairs of foreign queens into 12 queenlesscolonies and monitored their acceptanceby workers.Workers killed at leastone queenin every colony, as predicted.More recently,Deslippe and Guo (unpublished) monitored worker execution rates of queensin the polygyne form of S, invicta. They established66 subsetcolonies with 1,3,5, l0 or 15queens, and found that mortalityrate of queenswas positively correlatedwith initial density of queens.Interestingly, the nature of the density-dependentresponse was under-compensating,a result consistentwith the ideaof mutualinhibition of pheromoneproduction among queens.

ll5 Fletcherand Blum (1983) also proposedthat individual differencesin pheromone production should lead workers to execute the lower ranking queens in the pheromone hierarchy when pheromone concentrationsexceed the optimal range for the colony. They tested this idea by introducing pairs of queensto queenlesscolonies, and then monitored which was killed. Each pair was composed of a physogastric and a non-physogastric queen, with the former being the more fecund in all likelihood. As predicted, workers almost always killed the non-physogastric female. Likewise, I have even observed some alate queensoccasionally killed when kept in laboratory colonies for some time (Fig. 2). These victims may have been among those alate queensthat begin ovarian development and pheromone production prematurely, and would be low ranking in the pheromone hierarchy.

FIG. 2. An alate queen (5. invicta) that had been attackedand killed by worker nestmates. Her gasterwas ripped opened and its contentsremoved by workers while she was still alive. The queen was several months old, and may have startedproducing new pheromonesprematurely (i.e., before dealation).

Besides the quantity of pherorhonescirculating through a colony, I propose that pulses or rapid changes in pheromone signals play a key role in worker execution of queens. Vargo and Laurel (1994) determined that virgin queens with their antennae removed dealatedboth in the presenceand absenceof a queen, and many of the virgins were killed once they were wingless. The queens may have been executed because workers detected a pulse of pheromones, as pheromone production typically begins shortly after dealation (Vargo 1999). Likewise, in an experiment in which either a winged or wingless queen was paired with a wingless queen, at least one queen was executedin only those colonies containing a winged queen. Ofthe 13 casesinvolving an alate queen, seven alateshad shed their wings within 40 days. Six ofthe 7 queenswere executed,and in thesecases, the time between dealation and execution was 2.8 + 1.2 days. In all but one case, the executed queen was the original alate queen (Deslippe and Guo unpublished).

116 Anecdotalevidence also points to a key role ofpheromonepulses, as threephysogastric queensfrom ar S. invictacolony were each executed by their workers,but only afterthey wereseparated from eachother (S.B. Vinson, personal communication).

ATTEMPTSTO EXTRACTTHE "EXECUTION''PHEROMONES

Although queenpheromones apparently trigger executions,the compoundshave neverbeen identified. I havetried to extractthe "execution"oheromone of S. invicta in organic solvents,as part of the processinvolved in characterizingthe chemical or chemicals.Early attemptswere only partially successful.For example,application of hexane extractsto colonies producedsignificantly more queen executionsthan did applications of hexane (control). This result confirmed the link between queen pheromonesand executions,but the extractswere prepared with hundredsofqueens, and the increasein executionrate was modest.In otherwords, the pheromoneprobably lost most of its activity, and was only effectivebecause extremely high concentrationswere prepared(Deslippe and Guo unpublished).Similarly, there was no differencein the percentof sexuallarvae and pupaeexecuted by workersexposed to acetoneextracts of queensand only acetone(control). However, when extractswere preparedin a buffered salt solution,they inducedworker executionof sexuallarvae and pupaeto the same degreeas living queens.The extractswere introduced to coloniesonce every 12 h for 96 h at concentrationsof only single-queenequivalents (Klobuchar and Deslippe unpublished).

CONCLUSION

Becausethe queenpheromone has been extracted with full activity,and it is stable in the buffered solution (Klobucharand Deslippeunpublished), identification of the compoundcan proceedin a straightforwardfashion. Whether the pheromoneis the same onethat inducesworkers to executemature queens remains to be seen,but onecan readily deducethat it is not the sameas thosequeen pheromones extractable in harshorganic solvents,like the athactionpheromone, venom alkaloids,or the compoundinhibiting dealation.The pheromoneappears to be proteinaceous,perhaps a small peptide,and its identifrcation should pave the way for a greater understandingof the chemical communicationsystem of ants,and enable exploitation of the communicationsystem.

ACKNOWLEDGMENT

I thankthe TexasImported Fire Ant Researchand Management Project and Texas Tech University for funding my researchon the regulation of queen production and abundancein antcolonies.

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