Levels of selection in a social insect: a review of conflict and cooperation during honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis>) queen replacement

The extended phenotype of a social insect colony enables selection to act at both the individual level (within-colony selection) and the colony level (between-colony selection). Whether a particular trait persists over time depends on the relative within- and between-colony selection pressures. Queen replacement in honey bee colonies exemplifies how selection may act at these different levels in opposing directions. Normally, a honey bee colony has only one queen, but a colony rears many new queens during the process of colony reproduction. The replacement of the mother queen has two distinct phases: queen rearing, where many queens develop and emerge from their cells, and queen elimination, where most queens die in a series of fatal duels. Which queens are reared to adulthood and which queens ultimately survive the elimination process depends on the strength and direction of selection at both the individual and colony levels. If within-colony selection is predominant, then conflict is expected to occur among nestmates over which queens are produced. If between-colony selection is predominant, then cooperation is expected among nestmates. We review the current evidence for conflict and cooperation during queen replacement in honey bees during both the queen rearing and queen elimination phases. In particular, we examine whether workers of different subfamilies exhibit conflict by acting nepotistically toward queens before and after they have emerged from their cells, and whether workers exhibit cooperation by collectively producing queens of high reproductive quality. We conclude that although workers may weakly compete through nepotism during queen rearing, workers largely cooperate to raise queens of similar reproductive potential so that any queen is suitable to inherit the nest. Thus it appears that potential conflict over queen replacement in honey bees has not translated into actual conflict, suggesting that between-colony selection predominates during these important events in a colonys life cycle.Communicated by A. Cockburn     

Queen fertility, egg marking and colony size in the ant Camponotus floridanus

In ant societies, workers do not usually reproduce but gain indirect fitness benefits from raising related offspring produced by the queen. One of the preconditions of this worker self-restraint is sufficient fertility of the queen. The queen is, therefore, expected to signal her fertility. In Camponotus floridanus, workers can recognize the presence of a highly fertile queen via her eggs, which are marked with the queen's specific hydrocarbon profile. If information on fertility is encoded in the hydrocarbon profile of eggs, we expect workers to be able to differentiate between eggs from highly and weakly fertile queens. We found that workers discriminate between these eggs solely on the basis of their hydrocarbon profiles which differ both qualitatively and quantitatively. This pattern is further supported by the similarity of the egg profiles of workers and weakly fertile queens and the similar treatment of both kinds of eggs. Profiles of queen eggs correspond to the cuticular hydrocarbon profiles of the respective queens. Changes in the cuticular profiles are associated with the size of the colony the queen originates from and her current egg-laying rate. However, partial correlation analysis indicates that only colony size predicts the cuticular profile. Colony size is a buffered indicator of queen fertility as it is a consequence of queen productivity within a certain period of time, whereas daily egg-laying rate varies due to cyclical oviposition. We conclude that surface hydrocarbons of eggs and the cuticular profiles of queens both signal queen fertility, suggesting a major role of fertility signals in the regulation of reproduction in social insects.     

Worker discrimination among queens in newly founded colonies of the fire ant Solenopsis invicta

Although colonies of the fire ant Solenopsis invicta are often founded by small groups of queens, all but one of the queens are soon eliminated due to worker attacks and queen fighting. The elimination of supernumerary queens provides an important context for tests of discrimination by the workers, since the outcome of these interactions strongly affects the workers' inclusive fitness. To test whether workers in newly founded colonies discriminate among nestmate queens, paired cofoundresses were narrowly separated by metal screens that prevented direct fighting, but through which the workers could easily pass. Soon after the first workers completed development, they often attacked one of the queens; these attacks were strongly associated with queen mortality. When one queen's brood was discarded, so that the adult workers were all the daughters of just one queen, the workers were significantly less likely to bite their mother than the unrelated queen; however, this tendency was comparatively weak. Queens kept temporarily at a higher temperature to increase their rate of investment in brood-rearing lost weight more rapidly than paired queens and were subsequently more likely to be attacked and killed by workers. Workers were more likely to bite queens that had been temporarily isolated than queens that remained close to brood and workers. When queens were not separated by screens, the presence of workers stimulated queen fights. These results show that workers discriminate strongly among equally familiar queens and that discrimination is based more on the queens' condition and recent social environment than on kinship. Received: 9 June 1998 / Accepted after revision: 10 October 1998     

Conflicts,social economics and life history strategies in ants

Summary This paper presents a life history model for a perennial social insect colony. The model's purpose is to explore the evolutionary consequences, in terms of fitness of different parties within the colony, of alternative life history strategies. The model has been specifically developed for colonies of the slave-making ant, Harpagoxenus sublaevis, which has reproductive workers organized in dominance orders. It incorporates empirically obtained parameters, and uses computer algorithms based on numerical optimization to determine the optimum policy for a colony queen in allocating resources between workers, queens, and males. Variants of the model also consider alternative situations in which either (1) orphaned workers do not slave-raid, or (2) workers are sterile. The results correspond closely to data on colony growth and reproductive allocation obtained from the field. They suggest that a colony queen would suffer reduced fitness in the two theoretical cases as compared to the real situation. Reproduction by orphaned workers posthumously enhances the colony queen's fitness because a queen with sterile workers cannot produce enough extra sexuals in her lifetime to balance her loss in grandson production. The results also suggest that the division of labour between slave-raiding and nonraiding workers observed in H. sublaevis colonies can be explained as an outcome of worker-worker reproductive conflict: reproductively-inhibited subordinate workers can increase their inclusive fitness by slaveraiding for dominant, nonraiding egg-layers. These findings emphasize the evolutionary importance of the orphanage period and of intracolony conflict in monogynous social insect colonies.     

Recognition of caste and mating status maintains monogyny in the ant Aphaenogaster senilis

In ants dispersing through colony fission, queens mate near their natal nest and found a new society with the help of workers. This allows potential future queens to challenge the mother queen’s reproductive monopoly. Conflicts might be resolved if the mated queen signals her presence and the workers control the developmental fate of the diploid larvae (whether they develop to worker or queen). In this study we sought to determine whether, in the fission-performing ant Aphaenogaster senilis, conflicts between queens for control of the colony are resolved by the resident queen signalling her mating status. Virgin queens were less effective than newly mated queens in inhibiting queen rearing. Moreover, potential challenger queens were recognized and heavily aggressed independent of mating status. Chemical analyses showed that mating status was associated with changes in cuticular hydrocarbon and poison gland composition, but not in Dufour’s gland composition. Cuticular dimethylalkanes were identified as potential constituents that signal both caste (present in queens only) and mating status (mated queens have higher amounts). We hypothesised that pheromone emission by virgin queens did not reach the threshold needed to fully inhibit larval development into queens but was sufficiently high to stimulate overt aggression by mated queens. These findings provide evidence for the complexity of chemical communication in social insects, in which a small number of signals may have a variety of effects, depending on the context.     

Fertility signaling in queens of a North American ant

In most species of advanced eusocial insects, the partitioning of reproduction between nestmates is thought to be regulated by means of primer pheromones or other chemical cues, which presumably influence the behavior of co-queens and workers such that they maximize their own inclusive fitness. Here we show that in multi-queen colonies of the Nearctic ant, Leptothorax sp. A, physical dominance in concert with chemical cues, which signal the ovarian development of a queen, are used to control reproduction of competing queens and to influence worker behavior. The analysis of ranks obtained during two fighting periods in the annual colony cycle revealed a strong link between individual aggressiveness of a queen and her fertility. During the adoption of newly mated queens in autumn, the resident, egg-laying α-queen was more likely to start aggression first and keep her high rank position compared to the fighting period after hibernation. We suggest that this is proximately caused by the α-queen having much stronger developed ovaries in autumn than the young queens, whereas after hibernation, the ovaries of all queens are similarly inactive. Interactions during the first weeks after the end of hibernation and intrinsic, individual differences in aggressiveness appear to be crucial for the dominance rank achieved later. Queens which were allowed to become fertile when their nestmate queens still were kept under prolonged hibernation, were immediately socially dominant over the latter when all queens were reunited, though no aggression occurred. In another experiment, queen antagonism was prevented by spatial separation in different parts of the same nest and all queens began to lay eggs. Workers stayed preferentially with queens with high actual fecundity rather than with those which had had high social status before separation. This and further evidence suggest that ovarian status is communicated, most likely by a chemical cue perceived by co-queens and workers, affects the direction of their aggressive behavior, and allows them to discriminate among queens. Received: 5 May 1998 / Accepted after revision: 29 August 1998     

Maternity of replacement queens in the thelytokous Cape honey bee Apis mellifera capensis

Unlike workers of all other honey bee (Apis mellifera) subspecies, workers of the Cape honey bee of South Africa (A. mellifera capensis) reproduce thelytokously and are thus able to produce female offspring that are pseudoclones of themselves. This ability allows workers to compete with their queen over the maternity of daughter queens and, in one extreme case, has led to a clonal lineage of workers becoming a social parasite in commercially managed populations of A. mellifera scutellata. Previous work (Jordan et al., Proc R Soc Lond B Biol Sci 275:345, 2008) showed that, in A. mellifera capensis, 59% of queen cells produced during swarming events contained the offspring of workers and that, of these, 65% were the offspring of non-natal workers. Here, we confirm that a substantial proportion (38.5%) of offspring queens is worker-laid. We additionally show that: (1) Although queens produce most diploid female offspring sexually, we found some homozygous or hemizygous queen offspring, suggesting that queens also reproduce by thelytoky. These parthenogenetic individuals are probably nonviable beyond the larval stage. (2) Worker-laid offspring queens are viable and become the resident queen at the same frequency as do sexually produced queen-laid offspring queens. (3) In this study, all but one of the worker-derived queens were laid by natal workers rather than workers from another nest. This suggests that the very high rates of social parasitism observed in our previous study were enhanced by beekeeping manipulations, which increased movement of parasites between colonies.     

Stable relatedness structure of the large-colony swarm-founding wasp Polybia paulista

In social-insect colonies, cooperation among nestmates is generally stabilized by their high genetic similarity. Thus, fitness gained through cooperation drops quickly as the number of reproductive females (queens) increases. In this respect, wasps of the tribe Epiponini have attracted special attention, because the colonies have tens, or even hundreds of queens. It has been empirically or genetically confirmed that relatedness within nestmates can be elevated by a mechanism known as cyclical monogyny, under which new queens are produced only after the number of old queens is reduced to one. Another likely factor that can increase relatedness within nestmates under polygyny is comb partitioning by queens. If queens concentrate their egg laying on one or a subset of the available combs, then workers may be able to rear closer relatives by focusing their work on the comb where they emerged. Using microsatellite markers, we tested the hypotheses of cyclical monogyny and comb partitioning by queens increasing relatedness within nestmates under polygyny in the large-colony epiponine wasp, Polybia paulista. There were no significant differences between relatedness within combs and between combs, and thus we ruled out the possibility that each queen partitions reproduction between combs. However, as cyclical monogyny predicts, a lower effective number of queens contributed to queen production than to worker production. Cyclical monogyny explained well the observed smaller effective number of queens for new queens than that for workers, but failed to explain the stable relatedness values throughout colony cycles.Communicated by L. Keller     

Dominance relationship in the establishment of reproductive division of labour in a primitively eusocial wasp (Ropalidia marginata)

In mature post-emergence colonies of the tropical primitively eusocial polistine wasp Ropalidia marginata, the queen is not a behaviourally dominant individual. Nevertheless, she completely suppresses reproduction by the workers and becomes the sole egg-layer in the colony. Mechanisms by which a female is able to establish her exclusive reproductive status in the colony can be investigated by examining dominance-submission relationships and hierarchy formation at particular stages of the colony cycle when reproductive competition is behaviourally manifest. Observations on the behaviour of R. marginata females (1) during early stages of colony-founding, (2) when potential queens challenge the existing queen, and (3) immediately after queen replacement show that these wasps use highly aggressive dominance interactions to establish their reproductive status. Both the frequency and the intensity of dominance behaviours are significantly higher at these stages than those observed at phases of the colony when there is no apparent reproductive strife. Once her position as the only egg-layer of the colony has been established, the levels of dominance interactions initiated by the queen decrease and the nature of these interactions also becomes comparatively milder. Thus, the mechanisms by which a queen establishes her social status in her colony and those by which she continues to suppress reproduction of her nestmates in the absence of overt physical dominance may be quite different. Received: 17 November 1995/Accepted after revision: 20 April 1996     

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     

The kin recognition system of carpenter ants (Camponotus spp.)

Summary The phenotypic cues that provide for rejection of non-nestmates by workers of the ant genus Camponotus could derive from any or all of four sources: (1) environmental odors; (2) the individual's own genetically-determined recognition pheromones or discriminators; (3) a gestalt or mixture of transferable discriminators, produced by each nestmate and absorbed by all; and/or (4) the discriminators of the queen applied to all nestmates. To test these hypotheses, four series of small experimental colonies were created: inter- and intraspecific mixed colonies containing queens, queenless worker groups, and pairs of worker groups between which a single queen was repeatedly switched. Intraspecific mixed colonies and queenless groups were further divided into groups receiving different diets. Aggression of workers in 165 experimental colonies was assayed in a total of 4064 neutral arena tests. Workers adopted into inter- and intraspecific mixed colonies with queens were highly aggressive to unfamiliar kin from pure colonies, independent of diet and of the proportion of different kin groups in the colony. However, queenless workers exhibited less aggression to unfamiliar kin than to non-kin, demonstrating the existence of worker discriminators. Diet differences slightly enhanced aggression among unfamiliar queenless kin. Non-kin sharing a switched queen were as unaggressive to one another as were sisters. The ability to adopt queenless workers between colonies gradually declined over 1–2 wks following their emergence from pupae. We propose a hierarchy of importance of cue sources in determining nestmate discrimination in small Camponotus colonies: Queen discriminators> worker discriminators>environmental cues. A flow-diagram model of social insect kin recognition, based on the phenotype matching concept of Holmes and Sherman (1983), is discussed.     

The dissolution of cooperative groups: mechanisms of queen mortality in incipient fire ant colonies

In several species of ants, queens often form temporary cooperative associations during colony foundation. These associations end soon after the eclosion of the first workers with the death or expulsion of all but one of the queens. This study examined competition between foundress queens of the fire ant Solenopsis invicta. Although attacks by the workers contributed to queen mortality, queens gained no advantage by producing more workers than their co-foundresses. Restriction fragment length polymorphism analysis of mitochondrial DNA showed that the queen producing more workers during colony founding was no more likely to survive than the less productive queen. In experimentally manipulated colonies in which all the workers were daughters of only one of the queens, the mother of the workers was no more likely to survive than the unrelated queen. Queens producing diploid males reared fewer offspring but were as likely to survive as queens producing only workers. These results suggest that workers do not discriminate between related and unrelated queens within colonies. Aggressive encounters between queens were common. Queens were more likely to die or be expelled if paired with heavier queens or if they lost more weight than their co-foundress during the claustral period. Finally, when queens were separated by screens through which workers could pass, the workers usually attacked and killed the queen farther from the brood. These results suggest that queen survival is promoted by a high fighting ability relative to co-foundresses, rather than by increased worker production, and that workers respond to queen differences that are independent of kinship. Received: 8 September 1995/Accepted after revision: 5 March 1996     

Nestmate recognition in the ant Cataglyphis niger : do queens matter?

This study compares two basic models for the origin and maintenance of colony gestalt odor in the polygynous ant species Cataglyphis niger. In the first model, queens are centers of de novo biosynthesis and distribution of recognition odors (“queen-centered” model); in the second, colony odors are primarily synthesized and distributed by workers (“worker-centered” model). We tested the behavioral patterns that are predicted from each model, and verified by biochemical means the distributional directionality of these signals. Encounters between nestmates originating from split colonies were as amicable as between nestmates from non-split colonies; queenless ants were as aggressive as their queenright nestmates, and both were equally aggressed by alien ants. These results indicate that queens have little impact on the recognition system of this species, and lend credence to the worker-centered model. The queen-centered model predicts that unique queen substances should be produced in appreciable quantities and that, in this respect, queens should be more metabolically active than workers. Analysis of the chemical composition of postpharyngeal glands (PPGs) or cuticular extracts of queens and workers revealed high similarity. Quantitatively, queens possessed significantly greater amounts of hydrocarbons in the PPG than workers, but the amount on the thoracic epicuticle was the same. Queens, however, possess a lower hydrocarbon biosynthesis capability than workers. The biochemical evidence thus refutes the queen-centered model and supports a worker-centered model. To elucidate the directionality of cue distribution, we investigated exchange of hydrocarbons between the castes in dyadic or group encounters in which selective participants were prelabeled. Queens tended to receive more and give less PPG content, whereas transfer to the epicuticle was low and similar in all encounters, as predicted from the worker-centered hypothesis. In the group encounters, workers transferred, in most cases, more hydrocarbons to the queen than to a worker. This slight preference for the queen is presumably amplified in a whole colony and can explain their copious PPG content. We hypothesize that preferential transfer to the queen may reflect selection to maintain her individual odor as close to the average colony odor as possible. Received: 4 November 1997 / Accepted after revision: 5 February 1998     

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.     

Colony founding,queen dominance and oligogyny in the Australian meat ant Iridomyrmex purpureus

Summary Field observations and laboratory experiments demonstrate that in the Australian meat ant, Iridomyrmex purpureus, the modes of colony founding are remarkably diverse. New colonies can originate from single foundresses (haplometrosis), or foundress associations (pleometrosis), or by colony budding, or the adoption of newly-mated queens that dig founding chambers next to mature nests (probably their natal nests, as workers protect them and may help them dig). Readoption of foundresses and pleometrosis lead to the coexistence of several queens in one nest. We discovered a striking antagonistic behavior among coexisting queens in young colonies, in the form of ritualized antennation bouts. These interactions result in a reproductive rank order in which dominant queens inhibit egg-laying by subordinates, but escalation into physical fighting is rare. Workers ignore queen dominance interactions and treat all queens equally. The first quantitative ethogram of dominance display behavior between multiple ant queens, and its reproductive consequences, is presented. As a colony grows, queens become intolerant of each other's presence and permanently separate within the nest. Once separated, queens appear to be equal in status, laying approximately equal numbers of eggs. All queens continue to be tolerated by workers, even when the colony has reached a size of several thousand workers and begun to produce reproductives. Such mature nests of I. purpureus fulfill the criteria of oligogyny, defined by worker tolerance toward more than one queen and antagonism among queens, such that a limited number of fully functional queens are spaced far apart within a single colony. Oligogynous colonies can arise in this species by pleometrotic founding (primary oligogyny) or by adoption of queens into existing nests (secondary oligogyny). The adaptive significance of the complex system of colony founding, queen dominance and oligogyny in I. purpureus is discussed.     

Dual mechanism of queen influence over sex ratio in the ant Pheidole pallidula

Social Hymenoptera are general models for the study of parent-offspring conflict over sex ratio, because queens and workers frequently have different reproductive optima. The ant Pheidole pallidula shows a split distribution of sex ratios with most of the colonies producing reproductives of a single sex. Sex ratio specialization is tightly associated with the breeding system, with single-queen (monogynous) colonies producing male-biased brood and multiple-queen (polygynous) colonies female-biased brood. Here, we show that this sex specialization is primarily determined by the queens influence over colony sex ratio. Queens from monogynous colonies produce a significantly more male-biased primary sex ratio than queens from polygynous colonies. Moreover, queens from monogynous colonies produce a significantly lower proportion of diploid eggs that develop into queens and this is associated with lower rate of juvenile hormone (JH) production compared to queens from polygynous colonies. These results indicate that queens regulate colony sex ratio in two complementary ways: by determining the proportion of female eggs laid and by hormonally biasing the development of female eggs into either a worker or reproductive form. This is the first time that such a dual system of queen influence over colony sex ratio is identified in an ant.     

Colony specificity of Dufour gland secretions in a functionally monogynous ant

Summary. Queens in colonies of the small myrmicine ant, Leptothorax gredleri Mayr 1855 (Hymenoptera, Formicidae) engage in dominance interactions and form social hierarchies, in which typically only the top-ranking queen lays eggs. Occasionally, queen antagonism escalates to violent mandible fighting, during which the sting is used to apply Dufour gland secretions onto the cuticle of the opponent. Contaminated queens often are attacked by nestmate workers. Here we show that the chemical composition of the Dufour gland is colony-specific and that workers can discriminate between secretions from their own and other colonies. Our findings suggest that Dufour gland secretions are involved in the establishment of hierarchies within a colony. When invading an alien colony the queen presumably employs the secretions during the expulsion of the resident queen. Apparently, Dufour gland secretions play a role in intraspecific queen competition similar to that in slave-making and inquiline formicoxenine ants, where they function as "propaganda substances" in an interspecific context. Received 7 July 1998; accepted 15 September 1998.     

Regional variation in queen and worker aggression in incipient colonies of the desert ant Messor pergandei

The fate of queen foundress associations in ants varies across taxa: in some, lethal fighting results in survival of a single queen, while in others, queens coexist long term. One hypothesis for this difference is that selection favors fighting when group sizes are small and tolerance when groups are large. In an experiment with the ant Messor pergandei, we formed small, medium, and large groups with newly mated queens from field populations that have different mean group sizes and differ in whether multiple queens occur in older established colonies. We found that whether queens are eliminated by fighting depends upon region of origin and not group size: regardless of co-foundress number, queens from sites with single-queen adult field colonies displayed agonistic behaviors and their colonies reduced to a single queen, while queens from sites with multiple-queen colonies did not fight and co-foundresses coexisted long term. Worker aggression towards and elimination of queens were also correlated with region of origin. Where fighting occurred, queens were as likely to be killed by workers as by other queens. An aggressive display was the most common form of agonistic interaction among queens, while fighting was relatively rare. We hypothesize that queen displays evolved in response to worker attacks because they increase the probability that workers will eliminate competitor queens. Our results suggest that the evolutionary interests of workers, as well as queens, could be important in determining the evolution and maintenance of queen elimination in foundress associations.     

Kinship discrimination in queen rearing by honey bees (Apis mellifera)

Summary Apis mellifera workers are able to discriminate the degree of relatedness to themselves of larvae and to preferentially rear queens from related larvae. They employ cues of genetic, not environmental origin, and workers which have only experienced unrelated brood nonetheless prefer related (but novel) over unrelated (but familiar) larvae. Thus worker bees possess the sensory capabilities and behavioral responses that would enable them to maximize their individual inclusive fitness through nepotism in queen rearing.     

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.