The effect of sex-allocation biasing on the evolution of worker policing in hymenopteran societies

Mutual policing is thought to be important in conflict suppression at all levels of biological organization. In hymenopteran societies (bees, ants, and wasps), multiple mating by queens favors mutual policing of male production among workers (worker policing). However, worker policing of male production is proving to be more widespread than predicted by relatedness patterns, occurring in societies headed by single-mated queens in which, paradoxically, workers are more related to the workers' sons that they kill than the queen's sons that they spare. Here we develop an inclusive-fitness model to show that a second reproductive conflict, the conflict over sex allocation, can explain the evolution of worker policing contrary to relatedness predictions. Among ants, and probably other social Hymenoptera, workers kill males to favor their more related sisters. Importantly, males are killed at the larval stage, presumably because workers cannot determine the sex of queen-laid eggs. Sex-allocation biasing favors worker policing because policing removes some males (the workers' sons) at low cost at the egg stage rather than at higher cost at the larval stage. Our model reveals an important interaction between two reproductive conflicts in which the presence of one conflict (sex allocation) favors the suppression of the other (male production by workers)

Task partitioning in insect societies. II. Use of queueing delay information in recruitment

The collection and handling of colony resources such as food, water, and nest-construction material is often divided into subtasks in which the material is passed from one worker to another. This is known as task partitioning. If task; are partitioned with direct transfer of material between foragers and receivers, queueing delays can occur as individuals search or wait for a transfer partner. Changes in environmental conditions and relative number of foragers and receivers affect these delays as well as colony ergonomic efficiency. These delays are used in recruitment in both honeybees and Polybia wasps. This study investigates the distribution of queueing delays and the information content and quality of those delays using a stochastic-simulation model. Information quality increases with colony size. When the relative proportions of foragers and receivers are suboptimal, the group in excess has better information. Individuals can increase information quality of delays by two mechanisms: averaging over consecutive trips and averaging over multiple transfers within a trip where direct transfer occurs. We suggest that multiple transfer occurs in the honeybee in order to improve information quality

Tragedy of the commons in Melipona bees

In human society selfish use of common resources can lead to disaster, a situation known as the ‘tragedy of the commons’ (TOC). Although a TOC is usually prevented by coercion, theory predicts that close kinship ties can also favour reduced exploitation. We test this prediction using data on a TOC occurring in Melipona bee societies

The effect of sex-allocation biasing on the evolution of worker policing in hymenopteran societies

Mutual policing is thought to be important in conflict suppression at all levels of biological organization. In hymenopteran societies (bees, ants, and wasps), multiple mating by queens favors mutual policing of male production among workers (worker policing). However, worker policing of male production is proving to be more widespread than predicted by relatedness patterns, occurring in societies headed by single-mated queens in which, paradoxically, workers are more related to the workers' sons that they kill than the queen's sons that they spare. Here we develop an inclusive-fitness model to show that a second reproductive conflict, the conflict over sex allocation, can explain the evolution of worker policing contrary to relatedness predictions. Among ants, and probably other social Hymenoptera, workers kill males to favor their more related sisters. Importantly, males are killed at the larval stage, presumably because workers cannot determine the sex of queen-laid eggs. Sex-allocation biasing favors worker policing because policing removes some males (the workers' sons) at low cost at the egg stage rather than at higher cost at the larval stage. Our model reveals an important interaction between two reproductive conflicts in which the presence of one conflict (sex allocation) favors the suppression of the other (male production by workers)

Task partitioning in insect societies. I. Effect of colony size on queueing delay and colony ergonomic efficiency

The collection and handling of colony resources such as food, water, and nest construction material is often divided into subtasks in which the material is passed from one worker to another. This is known as task partitioning. When material is transferred directly from one individual to another, queueing delays frequently occur because individuals must sometimes wait for a transfer partner. A stochastic simulation model was written to study the effect of colony size on these delays. Queueing delay decreases roughly exponentially with colony size because stochastic fluctuations in the arrival of individuals are lower in larger colonies. These results support empirical studies of Polybia occidentalis and other theoretical studies of honeybees. The effect of the relative number of individuals in the two subtask groups was also studied. There is a unique optimal ratio of the number of workers associated with each of the subtasks that simultaneously minimizes mean queueing delay and maximizes colony nectar-processing rate. Deviations from this optimal ratio, for example, as a result of forager mortality or changes in nectar productivity that affect foraging trip duration, increase mean queueing delays greatly, especially in smaller colonies

Parasitic Cape honeybee workers, Apis mellifera capensis, evade policing

Relocation of the Cape honeybee, Apis mellifera capensis, by bee-keepers from southern to northern South Africa in 1990 has caused widespread death of managed African honeybee, A. m. scutellata, colonies. Apis mellifera capensis worker bees are able to lay diploid, female eggs without mating by means of automictic thelytoky (meiosis followed by fusion of two meiotic products to restore egg diploidy), whereas workers of other honeybee subspecies are able to lay only haploid, male eggs. The A. m. capensis workers, which are parasitizing and killing A. m. scutellata colonies in northern South Africa, are the asexual offspring of a single, original worker in which the small amount of genetic variation observed is due to crossing over during meiosis (P. Kryger, personal communication). Here we elucidate two principal mechanisms underlying this parasitism. Parasitic A. m. capensis workers activate their ovaries in host colonies that have a queen present (queenright colonies), and they lay eggs that evade being killed by other workers (worker policing)—the normal fate of worker-laid eggs in colonies with a queen. This unique parasitism by workers is an instance in which a society is unable to control the selfish actions of its members

When resistance is useless: policing and the evolution of reproductive acquiescence in insect societies

In social groups composed of kin, inclusive fitness benefits can favor greater cooperation. Alternatively, cooperation can be enforced through the policing of less cooperative individuals. Here, we show that the effect of policing can be twofold: not only can it directly suppress individual selfishness, it can also entirely remove the incentive for individuals to act selfishly in the first place. We term such individual restraint in response to socially imposed policing "acquiescence" and illustrate the concept using examples drawn from the social Hymenoptera (the ants, bees, and wasps). Inclusive fitness models confirm that when a policing system is in place, individuals should be less tempted to act selfishly. This is shown to have important consequences for the resolution of conflict within their societies. For example, it can explain why in many species very few workers attempt to reproduce and why immature females usually do not attempt to develop as queens rather than workers. Although our analyses are primarily focused on the social insects, our conclusions are likely to be general and to apply to other societies as well

The organization of soil disposal by ants

Colonies of Pheidole ambigua ants excavate soil and drop it outside the nest entrance. The deposition of thousands of loads leads to the formation of regular ring-shaped piles. How is this pattern generated? This study investigated soil pile formation on level and sloping surfaces, both empirically and using an agent-based model. We found that ants drop soil preferentially in the direction in which the slope is least steeply uphill from the nest entrance, both when adding to an existing pile and when starting a new pile. Ants respond to cues from local slope to choose downhill directions. Ants walking on a slope increase the frequency and magnitude of changes in direction, and more of these changes of direction take them downhill than uphill. Also, ants carrying soil on a slope wait longer before dropping their soil compared to ants on a level plane. These mechanisms combine to focus soil dropping in the downhill direction, without the necessity of a direct relationship between slope and probability of dropping soil. These empirically determined rules were used to simulate soil disposal. The slight preference for turning downhill measured empirically was shown in the model to be sufficient to generate biologically realistic patterns of soil dumping when combined with memory of the direction of previous trips. From simple rules governing individual behaviour an overall pattern emerges, which is appropriate to the environment and allows a rapid response to changes

Killing and replacing queen-laid eggs: low cost of worker policing in the honey bee

Worker honeybees, Apis mellifera, police each other’s reproduction by killing worker-laid eggs. Previous experiments demonstrated that worker policing is effective, killing most (∼98%) worker-laid eggs. However, many queen-laid eggs were also killed (∼50%) suggesting that effective policing may have high costs. In these previous experiments, eggs were transferred using forceps into test cells, mostly into unrelated discriminator colonies. We measured both the survival of unmanipulated queen-laid eggs and the proportion of removal errors that were rectified by the queen laying a new egg. Across 2 days of the 3-day egg stage, only 9.6% of the queen-laid eggs in drone cells and 4.1% in worker cells were removed in error. When queen-laid eggs were removed from cells, 85% from drone cells and 61% from worker cells were replaced within 3 days. Worker policing in the honeybee has a high benefit to policing workers because workers are more related to the queen’s sons (brothers, r = 0.25) than sister workers’ sons (0.15). This study shows that worker policing also has a low cost in terms of the killing of queen-laid eggs, as only a small proportion of queen-laid eggs are killed, most of which are rapidly replaced

Pretender punishment induced by chemical signalling in a queenless ant

Animal societies are stages for both conflict and cooperation. Reproduction is often monopolized by one or a few individuals who behave aggressively to prevent subordinates from reproducing (for example, naked mole-rats, wasps and ants). Here we report an unusual mechanism by which the dominant individual maintains reproductive control. In the queenless ant Dinoponera quadriceps, only the alpha female reproduces. If the alpha is challenged by another female she chemically marks the pretender who is then punished by low-ranking females. This cooperation between alpha and low-rankers allows the alpha to inflict punishment indirectly, thereby maintaining her reproductive primacy without having to figh