The role of the queen mandibular gland pheromone in honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis>): honest signal or suppressive agent?

Queen pheromones interfere with worker reproduction in social insects. However, there is still an unresolved question as to whether this pheromone acts as an “honest” signal for workers, giving a reliable indication of the queen’s reproductive value, or as a suppressive agent, inhibiting worker reproduction independent of the queen’s reproductive capacity. In honeybees (Apis mellifera), the queen’s mandibular gland secretion, a mix of fatty acids and some aromatic compounds, is crucial for regulating the reproductive division of labor in the colony inhibiting ovary development in workers. We quantified the mandibular gland secretions of virgin, drone-laying, and naturally mated queens using gas chromatography to test whether the queens’ mating, ovary activation, or the reproductive value for workers correlated with the composition of the secretion. Although the absolute amounts of the “queen substance” 9-oxo-2(E)-decenoic acid (9-ODA) were similar among the three groups, the proportions of 9-ODA decreased with increasing reproductive quality. Furthermore, the ratios of queen to worker compounds were similar in all three treatment groups, irrespective of the reproductive capacity. A multivariate analysis including all six compounds could not separate drone-laying queens from naturally mated ones, both with active ovaries but only the latter ensuring colony survival. We suggest that the mandibular gland pheromones are unlikely to function as reliable indicators of queen reproductive value and rather operate as an agent to suppress worker reproduction. This does not exclude the possibility that other “honest” pheromone signals exist in the honeybee colony, but these would have to arise from other semiochemicals, which could be produced by both the queen and the brood.     

Retinue attraction and ovary activation: responses of wild type and anarchistic honey bees (Apis mellifera) to queen and brood pheromones

In most social insect colonies, workers do not attempt to lay eggs in the presence of a queen. However, in the honey bee (Apis mellifera), a rare phenotype occurs in which workers activate their ovaries and lay large numbers of male eggs despite the presence of a fecund queen. We examined the proximate mechanisms by which this ‘anarchistic’ behaviour is expressed. We tested the effects of brood and queen pheromones on retinue attraction and worker ovary activation using caged worker bees. We found no difference between the anarchistic and wild type queen pheromones in the retinue response elicited in either wild type or anarchistic workers. Further, we found that anarchistic queens produce a pheromone blend that is as effective at inhibiting ovary activation as the wild type queen pheromone. However, anarchistic workers are less inhibited by queen pheromones than their wild type counterparts, in a dose-dependent manner. These results show that the anarchistic phenomenon is not due to changes in the production of queen pheromones, but rather is due in part to a shift in the worker response to these queen-produced signals. In addition, we demonstrate the dose-dependent nature of the effect of queen pheromones on honey bee worker ovary activation.     

Reproductive plasticity in bumblebee workers (<Emphasis Type="Italic">Bombus terrestris</Emphasis>)—reversion from fertility to sterility under queen influence

Worker sterility in the bumblebee Bombus terrestris is conditional and is linked to the social development of the colony. Workers refrain from reproducing or overtly challenging the queen until gyne production has initiated, at the so-called competition point (CP). It is not known whether this behavior is hard-wired or workers show reproductive plasticity. It also remains unclear whether worker reproductive decision is under queen and/or worker control. In this study, we tested worker reproductive plasticity in an attempt to assess whether and under which conditions worker sterility/fertility are reversible. We introduced egg-laying workers into colonies with different social structures for 1 week then monitored their reproductive status. We revealed a remarkable reproductive plasticity in the introduced workers that was social-condition-dependent. In the presence of a pre-CP queen, the introduced workers reverted to sterility, whereas in the presence of a post-CP queen, such workers remained egg-layer. Reversion to sterility does not occur when direct contact with the queen is prevented, as the introduced workers remained egg-layer in the queenright colonies with a confined queen. Egg-laying workers that were introduced into queenless colonies mostly maintained their fertility regardless of colony social phase. This shows that worker transition from cooperative to selfish behavior is reversible depending on the social context.     

Queen and young larval pheromones impact nursing and reproductive physiology of honey bee (Apis mellifera) workers

Several insect pheromones are multifunctional and have both releaser and primer effects. In honey bees (Apis mellifera), the queen mandibular pheromone (QMP) and e-beta-ocimene (eβ), emitted by young worker larvae, have such dual effects. There is increasing evidence that these multifunctional pheromones profoundly shape honey bee colony dynamics by influencing cooperative brood care, a fundamental aspect of eusocial insect behavior. Both QMP and eβ have been shown to affect worker physiology and behavior, but it has not yet been determined if these two key pheromones have interactive effects on hypopharyngeal gland (HPG) development, actively used in caring of larvae, and ovary activation, a component of worker reproductive physiology. Experimental results demonstrate that both QMP and eβ significantly suppress ovary activation compared to controls but that the larval pheromone is more effective than QMP. The underlying reproductive anatomy (total ovarioles) of workers influenced HPG development and ovary activation, so that worker bees with more ovarioles were less responsive to suppression of ovary activation by QMP. These bees were more likely to develop their HPG and have activated ovaries in the presence of eβ, providing additional links between nursing and reproductive physiology in support of the reproductive ground plan hypothesis.     

Social regulation of ovary activation in ’anarchistic’ honey-bees (Apis mellifera)

Honey-bee (Apis mellifera) colonies exhibit extreme reproductive division of labour. Workers almost always have inactive ovaries and the queen monopolises egg laying. Although extremely rare, ’anarchistic’ colonies exist in which workers produce male offspring despite the presence of the queen. By comparing the rates of ovary activation in anarchistic and wild-type bees fostered to host colonies of different genotype (i.e. anarchist and non-anarchist) and queen status (i.e. queenless and queenright), we investigated the factors involved in inhibiting ovary activation. Fostered anarchist workers always had a higher level of ovary development than fostered wild-type bees in both anarchist and non-anarchist host colonies. Fostered workers of both genotypes had more active ovaries in anarchistic than in wild-type hosts. Fostered workers of both strains also had more active ovaries in queenless than in queenright hosts. The results suggest that selection for worker reproduction in the anarchistic line has both reduced the effects of brood and queen pheromones on worker ovary inhibition and increased the likelihood that workers of the anarchistic line will develop ovaries compared to wild-type workers. Received: 14 June 2000 / Revised: 26 September 2000 / Accepted: 7 October 2000     

Social parasitism by honeybee workers (Apis mellifera capensis Esch.): evidence for pheromonal resistance to host queen’s signals

Social parasites exploit their host’s communication system to usurp resources and reproduce. In the honeybee, Apis mellifera, worker reproduction is regulated by pheromones produced by the queen and the brood. Workers usually reproduce when the queen is removed and young brood is absent. However, Cape honeybee workers, Apis mellifera capensis, are facultative intraspecific social parasites and can take over reproduction from the host queen. Investigating the manner in which parasitic workers compete with host queens pheromonally can help us to understand how such parasitism can evolve and how reproductive division of labour is regulated. In A. m. capensis, worker reproduction is associated with the production of queen-like pheromones. Using pheromonal contest experiments, we show that Apis mellifera scutellata queens do not prevent the production of queen-like mandibular gland compounds by the parasites. Given the importance of these pheromones in acquiring reproductive status, our data suggest that the single invasive lineage of parasitic workers occurring in the range of A. m. scutellata was selected for its superior ability to produce these signals despite the presence of a queen. Such resistance was indeed less frequent amongst other potentially parasitic lineages. Resistance to reproductive regulation by host queens is probably the key factor that facilitates the evolution of social parasitism by A. m. capensis workers. It constitutes a mechanism that allows workers to evade reproductive division of labour and to follow an alternative reproductive option by acquiring direct fitness in foreign colonies instead of inclusive fitness in their natal nests.     

Sneak in or repel your enemy: Dufour's gland repellent as a strategy for successful usurpation in the slave-maker Polyergus rufescens

Summary. The dulotic queen ant, Polyergus rufescens, must first penetrate a host colony and kill the resident queen in order to successfully founding a new colony. Successful usurpation by a newly mated queen predictably depends on a dual strategy. Although, it can sneak in by being “chemically insignificant” with respect to cuticular hydrocarbons, it may also need to deter prospective host-worker aggressors. Chemical analysis of Dufour's gland secretion of P. rufescens queens and workers by GS/MS revealed that queen secretion is typified by esters of butanoic acid and acetic acid, of which decyl butanoate comprises over 80%. Butanoates and acetates are also present in the workers' secretion, but these are of higher molecular weight, and octadecyl butanoate represents the major compound. Using synthetic mixtures of queen and worker Dufour's gland, we tested the hypothesis that these secretions modify the aggressive behavior of the host species Formica cunicularia>. The queen-like synthetic mixture significantly reduced aggression of the host workers towards alien conspecifics, but neither pentane nor the worker-like synthetic mixture showed this effect. Although Dufour's gland content of >Polyergus queens was suggested to function as an appeasement pheromone (Topoff et al. 1988; Mori et al. 2000), we hypothesized that it may in fact act as a repellent. In order to test this hypothesis we exposed starved F. cunicularia workers to a droplet of honey on a glass slide applied with one of the following compounds: decyl butanoate (queen major compound), octadecyl butanoate (worker main compound), limonene (a reported ant repellent), and pentane (solvent control). Of these, the workers were repelled only by the decyl butanoate and did not approach the honey. We conclude that during usurpation the queen actively repels aggressive workers by emitting Dufour's gland repellent, comprising the alternative tactic in the usurpation dual strategy. This represents another chemical weapon in the diverse arsenal used by parasites to overcome the host's resistance. Received 7 April 2000; accepted 17 May 2000     

Dufour's gland secretion of the queen honeybee (Apis mellifera): an egg discriminator pheromone or a queen signal?

The role of Dufour's gland secretion as an egg discriminator pheromone was reevaluated by simultaneously exposing workers to two combs, one containing queen- or worker-laid eggs and the second containing treated or untreated worker-laid eggs. Treatments included extracts of Dufour's gland secretion as well as the synthetic esters that were identified in the secretion. Policing was clearly detected both in queenright and queenless colonies by the swift removal of worker, but not of queen eggs. However, neither the glandular secretion nor its synthetic ester constituents were able to protect worker-born eggs from policing. Treated worker eggs were removed significantly faster than queen eggs, and at the same rate as non-treated worker eggs. These results are not consistent with the hypothesis that the secretion serves as an egg-marking pheromone. Chemical analyses of the queen abdominal tips revealed the presence of Dufour's esters, indicating that the glandular secretion oozes out and spreads over the cuticle around the genital chamber. However, contamination while ovipositing may also explain the minute amounts of these esters that were detected on the egg surface. Dufour's gland caste-specific composition suggests that in queens it may constitute a signal that plays a role in queen-worker interactions. Attraction bioassays revealed that the queen secretion, but not that of workers, is very attractive to workers. When applied either on a glass slide or on another worker, a retinue formed around the "surrogate queen". We conclude that Dufour's gland secretion constitutes part of a complex queen signal that is the basis for the social integrity of the honeybee colony.     

Regulation of worker reproduction in bumblebees (Bombus terrestris): workers eavesdrop on a queen signal

In the annual bumblebee Bombus terrestris, the onset of queen-worker conflict over male production is seasonally and socially constrained. Workers will do better if they start to reproduce (the so-called competition phase) only after ascertaining that larvae are committed to gyne development but before the season ends because they gain more by rearing sister-gynes than their own sons. Here, we tested two nonmutually exclusive hypotheses as to what triggers the onset of worker reproduction: Workers can directly monitor larval development and/or workers eavesdrop on the queen signal that directs gyne development. Exposing workers to gyne larvae through a double mesh did not advance the competition phase compared to control colonies. However, when workers, but not the queen, were allowed contact with gyne larvae, both the competition phase and gyne production were advanced. Thus, while larvae do not emit a volatile pheromone that discloses their developmental route, the physical contact of workers with such larvae triggers early competition phase. However, workers exclusively exposed to worker larvae (colonies prevented from producing gyne larvae) started to reproduce at the same time as control colonies. Replacing the resident queen with an older queen (from gyne-rearing colonies) advanced the competition phase, irrespective of worker age. The results are consistent with the hypothesis that workers eavesdrop on the queen pheromones. This is adaptive because it allows workers a broader time-window for reproduction and thus to gain fitness from rearing both sister-gynes and sons before the season ends without affecting colony development.     

Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size

Models based on the kin selection theory predict that in social hymenopterans, queens may favor a lower investment in the production of sexuals than workers. However, in perennial colonies, this conflict may be tuned down by colony-level selection because of the trade off between colony survival and reproductive allocation. In this study, we present a survey of sexual production in colonies of Aphaenogaster senilis, a common species of ant in the Iberian Peninsula. Similar to most species that reproduce by fission, males were found in large excess compared to gynes (172:1). Sexuals were more likely to be found in queenless than in queenright (QR) field colonies. However, we also found a few gynes and numerous males in very large QR colonies. We compared these data with those available in the literature for A. rudis, a congeneric species from North America that has independent colony founding. The sex ratio in this species was only five males for each female, and sexuals were mostly found in QR nests, irrespective of colony size. We confirmed queen inhibition of sexual production in A. senilis in laboratory experiments and provide evidence that this inhibition is mediated by a nonvolatile pheromone. To seek the potential source of such a queen pheromone, we analyzed the secretions of two conspicuous exocrine glands, the Dufour’s and postpharyngeal glands (DG and PPG, respectively) in both queens and workers. Both secretions were composed of hydrocarbons, but that of DG also contained small quantities of tetradecanal and hexadecanal. The hydrocarbon profile of the DG and PPG showed notable caste specificity suggesting a role in caste-related behavior. The PPG secretions also differed between colonies suggesting its role in colony-level recognition. We suggest that in A. senilis, there are two modes of colony fission: First, in very large colonies, gynes are produced, probably because of the dilution of the queen pheromone, and consequently one or more gynes leave the mother colony with workers and brood to found a new nest. This is beneficial at the colony level because it avoids the production of costly sexuals in small colonies. However, because the queen and workers have different optima for sexual production, we hypothesize that queens tend to overproduce the pheromone to delay their production. This in turn may drive workers to leave the mother colony during nest relocation and to produce sexuals once they are away from the queen’s influence, creating a second mode of colony fission.     

Production and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromone

Summary The social cohesiveness of eusocial insect colonies is maintained primarily through the utilization of pheromones. In this study we quantitatively elucidated the production, secretion, and transmission of 9-keto2(E)-decenoic acid (9-ODA), one of the components of the mandibular gland pheromone of the honey bee queen Apis mellifera; this is the only identified primer pheromone complex in the eusocial insects. Mated queens produce 12–400 g of 9-ODA/day, or between 10% and 170% the average amount found in the glands at any one time. Approximately 0.5 g of 9-ODA is maintained on the body surface of queens by an equilibrium between exudation, internalization, tracking on the comb, and removal by workers. Retinue bees, attending the queen, remove the greatest amount, although the role of the wax as both a sink and a medium for pheromone transfer has been previously underestimated. Only about 1 in 10 retinue workers pick up substantial quantities of pheromone while attending the queen and, within seconds, most of the acquired 9-ODA is found externally on the abdomen, or in the gut. These attendants, also called messenger bees, transfer 9-ODA to other workers, mostly through direct contacts, but also via the wax. A model evaluating the pathways and relative quantities of 9-ODA transferred throughout the nest is presented. As well as being important for a basic understanding of the system, the results have implications for the proper design and use of pheromones in bee management.Offprint requests to: K. Naumann     

Dufour’s gland pheromone as a reliable fertility signal among honeybee (Apis mellifera) workers

When a colony becomes queenless and without the possibility of requeening, honeybee workers initiate reproduction and lay male eggs about a week later. Assays in which two bees were confined in a small arena revealed that they establish a reproductive dominance hierarchy, i.e., one worker demonstrates greater ovarian development than her paired bee. Reproductive dominance is independent of relatedness, and can be established between full sisters, cousins, or random nestmates. A social environment, however, is obligatory, as singly housed bees fail to develop ovaries on the same time scale. Allowing varying degrees of social interactions between the paired bees revealed that olfaction of volatile bee compounds, as well as tactile communication, seem to provide the necessary social environment. Ovarian development was accompanied by the production of queen-like Dufours gland secretion in these workers. Especially notable was the increase in the queen-like esters. This increase was tightly linked to ovarian development and not necessarily to the dominance status of the bees in the pair. Thus, the occurrence of queen-like esters can serve as a reliable fertility signal. Advertising ovarian status may recruit helper workers with less developed ovaries (and which are less likely to successfully reproduce before colony breakdown) to assist their nestmates and thereby gain inclusive fitness. Revealing the role of Dufours gland secretion as a fertility signal adds another dimension to our understanding of how queen pheromones operate. The mandibular-gland secretion is a good predictor of dominance hierarchy, being correlated with false-queen characteristics but not fertility, whereas Dufours gland secretion is a good predictor of fertility but not dominance hierarchy.Communicated by R.F.A. Moritz     

A quantitative study of worker reproduction in honey bee colonies

Summary In 11 Apis mellifera colonies with laying queens, about 0.12% of the males produced derived from eggs laid by workers. This result requires explanation both of why workers produce any males, and, since they do, why they produce so few. Workers may maximize their inclusive fitness by forgoing reproduction, or their sterility may be due to to enforcement of the interests of the queen or those of other workers. The presence of laying workers might then result from developmental noise in the workers, from a failure of communication of the queen's presence, or a failure of enforcement mechanisms. Selection for worker reproduction in colonies following queen loss may also play a role in shaping worker reproduction in colonies with a queen. The hypothesis of worker sterility enforced by other workers seems most likely to be correct, but further studies on these hypotheses are needed.     

Ovariole number—a predictor of differential reproductive success among worker subfamilies in queenless honeybee (Apis mellifera L.) colonies

A honeybee queen normally mates with 10–20 drones, and reproductive conflicts may arise among a colony’s different worker patrilines, especially after a colony has lost its single queen and the workers commence egg laying. In this study, we employed microsatellite markers to study aspects of worker reproductive competition in two queenless Africanized honeybee colonies. First, we determined whether there was a bias among worker patrilines in their maternity of drones and, second, we asked whether this bias could be attributed to differences in the degree of ovary activation of workers. Third, we relate these behavioral and physiological factors to ontogenetic differences between workers with respect to ovariole number. Workers from each of three (colony A) and one (colony B) patrilineal genotypes represented less than 6% of the worker population, yet each produced at least 13% of the drones in a colony, and collectively they produced 73% of the drones. Workers representing these genotypes also had more developed follicles and a greater number of ovarioles per ovary. Across all workers, ovariole development and number were closely correlated. This suggests a strong effect of worker genotype on the development of the ovary already in the postembryonic stages and sets a precedent to adult fertility, so that “workers are not born equal”. We hypothesize a frequency-dependent or “rare patriline” advantage to queenless workers over the parentage of males and discuss the maintenance of genetic variance in the reproductive capacity of workers.Electronic supplementary material Supplementary material is available for this article at and is accessible for authorized users.     

Control of reproduction in social insect colonies: individual and collective relatedness preferences in the paper wasp, Polistes annularis

Social insect colonies often have one or a few queens. How these queens maintain their reproductive monopoly, when other colony members could gain by sharing in the reproduction, is not generally known. DNA microsatellite genotyping is used to determine reproductive interests of various classes of colony members in the paper wasp, Polistes annularis. The relatedness estimates show that the best outcome for most individuals is to be the reproductive egg-layer. For workers, this depends on the sex of offspring: they should prefer to lay their own male eggs, but are indifferent if the queen lays the female eggs. The next-best choice is usually to support the current queen. As a rule, subordinates and workers should prefer the current queen to reproduce over other candidates (though subordinates have no strong preference for the queen over other subordinates, and workers may prefer other workers as a source of male eggs). This result supports the theory that reproductive monopoly stems from the collective preferences of non-reproductives, who suppress each other in favor of the queen. However, we reject the general hypothesis of collective worker control in this species because its predictions about who should succeed after the death of the present queen are not upheld. The first successor is a subordinate foundress even though workers should generally prefer a worker successor. If all foundresses have died, an older worker succeeds as queen, in spite of a collective worker preference for a young worker. The results support the previous suggestion that age serves as a conventional cue serving to reduce conflict over queen succession. Received: 3 May 1996 / Accepted after revision: 22 September 1996     

Queen primer pheromone affects conspecific fire ant (<Emphasis Type="Italic">Solenopsis invicta</Emphasis>) aggression

Monogyne fire ant, Solenopsis invicta, colony workers are territorial and are aggressive toward members of other fire ant colonies. In contrast, polygyne colony workers are not aggressive toward non-nestmates, presumably due to broader exposure to heritable and environmentally derived nestmate recognition cues (broad template). Workers from both monogyne and polygyne fire ant colonies execute newly mated queens after mating flights. We discovered that monogyne and polygyne queens have a remarkable effect on conspecific recognition. After removal of their colony queen, monogyne worker aggression toward non-nestmate conspecifics quickly drops to merely investigative levels; however, heterospecific recognition/aggression remains high. Queenless monogyne or polygyne worker groups were also not aggressive toward newly mated queens. Queenless worker groups of both forms that adopted a monogyne-derived newly mated queen became aggressive toward non-nestmate workers and newly mated queens. We propose that the powerful effect of fire ant queens on conspecific nestmate recognition is caused by a queen-produced recognition primer pheromone that increases the sensitivity of workers to subtle quantitative differences in nestmate recognition cues. This primer pheromone prevents the adoption of newly mated queens (regulation of reproductive competition) in S. invicta and when absent allows queenless workers to adopt a new queen readily. This extraordinary discovery has broad implications regarding monogyne and polygyne colony and population dynamics.     

Complex chemical communication in the crazy ant <Emphasis Type="Italic">Paratrechina longicornis</Emphasis> Latreille (Hymenoptera: Formicidae)

Summary. The formicine ant Paratrechina longicornis is known for its extremely opportunistic foraging behaviour. Only a single trail pheromone source, the rectum, was previously described from this ant. Our detailed examination of this ant’s chemical communication system revealed the presence of at least four sources of pheromones. Rectum, poison sac, and Dufour gland contain orientation components with decreasing effectiveness and persistence (in the sequence mentioned) as well as attractants with increasing effectiveness. Furthermore, the mandibular gland contains repellents, and a releaser of defensive behaviour. This set of various signals of different strength and persistence allows an extraordinary degree of flexibility and efficiency in the collective behaviour of P. longicornis, especially food exploitation, and thus may contribute to this insect’s overall ecological success.     

Trail-following behaviour in two Aphaenogaster ants

In the course of our studies on the chemical ecology of the widely distributed Mediterranean ant Aphaenogaster senilis, we found that trail following is triggered by extracts of the poison gland and Dufour’s gland. To assess the specificity of the trail pheromone, we examined whether a cross-reaction exists between trails of A. senilis and the closely related species A. iberica. Specificity seemed to differ amongst these two species, because workers of A. senilis did not follow trails of A. iberica, whereas the latter followed trails made by both species. Chemical analyses of the glandular contents reveal that Dufour’s glands of both species contain mainly alkanes and alkenes exhibiting species-specific profiles. However, differences in the poison gland content of the two species were dramatic, with A. senilis showing high amounts of alkaloids that were completely absent in A. iberica.     

Co-occurrence of three types of egg policing in the Norwegian wasp <Emphasis Type="Italic">Dolichovespula norwegica</Emphasis>

In insect societies, workers often try to challenge the reproductive monopoly of the queen by laying their own eggs. Successful worker reproduction, however, is frequently prevented by queen policing or worker policing, whereby either the mother queen or non-reproductive workers selectively kill worker-laid eggs. Recently, a third mechanism—“selfish” worker policing—has also been described in which the workers selectively police worker-laid eggs but also lay eggs themselves. Here, we present results from the monogynous wasp Dolichovespula norwegica, which show that all three kinds of policing—queen policing, worker policing and “selfish” worker policing—co-occur. The net effect of these three kinds of policing collectively favoured the queen’s reproduction, as within 1 day 44% of the worker-laid eggs versus only 8% of the queen-laid eggs were eaten. Of the worker-laid eggs that were killed by workers, approximately two thirds were eaten by the reproductive workers even though these made up only a small proportion, 8%, of the work force. This means that policing workers obtained both direct fitness benefits as well as indirect (inclusive) fitness. In addition, we show that worker policing was carried out by a limited, specialised set of workers that was estimated to constitute approximately one quarter of the whole colony and of which 66% were non-reproductive.     

Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review

Honey-bees, Apis, are an important model system for investigating the evolution and maintenance of worker sterility. The queen is the main reproductive in a colony. Workers cannot mate, but they can lay unfertilized eggs, which develop into males if reared. Worker reproduction, while common in queenless colonies, is rare in queenright colonies, despite the fact that workers are more related to their own sons than to those of the queen. Evidence that worker sterility is enforced by 'worker policing' is reviewed and worker policing is shown to be widespread in Apis. We then discuss a rare behavioural syndrome, 'anarchy', in which substantial worker production of males occurs in queenright colonies. The level of worker reproduction in these anarchic colonies is far greater than in a normal queenright honey-bee colony. Anarchy is a counterstrategy against worker policing and an example of a 'cheating' strategy invading a cooperative system.