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The Adaptive Significance of Inquiline Parasite Workers

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The Adaptive Significance of Inquiline Parasite Workers Received 5December 2002 Accepted 29January 2003 Publishedonline 30April 2003 Theadaptive significance of inquilineparasite workers Seirian Sumner * ,David R.Nash and Jacobus J.Boomsma Departmentof Population Ecology, Zoological Institute, University ofCopenhagen, Universitetsparken 15, DK-2100Copenhagen, Denmark Social parasites exploit thesocially managed resourcesof their host’s society.Inquiline social parasites are dependenton their hostthroughout their life cycle,and so many ofthe traits inherited from their free-living ancestorare removedby natural selection.One trait that is commonly lostis theworker caste, thefunctions of which are adequately fulfilled by hostworkers. The fewinquiline parasites that have retaineda worker casteare thought tobe at atransitional stage in theevolution of social parasitism, and their worker castesare consideredvestigial andnon-adaptive. However, this idea has notbeen tested. Furthermore, whetherinquiline workershave anadaptive role outsidethe usual worker repertoire of foraging, broodcare andcolony maintenance has notbeen examined. In this paper, wepresentdata that suggestthat workersof the inquiline ant Acromyrmexinsinuator play avital role in ensuringthe parasite’ s fitness.We show that thepresence of these parasite workershas apositive effecton the production of parasite sexualsand a negative effecton the production of host sexuals. This suggeststhat inquiline workersplay avital role in suppressinghost queen reproduction, thus promoting therearing ofparasite sexuals.To ourknowledge, these are thefirst experiments oninquiline workersand the first toprovide evidencethat inquiline workershave an adaptive role. Keywords: reproductive suppression;social parasitism; Acromyrmexinsinuator ;adaptation 1. INTRODUCTION gained from producing both sexualsand workers, then a workerlessstate is expectedto evolve quickly (Nonacs& Social parasites capitalize onthe socially managed Tobin 1992). However,a handfulof inquilines doinvest resourcesof their hosts,rather like thedistant relative who in aworker caste(nine out of 67 specieslisted in takesup an offerof a bedfor thenight andnever leaves. Ho¨lldobler &Wilson(1990)). This has beeninterpreted While theunwanted guest exercises strategies toexploit asincomplete adaptation toinquilinism by parasites at a theresources of the host’ s home,the host must respond primitive stage in their evolution (Wilson1984; by detectingand ultimately evicting them.This studyis Ho¨lldobler &Wilson 1990; Nonacs& Tobin 1992). concernedwith theadaptive strategies ofthe unwanted There is little evidencethat inquiline workersare effec- guest,the social parasite. tive in performing tasksthat are typical offree-living work- Social parasitism is commonthroughout theanimal ers.They are apparently unmotivatedin broodrearing and kingdom; for example, cuckoosparasitize thebrood- transportation (e.g. Kyidris yaleogyna ;Wilson &Brown caring abilities ofanother speciesby laying their eggs in 1956) andare ineffectivehunters, foragers andnest build- thenests of their hosts(Brook &Davies 1988). Social ers (K.yaleogyna ;Wilson& Brown1956; Polyrhachislama ; parasites are commonin thehymenopteran societies,and Maschwitz et al. 2000). There is only oneaccount from a they have evolved repeatedly in thebees, wasps and ants single colonyof Monomoriummetoecus in which inquiline (Wcislo 1987). In somecases, hymenopteran social para- workersappear toforage effectively (Wilson& Brown sitesproduce a worker castethat clearly has an adaptive 1958). However,inquiline workersmay perform some function(e.g. workers of slave-making antsare crucial for adaptive functionthat falls outsidethe normal worker rep- raiding other hostcolonies; Ho ¨lldobler &Wilson1990). ertoire, asis observed,for example, in slave-making ants. However,most permanent hymenopteran social parasites Theseworkers show a regressionof typical worker func- producesexuals but no workers, and the selection pressure tionssuch as brood caring, foraging andnest-building for theloss of the worker casteis likely tobe strong if the abilities (Alloway 1979; Ho¨lldobler &Wilson 1990) but social parasite cansuccessfully exploit theworker func- are highly adaptednest raiders (Foitzik &Herbers2001). tionsof its host. Weknowof only onedescription of inquiline workersper- Permanent social parasites, or parasitic inquilines,are forming an adaptive function: P. lama parasite workers dependenton their host’s societythroughout their life appear able tocare selectively for parasite brood,albeit becausethey donot kill thehost queen. Most inquiline lesseffectively than their hostcounterparts (Maschwitz et specieshave losttheir worker caste,since they rely ona al. 2000). constantsupply ofhost workers (e.g. Pseudomyrmex In this paper, weintroducethe idea that theproduction leptosus;Ward 1996). If thefitness gained by aparasite ofworkersmay bea fitnessinsurance policy for incipient from producing only sexual broodis greater than that inquilines.We suggest that they may help tosuppress host-queenreproduction in incipient systemswhere more *Authorand address for correspondence: SmithsonianTropical Research complex methodsof controlhave notevolved. We present Institute,Balboa, Panama, Republicof Panama ([email protected]). asetof predictionsfrom thehypothesis and test them with Proc.R. Soc.Lond. B (2003) 270, 1315–1322 1315 Ó 2003 TheRoyal Society DOI10.1098/ rspb.2003.2362 1316S. Sumnerand others Adaptiveparasite workers field data andmanipulation experiments onan inquiline produceworkers that, like thequeens, closely resemble socially parasitic fungus-growingant. their hostcounterparts (Schultz et al. 1998; Bekkevold & Boomsma 2000). Parasite workerscan be distinguished (a) Ahypothesisfor themaintenance ofadaptive from thehosts by their relatively smaller metapleural inquiline workers glands (Sumner et al. 2003b),facilitating in vivo manipu- Inquiline parasites are selectedto increase their ownfit- lation experiments.Colonies of A.echinatior consistof sev- nessby redirecting theresources of the host colony. One eral thousandworkers (Weber 1972; Bekkevold & way in which they dothis is by suppressingthe host Boomsma 2000). Sexual reproductionby theparasite is queen’sreproduction,so allowing resourcesto beinvested essentially semelparousand can occur in hostcolonies of in parasite rather than hostsexuals (e.g. Wilson & Brown any size,with sexual broods(male andfemale) varying 1956; Passera et al. 2001). Weproposethat parasite work- from twoto 326 individuals (Bekkevold &Boomsma ersof incipient inquilines may play akey role in redirecting 2000). After theemergence of parasite sexuals,the host hostresources, by aiding thesuppression of host repro- colonydeclines and eventually dies,putatively owing to ductionand promoting theproduction of parasite sexuals. thesuppression of host worker production(Bekkevold & This hypothesismakes several predictionsabout how Boomsma 2000). Acromyrmexinsinuator and A.echinatior selectionacts on incipient inquilines. are both facultatively polygynous,with upto fourhost and First, thepresence of parasite workerswill beassociated nineparasitic queensin asingle colony(Bekkevold et al. with thepresence of parasite sexuals.As a corollary, if host 1999; this paper), andcolonies of different gyny are of resourcesare divertedvia suppressionof host repro- similar size(see § 3b). The effectof queen numbers on duction,a negative relationship betweenparasite worker theproduction of parasite workersand sexuals is, there- productionand host sexual productionis expected fore,easily testedusing data from field colonies. (prediction 1). Although thereis little data available, observationson The numberof parasite andhost queens present in a A.insinuator already indicatethat its investmentin the colonycan affect parasite worker production.If, in worker castehas beenreduced from that ofa free-living addition toworkers, parasitic queensplay adirectrole in stateand that theworkers are notfully functional.First, theredirection of host resources, then fewer parasite work- A.insinuator producesminor workersprior tosexual pro- erswill berequired for sexual reproductionwhen the duction,and these constitute on average 25% ofthetotal numberof parasite queensis high. Furthermore, in poly- worker forcein colonieswhere they are produced.They gynoushost colonies we expect the combined number of only rarely investin large workersthat wouldbe able to parasite workersand queens required for effectivesup- forage, probably whenhost foragers are in shortsupply, as pressionto be greater than in monogynouscolonies suggestedby prediction 6(Sumner et al. 2003b). Second, (prediction 2). A.insinuator workersfare poorly in diseasedefence relative To assessthe success of resource distribution andto totheir hostcounterparts (Sumner et al. 2003b), as in pre- determinewhen to start rearing parasite sexuals,parasite diction5. However,these observations are also consistent workersmust be capable ofdistinguishing betweenhost with thenull hypothesisthat workersare vestigial and andparasite brood(prediction 3). This feedbackmech- functionless. anism assumesthat castedetermination is at least partly In this paper, weaddressthe remaining fourhypotheses. underworker control.This is consistentwith thecurrent Weusedata from field coloniescollected over 10 years to view ofcaste determination in ants,whereby gyne devel- assessthe influence of parasite worker productionon sex- opmentmay beswitched on by queenpheromones, but is ual production(prediction 1) andhow production of para- ultimately
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