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.     

Worker policing in the German wasp Vespula germanica

In some ants, bees, and wasps, workers kill or "police" maleeggs laid by other workers in order to maintain the reproductiveprimacy of the queen. Kin selection theory predicts that multiplemating by the queen is one factor that can selectively favorworker policing. This is because when the queen is mated tomultiple males, workers are more closely related to the queen'ssons than to the sons of other workers. Earlier work has suggestedthat reproductive patterns in the German wasp Vespula germanicamay contradict this theory, because in some colonies a largefraction of the adult males were inferred to be the workers'sons, despite the effective queen mating frequency being greaterthan 2 (2.4). In the present study, we reexamine the V. germanicacase and show that it does support the theory. First, geneticanalysis confirms that the effective queen mating frequencyis high, 2.9, resulting in workers being more related to thequeen's sons than to other workers' sons. Second, behavioralassays show that worker-laid eggs are effectively killed byother workers, despite worker-laid eggs having the same intrinsicviability as queen-laid ones. Finally, we estimate that approximately58.4% of the male eggs but only 0.44% of the adult males areworker derived in queenright colonies, consistent with workerreproduction being effectively policed.     

Towards greater realism in inclusive fitness models: the case of worker reproduction in insect societies

The conflicts over sex allocation and male production in insect societies have long served as an important test bed for Hamilton''s theory of inclusive fitness, but have for the most part been considered separately. Here, we develop new coevolutionary models to examine the interaction between these two conflicts and demonstrate that sex ratio and colony productivity costs of worker reproduction can lead to vastly different outcomes even in species that show no variation in their relatedness structure. Empirical data on worker-produced males in eight species of Melipona bees support the predictions from a model that takes into account the demographic details of colony growth and reproduction. Overall, these models contribute significantly to explaining behavioural variation that previous theories could not account for.     

意大利蜜蜂工蜂监督研究进展

在许多膜翅目中营社会性生活的昆虫群体里,亲属辨认、监督与优惠对昆虫个体和群体繁衍都非常重要。作者在国内外相关研究的基础上,对意大利蜜蜂Apismellifera蜂群中工蜂监督产生的理论依据、监督现象、监督效率、监督机理等研究进展进行综合论述,并对今后的研究趋势作扼要介绍。     

A quantitative study of worker reproduction in queenright colonies of the Cape honey bee, Apis mellifera capensis

Reproduction by workers is rare in honey bee colonies that have an active queen. By not producing their own offspring and preventing other workers from producing theirs, workers are thought to increase their inclusive fitness due to their higher average relatedness towards queen-produced male offspring compared with worker-produced male offspring. But there is one exception. Workers of the Cape honey bee, Apis mellifera capensis, are able to produce diploid female offspring via thelytokous parthenogenesis and thus produce clones of themselves. As a result, worker reproduction and tolerance towards worker-produced offspring is expected to be more permissive than in arrhenotokous (sub)species where worker offspring are male. Here we quantify the extent to which A. m. capensis workers contribute to reproduction in queenright colonies using microsatellite analyses of pre-emergent brood. We show that workers produced 10.5% of workers and 0.48% of drones. Most of the workers' contribution towards the production of new workers coincided with the colonies producing new queens during reproductive swarming.     

Colony kin structure and male production in Dolichovespula wasps

In annual hymenopteran societies headed by a single outbred queen, paternity (determined by queen mating frequency and sperm use) is the sole variable affecting colony kin structure and is therefore a key predictor of colony reproductive characteristics. Here we investigate paternity and male production in five species of Dolichovespula wasps. Twenty workers from each of 10 colonies of each of five species, 1000 workers in total, were analysed at three DNA microsatellite loci to estimate paternity. To examine the relationship between kin structure and reproductive behaviour, worker ovary activation was assessed by dissection and the maternal origin of adult males was assessed by DNA microsatellites. Effective paternity was low in all species (D. media 1.08, D. maculata 1.0, D. sylvestris 1.15, D. norwegica 1.08 and D. saxonica 1.35), leading to the prediction of queen-worker conflict over male production. In support of this, workers with full-size eggs in their ovaries (four out of five species) and adult males that were workers' sons (all five species) were found in queenright colonies. However, workers were only responsible for a minority of male production (D. media 7.4%, D. maculata 20.9%, D. sylvestris 9.8%, D. norwegica 2.6% and D. saxonica 34.6%) suggesting that the queen maintains considerable reproductive power over the workers. Kin structure and reproductive conflict in Dolichovespula contrast with their sister group Vespula. Dolichovespula is characterized by low paternity, worker reproduction, and queen-worker conflict and Vespula by high paternity, effective worker policing and absence of worker reproduction. The trend revealed by this comparison is as predicted by kin selection theory suggesting that colony kin structure has been pivotal in the evolution of the yellowjacket wasps.     

Queen-controlled sex ratios and worker reproduction in the bumble bee Bombus hypnorum,as revealed by microsatellites

Social insect colonies provide model systems for the examination of conflicts among parties with different genetic interests. As such, they have provided the best tests of inclusive fitness theory. However, much remains unknown about in which party's favour such conflicts are resolved, partly as a result of the only recent advent of the molecular tools needed to examine the outcome of these conflicts. Two key conflicts in social insect colonies are over control of the reproductive sex ratio and the production of male offspring. Most studies have examined only one of these conflicts but in reality they occur in tandem and may influence each other. Using microsatellite analyses, the outcome of conflict over sex ratios and male production was examined in the bumble bee, Bombus hypnorum. The genotypes were determined for mother queens, their mates and males for each of 10 colonies. In contrast to other reports of mating frequency in this species, all of the queens were singly mated. The population sex ratio was consistent with queen control, suggesting that queens are winning this conflict. In contrast, workers produced over 20% of all males in queen-right colonies, suggesting that they are more effective in competing over male-production. Combining these results with previous work, it is suggested that worker reproduction is a labile trait that may well impose only small costs on queen fitness.     

Colony size,social complexity and reproductive conflict in social insects

The broad limits of mature colony size in social insect species are likely to be set by ecological factors. However, any change in colony size has a number of important social consequences. The most fundamental is a change in the expected reproductive potential of workers. If colony size rises, workers experience a fall in their chances of becoming replacement reproductives and, it is shown, increasing selection for mutual inhibition of one another's reproduction (worker policing). As workers’ reproductive potential falls, the degree of dimorphism between reproductive and worker castes (morphological skew) can rise. This helps explain why small societies have low morphological skew and tend to be simple in organization, whereas large societies have high morphological skew and tend to be complex. The social consequences of change in colony size may also alter colony size itself in a process of positive feedback. For these reasons, small societies should be characterized by intense, direct conflict over reproduction and caste determination. By contrast, conflict in large societies should predominantly be over brood composition, and members of these societies should be relatively compliant to manipulation of their caste. Colony size therefore deserves fuller recognition as a key determinant, along with kin structure, of social complexity, the reproductive potential of helpers, the degree of caste differentiation, and the nature of within-group conflict.     

Worker reproduction and policing in insect societies: an ESS analysis

Insect societies are vulnerable to exploitation by workers who reproduce selfishly rather than help to rear the queen's offspring. In most species, however, only a small proportion of the workers reproduce. Here, we develop an evolutionarily stable strategy (ESS) model to investigate factors that could explain these observed low levels of reproductive exploitation. Two key factors are identified: relatedness and policing. Relatedness affects the ESS proportion of reproductive workers because laying workers generally work less, leading to greater inclusive fitness costs when within-colony relatedness is higher. The second key factor is policing. In many species, worker-laid eggs are selectively removed or 'policed' by other workers or the queen. We show that policing not only prevents the rearing of worker-laid eggs but can also make it unprofitable for workers to lay eggs in the first place. This can explain why almost no workers reproduce in species with efficient policing, such as honeybees, Apis, and the common wasp, Vespula vulgaris, despite relatively low relatedness caused by multiple mating of the mother queen. Although our analyses focus on social insects, the conclusion that both relatedness and policing can reduce the incentive for cheating applies to other biological systems as well.     

Colony fusion and worker reproduction after queen loss in army ants

Theory predicts that altruism is only evolutionarily stable if it is preferentially directed towards relatives, so that any such behaviour towards seemingly unrelated individuals requires scrutiny. Queenless army ant colonies, which have anecdotally been reported to fuse with queenright foreign colonies, are such an enigmatic case. Here we combine experimental queen removal with population genetics and cuticular chemistry analyses to show that colonies of the African army ant Dorylus molestus frequently merge with neighbouring colonies after queen loss. Merging colonies often have no direct co-ancestry, but are on average probably distantly related because of overall population viscosity. The alternative of male production by orphaned workers appears to be so inefficient that residual inclusive fitness of orphaned workers might be maximized by indiscriminately merging with neighbouring colonies to increase their reproductive success. We show that worker chemical recognition profiles remain similar after queen loss, but rapidly change into a mixed colony Gestalt odour after fusion, consistent with indiscriminate acceptance of alien workers that are no longer aggressive. We hypothesize that colony fusion after queen loss might be more widespread, especially in spatially structured populations of social insects where worker reproduction is not profitable.     

Anarchy in the UK: Detailed genetic analysis of worker reproduction in a naturally occurring British anarchistic honeybee,Apis mellifera,colony using DNA microsatellites

Anarchistic behaviour is a very rare phenotype of honeybee colonies. In an anarchistic colony, many workers' sons are reared in the presence of the queen. Anarchy has previously been described in only two Australian colonies. Here we report on a first detailed genetic analysis of a British anarchistic colony. Male pupae were present in great abundance above the queen excluder, which was clearly indicative of extensive worker reproduction and is the hallmark of anarchy. Seventeen microsatellite loci were used to analyse these male pupae, allowing us to address whether all the males were indeed workers' sons, and how many worker patrilines and individual workers produced them. In the sample, 95 of 96 of the males were definitely workers' sons. Given that approximately 1% of workers' sons were genetically indistinguishable from queen's sons, this suggests that workers do not move any queen-laid eggs between the part of the colony where the queen is present to the area above the queen excluder which the queen cannot enter. The colony had 16 patrilines, with an effective number of patrilines of 9.85. The 75 males that could be assigned with certainty to a patriline came from 7 patrilines, with an effective number of 4.21. They were the offspring of at least 19 workers. This is in contrast to the two previously studied Australian naturally occurring anarchist colonies, in which most of the workers' sons were offspring of one patriline. The high number of patrilines producing males leads to a low mean relatedness between laying workers and males of the colony. We discuss the importance of studying such colonies in the understanding of worker policing and its evolution.     

Colony structure of a slavemaking ant. I. Intracolony relatedness, worker reproduction, and polydomy

Colony and population structure of the obligate slavemaker ant Protomognathus americanus was analyzed via four nuclear microsatellite loci and mitochondrial DNA (mtDNA) markers. Colonies of P. americanus usually contain a single queen, and here we show that she is singly inseminated. Nestmate workers are generally full sisters and their relatedness does not deviate from the expected value of 0.75. Even though colonies were strictly monogynous, we were able to infer that colony takeover by related queens was common and queen replacement by unrelated queens was rare. Polydomy is widespread, with neighboring nests having the same genetic composition. Although we found no evidence of population viscosity or inbreeding from nuclear markers, mtDNA markers provided evidence for small-scale genetic structuring. Haplotype structuring and takeover by related queens suggest philopatry of newly mated queens. In this species, workers reproduce in queenright and queenless nests and worker reproduction accounts for more than 70% of all males. Although sex-ratio theory points to slavemaking ants as important systems for studying queen-worker conflict, our results indicate no basis for such conflict in P. americanus, because extensive worker reproduction generates shifts in relatedness values. Rather, the dual effects of independent polydomous nest units and local resource competition among queens produce male-biased allocation ratios in this species.     

Chemical correlates of reproduction and worker policing in a myrmicine ant

In a number of wasps, bees, and in particular ponerine ants, quantitative and qualitative variation in the profile of cuticular hydrocarbons is associated with variation in fecundity and is likely to serve for communicating the reproductive status of an individual. Here, we demonstrate that the chemical profile on the cuticle of fertile workers and queens of the myrmicine ant Temnothorax unifasciatus is different from that of non-reproductive workers. Fertility and apparently also cuticular signatures are reversible under the influence of policing by worker aggression. Though no policing by egg-eating occurs in this species, queen and worker laid eggs also differed in their chemical profile.     

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. Received 30 January 2006; revised 2 May 2006; accepted 5 May 2006.     

Local dynamics of worker activity of the invasive Vespula germanica and V. vulgaris (Hymenoptera: Vespidae) wasps in Argentina

1. The abundance of insects depends essentially on the reproductive success of individuals. In social insects, however, the abundance of sterile workers outside a nest depends on colony size but is also determined by ontogeny, nest demands, and local environmental factors. For invasive social wasps, the drivers of worker abundance are important because they determine the impact that these species have on the native systems, people, and their goods. 2. The aim of the present study was to understand the relative importance of endogenous and exogenous factors on the abundance of workers of populations of Vespula spp., by analysing 12 years of trap captures in NW Patagonia. This is the first attempt to model the activity levels of invasive Vespula spp. wasps over time in Argentina. 3. It was shown that between years, the worker activity of both vespids presents fluctuations, and that of V. germanica is determined by the spring mean temperatures. Within the flight season, V. germanica worker activity is affected by the relative abundance of workers in that year, whereas for V. vulgaris, activity it is affected by the relative abundance of both species that year. We found no relationship between individual weather variables and activity within a flight season for both wasps. 4. The patterns observed for Argentina are similar to those observed in all invaded temperate areas where Vespula spp. are established. This study provides useful information to understand the driving factors that affect Vespula spp. worker activity in Argentina. This could be a necessary step to develop plans to manage these invasive social insects.     

Kin selection, relatedness, and worker control of reproduction in a large-colony epiponine wasp, Brachygastra mellifica

Hamilton's kin selection theory predicts conflicts of interestamong relatives, even within highly cooperative social insectsocieties. Because workers are the most numerous caste, collectiveworker interests may be an important force in determining theoutcome of conflicts. In this study, we used genotypes fromtwo DNA microsatellite loci to show that two kinds of collectiveworker interests are satisfied in Brachygastra mellifica, amember of the multiqueen epiponine wasps. First, from the highrelatedness of queens (0.66) and the fact that queens are singlymated (shown by genotyping their stored sperm), we calculatedthat new queens are reared in colonies with a harmonic meanof 1.2 old queens, whereas males are reared in colonies withmuch higher queen numbers. This split sex ratio result is predictedunder worker control. It matches other studies of epiponines,but B. mellifica has much larger mature colonies (averaging7951 adults) with many more queens (averaging 398), showingthe pattern holds for large-colony species. Second, we reportthe first genetic data on parentage of males in epiponines andshow that these are also consistent with collective worker interests.Workers are on average significantly more related to queensthan to other workers (r = .37 versus .23) and should thereforesuppress each other and allow the queens to lay haploid (male)eggs. Though many workers have developed ovaries and could layeggs, the genetic analyses showed that most or all males comefrom queens.     

The evolution of extreme altruism and inequality in insect societies

In eusocial organisms, some individuals specialize in reproduction and others in altruistic helping. The evolution of eusociality is, therefore, also the evolution of remarkable inequality. For example, a colony of honeybees (Apis mellifera) may contain 50 000 females all of whom can lay eggs. But 100 per cent of the females and 99.9 per cent of the males are offspring of the queen. How did such extremes evolve? Phylogenetic analyses show that high relatedness was almost certainly necessary for the origin of eusociality. However, even the highest family levels of kinship are insufficient to cause the extreme inequality seen in e.g. honeybees via ‘voluntary altruism’. ‘Enforced altruism’ is needed, i.e. social pressures that deter individuals from attempting to reproduce. Coercion acts at two stages in an individual''s life cycle. Queens are typically larger so larvae can be coerced into developing into workers by being given less food. Workers are coerced into working by ‘policing’, in which workers or the queen eat worker-laid eggs or aggress fertile workers. In some cases, individuals rebel, such as when stingless bee larvae develop into dwarf queens. The incentive to rebel is strong as an individual is the most closely related to its own offspring. However, because individuals gain inclusive fitness by rearing relatives, there is also a strong incentive to ‘acquiesce’ to social coercion. In a queenright honeybee colony, the policing of worker-laid eggs is very effective, which results in most workers working instead of attempting to reproduce. Thus, extreme altruism is due to both kinship and coercion. Altruism is frequently seen as a Darwinian puzzle but was not a puzzle that troubled Darwin. Darwin saw his difficulty in explaining how individuals that did not reproduce could evolve, given that natural selection was based on the accumulation of small heritable changes. The recognition that altruism is an evolutionary puzzle, and the solution was to wait another 100 years for William Hamilton.     

The evolution of queen control over worker reproduction in the social Hymenoptera

A trademark of eusocial insect species is reproductive division of labor, in which workers forego their own reproduction while the queen produces almost all offspring. The presence of the queen is key for maintaining social harmony, but the specific role of the queen in the evolution of eusociality remains unclear. A long‐discussed scenario is that a queen either behaviorally or chemically sterilizes her workers. However, the demographic and ecological conditions that enable such manipulation are still debated. We study a simple model of evolutionary dynamics based on haplodiploid genetics. Our model is set in the commonly observed case where workers have lost the ability to lay female (diploid) eggs by mating, but retain the ability to lay male (haploid) eggs. We consider a mutation that acts in a queen, causing her to control the reproductive behavior of her workers. Our mathematical analysis yields precise conditions for the evolutionary emergence and stability of queen‐induced worker sterility. These conditions do not depend on the queen's mating frequency. We find that queen control is always established if it increases colony reproductive efficiency, but can evolve even if it decreases colony efficiency. We further derive the conditions under which queen control is evolutionarily stable against invasion by mutant workers who have recovered the ability to lay male eggs.     

Determination of the cost of worker reproduction via diminished life span in the ant Diacamma sp

Workers of social Hymenoptera can usually produce male offspring, but rarely do so in the presence of a queen despite the potential individual fitness benefit. Various mechanisms have been hypothesized to regulate worker reproduction, including avoiding the colony-level cost of worker reproduction. However, firm quantitative evidence is lacking to support that hypothesis. Here, we accurately quantified this cost by studying an ant species (Diacamma sp.) in which worker reproduction is rare in the presence of the gamergate (the functional queen). A series of experiments to manipulate worker-gamergate contact revealed that short-term brood-production efficiency is not changed by the presence of worker reproduction. However, when workers reproduce, their average life span is reduced to between 74% and 88% of that in the absence of reproduction, indicating a long-term cost to the colony. In theory, this cost can explain the policing of worker reproduction under a queen-single mating system, but the cost does not appear to be high enough to stop worker reproduction. When contact with the gamergate is lost, it is only the nonreproductive workers whose life span was reduced; the reproductive workers lived as long as nonorphaned workers. We suggest that an increased workload can account for the reduction in life span better than a trade-off between reproduction and longevity.