Organizarea Colomiei de Albine

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  • Review

    Organization of honeybee colonies: characteristicsand consequences of a superorganism concept

    Robin F.A. Moritz Stefan Fuchs

    aInstitut fr Zoologie, Martin-Luther-Universitt,Krllwitzer Str. 44, D-06099 Halle/Saale, GermanybInstitut fr Bienenkunde, Universitt, Frankfurt/Main,Karl-von-Frisch-Weg 2, 61440 Oberursel, Germany

    (Received 24 September 1997; accepted 10 December 1997)

    Abstract-The colonial organization of honeybees reveals numerous analogies to multicellularorganisms which makes it tempting to use the term superorganism. The sterile workers fulfill therole of the somatic cells in organisms with intricate and complex interactions. These interac-tions are under partial control of hierarchical signals (pheromones) which are primarily used forglobal information of the colony. The majority of the activities in the colony is, however, regu-lated through local decision making and through self-organized processes which are regulatedthrough worker threshold response variability. In honeybees this is enhanced through the highlypolyandrous mating system which allows for wide genotypic variance and the presence of geneticspecialists. Although both individual and colony level selection can be observed in honeybees thelatter seems to be the predominant selective force. This is similar to organismic selection whereselection among or within cells is less relevant to evolutionary processes than fitness at theorganismic level. Inra/DIB/AGIB/Elsevier, Paris

    social organization / superorganism / division of labor / self-organization / polyandry / Apismellifera

    1. INTRODUCTION

    Honeybees live in tight societies, whereevery individual is highly integratedbehaviorally and dependent in its survivaland reproduction. The social group is anessential entity for inclusive fitness of anygiven honeybee, and the fitness of each

    member is zero if deprived of the groupcontext. In a colonial context, however,honeybees are extremely efficient. Theycan regulate intracolonial environmentsuch that they buffer even exceptionalfluctuations in ambient conditions. Theirability of thermal intracolonial control andtheir ability to store nectar and pollen

    * Correspondence and reprintsTel.: (49) 6171 21 278; fax: (49) 6171 25 769; e-mail: [email protected]

  • allows them to sustain extended periodsof dearth and cold. Clusters of bees areable to survive ambient temperatures aslow as -80 C (Southwick, 1988). As aconsequence of this homeostatic ability,Apis mellifera L. was able to colonize mostdiverse habitats ranging from northernEurope to the Cape of South Africa (Rut-tner, 1988; Smith, 1991).

    2. ORGANISMS ANDSUPERORGANISMS

    Honeybee colonies have often beencalled superorganisms in analogy to acomplex higher organism being composedof numerous single cells (Wheeler, 1928;Seeley, 1989; Moritz and Southwick, 1992).There is obviously something tempting inthis view, and certainly beekeepers prefer tothink of bees in terms of colonies ratherthan individuals. Although many of theprincipal features may also be found inother socially organized animals such aswolf packs or groups of mongoose, thereis something special about the tightness ofbee colonies which closely resembles atleast more primitive multicellular organ-isms, and thus seems to call for a term suchas superorganism.

    Although such a definition may at firstglance have heuristic appeal, the issue ofwhether the use of the term is helpful inunderstanding the biological processesgoverning life history of honeybeesremains controversial. For a critical eval-uation, there are at least three aspects toconsider: analogies in structure, analogiesin the perspective of genetics and selec-tion, and analogies in organizational prin-ciples. We deal with these each in turnand finally show how we think the partic-ular organizational demands may affectgenetic transmission.

    2.1. Analogies in structure

    The first and basic analogy between anorganism and a honeybee colony is thatboth are composed of single units, cellsand bees, respectively, which depend onthe functioning of the higher unit for theirsurvival. Individual cells have life cycleswithin the organism, and isolated cells areusually unable to develop outside theorganismic environment. It requiresfocused technical efforts to obtain con-trolled cell growth and differentiation within-vitro cell culture. The development of anindividual honeybee does not differ muchfrom that of any other holometabolic insectin principle, yet there are dramatic bioticconstraints which govern the developmentof a honeybee. Most evident is the devel-opmental pathway from egg to adult whichcan only occur in the presence of largenumbers of other bees. The large body ofworkers is instrumental for brood rearing.They provide the combs where the queendeposits the eggs. They feed and foster thelarvae and maintain the correct tempera-ture for brood development. They also pro-vide a nest site which is of crucial impor-tance for temperature control andprotection of the stores and the broodagainst predators. Thus the successful com-pletion of the above developmental cycledepends intricately on the presence of anintact colony comprised of a nest cavity,combs and a large number of other bees.

    The next structural analogy is differ-entiation. During development of anorganism, cell lines are extremely versatileand can specialize into an amazing varietyof different forms. Although somethingsimilar is observed in many ants, whichhave distinct castes of soldiers, nurses orforagers, nothing of this kind is found inhoneybees. The only exception is the dif-ferentiation into workers and reproduc-tives. This, however, does not imply thatthere is no specialization among workerhoneybees. A honeybee colony also

  • requires a variety of tasks to be performed.Worker specialization is, however, notsolved through phenotypic castes, and wewill deal with that crucial aspect later indiscussing organizational principles. Thestructural analogy between honeybeecolony and organisms is in the degree oflocal organization, resembling the struc-turing of an organisms cells into a com-posite whole with different organs. In abee colony there are distinct regions forproliferation (the brood nest) and for stor-age of carbohydrates or proteins. Thesemight be seen as analogues of if notorgans, then certainly a primitive organ-isms shape.

    Another striking analogy is thatbetween workers in a colony and somaticcells in an organism. Both have sacrificedtheir direct fitness in support of other enti-ties: the sexual reproductives in the case ofhoneybees, and the germ line cells in thecase of organismic cells. Most honeybeelarvae develop into workers, which usu-ally neither reproduce nor compete forreproductive success. This is very differ-ent indeed to comparable solitary organ-isms where interindividual competitionfor resources and reproduction is the rule.

    Although these analogies seem con-vincing at first sight, they are based onplain phenological and very proximatesimilarities. As such, they are least tellingfor ultimate arguments and may invitemisunderstandings rather than insights.We therefore proceed to investigate analo-gies which are based on more general prin-ciples, rather than on possibly accidentalresemblances.

    2.2. Analogies in evolutionarymechanisms

    Attitudes to the superorganismic con-cept have undergone considerable change.Evolutionary biologists have proposedrather polarized views during the past

    decades. In reaction to the refutation ofnon-Darwinian group selection ideas(Wynne Edwards, 1962), the individualwas firmly reestablished as the unit ofselection (Williams, 1966; Maynard-Smith, 1964). Groups were banned fromthe selection arena, and consequently therewas no longer any room left for superor-ganisms. With concepts of inclusive fit-ness (Hamilton, 1964a,b), and genes asprimary units of selection (Dawkins, 1976)this individual-centered view softened andgroup selection regained credibility (Wil-son, 1975, 1977). Subsequently, the super-organismic view regained momentum(Wilson and Sober, 1989; Seeley, 1989).In defining gene action as primarily a log-ical relation between a replicator and anoutside effect, Dawkins (1982) furtherdevaluated the role of the individual tothat of a mere vehicle for gene replica-tion. This radical view removed all barri-ers to regard colonial properties as geneactions which might be traced via indi-vidual behavioral traits to the genes in theindividuals. Indeed Hunt et al. (1995) wereable to map quantitative trait loci withindividuals that influenced pollen hoardingat the colonial level, thus proving the prac-tical value of this concept of the colonyas an extended phenotype (Dawkins,1982).

    This change in attitude invited a reeval-uation of the significance of individualorganisms for evolution. Dawkins (1982)pointed out that genetic bottlenecks in thetransmission of genes from generation togeneration are a necessary condition forthe evolution of stable units with minimalor reduced intraorganismic conflict. Inhoneybee colonies, this condition is met,as genes are transmitted through the bot-tleneck of a queen and a few drones, fromwhich all individuals of the next-genera-tion superorganism are derived.

    Critics of the superorganism concepthave correctly pointed out that there is aconceptual difference between coopera-

  • tion of somatic cells with identicalgenomes and cooperative behavior ofgenotypically different organisms. In thelatter case there is a strong conflict poten-tial between direct individual reproduc-tion and fitness gains through kin selec-tion. Each individual worker has to decidehow to invest its individual resources inthe colony. Should it favor females overmales? Should it behave nepotistically torelated nestmates? For the evolution ofentities, genetic bottlenecks are logicallymore important than the internal distribu-tion of the genes over the entities. Therewill be greater potential for intraorganis-mic conflict with wider genetic bottle-necks, and smaller if these are narrow.The extreme degree of polyandry of thehoneybee queen may yield a relativelywide bottleneck if queens of many patri-lines are reared. However, this seems tobe a weak argument against the superor-ganism concept since in a huge variety oforganisms this bottleneck is not minimizedeither, by the transmission of two or moresets of genes in the formation of a zygote.

    While these general considerations dostrengthen the superorganism analogy, fur-ther support comes from the understandingof the evolution of simple multicellularorganisms. Slime molds provide an exam-ple where the component cells move inde-pendently, until they aggregate and dif-ferentiate into somatic stalk cells and germline spore cells (Bonner, 1995). In a radi-cal reevaluation of early evolution, Buss(1987) envisaged organisms as lines ofcells, competing for proliferation andaccess to the germ line. He stated thatorganismic selection is a two-level pro-cess, acting on cell lines and organisms,with possibly conflicting interests andan increasing ability of organisms to con-trol the selfish tendencies of their cell lines.It is thus an interesting twist in the dis-cussion of the superorganism analogy, thatit is recently supported by the discoveryof the similarity of organisms to superor-

    ganisms, with two-level selection consid-erations for organisms strikingly familiarto the student of insect societies. The mainsupport of this analogy thus is that thehigher-level selection outweighs the lower-level selection. This is certainly true inhoneybees which show remarkable lowintracolonial conflict in spite of a hugeconflict potential (Visscher, 1998).

    2.3. Analogies in organizationalprinciples

    The organization in multicellular organ-isms is characterized by the cooperationof thousands of subunits towards the ful-fillment of the multitude of different func-tions crucial for the welfare of the organ-ism. It seemed to be clear to Wilson EO(1975) that: "the remarkable qualities ofsocial life are mass phenomena thatemerge from the meshing of these simpleindividual patterns by means of commu-nication". So, how do the mass phenomenaemerge and, what type of communicationand individual patterns, if any, are behindthese in honeybees?Two organizational principles can be

    observed in organisms. One is the coor-dination of the different cell functions, theother is the specialization of cell groupsfor different purposes with a differentiationinto highly specialized tissues. We want toshow that striking similarities exist to theorganizational principles found in honeybees. We also want to emphasize somedifferences. The coordination betweencells and between honeybee workers fol-low surprisingly similar general patterns,which involve self-organization, localdecisions, feedback loops, non-linear inter-actions and central control, but differ inthe relative contribution of these compo-nents. Differentiation and specializationamong honeybee workers are achieved bytemporal castes and genetic variation. Thislatter process may be an important cue to

  • understand some peculiarities in honey-bee reproductive biology.

    2.4. Coordination by self-organizationand local decisions

    Cells in organisms respond to local con-ditions without knowing about the globalcondition of the organism. Many exam-ples of self-organizing processes are foundin developmental biology, where the cellsreact to the immediate conditions definedby their environment, in part formed bythe neighboring cells. Ordered structuresand responses emerge as a result of localinteractions, rather than from centralizedcontrol.

    Of course a global knowledge of thestate of the colony and its environmentmight be quite helpful for an individualbee to decide whether or not to participatein a certain task. However, it is extremelyunlikely that any individual in the colonyhas such knowledge at any given time.Decisions are much more likely to bemade on the basis of local stimuli. Themost famous local decisions are thoseresulting from the dance language (vonFrisch, 1967). The returning foragerrecruits locally other workers to visit thesame food source. Intensity of foragingand switching between resources is medi-ated by the perception of local stimuliwhich are correlated to colony needs andfood source profitability (Seeley, 1986),rather than by direct perception of theseconditions. Many others mechanisms havebeen described. Studying water foragers,Lindauer (1954) found that the regulationof cooperative behavior is not governedthrough a global knowledge, but rather byvery simple local rules. Individual beesrespond to simple local behavioral inter-actions with nest mates or their local nestenvironment to start, continue, or stop aspecific task (Seeley, 1989, 1995;Camazine, 1991; Watmough and

    Camazine, 1995; Robinson and Page,1989). The queen does not decide from aglobal knowledge of all empty drone andworker cells in the brood nest area,whether to lay a drone or worker egg.Before she deposits an egg, she inspectscell by cell and measures the cell widthto determine whether to lay a male orfemale egg (Koeniger, 1970) and thusresponds to a local stimulus threshold, eggpresence and cell diameter. Equally, combusage for pollen and nectar (Camazine etal., 1990) and comb construction followlocal decision rules which are based onstimulus thresholds. Such self-organizedpatterns have been suggested to play avery prominent role in the organization ofcomplex systems [reviewed by Kauffman(1993)]. The idea is that on the basis ofvery simple rules complex patterns emergethat result in seemingly intelligent coop-eration. In honeybees self-organized pat-terns have been suggested for foraging(Camazine and Sneyd, 1991), comb usage(Camazine, 1991) and colonial circadianrhythms (Moritz and Kryger, 1994). Usinga Boolean network, Page and Mitchell(1991) showed that ordered group struc-tures and patterns can easily emerge fromrandom aggregations of individuals in hon-eybee colonies. Clearly self-organizationas a mechanism is common in complexsystems and a priori has nothing to do withevolution (Page and Mitchell, 1989, 1998).Also abiotic complex systems tend to fallinto organized patterns which are clearlyfree of fitness functions (Prigogine andStengers, 1980). There is no reason toassume that self-organization as a mecha-nism is the result of selection in social sys-tems, it is rather predicted by the systemcomplexity itself. Self-organization ininsect colonies is not surprising, on thecontrary it would be extremely odd not tofind self-organized patterns. Nevertheless,we would like to clearly point out that thisdoes not mean that evolution does not actupon self-organized patterns in honeybees.The self-organized structures shape the

  • colonial phenotype and will, therefore, beaffected by natural selection. One possi-bility to tune colonial phenotypes are shiftsin the overall stimulus threshold frame-work in the colony. Such changes cancause dramatic variability in pattern for-mation as shown by Hunt et al. (1995) forpollen foraging. Selection may then mod-ify response levels and even shape non-additive group behavior. Compositegroups of honeybees often do not expressthe arithmetic mean behavior of their sin-gle tendencies, but instead show distinctlyhigher or lower expression levels thanexpected in an additive model (Trump etal., 1967; Moritz and Hillesheim, 1989;Moritz and Southwick, 1987; Guzmn-Novoa and Page, 1994; Oldroyd et al.,1992; Fuchs and Schade, 1994).

    2.5. Coordination by feedback loopsand non-linear interactions

    The homeostatic abilities of honeybeesocieties thus do not demand any kind ofglobal control. Simple feedback loops canemerge as a property of the self-organizedstructures. For example the individual heatproduction of the surface bees in a beecluster, removes the cold temperature stim-ulus for neighboring workers, causing aseemingly well-organized temperaturecontrol (Watmough and Camazine, 1995).One mechanism to explain such nonlin-ear behavioral interactions is throughrecurrent feedback loops which let the per-formance of one individual affect thoseof others. The mechanism underlying thealarm response may give us a simpleexample of such a mechanism. Defensiveflights can be released by swift movingdark objects (Stort, 1974). The attackingbee releases the alarm pheromone whichattracts other bees and reduces theresponse threshold for attacks. If the targetstays in place more bees will release alarmpheromone, further reducing the stimulusthreshold, and even more bees will attack,

    eventually resulting in the extreme massattacks known from African and African-ized bees in the tropics (Collins et al.,1980). If the stimulus disappears condi-tions return to normal threshold levels.This example seems easy to understandbecause we know the behavioral basiswhich is under pheromone control. In mostcases no pheromone will be involved butthe principle will be the same. Workersare engaged in a specific activity and bydoing so, modify the local conditions toexceed the stimulus response threshold ofother workers (positive feedback). Alsothe opposite can be possible: the activity ofa worker reduces the stimulus below theresponse threshold which then stops beinginvolved in that task. Let us look at a pos-sible mechanism for the regulation ofguarding as a hypothetical example toillustrate how an individual workers activ-ity can be regulated by individual responsethresholds. Let us assume the workers ofa given colony have a threshold of fiveguard workers for the task of guarding.Thus if a worker passes the flight entranceand notices less than five workers, it willswitch from its current task to guarding.As soon as five workers are present, nofurther workers will be recruited for guard-ing because the threshold is reached. Thesystem becomes dynamic if we consider adecline in the behavioral threshold of theguards over time. If, for example, after 10min of guarding the threshold for the crit-ical number of guards drops to four (amechanism similar to habituation), thefirst worker will leave the guard groupand choose a different task [perhaps themost favorite task which is doing abso-lutely nothing, Lindauer (1952)]. A newworker with a high threshold will now berecruited to the reestablish the correctnumber of guards, causing a turnover inguarding bees. Thus a complex system ofseemingly intelligent division of labor canemerge through variable and dynamicresponse thresholds of individual work-ers.

  • 2.6. Coordination by hierarchicalcontrol structures

    Higher organisms are characterized bythe ability to release hierarchically con-trolled global signals which regulate cellactivity. For example, hormones can bereleased that elicit specific reactions incertain organs. Neuronal control is an evenstronger example of hierarchical decisions.Clearly global signals cannot sufficientlyorganize the full complexity of the colony.In fact they only modify the existing pat-terns created by self-organization and localdecisions. Compared to the pronouncedcentral control in many higher organisms,central control is rather weakly developedin honeybee societies. We find no rapidelectrical communication pathways in hon-eybee colonies, but several ways of chem-ical communication have evolved whichare of prime significance for regulatingcolonial life [for a review see Free (1987)].The best example of such hierarchical sig-nals in honeybees is the queens mandibu-lar gland pheromone which signals to thecolony members the presence of the queenand releases a variety of specific reactionsin the workers (Winston et al., 1989, 1990,1991; Kaatz et al., 1992a,b; Engels et al.,1993). Indeed one is tempted to see thisas a superb evolutionary step towardscoordinated colonial life.

    Pheromones are most often used inhoneybee communication for essentialmessages which require swift global reac-tions. A typical example for such areleaser pheromone is the alarm com-munication in workers. Pheromone releaseelicits swift recruitment of a large num-ber of workers, and lowers their behav-ioral threshold for defensive stingingflights (Maschwitz, 1964a,b). Severalother pheromones are currently known inhoneybee communication (Moritz andSouthwick, 1992) yet clearly in light ofthe highly complex interactions the num-ber of identified pheromones seems com-

    paratively small. Though honeybees haveevolved a number of communication sig-nals to control their society, these may beless important than initially thought, andrestricted to the modification of local deci-sions of workers.

    2.7. Differentiation and specializationby division of labor

    It is a common feature of higher organ-isms, that their cells differentiate into var-ious types, serving different purposes. It isthe amazing versatility of the cells basicstructures, that allows for the complexityof the organismic world. In contrast, thelack of apparent differences between theworkers composing the complexity of hon-eybee colonies is rather surprising. If welook at ant societies we find a huge phe-notypic plasticity with a great variability ofdifferent castes. Soldiers, foragers, majors,minors: castes in ants can cause individu-als to vary orders of a magnitude (Wilsonand Hlldobler, 1990). The presence ofmany discrete classes in the complex sys-tems enhances the ease of pattern forma-tion and prevents chaotic system reactions.Page and Mitchell (1991) argue thatthreshold diversity stabilizes the colonyby avoiding complexity catastrophes. Sowhat about honeybees?

    Worker bees are all very similar andphenotypic variability dividing the work-ers into specific castes seems absent. Per-haps constraints due to the flight abilityprevent the evolution of extreme pheno-typic caste differences such as thoseobserved in ants. While distinct workercastes are lacking, interindividual behav-ioral threshold variability can neverthe-less be very pronounced as we discussedabove. Two principal mechanisms for taskspecialization are known. First, division oflabor is controlled through the well-known temporal polyethism (Rsch,1927; Lindauer, 1952; Seeley, 1982),

  • which provides an extremely flexible sys-tem of worker allocation (Rsch, 1930).More recently, however, it has beenrepeatedly shown that task division is alsosubject to genetic variability within agecohorts (Moritz and Hillesheim, 1989;Page and Robinson, 1991; Robinson andPage, 1988). Specialists for certain tasksare expected to have a specifically lowthreshold for this specific task (Robinsonand Page, 1989), and members of specificsubfamilies in the colony proved to showpreferences for specific tasks. This is mostextreme in the Cape honeybee A. m.capensis where almost all of the layingworkers in a colony originate from a sin-gle subfamily (Moritz et al., 1996). Geno-typic variability is thus clearly a factorcontributing to intracolonial responsethreshold variability.

    If pattern formation is critical for thefunctioning of the complex colony, thenevolution should favor mechanisms thatfacilitate self-organization. Genotypic vari-ability would be a possible way to achievethis goal. In honeybees threshold vari-ability is not achieved through a wide arrayof phenotypic castes (as in ants) but ratherthrough temporal polyethism, in combi-nation with genotypic diversification. Asmany as 35 effective matings have beenfound in colonies of A. dorsata (Moritz etal., 1995; Oldroyd et al., 1996) which iscurrently the most extreme report ofpolyandry in social insects. It is a basicdifference between the honeybee super-organism and a multicellular organism,that its components are genetically differ-ent. But perhaps, it is exactly this crucialdifference which has opened the possibil-ity to exploit advantages through intra-superorganismic genetic diversity; anadvantage which cannot be used by mul-ticellular organisms.

    Comparatively little attention has beengiven to this aspect, and the significanceof polyandry impact may have beenunderrated. The role of intracolonial

    genetic diversity and patriline composi-tion on colony performance is far fromclear. Page et al. (1989) developed a deter-ministic two-locus model for increasedcolonial fitness through genetic specialistworkers. There is sufficient evidence thatnonlinear worker interactions occur in avariety of social behaviors includinghygienic behavior (Trump et al., 1967),hoarding behavior (Moritz andHillesheim, 1989), and the alarm response(Moritz and Southwick, 1987; Guzmn-Novoa and Page, 1994). In some studiesintracolonial genotypic variability waspositively correlated with performance(Kolmes et al., 1989; Oldroyd et al., 1992;Fuchs and Schade, 1994), but in othersthis was not the case. Page et al. (1995)found mostly intermediate phenotypes ingenotypically mixed colonies, but alsoobserved that genotypically variablecolonies displayed more average pheno-types thus behaving less chaotically andmore homeostatically. In a recent studyon a large number of colonies with natu-rally mated queens, Neumann and Moritz(1996) estimated only 10 % of honey pro-duction to be determined through the mat-ing frequency of the queen. This weakcontribution was not significantly differ-ent from zero. In addition, effects of geno-typic variability on group efficiency werenot necessarily always positive. Moritzand Hillesheim (1989) found thatincreased genotypic variability in exper-imental groups reduced the ability ofhoarding behavior. Fuchs et al. (1996)reported a decreased ability of anti-para-site behavior in colonies of increasedworker variability. Obviously althougheffects at the colonial level can take manydifferent forms, they have one thing incommon: they are difficult to detect. Thisempirical deficiency, however, certainlydoes not rule out their possible impactduring long-term evolution.

  • 2.8. Evolution of polyandry

    Colony advantages of genotypic diver-sity might even provide a possible expla-nation of their main cause, which is thepolyandry of the honeybee queen. We

    modeled how extreme polyandry canevolve on the basis genotypic task spe-cialization (Fuchs and Moritz, unpublisheddata; figure 1). Because alleles coding forspecialists are rare by definition, the queenneeds to mate with many males to make

  • sure she samples at least one male whichcarries the desired rare specialist allele.At the same time she needs to mate withmany males to keep the specialist alleleat a low intracolonial frequency. A highspecialist allele frequency in the colonywith too many specialist workers may bedetrimental. The argument is thus basedon the idea that both a complete lack ofspecialists and too many specialists havea negative effect on colony fitness. Wethus have a case of intracolonial fre-quency-dependent selection similar to thatmodeled by Moritz (1989). In fact fromthe numerous hypotheses for the evolu-tion of polyandry [for a recent review seeBoomsma and Ratnieks (1996)] thegenetic specialist model is currently theonly genetic model which can plausiblypredict the extremely high mating fre-quencies found in honeybees.

    3. CONCLUSIONS

    The social organization of the honeybeecolony takes a next step in evolution, inorganizing thousands of individuals into atightly integrated superorganism. This canbe compared to multicellular organismsin many aspects. Some comparisons aresuperficial, as composition of dependentsubunits, the allocation of sexual func-tions to a minority, or a degree of localstructuring. However, we argue thatcolonies can be envisaged as vehicles forgenes similar to individuals, provided thatsufficient genetic homogeneity is main-tained through the genetic bottlenecks ofreproduction. It makes sense to talk aboutorganisms to indicate that individual cellsare an integral part of a higher organiza-tional level. Selection within or betweencells steps far back behind selection at theorganismal level. Obviously the honey-bees have reached the next level of com-plexity, where the individuals are integralparts of the colony, and selection primar-ily operates on the colonial level. While

    this does not exclude intracolonial selec-tion processes, and these are in fact wellknown (Moritz et al., 1996), it does how-ever mean that selection at the coloniallevel is epistatic over intracolonial selec-tion processes. If the colony dies, it doesnot make any difference which individualhad won the intracolonial competition forreproduction and had pursued the mostsuccessful tactics. The best example thatcolony fitness sets the scene for selectionmay come from applied bee breeding.Beekeepers design the breeding schemesby selecting queens from the best colonies.If they had a means to determine the bestqueens without testing the colony, theywould certainly take advantage. Alas, nei-ther beekeepers nor nature can select theproperties of a colony from the phenotypeof a newly mated queen.

    Organisms and superorganisms areorganized by similar principles. Severaldifferent mechanisms interact, and thecomplex picture is governed through clearsignal chains on the one hand and self-organized patterns on the other. The signalchains are relatively easy to identifybecause we can identify chemical com-pounds that release a certain behavior. It isthen possible to argue that the activepheromonal compounds resulted fromadaptive selection at the individual orcolony level. Much more intricate is thesearch for adaptive processes in self-orga-nized behavioral patterns. The patternsemerge as a result of the interactions ofthe bees in the social group. The colonialphenotype is determined by the numbersof workers involved in a task, and bythreshold values and variability, leavingthe individual worker and its quality ratherinsignificant. Returning to the analogybetween organism and superorganism, ina vertebrate brain it is not so much thequality of individual neurons rather thanthe sheer number of neurons which makesit work.

  • ACKNOWLEDGEMENTS

    We are grateful to R.E. Page for stimulatingdiscussions, which helped to clarify many ofthe aspects addressed in this paper.

    Rsum - Lorganisation des coloniesdabeilles mellifres. Caractristiqueset consquences du concept de super-organisme. Les colonies dabeilles viventen socits trs denses o chaque individuest fortement intgr sur le plan compor-temental et dpendant pour sa survie et sareproduction. Ces socits ont souvent tdsignes par le terme de superorganismepar analogie avec les organismes sup-rieurs, complexes et multicellulaires. Desanalogies de structure, telles que la consti-tution partir de sous-units, la repro-duction limite quelques-unes de cessous-units et la sous-organisation localesont dordre purement phnomnologiqueet peuvent tre trompeuses. Beaucoup plussignificatives sont en revanche les analo-gies des mcanismes dvolution. Au seindu concept de lactivit gnique commerelation logique entre un gne et un effetexterne et de lindividu comme unit deslection, lvolution des superorganismessinscrit sans contradiction dans la thoriesynthtique de lvolution. De fait il existedes parallles qui aident approfondir lacomprhension de la coopration entre lescellules dun organisme. La comparaisondes principes organisationnels met en vi-dence des analogies mais aussi des diff-rences. De vastes processus dauto-orga-nisation et de raction aux conditionslocales jouent un rle important dans lacoordination de lactivit des sous-unitschez les organismes et les superorga-nismes. Au niveau suivant les boucles dertroaction et laction combine non addi-tive des composants ont de limportance.Les fonctions hirarchiques de rgulationdans le domaine des phromones ressem-blent celles des hormones chez les orga-nismes suprieurs, bien quil manque une

    structure centrale hautement dveloppede rgulation telle que le systme nerveuxchez les animaux suprieurs. La diffren-ciation et la division du travail jouent unrle important. Les cellules dun orga-nisme se diffrencient trs largement endes types morphologiques varis, mais telnest pas le cas chez la plupart des insectessociaux. la place, existe la plupart dutemps un systme de division temporairedu travail. En effet il existe chez lesinsectes sociaux la possibilit dune dif-frenciation gntique des ouvrires, dontles consquences et le potentiel de dve-loppement ne sont compris que dans leursrudiments et sont peut-tre sous-valus ;chez les colonies dabeilles en particulier,o il y a accouplement multiple de la reine,cet aspect pourrait revtir un rle impor-tant. Les recherches portant sur les cons-quences de la variabilit gntique plusou moins forte des ouvrires ou des fra-tries qui cooprent de faon spcifiquenon additive ont donn jusqu prsentune image contradictoire ; il existe nan-moins des donnes qui indiquent que ceseffets ont un certain impact. Lune desconsquences thoriques pourrait tre quela variabilit gntique soutient les pro-cessus dauto-organisation et dmergencedune structure. Une autre consquenceest que laccouplement multiple de la reineavec un grand nombre de mles drivesans aucun doute de la possibilit dexploi-ter les avantages dun nombre rduit despcialistes gntiques. Les coloniesdabeilles prsentent donc de fortes simi-litudes avec les organismes suprieurs, cequi justifie la notion de superorganismeet de progression vers la complexit sup-rieure. Tandis que les principes de struc-ture, dvolution et dorganisation concor-dent trs largement, il rsulte de ladiversit gntique des composants despossibilits dvolution ; de plus amplesrecherches sont ncessaires pour prciserdans quelle mesure et de quelle faon ellessont utilises par les colonies dabeilles. Inra/DIB/AGIB/Elsevier, Paris

  • Apis mellifera / organisation sociale /superorganisme / division travail / auto-organisation / polyandrie

    Zusammenfassung - Organisation vonBienenvlkern: Charakteristiken undKonsequenzen eines Superorganis-muskonzeptes. Bienenvlker leben in sehrdichten und in sich weitgehend abge-schlossenen Sozietten, auf die die ein-zelnen Tiere fr berleben und Repro-duktion angewiesen sind. Diese Soziettensind in Analogie zu den aus Zellen zusam-mengesetzten komplexen hheren Orga-nismen wiederholt als Superorganismenbezeichnet worden. Strukturelle Analo-gien wie die Zusammensetzung aus Unter-einheiten, die Begrenzung der Reproduk-tion auf wenige dieser Untereinheiten undlokale Untergliederung sind rein phno-menologisch und mglicherweise irre-fhrend. Wesentlich tragfhiger sinddagegen Analogien der Evolutionsme-chanismen. Innerhalb des Konzeptes derGenaktion als logischer Verbindung zwi-schen Gen und Effekt in der Auenwelt,und der damit entfallenden Fixierung aufdas Individuum als Selektionseinheit ord-net sich die Evolution von Superorganis-men widerspruchsfrei in die synthetischeEvolutionstheorie ein. Tatschlich erge-ben sich Parallelen, die ihrerseits das Ver-stndnis der Zusammenarbeit zwischenden Zellen eines Organismus vertiefenhelfen. Der Vergleich organisierenderPrinzipien zeigt Analogien auf, aber auchDifferenzen. In der Koordination der Akti-vitt der Untereinheiten spielen bei Orga-nismen und Superorganismen weitgehendeProzesse von Selbstorganisation und vonReaktionen auf lokale Bedingungen einetragende Rolle. Auf der nchsten Ebenesind Rckkoppelungsschleifen und nicht-additives Zusammenwirken der Kompo-nenten von Bedeutung. HierarchischeSteuerungsfunktionen auf der Ebene vonPheromonen hneln der durch Hormone

    bei hheren Organismen, allerdings fehlteine hochentwickelte zentrale Steue-rungsstruktur, wie sie das Nervensystemhherer Tiere darstellt. Eine wichtige Rollespielt die Differenzierung und Arbeitstei-lung. Whrend die Zellen eines Organis-mus sich sehr weitgehend in morpholo-gisch unterschiedliche Typendifferenzieren, ist dies bei den meistensozialen Insekten nicht der Fall. Stattdes-sen besteht zumeist ein System tempor-rer Arbeitsteilung. Allerdings besteht beiInsektenstaaten die Mglichkeit einergenetischen Differenzierung der Arbeite-rinnen, deren Konsequenzen und Ent-wicklungspotentiale erst in den Anfngenverstanden sind und mglicherweise unter-schtzt werden. Insbesondere bei Bienen-vlkern mit einer Vielfachverpaarung derBienenkniginnen knnte diesem Aspekteine wichtige Rolle zukommen. Die bis-herigen Untersuchungen zu Auswirkun-gen hherer oder geringerer genetischerVariabilitt der Arbeiterinnen in den Bie-nenvlkern, oder spezifischer nicht-addi-tiv zusammenwirkender, von jeweilseinem Drohn abstammender Subfamilienergaben bislang ein widersprchlichesBild. Es zeichnet sich aber ab, da sichdiese Effekte auswirken. Eine mglicheFolge knnte sein, da genetische Varia-bilitt die Prozesse der Selbstorganisationund Musterbildung untersttzt. Eine wei-tere Folge ist, da die Mehrfachverpaa-rung der Bienenknigin mit sehr hohenDrohnenzahlen sich zwanglos aus derMglichkeit zur Nutzung von Vorteilenaus geringen Anzahlen genetischer Spe-zialisten ableiten lt. Bienenvlker wei-sen damit erhebliche hnlichkeiten mithheren Organismen auf, die eineBezeichnung als Superorganismus unddamit als weiterer Schritt zu hherer Kom-plexitt rechtfertigen. Whrend struktu-relle, evolutionre und organisatorischePrinzipien sehr weitgehend bereinstim-men, erwachsen aus der genetischenUnterschiedlichkeit der Komponentenzustzliche Entwicklungsmglichkeiten,

  • deren Ausschpfung bei Bienenvlkernweiterer Untersuchungen bedarf. Inra/DIB/AGIB/Elsevier, Paris

    Soziale Organisation / Superorganis-mus / Arbeitsteilung / Selbstorganisa-tion / Polyandrie / Apis mellifera

    REFERENCES

    Bonner JT (1995) Life Cycles: Reflections of an Evo-lutionary Biologist. Princeton Univ Press, NewJersey

    Boomsma JJ, Ratnieks FLW (1996) Paternity insocial Hymenoptera. Phil Trans R Soc Lond B351, 941-957

    Buss LW (1987) The Evolution of Individuality.Princeton Univ Press, New Jersey

    Camazine S (1991) Self-organizing pattern formationin the combs of honey bee colonies. Behav EcolSociobiol 28, 61-76

    Camazine C, Sneyd J (1991) A model of collectivenectar source selection by honey bees: Self-orga-nization through simple rules. J Theor Biol 149,547-571

    Camazine S, Sneyd J, Jenkins MJ, Murray JD (1990)A mathematical model of self-organized patternformation on the combs of honeybee colonies. JTheor Biol 147, 553-571

    Collins AM, Rinderer TE, Tucker KW, SylvesterHA, Lackett JJ (1980) A model of honey beedefensive behavior. J Apic Res 19, 224-231

    Dawkins R (1976) The Selfish Gene. Oxford UnivPress, Oxford, UK

    Dawkins R (1982) The Extended Phenotype. OxfordUniv Press, Oxford, UK

    Engels W, Adler A, Rosenkranz P, Lbke G, FrankeW (1993) Dose-dependent inhibition of emer-gency queen rearing by synthetic )-ODA in thehoney bee, Apis mellifera carnica. J Comp Phys-iol B 163, 363-366

    Free JB (1987) Pheromones of Social Bees. CornellUniv Press,Ithaca, NY

    Frisch K von (1967) Tanzsprache und Orientierungder Bienen. Springer, Berlin

    Fuchs S, Schade V (1994) Lower performance inhoney bee colonies of uniform paternity. Api-dologie 25, 155-168

    Fuchs S, Bchler R, Hoffmann S, Bienefeld K (1996)Non-additive effects on Honey bee (Apis mellif-era) colony performance by artificial insemina-tion of queens with mixed semen from dronesof several bee lines (Apidae: Hymeneoptera).Proceedings of the XX International Congressof Entomology, Firence, Italy

    Guzmn-Novoa E, Page RE Jr (1994) Genetic dom-inance and worker interactions affect honeybeecolony defense. Behav Ecol 5, 91-97

    Hamilton WD (1964a) The genetical theory of socialbehavior I. J Theor Biol 7, 1-16

    Hamilton WD (1964b) The genetical theory of socialbehavior II. J Theor Biol 7, 17-52

    Hunt GJ, Page RE, Fondrk MK, Dullum CJ (1995)major qantitative trait loci affecting honeybeeforaging behavior. Genetics 141, 1537-1545

    Kaatz HH, Engels W , Fischer LC Hildebrandt H(1992a) Pheromonal Control of Oogenesis inWorker Honey Bees (Benettova B, Belbic I, Sol-dan T, eds), Czech Acad Sci

    Kaatz HH, Hildebrandt H, Engels W (1992b) Primereffect of queen pheromone on juvenile hormonebiosynthesis in adult worker honey bees. J CompPhysiol B 162, 588-592

    Kauffmann SA (1993) The Origins of Order: Self-organization and Selection in Evolution. OxfordUniv Press, Oxford, UK

    Koeniger N (1970) Factors determining the laying ofdrone and worker eggs by the queen honeybee.Bee World 51, 166-169

    Kolmes SA, Winston ML, Fergusson LA (1989) Thedivision of labour among worker honey bees(Hymenoptera: Apidae): The effects of multiplepatrilines. J Kans Entomol Soc 62, 80-95

    Lindauer M ( 1952) Ein Beitrag zur Frage der Arbeits-teilung im Bienenstaat, Z Vgl Physiol 34,299-345

    Lindauer M (1954)Temperaturregulierung undWasserhaushalt im Bienenstaat. Z Vgl Physiol36, 391-432

    Maschwitz UW (1964a) Alarm substances and alarmbehavior in social Hymenoptera. Nature (Lond)204, 324-327

    Maschwitz UW (1964b) Gefahrenalarmstoffe undGefahrenalarmierung by sozialen Hymenopteren.Z Vgl Physiol 47, 596-655

    Maynard Smith J (1964) Group selection and kinselection. A rejoinder. Nature 201, 1145-1147

    Moritz RFA (1989) Colony level and within colonylevel selection in honeybees: A two allele popu-lation model for Apis mellifera capensis. BehavEcol Sociobiol 25, 437-444

    Moritz RFA, Hillesheim E (1989) Genotypic intra-group variance and hoarding behavior in Hon-eybees (Apis mellifera L.). Apidologie 20,383-390

    Moritz RFA, Southwick EE (1987) Phenotype inter-actions in group behavior of honey bee workers(Apis mellifera L.). Behav Ecol Sociobiol 21,53-57

    Moritz RFA, Southwick EE (1992) In: Bees asSuperorganisms. An Evolutionary Reality (FineA, Forbes M, Wessels L, eds), Philosophy of Sci-

  • ence Association, East Lansing, Michigan, PSA1990 vol 2, 289-298

    Moritz RFA, Kryger P (1994) Self-organization ofcicadian rhythms in groups of honeybees (Apismellifera L). Behav Ecol Sociobiol 34, 211-215

    Moritz RFA, Kryger P, Koeniger G, Koeniger,Estoup A, Tingek S (1995) High degree ofpolyandry in Apis dorsata queens detected byDNA microsatellite variability. Behav Ecol Socio-biol 37, 357-363

    Moritz RFA, Kryger P, Allsopp M (1996) Compe-tition for royalty in bees. Nature 384, 31

    Neumann P, Moritz RFA (1996) Comparing per-formance data of honey bee colonies with matingfrequencies of honeybee queens (Apis mellifera)using single locus DNA fingerprinting. Api-dologie 27, 300-301

    Oldroyd BP, Rinderer TE, Harbo JR, Buco SM(1992) Effects of intracolonial genetic diversityon honey bee (Hymenoptera: Apidae) colonyperformance. Ann Entomol Soc Am 85, 335-343

    Oldroyd BP, Smolenski AJ, Cornuet JM, Wongsiri S,Estoup A, Rinderer TE, Crozier RH (1996) Lev-els of polyandry and intracolonial genetic rela-tionships in Apis dorsata (Hymenoptera: Api-dae). Ann Entomol Soc Am 89, 276-283

    Page RE Jr, Mitchell S (1991) In: Self Organizationand Adaption in Insect Societies (Fine A, ForbesM, Wessels L, eds), Philosophy of Science Asso-ciation, East Lansing, Michigan, PSA 1990 vol 2,289-298

    Page RE Jr, Mitchell S (1998) Self organization andthe evolution of division of labor. Apidologie 29,171-190

    Page RE, Robinson GE (1991) The genetics of divi-sion of labour in the honey bee. Adv Insect Phys-iol 23, 117-169

    Page RE Jr, Robinson GE, Calderone NW, Rothen-buhler WC (1989) Genetic structure, division oflabor, and the evolution of insect societies. In:The Genetics of Social Evolution (Breed MD,Page RE, eds), Westview Press, Boulder, CO,15-29

    Page RE, Robinson GE, Fondrk MK, Nasr ME(1995) Effects of worker genotypic diversity onhoney bee colony development and behavior(Apis mellifera L.). Behav Ecol Sociobiol 36,387-396

    Prigogine I, Stengers I (1980) Dialog mit der Natur.Piper, Mnchen, Zrich

    Robinson GE, Page RE jr (1988) Genetic determi-nation of guarding and undertaking in honeybeecolonies. Nature (Lond) 333, 356-358

    Robinson GE, Page RE jr (1989) Genetic basis fordivision of labor in an insect society. In: TheGenetics of Social Evolution (Breed MD, PageRE, eds), Westview Press, Boulder, CO, 61-80

    Rsch GA (1927) Untersuchungen ber die Arbeit-steilung im Bienenstaat. I. Die Ttigkeiten imnormalen Bienenstaate und ihre Beziehungenzum Alter der Arbeitsbiene, Z Vgl Physiol 6,268-298

    Rsch GA (1930) Untersuchungen ber die Arbeits-teilung im Bienenstaat. I. Die Ttigkeiten derArbeitsbienen unter experimentell verndertenBedingungen. Z Vgl Physiol 6, 268-298

    Ruttner F (1988) Biogeography and Taxonomy ofHoneybees. Springer, Berlin

    Seeley TD (1982) Adaptive significance of the agepolyethism schedule in honeybee colonies. BehavEcol Sociobiol 11, 287-293

    Seeley TD (1986) Social foraging in honey bees:How colonies allocate foragers between patchesof flowers. Behav Ecol Sociobiol 19, 343-354

    Seeley TD (1989) The honey bee colony as a super-organism. Am Scientist 77, 546-553

    Seeley TD (1995) The Wisdom of the Hive. HarvardUniv Press, Cambridge, MA

    Smith DR (1991) Diversity in the Genus Apis. West-view Press, Boulder, CO

    Southwick EE (1988) Thermoregulation in honeybeecolonies. In: Africanized Honey Bees and BeeMites (Needham G, page RE, Delfinado-BakerM, Bowman CE, eds), Wiley, New York,223-236

    Stort AC (1974) Genetic study of the aggressive-ness of two subspecies of Apis mellifera in Brazil.1. Some tests to measure aggressiveness. J ApicRes 13, 32-38

    Trump RF, Thompson VC, Rothenbuhler WC (1967)Behavior genetics of nest cleaning in honeybeesV. Effect of previous experience and compositionof mixed colonies in response to disease-killedbrood. J Apic Res 6, 127-131

    Visscher PK (1998) Colony integration and repro-ductive conflict in honey bees. Apidologie 29,23-45

    Watmough J, Camazine S (1995) Self-organizedthermoregulation of honey bee clusters. J TheorBiol 176, 391-402

    Wheeler WM (1928) The Social Insects: Their Ori-gin and Evolution. Kegan, Paul, Trench, Trubner& Co, London

    Williams GC (1966) Adaption and Natural Selec-tion. Princeton Univ Press, New Jersey

    Wilson DS (1975) A theory of group selection. ProcNatl Acad Sci USA 72, 143-146

    Wilson DS (1977) Structured demes and the evolu-tion of group-advantageous traits. Am Nat 111,157-185

    Wilson DS, Sober E (1989) Reviving the superor-ganism. J Theor Biol 136, 337-356

    Wilson EO (1975) Sociobiology: The New Synthesis.Harvard Univ Press, Cambridge, MA

  • Wilson EO, Hlldobler B (1990) The Ants. Springer,Berlin

    Winston ML, Slessor KN, Smirle MJ, Kandil AA(1989) The influence of a queen-produced sub-stance, 9HDA, on swarm clustering behavior inthe honey bee Apis mellifera L. J Chem Ecol 8,1283-1288

    Winston ML, Higo H, Slessor KN (1990) The effectof various dosages of queen mandibularpheromone on the inhibition of queen rearing in

    the honey bee (Hymenoptera: Apidae). Ann Ento-mol Soc Am 83, 234-238

    Winston ML, Higo H, Colley SJ, Pankiw T, SlessorKN (1991) The role of queen mandibularpheromone and colony congestion in honey bee(Apis mellifera L) reproductive swarming. JInsect Behav 4, 649-660

    Wynne-Edwards VC (1962) Animal Dispersion inRelation to Social Behaviour. Oliver Boyd, Edin-burgh