蜜蜂群内生殖分工体系的形成及其维持

本文对蜜蜂群内生殖分工体系的形成及其维持机制进行综述。蜜蜂群体具有完善的劳动分工(包括生殖分工)体系,蜂王垄断生殖权力,而工蜂生殖器官发育不完全,在蜂王信息素和幼虫信息素的作用下产卵受到抑制。蜂王的多雄交配机制降低了群内个体间的亲缘关系,但也促进了工蜂间相互监督机制的形成。工蜂间的相互监督,结合蜂王和幼虫信息素对工蜂卵巢发育的影响,解决了蜂王与工蜂、工蜂与工蜂间的生殖利益冲突,保障了蜂群内的生殖分工体系,提高了群体效率,维护了蜂群的真社会性。     

Queen-worker conflicts over male production and sex allocation in a primitively eusocial wasp

Abstract In a colony headed by a single monandrous foundress, theories predict that conflicts between a queen and her workers over both sex ratio and male production should be intense. If production of males by workers is a function of colony size, this should affect sex ratios, but few studies have examined how queens and workers resolve both conflicts simultaneously. We conducted field and laboratory studies to test whether sex-ratio variation can be explained by conflict over male production between queen and workers in the primitively eusocial wasp Polistes chinensis antennalis.
Worker oviposition rate increased more rapidly with colony size than did queen oviposition. Allozyme and micro-satellite markers revealed that the mean frequency of workers' sons among male adults in queen-right colonies was 0.39 ± 0.08 SE (n = 22). Genetic relatedness among female nestmates was high (0.654–0.796), showing that colonies usually had a single, monandrous queen. The mean sex allocation ratio (male investment/male and gyne investments) of 46 queen-right colonies was 0.47 ± 0.02, and for 25 orphaned colonies was 0.86 ± 0.04. The observed sex allocation ratio was likely to be under queen control. For queen-right colonies, the larger colonies invested more in males and produced reproductives protandrously and/or simultaneously, whereas the smaller colonies invested more in females and produced reproductives protogynously. Instead of positive relationships between colony size and worker oviposition rate, the frequency of workers' sons within queen-right colonies did not increase with colony size. These results suggest that queens control colony investment, even though they allow worker oviposition in queen-right colonies. Eggs laid by workers may be policed by the queen and/or fellow workers. Worker oviposition did not influence the outcome of sex allocation ratio as a straightforward function of colony size.     

No evidence that reproductive bumblebee workers reduce the production of new queens

Kin selection theory predicts potential conflict between queen and workers over male parentage in hymenopteran societies headed by one, singly mated queen, because each party is more closely related to its own male offspring. In ‘late-switching’ colonies of the bumblebee Bombus terrestris, i.e. colonies whose queens lay haploid eggs relatively late in the colony cycle, workers start to lay male eggs shortly after the queen lays the female eggs that will develop into new queens. It has been hypothesized that this occurs because workers recognize, via a signal given by the queen instructing female larvae to commence development as queens, that egg laying is now in their kin-selected interest. This hypothesis assumes that aggressive behaviour in egg-laying workers does not substantially reduce the production of new queens, which would decrease the workers' fitness payoff from producing males. We tested the hypothesis that reproductive activity inB. terrestris workers does not reduce the production of new queens. We used microsatellite genotyping to sex eggs and hence to select eight size-matched pairs of ‘late-switching’ colonies from a set of commercial colonies. From one colony of each pair we removed every egg-laying or aggressive worker observed. From the other colony, we simultaneously removed a nonegg-laying, nonaggressive worker. Removed workers were replaced with young workers from separate colonies at equal frequencies within the pair. There was no significant difference in queen productivity between colonies with reduced or normal levels of egg-laying or aggressive workers. Therefore, as predicted, reproductive B. terrestris workers did not significantly reduce the production of new queens.     

Queen–worker ratio affects reproductive skew in a socially polymorphic ant

The partitioning of reproduction among individuals in communally breeding animals varies greatly among species, from the monopolization of reproduction (high reproductive skew) to similar contribution to the offspring in others (low skew). Reproductive skew models explain how relatedness or ecological constraints affect the magnitude of reproductive skew. They typically assume that individuals are capable of flexibly reacting to social and environmental changes. Most models predict a decrease of skew when benefits of staying in the group are reduced. In the ant Leptothorax acervorum, queens in colonies from marginal habitats form dominance hierarchies and only the top‐ranking queen lays eggs (“functional monogyny”). In contrast, queens in colonies from extended coniferous forests throughout the Palaearctic rarely interact aggressively and all lay eggs (“polygyny”). An experimental increase of queen:worker ratios in colonies from low‐skew populations elicits queen–queen aggression similar to that in functionally monogynous populations. Here, we show that this manipulation also results in increased reproductive inequalities among queens. Queens from natural overwintering colonies differed in the number of developing oocytes in their ovaries. These differences were greatly augmented in queens from colonies with increased queen:worker ratios relative to colonies with a low queen:worker ratio. As assumed by models of reproductive skew, L. acervorum colonies thus appear to be capable of flexibly adjusting reproductive skew to social conditions, yet in the opposite way than predicted by most models.     

Why acquiesce? Worker reproductive parasitism in the Eastern honeybee (Apis cerana)

Most societies are vulnerable to rogue individuals that pursue their own interests at the expense of the collective entity. Societies often protect themselves from selfish behaviour by ‘policing’, thereby enforcing the interests of the collective over those of individuals. In insect societies, for example, selfish workers can activate their ovaries and lay eggs, exploiting the collective brood rearing system for individual benefit. Policing, usually in the form of oophagy of worker‐laid eggs, controls selfish behaviour. Importantly, once an effective system of policing has evolved, the incentive for personal reproduction is lost, and ‘reproductive acquiescence’ in which ovary activation is rare or absent is predicted to evolve. Studies of social Hymenoptera have largely supported the prediction of worker ‘acquiescence’; workers of most species where policing is well developed have inactive ovaries. However, the eastern honeybee Apis cerana appears to be an exception. A. cerana colonies are characterized by highly efficient policing, yet about 5% of workers have active ovaries, even when a queen is present. This suggests that the evolution of acquiescence is incomplete in A. cerana. We regularly sampled male eggs and pupae from four A. cerana colonies. Workers had high levels of ovary activation overall (11.7%), and 3.8% of assignable male eggs and 1.1% of assignable male pupae were worker‐laid. We conclude that workers with active ovaries lay their eggs, but these rarely survive to pupation because of intense policing. We then used our findings as well as previously published data on A. cerana and A. mellifera to redo the meta‐analysis on which reproductive acquiescence theory is based. Including data on both species did not affect the relationship between effectiveness of policing and levels of worker reproduction. Their inclusion did, however, seriously weaken the relationship between relatedness among workers and levels of worker reproduction. Our work thus suggests that relatedness among workers does not affect the probability that workers will attempt to reproduce, but that it is coercion by peers that limits worker reproduction.     

It's good to be queen: classically eusocial colony structure and low worker fitness in an obligately social sweat bee

Lasioglossum malachurum, a bee species common across much of Europe, is obligately eusocial across its range but exhibits clear geographic variation in demography and social behaviour. This variation suggests that social interactions between queens and workers, opportunities for worker oviposition, and patterns of relatedness among nest mates may vary considerably, both within and among regions. In this study, we used three microsatellite loci with 12-18 alleles each to examine the sociogenetic structure of colonies from a population at Agios Nikolaos Monemvasias in southern Greece. These analyses reveal that the majority of colonies exhibit classical eusocial colony structure in which a single queen mated to a single male monopolizes oviposition. Nevertheless, we also detect low rates of multiqueen nest founding, occasional caste switching by worker-destined females, and worker oviposition of both gyne and male-producing eggs in the final brood. Previous evidence that the majority of workers show some ovarian development and a minority (17%) have at least one large oocyte contrasts with the observation that only 2-3% of gynes and males (the so-called reproductive brood) are produced by workers. An evaluation of the parameters of Hamilton's Rule suggests that queens benefit greatly from the help provided by workers but that workers achieve greater fitness by provisioning and laying their own eggs rather than by tending to the queen's eggs. This conflict of interest between the queen and her workers suggests that the discrepancy between potential and achieved worker oviposition is due to queen interference. Comparison of relatedness and maternity patterns in the Agios Nikolaos Monemvasias population with those from a northern population near Tübingen, Germany, points to a north-south cline of increasingly effective queen control of worker behaviour.     

Colony stage and not facultative policing explains pattern of worker reproduction in the Saxon wasp

Inclusive fitness theory predicts that in colonies of social Hymenoptera headed by a multiple‐mated queen, workers should benefit from policing eggs laid by other workers. Foster & Ratnieks provided evidence that in the vespine wasp Dolichovespula saxonica, workers police other workers’ eggs only in colonies headed by a multiple‐mated queen, but not in those headed by a single‐mated one. This conclusion, however, was based on a relatively small sample size, and the original study did not control for possible confounding variables such as the seasonal colony progression of the nests. Our aim, therefore, was to reinvestigate whether or not facultative worker policing occurs in D. saxonica. Remarkably, our data show that in the studied Danish population, there was no correlation between worker–worker relatedness and the percentage of worker‐derived males. In addition, we show that variability in cuticular hydrocarbon profiles among the workers did not significantly correlate with relatedness and that workers therefore probably did not have sufficient information on queen mating frequency from the workers’ cuticular hydrocarbon profiles. Hence, there was no evidence that workers facultatively policed other workers’ eggs in response to queen mating frequency. Nevertheless, our data do show that the seasonal progression of the nest and the location in which the males were reared both explain the patterns of worker reproduction found. Overall, our results suggest that the earlier evidence for facultative worker policing in D. saxonica may have been caused by accidental correlations with certain confounding variables, or, alternatively, that there are large interpopulation differences in the expression of worker policing.     

Kin structure and colony male reproduction in the hornet<Emphasis Type="Italic"> Vespa crabro</Emphasis> (Hymenoptera: Vespidae)

We estimated queen mating frequency, genetic relatedness among workers, and worker reproduction in Vespa crabro flavofasciata using microsatellite DNA markers. Of 20 colonies examined, 15 contained queens inseminated by a single male, 3 colonies contained queens inseminated by two males, and 2 colonies contained queens inseminated by three males. The genetic relatedness among workers was estimated to be 0.73±0.003 (mean±SE). For this high relatedness, kin selection theory predicts a potential conflict between queens and workers over male production. To verify whether males are derived from queens or workers, 260 males from 13 colonies were genotyped at four microsatellite loci. We found that all of the males were derived from the queens. This finding was further supported by the fact that only 33 of 2,990 workers dissected had developed ovaries. These workers belonged to 2 of the 20 colonies. There was no relationship between queen mating frequency and worker reproduction, and no workers produced male offspring in any of the colonies. These results suggest that male production dominated by queens in V. crabro flavofasciata is possibly due to worker policing.     

Worker policing persists in a hopelessly queenless honey bee colony (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Summary In queenright colonies of Apis mellifera, worker policing normally eliminates worker-laid eggs thereby preventing worker reproduction. However, in queenless colonies that have failed to rear a replacement queen, worker reproduction is normal. Worker policing is switched off, many workers have active ovaries and lay eggs, and the colony rears a last batch of male brood before dying out. Here we report a colony which, when hopelessly queenless, did not stop policing although a high proportion of workers had active ovaries (12.6%) and many eggs were laid. However, all these eggs and also worker-laid eggs transferred from another colony were policed. This unusual pattern was repeated eight weeks later by a second queenless colony made using worker bees from the same mother colony, which strongly suggests genetic determination.Received 19 May 2003; revised 11 September 2003; accepted 23 September 2003.     

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.     

Workers of the primitively eusocial wasp <Emphasis Type="Italic">Ropalidia marginata</Emphasis> do not perceive their queen across a wire mesh partition

Queens of primitively eusocial wasps generally have active and behaviourally dominant queens who use physical aggression to suppress worker reproduction. Although a Ropalidia marginata queen is strikingly docile and behaviourally non-dominant, she is completely successful in maintaining reproductive monopoly. R. marginata queens must achieve such reproductive monopoly by some means other than overt physical aggression. Upon loss or removal of the queen, one of the workers (referred to as the potential queen) becomes extremely aggressive and will eventually go on to become the next queen of the colony, if the original queen is not returned. The fact that potential queens are not discernible in the presence of the queen but become obvious within minutes after removal of the queen raises the question of how workers in general and the potential queens in particular, perceive the presence or absence of their queens. Here, we have conducted experiments in which we separate half of the workers from their queen by a wire mesh screen and study their behavioural response to such separation. We demonstrate that the presence of the queen is not perceived across the wire mesh screen, which suggests that if the queen uses a pheromone to signal her presence, then that pheromone is not very volatile.     

Worker reproduction in Formica ants

A potential tragedy of the commons arises in social-insect colonies where workers are fertile if egg-laying workers decrease their contribution to other tasks. We studied worker ovary development and egg laying in relation to kin structure, colony size, and the presence of a queen in nine species (11 populations) of Formica ants. Workers were highly fertile and laid eggs in the presence of a queen in five out of the seven species where egg samples were obtained. Worker fertility correlated neither with colony size nor with kin structure, which suggests that colony-level costs and efficiency of policing precede relatedness as the most important conflict determinant. We conclude that careful quantification of the costs of worker reproduction and policing is essential for inferences about the tragedy of the commons.     

Mating structure and male production in Vespa analis and Vespa simillima (Hymenoptera: Vespidae)

We estimated queen mating frequency, genetic relatedness between workers and worker reproduction in the hornets Vespa analis and Vespa simillima using microsatellite DNA genotyping. The 20 V. analis colonies studied each contained a queen inseminated by a single male. Of the 15 V. simillima colonies studied, nine had a queen inseminated by a single male, four had a queen inseminated by two males, and two had a queen inseminated by three males. The estimated effective number of matings was 1.33 ± 0.74 (mean ± SD), with 75–85% of the offspring of the six multiply mated queens sired by single males. The values for genetic relatedness between the workers of V. analis and V. simillima were 0.739 ± 0.004 and 0.698 ± 0.013 (mean ± SD), respectively. We conclude that V. analis and V. simillima colonies are genetically monogynous and monandrous. When high relatedness between the workers occurs within colonies, kin selection theory predicts a potential conflict between queens and workers over male production. To determine whether males were derived from queens or workers, males from V. analis and V. simillima colonies were genotyped at four microsatellite loci and the level of ovary activation in workers was determined. None of the 787 V. analis workers and only 15 of 3520 V. simillima workers had developed ovaries. Furthermore, the genotyping identified no worker‐produced males in any colony. The presence of reproductive workers correlated positively with the number of workers within the colony. These results suggest that eusocial colonies with an annual life cycle tend to break down socially when they become large and are close to dying.     

Cheaters sometimes prosper: targeted worker reproduction in honeybee (Apis mellifera) colonies during swarming

Kin selection theory predicts that honeybee (Apis mellifera) workers should largely refrain from producing their own offspring, as the workers collectively have higher inclusive fitness if they rear the sons of their mother, the queen. Studies that have quantified levels of ovary activation and reproduction among workers have largely supported this prediction. We sampled pre‐emergent male pupae and adult workers from seven colonies at regular intervals throughout the reproductive part of the season. We show that the overall contribution of workers to male (drone) production is 4.2%, nearly 40 times higher than is generally reported, and is highest during reproductive swarming, when an average of 6.2% of the males genotyped are worker‐produced. Similarly, workers in our samples were 100 times more likely to have active ovaries than previously assumed. Worker reproduction is seasonally influenced and peaks when colonies are rearing new queens. Not all worker subfamilies contribute equally to reproduction. Instead, certain subfamilies are massively over‐represented in drone brood. By laying eggs within the period in which many colonies produce virgin queens, these rare worker subfamilies increase their direct fitness via their well‐timed sons.     

How queen and workers share in male production in the stingless bee Melipona subnitida Ducke (Apidae, Meliponini)

Summary. Potential conflict between the queen and workers over the production of males is expected in stingless bees as a result of the higher relatedness of workers with their sons than with their brothers. This conflict was studied in Melipona subnitida by observing how the queen and the workers share in male production. The oviposition of individual cells was observed in two colonies with individually marked workers for a period of 51 and 40 days respectively. The gender that developed from these cells was then determined. The results revealed that most male production was concentrated in a 2–3-week period, during which laying workers were present. During these weeks, the queens produced twice as many males as all laying workers together. Outside this distinct period, the queens produced an occasional male. A reproductive worker either oviposited before the queen did, in which case she immediately proceeded to close the cell and thus prevented the queen from oviposition, or oviposited and sealed the cell after the queen had laid an egg. When cell construction and oviposition occured on several combs simultaneously, the workers preferentially laid male eggs on the newest combs. We discuss the proximate mechanism and ultimate cause of the way in which queen-worker male production occurred. In conclusion, we argue that overt behavioural conflict, occasionally displayed by reproductive workers of this species, can be of great cost to the colony.Received 27 February 2004; revised 6 September 2004; accepted 1 October 2004.     

Convergent evolution of worker policing by egg eating in the honeybee and common wasp

Mutual policing, where group members suppress each others' reproduction, is hypothesized to be important in the origin and stabilization of biological complexity. Mutual policing among workers in social insects can reduce within-colony conflict. However, there are few examples. We tested for worker policing in the common wasp Vespula vulgaris. Workers rapidly removed worker-laid eggs but left most queen-laid eggs (four out of 120 worker eggs versus 106 out of 120 queen eggs remained after 1h). Ovary dissection (1150 workers from six colonies) revealed that a small but significant number of workers have active ovaries (4%) equivalent to approximately five to 25 workers per colony. Consistent with effective policing of worker reproduction, microsatellite analysis of males (270 individuals from nine colonies) detected no workers' sons. Worker policing by egg eating has convergently evolved in the common wasp and the honeybee suggesting that worker policing may have broad significance in social evolution. Unlike the honeybee, relatedness patterns in V. vulgaris do not explain selection for policing. Genetic analysis (340 workers in 17 nests) revealed that workers are equally related to the queen's and other workers' sons (worker-worker relatedness was 0.51 +/- 0.04, 95% confidence interval). Worker policing in V. vulgaris may be selected due to the colony-level benefit of conflict suppression.     

THE EVOLUTION OF WORKER STERILITY IN HONEY BEES: AN INVESTIGATION INTO A BEHAVIORAL MUTANT CAUSING FAILURE OF WORKER POLICING

Normally, worker honey bees (Apis mellifera) only lay eggs when their colony is queenless. When a queen is present, worker egg-laying is controlled by mutual “policing” behavior in which any rare worker-laid eggs are eaten by other workers. However, an extremely rare behavioral phenotype arises in which workers develop functional ovaries and lay large numbers of eggs despite the presence of the queen. In this study, microsatellite analysis was used to determine the maternity of drones produced in such a colony under various conditions. One subfamily was found to account for about 90% of drone progeny, with the remainder being laid by other subfamilies or the queen. No evidence of queen policing was found. After a one-month period of extreme worker oviposition in spring, the colony studied reverted to normal behavior and showed no signs of worker oviposition. However, upon removal of the queen, workers commenced oviposition very quickly. Significantly, the subfamily that laid eggs when the queen was present did not contribute to the drone production when the colony was queenless. However, another subfamily contributed a disproportionately large number of drones. The frequency of worker oviposition appears to be determined by opposing selective forces. Individual bees benefit from personal reproduction, whereas other bees and the colony are disadvantaged by it. Thus a behavioral polymorphism can be maintained in the population in which some workers can escape worker policing, with balancing selection at the colony level to detect and eliminate these mutations.     

Worker policing limits the number of reproductives in a ponerine ant

Reproductive division of labour is an essential feature of insect sociality, but the regulation of sterility among colony members remains incompletely understood. Ant workers and queens are morphologically divergent and workers are only capable of producing males in a colony, although they usually do not do so. Worker policing is one mechanism proposed for their infertility and it can be expressed as either aggressive inhibition of ovarian activity among workers or destruction of worker-laid eggs. A few studies have shown that workers with developed ovaries are preferentially attacked by nest-mates, but adequate demonstration of worker policing also requires evidence that these attacks result in the suppression of ovarian activity or death. We investigated worker policing in the ponerine ant Harpegnathos saltator in which workers are able to mate and replace the founding queen. Five colonies were each divided into two groups, one of which consisted exclusively of infertile workers. Some individuals in the orphaned groups began laying eggs during the three-week separation and upon reunification these were vigorously attacked by infertile workers of the other groups. The ovarian activity of these new egg layers became inhibited, as revealed by subsequent dissection of marked individuals. Worker policing in H. saltator appears to function primarily in preventing an excess of reproductive workers.     

The effects of honey bee (Apis mellifera L.) queen reproductive potential on colony growth

Reproduction in species of eusocial insects is monopolized by one or a few individuals, while the remaining colony tasks are performed by the worker caste. This reproductive division of labor is exemplified by honey bees (Apis mellifera L.), in which a single, polyandrous queen is the sole colony member that lays fertilized eggs. Previous work has revealed that the developmental fate of honey bee queens is highly plastic, with queens raised from younger worker larvae exhibiting higher measures in several aspects of reproductive potential compared to queens raised from older worker larvae. Here, we investigated the effects of queen reproductive potential (“quality”) on the growth and winter survival of newly established honey bee colonies. We did so by comparing the growth of colonies headed by “high-quality” queens (i.e., those raised from young worker larvae, which are more queen-like morphologically) to those headed by “low-quality” queens (i.e., those raised from older worker larvae, which are more worker-like morphologically). We confirmed that queens reared from young worker larvae were significantly larger in size than queens reared from old worker larvae. We also found a significant positive effect of queen grafting age on a colony’s production of worker comb, drone comb, and stored food (honey and pollen), although we did not find a statistically significant difference in the production of worker and drone brood, worker population, and colony weight. Our results provide evidence that in honey bees, queen developmental plasticity influences several important measures of colony fitness. Thus, the present study supports the idea that a honey bee colony can be viewed (at least in part) as the expanded phenotype of its queen, and thus selection acting predominantly at the colony level can be congruent with that at the individual level.