NetherlandsJournal of 52(1):77-86 (2002)

SPERM TRANSFERIN THEJAPANESEQUEENLESSANT SP.(:FORMICIDAE)

by

1,4, 1 2 3 1 D. ALLARD ¤, B. GOBIN , F. ITO , K. TSUJI andJ. BILLEN (1 ZoologicalInstitute, University of Leuven, Naamsestraat 59, 3000 Leuven, Belgium ; 2 Facultyof Agriculture,Kagawa University, Ikenobe, Miki 761-0795, Japan ; 3 Faculty of Agriculture,University of theRyukyus, Okinawa 903-0213, Japan ; 4 ResearchAssistant oftheFund of ScientiŽ c Research— Flanders )

ABSTRACT Spermtransfer in the Japanese ponerine Diacamma sp.was studied by making histologicalsections through copulating pairs. Males of thisspecies remain attached to the femaleby theirgenitalia for several hours, during which they are killed by thegamergate andher nestmates. Our sections revealed that males clasp the female’ s laststernite with twochelate appendices of the male copulatory organ, called volsellae. W ealsofound thatthe male inserts his sharp sclerotised penis valves in the female bursa copulatrix, a dorsalevagination of the genital chamber. The penis is in ated inside the female genital chamber,possibly strengthening the connection between the partners. We noticed that themale transfers his sperm to the female in a sheathof gelatinous material, called a spermatophore.Eventually the male’ s abdomenis removedby the . Prolonged copulationsare viewed as an effectivemale strategy to ensureunique fatherhood.

KEY WORDS: Diacamma sp.,prolonged copulation, sperm transfer, spermatophore.

INTRODUCTION

Themechanism ofsperm transfer has beenstudied quite extensivelyin several orders,but in studies ofant matingsystems it has received little attention. Antqueens typically acquirea lifetime supplyof sperm (fromone or several males) in asingle mating episodeat the beginning oftheir life, andstore it in their spermatheca.Most studies report the copulatorybehaviour and the numberof sperm transferred between partners (PETERSEN & BUSCHINGER, 1971; KELLER & PASSERA, 1992; HEINZE,1997).As far as weknow, the onlyrecord of the mechanism ofsperm transfer in deals with the myrmicine Carebaravidua studied by ROBERTSON (1995).After ashort dispersal ight,winged females ofthis species attract males with .Copulation lasts

¤ Correspondingauthor; e-mail: [email protected] .ac.be

© KoninklijkeBrill NV ,Leiden,2002 Alsoavailable online - www.brill.nl 78 ALLARD, GOBIN, ITO, TSUJI &BILLEN forabout 4 min,and females havebeen reported to mate withup tofour males. Duringcopulation, the male inserts his aedeagusinto the bursa copulatrixof the female with the volsellae holdingthe ventral edgeof her terminal gastral tergite. Thesevolsellae are twopincerlike appendages ofthe male copulatoryorgan, terminating inan outer rigid cuspis and aninner articulated digitus. Spermis transferred in aspermatophore, formedby accessory glandsecretions (R OBERTSON,1995).With regard toother Hymenopterans, sperm transfer has beenthoroughly studied inseveral species of Apis (KOENIGER & KOENIGER,1991).Sperm is transferred directly fromthe male seminal vesicles into the female oviductor spermatheca, without formation of a spermatophore.During the copulationin free ight,males remain attached to the female by their endophallus,and in some species this connectionis strengthenedby special adhesiveorgans on the hindlegsof the drone. TheJapanese queenless ant species Diacamma sp.belongs to the sub- family .This subfamily is characterised bythe occurrenceof alimited queen-worker-dimorphismand the absenceof a queencaste in some genera(P EETERS & ITO,2001),including Diacamma (PEETERS, 1991). D. sp.from Japan is the only Diacamma species foundin the Cen- tral andSouthern Ryukyu Islands. It was previouslyreferred to as D. ru- gosum (LeGuillou) by F UKUMOTO et al. (1989)but is, in anongoing revision,considered to be D. indicum (PEETERS,personalcommunica- tion).Reproductive tasks are performedby a single gamergate,which is amated workerlaying fertilised eggs(P EETERS & CREWE,1984).Every workerecloses with apair oftiny bladderlikeappendages of the mesotho- rax,called gemmae(P EETERS & BILLEN,1991).Reproductive division oflabourin several Diacamma species is regulatedby mutilation ofthese gemmae (FUKUMOTO et al., 1989; PEETERS & HIGASHI, 1989; SOM- MER et al.,1993).Shortly after eclosion,the gemmaeare aggressively removedby the gamergate(which is the onlyindividual in the colonythat retains hergemmae) and her nestmates. This mutilation affects the be- haviourand reproductive capacities ofthe callow.Mutilated workershave neverbeen observed to mate andoviposition is rare inthe presenceof a gamergate(K IKUTA & TSUJI, 1999). Coloniesmultiply byŽ ssion, aprocess whichfrequently occurs when movefrom one nest-site toanother (F UKUMOTO & ABE, 1983). If acolonyloses its gamergate,a newlyeclosed workerretains hergemmae, mates with amale andbecomes the newgamergate. The mating sequence of D. rugosum has beendescribed by F UKUMOTO et al. (1989) and NAKATA et al. (1998)and corresponds to the female calling syndrome (HÖLLDOBLER & BARTZ,1985).Males leave the parental nest inthe early evening2 daysafter eclosion,actively yingaround in search for