Worker Policing Research Articles

“Selfish worker policing” controls reproduction in a Temnothorax ant

Animal societies, including those of humans, are under constant threat by selfish individuals, who attempt to enforce their own interests at the cost of the group. In the societies of bees, wasps, and ants, such individual selfishness can be prevented by “policing,” whereby workers or queens impede the reproduction of other individuals by aggression, immobilization, or egg eating. In this study, we report on a particular kind of reproduction control in the ant Temnothorax unifasciatus, which can be considered as a selfish act itself. We experimentally induced workers to lay eggs by dividing several colonies into two halves, one with and one without a queen. In queenless colonies, workers established rank orders by aggression and several top-ranking workers started to reproduce. Upon reunification, egg-laying workers mostly stopped behaving aggressively. They were neither attacked by the queen nor by random workers, but instead received infrequent, nondestructive, targeted aggression from a few workers, most of which became fertile when the queen was later removed. The introduction of differentially stained worker-laid and queen-laid eggs in queenright fragments did not lead to a selective removal of worker-laid eggs. Hence, there appears to be no collective worker policing in T. unifasciatus. Instead, reproduction appears to be controlled mostly through a few attacks from high-ranking workers, which, in this way, might attempt to selfishly increase their chances of future reproduction.

Worker policing and nest mate recognition in the ant Formica fusca

A conflict over male production arises in social insects where workers are able to lay unfertilized male eggs. This happens because each female (queen or worker) is most closely related to her own sons and is thus predicted to reproduce. The conflict is modulated by worker policing where workers prevent each other from reproducing by aggression or egg cannibalism. In this study, we show that in the ant Formica fusca, worker policing occurs by egg cannibalism rather than by overt aggression among workers. Furthermore, we show that, contrary to bees, wasps and other ant species, egg discrimination in F. fusca is not based only on a universal queen signature chemical and that nest mate recognition of eggs occurs.

Worker policing in the common wasp Vespula vulgaris is not aimed at improving colony hygiene

In insect societies, eggs laid by workers are frequently killed by other workers – a behaviour known as “worker policing”. The traditional explanation of worker policing is that it is a mechanism to resolve intracolony conflict, and maintain the reproductive monopoly of the queen. Recently, Pirk et al. (2004) proposed that worker policing instead is aimed at removing unviable worker-laid eggs and is ultimately just another example of hygienic behaviour. Here we test this hypothesis for the common wasp Vespula vulgaris, a species with highly effective worker policing. We show that worker-laid eggs from queenless colonies have a lower hatch rate (68%) than queen-laid eggs (82%). Analysis of egg laying rates of queens and workers, however, shows that the difference is not big enough to explain the apparent absence of adult worker-derived males in this species.

Comparative Analysis of Worker Reproduction and Policing in Eusocial Hymenoptera Supports Relatedness Theory

In many bees, wasps, and ants, workers police each other in order to prevent individual workers from selfishly producing their own male offspring. Although several factors can selectively favor worker policing, genetic relatedness is considered to be of special importance. In particular, kin selection theory predicts that worker policing should be more common in species where workers are more related to the queen's sons than to other workers' sons. Here we provide strong novel support for this theory based on a comparative analysis of policing and male parentage in 109 species of ants, bees, and wasps. First, an analysis of behavioral data confirms that worker policing occurs more frequently in species where workers are more related to the queen's sons than to other workers' sons. Second, an analysis of male parentage shows that a significantly higher percentage of the males are workers' sons in species where the workers are more related to other workers' sons. Both conclusions also hold if data are analyzed using phylogenetically independent contrasts. Although our analysis provides strong overall support for the theory that relatedness affects kin conflict over male parentage, there is also significant residual variation. Several factors that may explain this variation are discussed.

Nepotism and brood reliability in the suppression of worker reproduction in the eusocial Hymenoptera

In many eusocial Hymenoptera, workers prevent each other from producing male offspring by destroying worker-laid eggs. Kin selection theory predicts that such 'worker policing' behaviour can evolve by increasing the average relatedness between workers and their male brood. Alternatively, if worker-laid eggs are of low relative viability, their replacement would increase the developmental reliability of the brood. Less colony investment in terms of time and resources would be lost on poor males. This gain is independent of the relatedness of the males. Unfortunately, both nepotistic and group efficiency benefits can simultaneously accrue with the replacement of worker-laid eggs. Therefore, worker behaviour towards eggs cannot completely resolve whether both processes have been equally evolutionarily important. Adequate resolution requires the presentation of worker-produced brood of various ages. The stage at which brood are replaced can discriminate whether worker policing occurs owing to a preference for closer genetic kin, a preference for the more reliable brood or both.

The reproductive dilemmas of queenless red dwarf honeybee (Apis florea) workers

Honeybee (Apis) workers cannot mate, but retain functional ovaries. When colonies have lost their queen, many young workers begin to activate their ovaries and lay eggs. Some of these eggs are reared, but most are not and are presumably eaten by other workers (worker policing). Here we explore some of the factors affecting the reproductive success of queenless workers of the red dwarf honeybee Apis florea. Over a 2-year period we collected 40 wild colonies and removed their queens. Only two colonies remained at their translocated site long enough to rear males to pupation while all the others absconded. Absconding usually occurred after worker policing had ceased, as evidenced by the appearance of larvae. Dissections of workers from eight colonies showed that in A. florea, 6% of workers have activated ovaries after 4 days of queenlessness, and that 33% of workers have activated ovaries after 3 weeks. Worker-laid eggs may appear in nests within 4 days and larvae soon after, but this is highly variable. As with Apis mellifera, we found evidence of unequal reproductive success among queenless workers of A. florea. In the two colonies that reared males to pupation and which we studied with microsatellites, some subfamilies had much higher proportions of workers with activated ovaries than others. The significance of absconding and internest reproductive parasitism to the alternative reproductive strategies of queenless A. florea workers is discussed.

Male parentage in army ants

In most social insects workers do not mate, but have retained the ability to produce haploid eggs that can develop into viable male offspring. Under what circumstances this reproductive potential is realized and how the ensuing worker-queen conflict over male production is resolved, is an area of active research in insect sociobiology. Here we present microsatellite data for 176 males from eight colonies of the African army ant Dorylus (Anomma) molestus. Comparison with worker genotypes and inferred queen genotypes from the same colonies show that workers do not or at best very rarely reproduce in the presence of the queen. Queens of D. (A.) molestus are known to be highly multiply mated. This implies that workers are on average more closely related to queen sons than to other workers' sons, so that our results are consistent with predictions from inclusive fitness theory. It remains unknown, however, whether worker sterility is maintained by active worker policing or by self-restraint.

The Evolution of Worker Caste Diversity in Social Insects

Morphological diversification of workers is predicted to improve the division of labor within social insect colonies, yet many species have monomorphic workers. Individual-level selection on the reproductive capacities of workers may counter colony-level selection for diversification, and life-history differences between species (timing of caste determination, colony size, genetic variation available) may mediate the strength of this selection. We tested this through phylogenetically independent contrast analyses on a new data set for 35 ant species. Evidence was found that early divergence of queen-worker developmental pathways may facilitate the evolution of worker diversity because queen-worker dimorphism was strongly positively associated with diversity. By contrast, risks for colonies that invest in specialized workers and colony size effects on costs of worker reproduction seem unlikely to strongly affect the evolution of worker diversity because there was no significant association between colony size and diversity when controlling statistically for queen-worker dimorphism. Finally, worker diversity was greater in species with multiple lineages per colony, and it was negatively associated with relatedness in monogynous species. This could be due to high intracolonial genetic variance favoring the expression and evolution of great worker diversity or to diversity evolving more easily when there is selection for repression of worker reproduction (worker policing).

Role of esters in egg removal behaviour in honeybee (Apis mellifera) colonies

In queen-right honeybee colonies workers detect and eat the vast majority of worker-laid eggs, a behaviour known as worker policing. However, if a colony becomes permanently queen-less then up to 25% of the worker population develops their ovaries and lay eggs, which are normally reared into a final batch of males. Ovary development in workers is accompanied by changes in the chemical secretion of the Dufour's gland with the production of queen-like esters. We show that ester production increases with the period that the colony is queen-less. The increased ester production also corresponds to an increase in persistence of worker-laid eggs in queen-right colonies, since the esters somehow mask the eggs true identity. However, in a rare queen-less colony phenotype, workers always eat eggs indiscriminately. We found that the egg-laying workers in these colonies were unusual in that they were unable to produce esters. This apparently maladaptive egg eating behaviour is also seen in queen-less colonies prior to the appearance of egg-laying workers, a period when esters are also absent. However, the indiscriminate egg eating behaviour stops with the appearance of ester-producing egg-laying workers. These observations suggest that esters are providing some contextual information, which affects the egg eating behaviour of the workers.

A TEST OF WORKER POLICING THEORY IN AN ADVANCED EUSOCIAL WASP, VESPULA RUFA

Mutual policing is an important mechanism for maintaining social harmony in group-living organisms. In some ants, bees, and wasps, workers police male eggs laid by other workers in order to maintain the reproductive primacy of the queen. Kin selection theory predicts that multiple mating by the queen is one factor that can selectively favor worker policing. This is because when the queen is mated to multiple males, workers are more closely related to queen's sons than to the sons of other workers. Here we provide an additional test of worker policing theory in Vespinae wasps. We show that the yellowjacket Vespula rufa is characterized by low mating frequency, and that a significant percentage of the males are workers' sons. This supports theoretical predictions for paternities below 2, and contrasts with other Vespula species, in which paternities are higher and few or no adult males are worker produced, probably due to worker policing, which has been shown in one species, Vespula vulgaris. Behavioral observations support the hypothesis that V. rufa has much reduced worker policing compared to other Vespula. In addition, a significant proportion of worker-laid eggs were policed by the queen.

Changes in the cuticular hydrocarbons of incipient reproductives correlate with triggering of worker policing in the bulldog ant Myrmecia gulosa

In social insects, conflicts over male parentage can be resolved by worker policing. However, the evolution of policing behavior is constrained by the ability of individuals to identify reproductive nestmates, or their eggs. We investigated the occurrence of worker policing and its underlying chemical communication in the bulldog ant Myrmecia gulosa. Although workers have functional ovaries and can lay male-destined eggs, they do not reproduce in queenright colonies. To determine if their sterility is a consequence of worker policing, we experimentally induced worker reproduction in the presence of a queen. Some individuals were seized and immobilized by nestmates, and sometimes killed as a consequence. Although the ovarian development of immobilized individuals was variable, their cuticular hydrocarbon profiles were intermediate between reproductive and nonreproductive workers, indicating they were in the process of starting to reproduce. Approximately 29% of these incipient reproductive workers were successfully policed. To test for policing on eggs, we transferred viable worker eggs to queenright colonies and monitored their acceptance. Furthermore, we compared the surface hydrocarbons of the different types of eggs to determine whether these chemicals could be involved in egg recognition. We found that although there were differences in hydrocarbon profiles and discrimination between queen and worker-laid eggs, viable eggs were not destroyed. Our results strongly support the idea that cuticular hydrocarbons are involved in the policing of reproductive workers. A low level of worker policing appears sufficient to select for self-restraint in workers when few fitness benefits are gained by selfish reproduction. Policing of eggs may thus be unnecessary.

Honeybee workers use cues other than egg viability for policing

Worker policing, wherein social insect workers prevent their sisters from reproducing by eating worker-laid eggs, is recognized as a textbook example of kin selection in action. However, the evolutionary basis of policing was recently challenged in a study that suggested that police-workers remove worker-laid eggs not because rearing workers' sons reduces worker fitness, but merely because worker-laid eggs have low viability. Here, we refute Pirk et al.'s conclusions. First, we confirm earlier work that showed equal viability of eggs laid by queens and workers. Second, a statistical analysis of the data of Pirk et al. reveals that their own data do not support the conclusion that worker-laid eggs are policed merely because of their low viability. Third, we present data that unequivocally show that police-workers cannot discriminate between dead and live eggs. Hence, our study seriously weakens the challenge to the kin-selected basis of policing in honeybees.

Fertility signaling—the proximate mechanism of worker policing in a clonal ant

In eusocial insects, the ability to regulate reproduction relies on cues that signal the presence of fertile individuals. We investigated the variation of cuticular hydrocarbons (CHCs) with reproductive status in Platythyrea punctata, an ant, in which all workers are capable of producing daughters from unfertilized eggs (thelytoky). Who reproduces is determined through dominance and worker policing. New reproductives, which developed their ovaries after separation from an old reproductive for a short period of time, were attacked by nonreproductives upon reintroduction into their colony. In contrast, aggression against new reproductives with fully developed ovaries, which had been separated over a longer period, was initiated by fights between old and new reproductives. CHC profiles varied with ovarian development. New reproductives were only attacked when they expressed a CHC profile similar to old reproductives, but not when it was similar to that of nonreproductives. CHCs appear to signal the fertility of individuals and induce policing behavior towards surplus reproductive workers.

The policing behavior ‘immobilization’ towards ovary-developed workers in the ant, Diacamma sp. from Japan

In social Hymenoptera worker policing that inhibits direct reproduction of workers occurs mainly in the two ways: (1) destruction of worker progenies (postovipositional policing), and (2) aggression towards ovary-developed workers (preovipositional policing). In the queenless ponerine ant, Diacamma sp. from Japan, the existence of the former type of worker policing has been reported, whereas previous studies have failed to find the latter type. We examine the presence of the latter type of worker policing in this species using more careful observational methods. By a series of experiments reuniting previously separated orphaned and non-orphaned subcolonies we found the following facts. Immediately after the colony reunification, aggression frequently took place. Unlike the one-on-one dominance interaction that occurs in non-manipulated colonies, aggression was often directed towards a single victim from multiple attackers, grasping and pulling the victim. The duration of each aggressive interaction was on average far longer in this situation than that of usual dominance interactions. Most victims consisted of ex-orphan workers, while the majority of the attackers were ex-non-orphan workers. Dissection after the above behavioral observation revealed that the ovaries of the victims were on average more active, often containing mature oocytes, than those of non-victims, while the ovaries of attackers were always inactive. The above findings indicate that worker policing via immobilization, which has been reported in some other Ponerinae, also exists in Diacamma sp. from Japan.

Self-restraint and sterility in workers of Acromyrmex and Atta leafcutter ants

Queens of leafcutter ants (Acromyrmex and Atta) are highly multiply mated, resulting in a potential queenworker and worker-worker conflict over who should produce the males in the colony. We studied whether this conflict is expressed, by determining the amount of reproductive egg-laying by workers in queenright colonies of Acromyrmex echinatior, Acromyrmex octospinosus, Atta cephalotes, and Atta sexdens through ovary dissections. Worker sons are absent or rare in queenright Acromyrmex colonies, but can be produced in orphaned colonies. In Atta, most workers have rudimentary ovaries that never produce eggs, but a few (mostly small and medium workers that form a retinue around the queen) lay many trophic eggs for consumption by the queen. These eggs are large, flaccid, and lacking in yolk compared to queen-laid eggs, and appear to be always inviable. In Acromyrmex, many workers (especially young large workers) lay eggs that are similar in size to queen-laid eggs, but mostly with a reduced amount of yolk. Trophic eggs appear to be an important source of food for larvae in Acromyrmex (especially in Ac. echinatior), but not in Atta. Five (0.8) of 616 dissected Ac. echinatior workers but no Ac. octospinosus workers (n = 552), had ready-to-lay reproductive eggs. Old workers in all four species are incapable of laying eggs due to ovary resorption. We conclude that Atta workers are sterile, while Acromyrmex workers display reproductive self-restraint, possibly representing an earlier stage in the evolution towards worker sterility. Worker selfrestraint in Acromyrmex may be maintained by a queen or worker policing mechanism, but individual cost-benefit explanations may also apply.

Queen and worker policing in the tree wasp Dolichovespula sylvestris

Insect societies are sometimes exploited by workers who reproduce selfishly rather than help to rear the queen’s offspring. This causes a conflict-of-interest with the mother queen and, frequently, with the non-reproductive workers as well. One mechanism that can reduce conflict is policing, whereby either the queen or other workers aggress egg-laying workers or destroy worker-laid eggs. Here we present the first direct observations of queen and worker policing in natural, unmanipulated colonies of a social insect, the tree wasp Dolichovespula sylvestris. Worker reproduction was common, with workers producing 50% of all male eggs. However, most worker-laid eggs, 91%, were policed within 1 day, whereas most queen-laid eggs, 96%, remained unharmed. The workers were responsible for 51% of all policing events and the queen for 49%. The workers and mother queen also commonly aggressed ovipositing workers, and successfully prevented them from depositing eggs in 14% and 6% of all attempted ovipositions. Hence, both queen policing and worker policing occur and policing acts via two distinct mechanisms: selective destruction of worker-laid eggs and aggression of ovipositing workers. At a general level, our study shows that both centralized and decentralized control can act together to suppress conflict within social groups.

Queen and worker policing in monogynous and monandrous colonies of a primitively eusocial wasp

Kin-selection theory predicts that a worker prefers to produce her own sons in a colony with monandry and monogyny because relatedness to her sons (0.5) and nephews (0.375) exceeds that to brothers (0.25). In spite of this prediction, recent studies reveal that workers police each other (mutual-worker egg removal) even in monandrous and monogynous colonies. We conducted field and laboratory studies to evaluate queen and worker policing in queen-right colonies of the primitively eusocial wasp Polistes chinensis antennalis. Genetic studies using microsatellite markers, as well as extensive observations of natural colonies, revealed that both queen and workers removed both queen- and worker-laid eggs in monogynous and monandrous colonies. The queen's eggs survived to hatching more successfully than those of the workers (88.5% versus 1.4%). We discuss the likely factors to explain these worker-policing behaviours.

Reproductive monopoly enforced by sterile police workers in a queenless ant

In societies of totipotent insects, dyadic dominance interactions generate a hierarchy that often underlies an extreme reproductive skew. Subordinates remain infertile but can maximize their indirect fitness benefits through collective power (worker policing): interference with challenging high-rankers can prevent an untimely replacement of the reproductive. However, police workers only benefit if they favor individuals with high fertility. In the monogynous queenless ant Streblognathus peetersi, we used behavioral, physiological, and chemical methods to show that police workers have the primary role in the selection of the reproductive, and that they probably use reliable information about fertility encoded in the cuticular hydrocarbons to make their decision. We successfully decreased an alpha’s fertility by using a hormonal treatment (Pyriproxyfen, a juvenile hormone analogue), and she was always removed from the hierarchy by police workers. In the preceding days, one of the high-rankers became aggressive, although her interactions were not directed at the treated alpha. All treated alphas (n ¼ 10) remained aggressive but ended up immobilized by low-ranking workers after a median time of 11.5 days. By then, the challenging high ranker exhibited dominance behaviors typical of the alpha rank. In parallel, the cuticular profile of the treated alpha exhibited predictable and opposite modifications to that of the challenger’s. This is the first study that uncouples dominance and fertility in a social insect: it gives a better understanding of the crucial role of sterile helpers in the control of reproductive skew in animal societies. Key words: cuticular hydrocarbons, fertility signal, gamergate, juvenile hormone, Ponerinae, reproductive skew, worker policing. [Behav Ecol 15:970–975 (2004)]

Why do honey bee workers destroy each other's eggs?

Hamilton’s theory of inclusive fitness predicts that in polyandrous colonies of social Hymenoptera, workers should prevent each other from reproducing and prefer to rear the queen’s sons rather than their nephews. This is because, in polyandrous colonies, unlike in monandrous colonies, workers are expected to be more closely related to their brothers than to their nephews. Honey bees clearly fulfill this expectation – queens mate multiply, worker reproduction is rare and the few eggs laid by workers are usually destroyed by other workers. Such mutual destruction of each other’s eggs by honey bee workers has been called worker policing and has achieved the status of a classic example of kin selection. However, recent evidence indicating that worker-laid eggs may be much less viable than queen-laid eggs opens up the possibility that worker policing may simply be a matter of destroying dead eggs and rearing live ones. If confirmed, this raises serious doubts about the widely accepted relatedness based argument for the evolution of worker policing. A major weakness of the kin selection-based explanation for worker policing is our ignorance of the proximate cues used by worker bees to distinguish between brother eggs and nephew eggs.

Egg marking pheromones of anarchistic worker honeybees (Apis mellifera)

In honeybees, worker policing via egg eating enforces functional worker sterility in colonies with a queen and brood. It is thought that queens mark their eggs with a chemical signal, indicating that their eggs are queen-laid. Worker-laid eggs lack this signal and are, therefore, eaten by policing workers. Anarchistic worker honeybees have been hypothesized to circumvent worker policing by mimicking the queen egg-marking signal. We investigated this phenomenon by relating chemical profiles of workers and their eggs to egg acceptability. We found that the ability of some workers (anarchistic workers in queenright colonies and deviant workers from a queenless colony) to lay more acceptable eggs is due to them producing significant amounts of queen-like esters from their Dufour's gland. These esters appear to be transferred to eggs during laying and increase egg survival. However, these esters cannot be the normal queen egg-marking signal, as they are generally absent from queen-laid eggs and only increase the short-term persistence of worker-laid eggs, because only 7?30% of anarchistic worker-laid eggs persisted to hatching versus 91?92% of queen-laid eggs. All workers can produce some esters, but only workers that greatly increase their ester production lay more acceptable eggs. The production of esters appears to be a flexible response, as anarchistic workers reared in queenless colonies did not increase their ester production, while some deviant workers in queenless colonies did increase their ester production.