at many levels, from genes within thegenome to individuals in human societies.

Sociality has evolved about a dozen timesin the Hymenoptera — bees, wasps and ants.This is probably linked to their unusualmethod of sex determination, called haplo-diploidy. In the Hymenoptera, sexual repro-duction always produces female offspring,which are diploid — they have two sets ofchromosomes, just like humans of both sexes.Male hymenopterans, however, develop fromunfertilized eggs, and carry only one set ofchromosomes.These ‘haploid’males producesperm that are genetically identical. This is different from diploid animals, which shuffle

Murder, torture and imprisonment— these are the standard tools ofrepressive regimes. But if you

imagine that human societies have amonopoly on such tactics, think again.Social insects perfected the police state longbefore people got in on the act.

The workers in bee,ant and wasp coloniesforgo their own reproduction to raise thebrood of their queen. Such is a workerhoneybee’s devotion to the collective, shewill eviscerate herself by stinging any animalrash enough to attack the hive — a selfless-ness that has long fascinated naturalists.

We now know that workers receive theirevolutionary payoff through their related-ness to the monarch. As the queen’s daugh-ters, they share many genes with her otheroffspring. By caring for the regal brood, theyensure their own genetic inheritance.

But in any society, it is possible to prosperby breaking the rules. Worker honeybees dooccasionally lay their own eggs. As well asbeing against the queen’s interests, this putsthem at odds with the rest of the workforce.And in the late 1980s, evolutionary ecologistFrancis Ratnieks, now at the University ofSheffield,UK,showed that honeybee workersact as a ‘police force’that cracks down on mis-creants, eating their eggs1. “Worker policing is a mechanism by which a society resolves itsconflicts,” says Ratnieks. “I think it’s the bestexample of conflict resolution in nature.”

Policing by egg-eating is common to allspecies of Apis,not just the familiar domestichoneybee, A. mellifera2. And bees are notalone — the phenomenon has recently beenobserved in some species of wasp3 and in agroup of ants4. “It may be very widespread,”says Ratnieks.

But sometimes policing breaks down.Beehives occasionally dissolve into anarchy,as workers begin to reproduce en masse5.And a parasitic subspecies of honeybee iswreaking havoc in South Africa, destroyingcolonies by evading their police6. Evolution-ary biologists hope that studying such face-offs between authoritarianism and anarchywill provide a deeper understanding of thebalance between cooperation and selfishness

maternal and paternal chromosomes intotheir haploid sperm or eggs, giving infinitegenetic possibilities.

Family tiesIn human families, brothers and sisters eachshare half of their genes by commondescent — their coefficient of relatedness(r), to use the technical term, is 0.5. Thesame is true for parents and offspring. Forhalf-brothers or half-sisters, r is 0.25.

But haplodiploidy creates some bizarrefamily dynamics (see diagram, opposite). Amother’s relatedness to her son is 0.5, but consider the same relationship from his perspective and r rises to 1.0. Sister–brotherrelationships are also unequal: from the sister’s viewpoint,r is 0.25; from the brother’s,it is 0.5. Mothers and daughters have a relatedness of 0.5, whichever way you look at it,and r for two sisters is always 0.75.

These final two figures are key, becausethey mean that a female can pursue hergenetic interests more effectively by raisingher mother’s daughters rather than her own.This helps to explain why most females insocial Hymenoptera do not reproduce. If the

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Police supervisor: Francis Ratnieks was the first to describe honeybees’ disciplinary tactics.

The police stateOn the surface, beehives and ant nests seem tobe model societies, with each individual strivingfor the common good. But maintaining this socialorder sometimes calls for brutal tactics. JohnWhitfield reports.

A honeybee kills an a renegade worker’s egg, left.

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hurl themselves into a frenzy of egg-laying10.Honeybees are the most advanced insect

police state so far discovered. Wasp societiesare smaller and simpler, but give another elegant example of animal behaviour match-ing evolutionary theory. Again, it all comesdown to r. In some species of vespine wasp,the queen mates with just one male, whereasin others she mates repeatedly.Where queensare monogamous, and all workers are there-fore full sisters, the relatedness between aworker and a fellow worker’s son rises to0.375, compared with 0.125 for species inwhich the queen mates several times. In bothcases, workers are related to the queen’s sonsby an r of 0.25.

So workers should tolerate one another’segg-laying if their queen mates just once —because 0.375 is greater than 0.25 — butclamp down on renegade egg-layers if thequeen is more promiscuous. Sure enough,this is what Ratnieks and his Sheffield col-league Kevin Foster found when they com-pared different wasp species3. They even sawpolicing varying within species: in the saxonwasp (Dolichovespula saxonica), queens may

mate once or several times. Policing onlyoccurs in colonies with promiscuous queens11.

The fascist regimeIn some ponerine ants, both social structureand policing are much less sophisticated. Liv-ing in colonies of 100 or fewer individuals intropical forests, these ants have no rigid div-ide between queen and workers. Instead, allfemales have the potential to reproduce sexu-ally. But only one or a few do, because smallcolonies cannot support many breeders.

Breeding females are called gamergates,and head a pecking order that has olderworkers at the bottom and younger workers— wannabe gamergates — in the middle.This hierarchy is enforced by both egg-eatingand more brutal policing methods. If ayoung worker attempts to reproduce, she isspreadeagled by her fellows and kept immo-bilized for hours or even days. At the end ofher sentence, the best she can hope for is areduction in rank and loss of reproductivecapability.Often she is mutilated or killed4.

But ponerine gamergates do not enforcethe same iron control over their security appa-

queen is mother to the entire female work-force, they have little to gain by producingtheir own daughters.

In many species, workers are physicallyincapable of mating. And in honeybees, themonarchs exploit their subjects by matingwith up to 20 males; workers are thus tendingto young that are mostly half, not full, sisters,with a relatedness of 0.375 rather than 0.75.

Worker honeybees cannot rebel by mat-ing, but they can lay unfertilized eggs that willdevelop into sons, with a relatedness of 0.5.But r once again explains why other workersdestroy sneakily laid eggs. To most of theworkforce, another worker’s son is a half-nephew,with a relatedness of just 0.125,so themajority gain if workers’ eggs are culled andeveryone concentrates on raising the queen’sbrood. The result, as Ratnieks has found, is a police force so pervasive that it rivals the former East Germany’s infamous Stasi.

God save the queenAt the top of the security apparatus sits thequeen, producing pheromones that instructthe workers to carry on with the usual busi-ness of repression. Most loyally shut downtheir ovaries and keep watch for any subver-sives. In this way, the success of workerpolicing is conspicuous by the rarity oftransgressors. Only about 3 of the 30,000 orso worker honeybees in a typical hive havefunctioning ovaries, showing the inequalityof the struggle between a lone selfish workerand the rest of her caste. Although theserogue females can lay about 7% of a colony’smale eggs, effective policing means that only1 in 1,000 males has a worker for a mother7.

Indeed, workers’ eggs usually get eatenwithin hours of being laid1, betrayed by theirlack of a chemical badge unique to thequeen’s eggs8. Honeybee workers also seemto detect when their colleagues are about tobreak the rules, becoming aggressive toworkers with active ovaries9. But as withhuman dictatorships, the death of the leader can trigger major societal changes.When the queen dies, and her pheromonesno longer pervade the hive, the workers

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...but this ponerine ant is assaulted by fellow workers as a punishment for attempting to reproduce.

Numbers game: to determine the degree of relatedness between a worker and her nest-mates, followthe arrows, multiplying the values on each route and adding the products.

Coefficients of relatedness

Sister Half-sister Own son Son offull sister

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ratus as honeybee queens. From time to time,the ant police force stages a coup, deserting afailing ruler for a young pretender.“When thecurrent reproductive is declining in fertility,workers can change allegiance,”says ChristianPeeters of the Pierre and Marie Curie Univer-sity in Paris,who studies ponerine ants.

Even in honeybees, workers can over-throw their monarch’s reproductive monop-oly by activating their ovaries and toleratingone another’s eggs5. But such anarchic hivesare very rare. Ben Oldroyd of the University of Sydney, who studies the phenomenon,has sought out examples by placing adverts in beekeeping magazines. “We’ve had tworeports in seven years of advertising,”he says.

Oldroyd suspects that this is becausehoneybee anarchy requires a mutationaldouble whammy: worker bees must ignorethe pheromones that suppress their ovaries,and must also produce eggs that evade polic-ing, probably by counterfeiting the queen’schemical signal. Oldroyd’s team has shownthat ovary activation and egg-faking areunder separate genetic control: they havemanaged to breed both egg-laying workerswhose eggs are detected and destroyed bytheir fellows, and workers that do not layeggs, but do not destroy workers’ eggs trans-planted into the colony12.

Breeding for anarchyNaturally anarchic hives contain a fewdozen laying workers, and seem to functionwell. But by selective breeding, Oldroyd andhis colleagues have got the egg-layers up toabout 40% of the workforce. In these hives,breeding workers neglect their chores andthe hives become decadent to the point ofcollapse2. “They can barely feed themselves,and they do weird things like trying to raisequeens out of male larvae,” Oldroyd says.

These selectively bred anarchist hives havesome other odd features. Normal workerstransplanted into them may start laying13,which suggests that the queen’s pheromonesare weaker than normal. Most strangely,taking the queen out of an anarchic colony —which triggers worker egg-laying in normalhives — causes anarchic workers’ eggs to losetheir deceptive properties. They are eaten iftransplanted into a normal hive,says Oldroyd.

Oldroyd and his team are trying to identifythe genes that influence anarchic behaviour.

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If they can find them, it will provide a long-awaited mechanism for theories about animalconflict and cooperation. “Anarchy genes aregenes for selfishness, and anti-anarchy genesare genes for altruism,”says Oldroyd.

A honeybee hive’s policing can also besubverted from the outside. In January thisyear6, Ratnieks’s team described studies of aparasitic form of the Cape honeybee (A. m.capensis), a freeloader that over the pastdecade has cut a swathe through hives of theAfrican honeybee (A. m. scutellata) in north-ern South Africa.The parasitic Cape workersare like Oldroyd’s anarchists in that they dolittle work. But instead of laying haploidmale eggs, they produce diploid female eggsthat are genetic copies of themselves14.

Ratnieks and his colleagues have shownthat the African workers cannot distinguishthese eggs from those of their own queen —presumably because the Cape bees use somesort of chemical counterfeit. As a result, theinvaders’ numbers grow so quickly that thecolony is destroyed within months. TheCape bees then move on to another hive.

Formerly confined to the southernmostpart of South Africa, Cape honeybees wereprobably spread to the hotter north of thecountry,which is favoured by A. m. scutellata,by South African beekeepers who move theirhives around to catch the blooming seasonsof different flowers. This nomadic beekeep-ing style is still aiding the parasite’s spread.

The parasitic Cape bee now plagues anarea of South Africa about 400 by 200 kilo-

metres in size, stretching from Pretoria to theborder with Mozambique. The parasite’s ability to produce exact clones of itself, keep-ing its clique of selfish genes together,makes ita formidable fifth-columnist. “We spread thenet as far as we could, and everything we’vecaught has been the offspring of a single worker,” says Per Kryger of the University ofPretoria,who is monitoring the problem.

Bees not for keeps“Many beekeepers are losing 100% of theircolonies each year,” Kryger says. “The onlyreason they’re still in business is that theycollect swarms from the wild.” Kryger esti-mates that 50,000–100,000 wild A. m. scutel-lata swarms per year are lost to domestication— and subsequent parasitism. If the trendcontinues, he says, the local survival of theAfrican honeybee will be threatened.

Kryger is trying to work out whether theparasitic form is also common in the Capebee’s home range. He suspects that A. m.capensis may have evolved countermeasuresto deal with its seditious element. Exactlywhat these might be remains unclear — nor-mal Cape honeybees show policing behav-iour,but this is not especially pronounced15.

Studies of such conflicts may also yieldinsights into other aspects of biology, andeven the social sciences. Laurence Hurst, anevolutionary geneticist at the University ofBath, UK, draws parallels between workerpolicing and the mechanisms that genomeshave evolved to prevent individual genesfrom inserting themselves into a dispropor-tionate number of sperm or eggs.

“Worker policing is a nice case history forexamining the conflicts present in any socialstructure,”Hurst says.He believes that it maybe possible to derive theoretical models tocapture accurately the dynamics of conflictin everything from genomes, through socialinsects, to human society.“There are impor-tant differences between different systems,but there are also abstract features that unitethem.It isn’t just a metaphor,”he says. ■

John Whitfield works in Nature’s news syndication team.

1. Ratnieks, F. L. W. & Visscher, P. K. Nature 342, 796–797 (1989).

2. Barron, A. W., Oldroyd, B. P. & Ratnieks, F. L. W. Behav. Ecol.

Sociobiol. 50, 199–208 (2001).

3. Foster, K. R. & Ratnieks, F. L. W. Behav. Ecol. Sociobiol. 50, 1–8

(2001).

4. Monnin, T. & Ratnieks, F. L. W. Behav. Ecol. Sociobiol. 50,

97–108 (2001).

5. Oldroyd, B. P., Smolenski, A. J., Cornuet, J. M. & Crozier, R. H.

Nature 371, 749 (1994).

6. Martin, S. J., Beekman, M., Wossler, T. C. & Ratnieks, F. L. W.

Nature 415, 163–165 (2002).

7. Visscher, P. K. Behav. Ecol. Sociobiol. 39, 237–244 (1996).

8. Ratnieks, F. L. W. J. Apic. Res. 34, 31–37 (1995).

9. Visscher, P. K. & Dukas, R. Anim. Behav. 49, 542–544 (1995).

10.Page, R. E. & Erickson, E. H. Behav. Ecol. Sociobiol. 23, 117–126

(1988).

11.Foster, K. R. & Ratnieks, F. L. W. Nature 407, 692–693 (2000).

12.Oldroyd, B. P. & Osborne, K. E. Proc. R. Soc. Lond. B. 266,

1335–1339 (1999).

13.Barron, A. B. & Oldroyd, B. P. Behav. Ecol. Sociobiol. 49, 214–219

(2001).

14.Verma, S. & Ruttner, F. Apidologie 14, 41–57 (1983).

15.Moritz, R. F. A., Kryger, P. & Allsopp, M. H. Behaviour 136,

1079–1092 (1999).Insect invasion: an African honeybee (right) unwittingly feeds one of an army of parasitic Cape bees.

Point of order: Ben Oldroyd has bred anarchicbee colonies, but this is very rare in nature.

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