Worker policing

Last updated

Worker policing is found in honey bees and other hymenopterans including some species of bumblebees, ants and wasps. Alanna Spence - queen bee (by).jpg
Worker policing is found in honey bees and other hymenopterans including some species of bumblebees, ants and wasps.

Worker policing is a behavior seen in colonies of social hymenopterans (ants, bees, and wasps) whereby worker females eat or remove eggs that have been laid by other workers rather than those laid by a queen. Worker policing ensures that the offspring of the queen will predominate in the group. In certain species of bees, ants and wasps, workers or the queen may also act aggressively towards fertile workers. Worker policing has been suggested as a form of coercion to promote the evolution of altruistic behavior in eusocial insect societies. [1] [ dubious – discuss ]

Contents

Proposed mechanisms for the recognition of worker-laid eggs or active reproductive workers include marker hydrocarbons on the surface of queen-laid eggs, cuticle hydrocarbons on reproductive workers, and recognition of nest-mates. [2] [3] [4] In rare cases, worker-laid eggs carry mimicked queen hydrocarbons and escape policing, a condition known as the anarchic syndrome. [5]

Not all forms of policing require the presence of a queen; it also occurs in a few species of ants which establish a dominance hierarchy of reproductive female workers, where top-ranking individuals reproduce. [6]

Evolutionary basis

The haplodiploid sex determination system has consequences for worker policing behavior Haplodiploid-sex-determination-system3.png
The haplodiploid sex determination system has consequences for worker policing behavior

In many social insect communities, sex is determined through haplodiploidy. Haploid male drones develop from unfertilized eggs while diploid females develop from fertilized eggs. Queens of a colony may mate with one or several drones. In many species of ants, bees, and wasps, workers retain functional ovaries, but cannot mate. [7] Thus, they only produce male offspring. On average, a queen shares half of her genes with her sons, but only shares a quarter of her genes with the sons of fertile female workers. Therefore, it is in the queen's best interests to have her own sons raised, and not the sons of workers.

By contrast, the worker shares half of her genes with her sons and only a quarter with her brothers. Furthermore, the workers in colonies with a single once-mated queen are related to their nephews by three eighths, higher than they are related to brothers. This results in a conflict in which the queen and worker females are at odds over the proportion of male offspring they contribute, since each side tries to maximize its reproductive fitness. [7] Queens favor production of their own sons while workers favor production of their own sons, and do not stop their sisters from laying because of the favorable relatedness to nephews.

Worker policing occurs when worker bees in the colony are genetically more closely related to the queen than the reproductive female. In many instances, the eggs of the female worker are eaten, or she is repeatedly attacked by other workers. This mechanism of egg removal ensures that the queen's sons predominate. [8]

Experiments confirming the role of kin selection in worker policing demonstrate the effects of multiple matings, which can lead to lower average relatedness between workers. Queens of the social wasp Dolichovespula saxonica mate singly or multiply. Researchers who study these wasps have observed a strong positive correlation between worker relatedness and male production. After controlling for the absolute number of eggs laid, these scientists conclude that the queen's multiple matings favor mutual worker policing. [9]

Although early theories of worker policing focused on the kin selection component, evidence from honey bees suggests that altruism is sometimes enforced. Fewer workers reproduce as policing effectiveness rises, and policing effectiveness decreases with increasing relatedness except in colonies with no queen. This suggests that worker policing is a social sanction imposed on selfish individuals. [10]

Proposed mechanisms for kin recognition

Formica fusca ants can recognize nest-mates Fusca feeding.jpg
Formica fusca ants can recognize nest-mates

Mechanisms suggested for egg discrimination in worker policing include queen hydrocarbons, fertile worker hydrocarbons, and nestmate recognition.

Queen hydrocarbons

A study of the carpenter ant Camponotus floridanus found a special surface hydrocarbon on queen-laid eggs. Workers in the colony with the queen's eggs refrained from egg-laying, whereas other groups that did not have queen-laid eggs showed worker reproduction. Thus, the hydrocarbon could act as a signal to alert workers to halt reproduction. More generally, however, the authors concluded that the hydrocarbons were a fertility signal. It is still unknown as to how the decision to restrain reproduction occurs or what minimum threshold of fertility in the queen is needed to reduce worker reproduction. [2]

Fertile worker hydrocarbons

The study of cuticle hydrocarbons has also been applied to the reproductive workers. In some colonies of the ponerine ant Platythyrea punctata , the presence of CHCs in new reproductive workers triggered aggressive behavior from the rest of the colony, often between new and old reproductive workers. Specifically, the old reproductive workers rubbed a marker hydrocarbon on the antennae of the new females, identifying them as rivals and targets for aggression. [3]

Nestmate recognition

In contrast to the other ant species, worker policing in the ant Formica fusca appears to incorporate nestmate recognition in addition to the queen hydrocarbons. Workers displayed higher levels of aggression toward non-nest mates and also removed some queen-laid eggs. Thus, queen hydrocarbons were not the only contributor to discrimination of the eggs. [4]

Examples from social Hymenoptera

Worker policing has evolved convergently in several social insect species. The following cases are examples:

Bees

Apis mellifera workers remove worker-laid eggs by eating them (oophagy) Apis mellifera carnica worker honeycomb 3.jpg
Apis mellifera workers remove worker-laid eggs by eating them (oophagy)

One of the first examples of worker policing to be discovered was in the honey bee, Apis mellifera . Worker policing is prevalent in most honey bee colonies, and worker reproduction is minimal (0.12%) in this species. [11] Worker policing occurs via egg-eating in Apis mellifera colonies. [8] In many of these hives, the activation of ovaries in fertile females is diminished, suggesting that there are disincentives to laying eggs. [8]

Workers in colonies of the dwarf honey bee, Apis florea , are also reported to engage in oophagy. Using microsatellite analysis, researchers concluded that no mature drones had non-queen alleles in the colonies they investigated. Thus, even though workers had activated ovaries and were capable of laying eggs, worker policing ensured the functional sterility of otherwise fertile workers. [12]

A higher percentage of female workers of the bee species Apis cerana are reported to activate their ovaries than those of Apis mellifera or Apis florea. When queens were removed, up to 40% of the workers activated their ovaries in subsequent days. However, policing workers continued to eat the worker-laid eggs, suggesting that the mechanism of policing in this species does not involve direct intervention from the queen. [13]

The observation that all these Apis species engage in polyandry has led researchers to conclude that worker policing is plesiomorphic for the Apis genus. [13]

Worker policing also occurs in the primitively eusocial bumblebees such as Bombus terrestris . [14]

Ants

Worker of Harpegnathos saltator killing a foreign queen Harpegnathos saltator fight.jpg
Worker of Harpegnathos saltator killing a foreign queen

In colonies of the ponerine ant, Pachycondyla inversa, workers eat the eggs of fertile female workers, known as gamergates, and display aggressive behavior towards egg-laying females. [15]

In colonies of the ant Gnamptogenys menadensis, workers will sometimes mate and lay eggs while others remain as virgins to lay trophic eggs to be used as food. In a display of policing, workers can immobilize female reproductive workers by biting their limbs; it is reported that 50% of the victims die from this treatment. The attacking workers may also drag offending workers outside the colony. Since workers can lay both male and female eggs, worker policing could be favored as the cost to the community is large. [16]

The ant species Aphaenogaster smythiesi japonica also display evidence of policing. When researchers separated and then reunited workers from colonies that did or did not have queens, workers from the queen-containing colonies attacked the workers with activated ovaries from the queenless colonies. [17]

In the queenless ant Streblognathus peetersi, policing helps to select gamergates. The workers immobilize gamergates with lowered fertility, enabling high-ranking workers to take over as new gamergates. [18]

In the ponerine ant Harpegnathos saltator , worker policing prevents the number of reproductive workers from becoming excessive. The species has gamergates, which lay eggs but rarely carry out any other tasks, so having too many of them would reduce the colony's efficiency. Gamergate numbers are rather stable, as infertile workers target newly ovipositing workers by jumping on and holding them: this efficiently inhibits them from laying eggs, and within a few weeks they revert to being subordinate and infertile workers. However, once new ovipositing workers attain a gamergate's level of ovarian activity, the infertile (policing) workers ignore them. The signal used by the policing workers consists of cuticle hydrocarbons transmitted only by direct contact, rather than being a pheromone detected by olfaction. Similarly, the inhibition of ovipositing workers is achieved by direct physical aggression by policing workers, not by any pheromone produced by queens or gamergates. [19]

Wasps

Dolichovespula sylvestris workers can display aggression towards other fertile workers GemeineWespe2.jpg
Dolichovespula sylvestris workers can display aggression towards other fertile workers

The tree wasp Dolichovespula sylvestris also displays worker policing. Both egg-eating and aggression are reported in these wasp communities, and the queen also engages in the policing process. [20] Similar behavior has been observed in the closely related species Dolichovespula media . [21]

In colonies of the paper wasp, Polistes chinensis antennalis , workers can lay up to a quarter of the male eggs in the colony. The number of eggs that survived to hatching, however, was minimal compared to the number produced by the queen. Analysis of the microsatellite markers showed that both queens and workers contributed to policing of worker and queen-laid eggs even in monogynous and monandrous colonies. [22]

The common wasp, Vespula vulgaris , engages in worker policing, and it is known that a significant number of workers have active ovaries. However, studies by researchers have suggested that relatedness may not be the key factor in the development of worker policing. Rather, it is hypothesized that worker policing has been selected due to conflict suppression in the colony. [23]

In a test of worker policing, researchers examined the removal of worker-laid eggs in Vespula rufa , a wasp that has low paternity. Under the testing conditions, worker policing was not as efficient, and some of the drones appeared to be from worker-laid eggs. [24]

The European Hornet, Vespa crabro, was previously thought to be under reproductive pheromone control by the queen, thus explaining why the other females did not reproduce, even though they were capable of doing so. Experiments by Foster showed that the workers were instead regulating sterility in each other, thus instead exhibiting worker policing. While each worker is capable of reproducing, the colony as a whole is more efficient and organized if the workers allow only the queen to lay larvae. [25]

Synoeca cyanea also engage in worker policing during times when queen repopulation is not needed. They will prevent females from laying eggs through aggressive behavior and egg-eating. [26]

Exceptions

Anarchic syndrome

Very rarely, female worker bees lay eggs that escape worker policing, in a process known as the anarchic syndrome. Female reproductive workers in these colonies activate their ovaries even in the presence of a queen. The worker eggs are allowed as they mimic queen hydrocarbons. Thus, female workers can maximize their reproductive fitness at the expense of the colony. Anarchic syndrome is an example of selection working in opposite directions at individual and group levels. [5]

Selfish worker policing

Temnothorax unifasciatus , a myrmicinid ant, has been shown not to have collective worker policing. However, when a queen is removed, a rank order for reproduction appears, where top ranking reproductives display aggression towards lower-order female workers. Thus, reductions in egg laying are created by dominance hierarchies. Individuals do not act in benefit of the colony, instead opting to increase their own fitness by laying their eggs and reducing the contributions of opponents. [6]

This type of policy is common in Dolichovespula norwegica wasps where despite being more related to other workers' sons, worker-laid eggs were consumed by other workers. [27]

Worker policing without genetic conflict

In the thelytokous ant Platythyrea punctata, colonies are clonal; therefore, workers are all equally related genetically, and worker policing is not expected as there is no genetic conflict. However, one would expect severe effects on the condition of the colony if reproductive workers were left unchecked. For example, more time spent on individual reproduction would be predicted to detract from care of the queen's offspring. In studies of these ants, workers did actually display worker policing, as evidenced by increased aggression towards reproductive workers. Worker policing here is favored for group efficiency. [28]

Related Research Articles

<span class="mw-page-title-main">Honey bee</span> Colonial flying insect of genus Apis

A honey bee is a eusocial flying insect within the genus Apis of the bee clade, all native to mainland Afro-Eurasia. After bees spread naturally throughout Africa and Eurasia, humans became responsible for the current cosmopolitan distribution of honey bees, introducing multiple subspecies into South America, North America, and Australia.

<i>Dolichovespula maculata</i> Species of wasp

Dolichovespula maculata is a species of wasp in the genus Dolichovespula and a member of the eusocial, cosmopolitan family Vespidae. It is known by many colloquial names, primarily bald-faced hornet, but also including bald-faced aerial yellowjacket, bald-faced wasp, bald hornet, white-faced hornet, blackjacket, white-tailed hornet, spruce wasp, and bull wasp. Technically a species of yellowjacket wasp, it is not one of the true hornets, which are in the genus Vespa. Colonies contain 400 to 700 workers, the largest recorded colony size in its genus, Dolichovespula. It builds a characteristic large hanging paper nest up to 58 cm (23 in) in length. Workers aggressively defend their nest by repeatedly stinging invaders.

<span class="mw-page-title-main">Dominance hierarchy</span> Type of social hierarchy

In the zoological field of ethology, a dominance hierarchy is a type of social hierarchy that arises when members of animal social groups interact, creating a ranking system. A dominant higher-ranking individual is sometimes called an alpha, and a submissive lower-ranking individual is called a beta. Different types of interactions can result in dominance depending on the species, including ritualized displays of aggression or direct physical violence. In social living groups, members are likely to compete for access to limited resources and mating opportunities. Rather than fighting each time they meet, individuals of the same sex establish a relative rank, with higher-ranking individuals often gaining more access to resources and mates. Based on repetitive interactions, a social order is created that is subject to change each time a dominant animal is challenged by a subordinate one.

<i>Apis florea</i> Species of bee

The dwarf honey bee, Apis florea, is one of two species of small, wild honey bees of southern and southeastern Asia. It has a much wider distribution than its sister species, Apis andreniformis. First identified in the late 18th century, Apis florea is unique for its morphology, foraging behavior and defensive mechanisms like making a piping noise. Apis florea have open nests and small colonies, which makes them more susceptible to predation than cavity nesters with large numbers of defensive workers. These honey bees are important pollinators and therefore commodified in countries like Cambodia.

<i>Vespula germanica</i> Species of wasp

Vespula germanica, the European wasp, German wasp, or German yellowjacket is a species of wasp found in much of the Northern Hemisphere, native to Europe, Northern Africa, and temperate Asia. It has spread and become well-established in many other places, including North America, South America, Australia, South Africa, and New Zealand. German wasps are part of the family Vespidae and are sometimes mistakenly referred to as paper wasps because they build grey paper nests, although strictly speaking, paper wasps are part of the subfamily Polistinae. In North America, they are also known as yellowjackets.

<span class="mw-page-title-main">Haplodiploidy</span> Biological system where sex is determined by the number of sets of chromosomes

Haplodiploidy is a sex-determination system in which males develop from unfertilized eggs and are haploid, and females develop from fertilized eggs and are diploid. Haplodiploidy is sometimes called arrhenotoky.

<i>Harpegnathos saltator</i> Species of ant

Harpegnathos saltator, sometimes called the Indian jumping ant or Jerdon's jumping ant, is a species of ant found in India. They have long mandibles and have the ability to leap a few inches. They are large-eyed and active predators that hunt mainly in the early morning. The colonies are small and the difference between workers and queens is very slight.

Cheating is a term used in behavioral ecology and ethology to describe behavior whereby organisms receive a benefit at the cost of other organisms. Cheating is common in many mutualistic and altruistic relationships. A cheater is an individual who does not cooperate but can potentially gain the benefit from others cooperating. Cheaters are also those who selfishly use common resources to maximize their individual fitness at the expense of a group. Natural selection favors cheating, but there are mechanisms to regulate it. The stress gradient hypothesis states that facilitation, cooperation or mutualism should be more common in stressful environments, while cheating, competition or parasitism are common in benign environments.

<span class="mw-page-title-main">Gyne</span> Primary reproductive female castes of insects, also known as queens

The gyne is the primary reproductive female caste of social insects. Gynes are those destined to become queens, whereas female workers are typically barren and cannot become queens. Having a queen is what makes a "queenright" hive, nest, or colony of eusocial insects. A colony with multiple queens is said to be a polygyne form, whereas one with only one is a monogyne form.

<span class="mw-page-title-main">East African lowland honey bee</span> Subspecies of honey bee native to Africa

The East African lowland honey bee is a subspecies of the western honey bee. It is native to central, southern and eastern Africa, though at the southern extreme it is replaced by the Cape honey bee. This subspecies has been determined to constitute one part of the ancestry of the Africanized bees spreading through North and South America.

<i>Harpegnathos</i> Genus of ants

Harpegnathos is a small ponerine genus of ants found in South and Southeast Asia. They are notable for their jumping ability, complex colony structure, and large to very large workers easily identifiable by their long mandibles and large eyes.

<span class="mw-page-title-main">Western honey bee</span> European honey bee

The western honey bee or European honey bee is the most common of the 7–12 species of honey bees worldwide. The genus name Apis is Latin for "bee", and mellifera is the Latin for "honey-bearing" or "honey carrying", referring to the species' production of honey.

<span class="mw-page-title-main">Eusociality</span> Highest level of animal sociality a species can attain

Eusociality is the highest level of organization of sociality. It is defined by the following characteristics: cooperative brood care, overlapping generations within a colony of adults, and a division of labor into reproductive and non-reproductive groups. The division of labor creates specialized behavioral groups within an animal society which are sometimes referred to as 'castes'. Eusociality is distinguished from all other social systems because individuals of at least one caste usually lose the ability to perform behaviors characteristic of individuals in another caste. Eusocial colonies can be viewed as superorganisms.

<i>Polistes annularis</i> Species of wasp

Polistes annularis is a species of paper wasp found throughout the eastern half of the United States. This species of red paper wasp is known for its large size and its red-and-black coloration and is variably referred to as a ringed paper wasp or jack Spaniard wasp. It builds its nest under overhangs near bodies of water that minimize the amount of sunlight penetration. It clusters its nests together in large aggregations, and consumes nectar and other insects. Its principal predator is the ant, although birds are also known to prey on it. Unlike other wasps, P. annularis is relatively robust in winter conditions, and has also been observed to store honey in advance of hibernation. This species has also been used as a model species to demonstrate the ability to use microsatellite markers in maternity assignment of social insects.

<i>Dolichovespula saxonica</i> Species of wasp

Dolichovespula saxonica, also known as the Saxon wasp, is a common social wasp found in the Palearctic region, specifically in large parts of Europe and in northern and central Asia. Although originally from continental Europe, D. saxonica has since colonised Britain, mainly in the south and east, but has been recorded as far north as East Lothian, Scotland. Most of their nests are above ground in trees and bushes, but they can also be found in buildings. Due to the proliferation of nests in urban areas and near residential homes, D. saxonica can be a pest for people. As a result, many human interventions are in place to remove Saxon nests. D. saxonica has been found to use chemical signaling in a lot of behaviours, such as alarm calls, fertility cues, and chemical trails.

<i>Dolichovespula norwegica</i> Species of wasp

The Norwegian wasp is a species of eusocial wasp. It is common in Scandinavia and can also be found in Scotland and other areas in Britain and Ireland. Often known for being a tree wasp, it nests in low branches and bushes and feeds on insects. It also obtains nectar from blueberry and snowberry flowers. Although D. norwegica is rarely considered a pest in the past, a few cases of pest problems relating to them have been reported. The species is not endangered.

<i>Dolichovespula sylvestris</i> Species of wasp

The tree wasp is a species of eusocial wasp in the family Vespidae, found in the temperate regions of Eurasia, particularly in western Europe. Despite being called the tree wasp, it builds both aerial and underground paper nests, and can be found in rural and urban habitats. D. sylvestris is a medium-sized wasp that has yellow and black stripes and a black dot in the center of its clypeus. It is most common to see this wasp between May and September during its 3.5 month colony cycle.

<span class="mw-page-title-main">Gamergate (ant)</span> Reproductively viable female worker ant

A gamergate is a mated worker ant that can reproduce sexually, i.e., lay fertilized eggs that will develop as females. In the vast majority of ant species, workers are sterile and gamergates are restricted to taxa where the workers have a functional sperm reservoir ('spermatheca'). In some species, gamergates reproduce in addition to winged queens, while in other species the queen caste has been completely replaced by gamergates. In gamergate species, all workers in a colony have similar reproductive potentials, but as a result of physical interactions, a dominance hierarchy is formed and only one or a few top-ranking workers can mate and produce eggs. Subsequently, however, aggression is no longer needed as gamergates secrete chemical signals that inform the other workers of their reproductive status in the colony.

<i>Dinoponera</i> Genus of ants

Dinoponera is a strictly South American genus of ant in the subfamily Ponerinae, commonly called tocandiras or giant Amazonian ants. These ants are generally less well known than Paraponera clavata, the bullet ant, yet Dinoponera females may surpass 3–4 cm (1.2–1.6 in) in total body length, making them among the largest ants in the world.

<i>Scaptotrigona postica</i> Species of bee

Scaptotrigona postica is a species of stingless bee that lives mainly in Brazil. It is a eusocial bee in the tribe Meliponini. S. postica is one of 25 species in the genus Scaptotrigona and is a critical pollinator of the tropical rain forests of Brazil. They construct their nests in hollowed sections of tree trunks, allowing for effective guarding at the nest entrance. This species shows colony structure similar to most members of the Meliponini tribe with three roles within the colony: queen, worker, and male. S. postica individuals have different forms of communication from cuticular hydrocarbons to pheromones and scent trails. Communication is especially useful during worker foraging for nectar and pollen through the Brazilian tropical rain forests. S. postica is a very important pollinator of the Brazilian tropical rain forests and is widely appreciated for its honey. Stingless bees account for approximately 30% of all pollination of the Brazilian Caatinga and Pantanal ecosystems and up to 90% of the pollination for many species of the Brazilian Atlantic Forest and the Amazon.

References

  1. ↑ Ratnieks, Francis L.W.; Heikki Helanterä (October 2009). "The evolution of extreme altruism and inequality in insect societies". Phil. Trans. R. Soc. B. 364 (1553): 3169–3179. doi:10.1098/rstb.2009.0129. PMC   2781879 . PMID   19805425.
  2. 1 2 Endler, Annett; Jürgen Liebig; Bert Hölldobler (February 2006). "Queen fertility, egg marking and colony size in the ant Camponotus floridanus". Behavioral Ecology and Sociobiology. 59 (4): 490–499. doi:10.1007/s00265-005-0073-0. S2CID   22084023.
  3. 1 2 Hartmann, Anne; Patrizia D'Ettorre; Graeme R. Jones; Jürgen Heinze (June 2005). "Fertility signaling—the proximate mechanism of worker policing in a clonal ant". Naturwissenschaften. 92 (6): 282–286. Bibcode:2005NW.....92..282H. doi:10.1007/s00114-005-0625-1. PMID   15770464. S2CID   11123443.
  4. 1 2 Helanterä, Heikki; Liselotte Sundström (June 2007). "Worker policing and nest mate recognition in the ant Formica fusca". Behavioral Ecology and Sociobiology. 61 (8): 1143–1149. doi:10.1007/s00265-006-0327-5. S2CID   9920557.
  5. 1 2 Oldroyd, Benjamin P.; Katherine E Osborne (July 1999). "The evolution of worker sterility in honeybees: the genetic basis of failure of worker policing". Proc. R. Soc. Lond. B. 266 (1426): 1335–1339. doi:10.1098/rspb.1999.0784. PMC   1690071 .
  6. 1 2 Stroeymeyt, Nathalie; Elisabeth Brunner; Jürgen Heinze (July 2007). ""Selfish worker policing" controls reproduction in a Temnothorax ant". Behavioral Ecology and Sociobiology. 61 (9): 1449–1457. doi:10.1007/s00265-007-0377-3. S2CID   3191624.
  7. 1 2 Ratnieks, Francis L.W.; P. Kirk Visscher (December 1989). "Worker policing in the honeybee". Nature. 342 (6251): 796–797. Bibcode:1989Natur.342..796R. doi:10.1038/342796a0. S2CID   4366903.
  8. 1 2 3 Wenseleers, Tom; Adam G. Hart; Francis L. W. Ratnieks (December 2004). "When Resistance Is Useless: Policing and the Evolution of Reproductive Acquiescence in Insect Societies" (PDF). The American Naturalist. 164 (6): E154–E167. doi:10.1086/425223. JSTOR   10.1086/425223. PMID   29641925. S2CID   4809642.
  9. ↑ Foster, Kevin R.; Francis L.W. Ratnieks (October 2000). "Social insects: Facultative worker policing in a wasp". Nature. 407 (6805): 692–693. Bibcode:2000Natur.407..692F. doi:10.1038/35037665. PMID   11048706. S2CID   4341647.
  10. ↑ Wenseleers, Tom; Francis L.W. Ratnieks (November 2006). "Enforced altruism in insect societies". Nature. 444 (7115): 50. Bibcode:2006Natur.444...50W. doi: 10.1038/444050a . PMID   17080081.
  11. ↑ Visscher, P. Kirk (1989). "A quantitative study of worker reproduction in honey bee colonies". Behavioral Ecology and Sociobiology. 25 (4): 247–254. doi:10.1007/bf00300050. JSTOR   4600337. S2CID   37903505.
  12. ↑ Halling, Luke A; Benjamin P. Oldroyd; Wandee Wattanachaiyingcharoen; Andrew B. Barron; Piyamas Nanork; Siriwat Wongsiri (2001). "Worker policing in the bee Apis florea". Behavioral Ecology and Sociobiology. 49 (6): 509–513. doi:10.1007/s002650100325. S2CID   9930323.
  13. 1 2 Oldroyd, Benjamin P.; Luke A. Halling; Gregory Good; Wandee Wattanachaiyingcharoen; Andrew B. Barron; Piyamas Nanork; Siriwat Wongsiri; Francis L. Ratnieks (2001). "Worker policing and worker reproduction in Apis cerana". Behavioral Ecology and Sociobiology. 50 (4): 371–377. doi:10.1007/s002650100376. S2CID   15558324.
  14. ↑ Zanette, L. R.; Miller, S. D.; Faria, C. M.; Almond, E. J.; Huggins, T. J.; Jordan, W. C.; Bourke, A. F. (December 2012). "Reproductive conflict in bumblebees and the evolution of worker policing". Evolution. 66 (12): 3765–3777. doi:10.1111/j.1558-5646.2012.01709.x. PMID   23206135. S2CID   36787898.
  15. ↑ D'Ettorre, Patrizia; Jürgen Heinze; Francis L W Ratnieks (July 2004). "Worker policing by egg eating in the ponerine ant Pachycondyla inversa". Proc Biol Sci. 271 (1546): 1427–1434. doi:10.1098/rspb.2004.2742. PMC   1691738 . PMID   15306343.
  16. ↑ Gobin, Bruno; J. Billen; C. Peeters (November 1999). "Policing behaviour towards virgin egg layers in a polygynous ponerine ant". Anim. Behav. 58 (5): 1117–1122. doi:10.1006/anbe.1999.1245. PMID   10564615. S2CID   16428974.
  17. ↑ Iwanishi, Satoru; Eisuke Hasegawab; Kyohsuke Ohkawaraa (September 2003). "Worker oviposition and policing behaviour in the myrmicine ant Aphaenogaster smythiesi japonica Forel". Animal Behaviour. 66 (3): 513–519. doi:10.1006/anbe.2003.2222. S2CID   28820297.
  18. ↑ Gadau, Jürgen; Fewell, Jennifer; Wilson, Edward O. (2009). Organization of Insect Societies: From Genome to Sociocomplexity. Harvard University Press. pp. 227–228. ISBN   978-0-674-03125-8.
  19. ↑ Liebig, Jürgen; Peeters, Christian; Höllldobler, Bert (1999). "Worker policing limits the number of reproductives in a ponerine ant". Proc. R. Soc. Lond. B. 266 (1431): 1865–1870. doi:10.1098/rspb.1999.0858. PMC   1690207 .
  20. ↑ Wenseleers, Tom; A. Tofilski; F. L. W. Ratnieks (2005). "Queen and worker policing in the tree wasp Dolichovespula sylvestris". Behavioral Ecology and Sociobiology. 58: 80–86. doi:10.1007/s00265-004-0892-4. S2CID   16813247.
  21. ↑ Foster, Kevin R. (2001). "Colony kin structure and male production in Dolichovespula wasps". Molecular Ecology. 10 (4): 1003–1010. doi:10.1046/j.1365-294X.2001.01228.x. PMID   11348506. S2CID   12009153.
  22. ↑ Saigo, T.; K. Tsuchida (December 2004). "Queen and worker policing in monogynous and monandrous colonies of a primitively eusocial wasp". Proc Biol Sci. 271 (Suppl 6): S509–S512. doi:10.1098/rsbl.2004.0238. PMC   1810092 . PMID   15801618.
  23. ↑ Foster, Kevin R.; Francis L. W. Ratnieks (January 2001). "Convergent evolution of worker policing by egg eating in the honeybee and common wasp". Proc Biol Sci. 268 (1463): 169–74. doi:10.1098/rspb.2000.1346. PMC   1088587 . PMID   11209887.
  24. ↑ Wenseleers, Tom; N. S. Badcock; K. Erven; A. Tofilski; F. S. Nascimento; A. G. Hart; T. A. Burke; M. E. Archer; F. L W. Ratnieks (June 2005). "A test of worker policing theory in an advanced eusocial wasp, Vespula rufa". Evolution. 59 (6): 1306–14. doi:10.1554/04-532. PMID   16050107. S2CID   15644821.
  25. ↑ Foster, K.R., Gulliver, J., Ratnieks, F.L.W. (2002). "Worker policing in the European hornet Vespa crabro". Insectes Sociaux. 49 (1): 41–44. doi:10.1007/s00040-002-8277-z. S2CID   45182961.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  26. ↑ Noda, Silvia Cristina Mari (2003). "Morphological and Physiological Caste Differences in Synoeca cyanea (Hymenoptero, Vespidae, Epiponini) According to the Ontogenetic Development of the Colonies". Sociobiology.
  27. ↑ Bonckaert, W.; Tofilski, A.; Nascimento, F.S.; Billen, J.; Ratnieks, F.L.W.; Wenseleers, T. (2001). "Co-occurrence of three types of egg policing in the Norwegian wasp Dolichovespsula wasp". Behavioral Ecology and Sociobiology. 65 (4): 633–640. doi:10.1007/s00265-010-1064-3. S2CID   2186614.
  28. ↑ Hartmann, Anne; J. Wantia; J.A. Torres; J. Heinze (October 2003). "Worker policing without genetic conflicts in a clonal ant". PNAS. 100 (22): 12836–12840. Bibcode:2003PNAS..10012836H. doi: 10.1073/pnas.2132993100 . PMC   240705 . PMID   14557542.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.