Social influences on body size and developmental time in the bumblebee Bombus terrestris

In many social insects, including bumblebees, the division of labor between workers relates to body size, but little is known about the factors influencing larval development and final size. We confirmed and extend the evidence that in the bumblebee Bombus terrestris the adult bee body size is positively correlated with colony age. We next performed cross-fostering experiments in which eggs were switched between incipient (before worker emergence) and later stage colonies with workers. The introduced eggs developed into adults similar in size to their unrelated nestmates and not to their same-age full sisters developing in their mother colony. Detailed observations revealed that brood tending by the queen decreases, but does not cease, in young colonies with workers. We next showed that both worker number and the queen presence influenced the final size of the developing brood, but only the queen influence was mediated by shortening developmental time. In colonies separated by a queen excluder, brood developmental time was shorter in the queenright compartment. These findings suggest that differences in body size are regulated by the brood interactions with the queen and workers, and not by factors inside the eggs that could vary along with colony development. Finally, we developed a model showing that the typical increase in worker number and the decrease in brood contact with the queen can account for the typical increase in body size. Similar self-organized social regulation of brood development may contribute to the optimization of growth and reproduction in additional social insects.     

Social parasitism by honeybee workers (Apis mellifera capensis Esch.): evidence for pheromonal resistance to host queen’s signals

Social parasites exploit their host’s communication system to usurp resources and reproduce. In the honeybee, Apis mellifera, worker reproduction is regulated by pheromones produced by the queen and the brood. Workers usually reproduce when the queen is removed and young brood is absent. However, Cape honeybee workers, Apis mellifera capensis, are facultative intraspecific social parasites and can take over reproduction from the host queen. Investigating the manner in which parasitic workers compete with host queens pheromonally can help us to understand how such parasitism can evolve and how reproductive division of labour is regulated. In A. m. capensis, worker reproduction is associated with the production of queen-like pheromones. Using pheromonal contest experiments, we show that Apis mellifera scutellata queens do not prevent the production of queen-like mandibular gland compounds by the parasites. Given the importance of these pheromones in acquiring reproductive status, our data suggest that the single invasive lineage of parasitic workers occurring in the range of A. m. scutellata was selected for its superior ability to produce these signals despite the presence of a queen. Such resistance was indeed less frequent amongst other potentially parasitic lineages. Resistance to reproductive regulation by host queens is probably the key factor that facilitates the evolution of social parasitism by A. m. capensis workers. It constitutes a mechanism that allows workers to evade reproductive division of labour and to follow an alternative reproductive option by acquiring direct fitness in foreign colonies instead of inclusive fitness in their natal nests.     

Reproductive plasticity in bumblebee workers (<Emphasis Type="Italic">Bombus terrestris</Emphasis>)—reversion from fertility to sterility under queen influence

Worker sterility in the bumblebee Bombus terrestris is conditional and is linked to the social development of the colony. Workers refrain from reproducing or overtly challenging the queen until gyne production has initiated, at the so-called competition point (CP). It is not known whether this behavior is hard-wired or workers show reproductive plasticity. It also remains unclear whether worker reproductive decision is under queen and/or worker control. In this study, we tested worker reproductive plasticity in an attempt to assess whether and under which conditions worker sterility/fertility are reversible. We introduced egg-laying workers into colonies with different social structures for 1 week then monitored their reproductive status. We revealed a remarkable reproductive plasticity in the introduced workers that was social-condition-dependent. In the presence of a pre-CP queen, the introduced workers reverted to sterility, whereas in the presence of a post-CP queen, such workers remained egg-layer. Reversion to sterility does not occur when direct contact with the queen is prevented, as the introduced workers remained egg-layer in the queenright colonies with a confined queen. Egg-laying workers that were introduced into queenless colonies mostly maintained their fertility regardless of colony social phase. This shows that worker transition from cooperative to selfish behavior is reversible depending on the social context.     

Social evolution and its correlates in bees of the subgenus Evylaeus (Hymenoptera; Halictidae)

Summary Eleven behavioural characteristics of eight species of the subgenus Evylaeus were analysed using principal components analysis. The first component axis represents social level and explains over forty percent of the total variation in the data. The following characteristics are highly correlated with social level — (i) a reduction in the proportion of males in the first brood, (ii) a reduction in the proportion of workers that mate, (iii) a reduction in the proportion of workers that have developed ovaries, (iv) an increase in the mean number of workers, (v) increased contact between adults and developing brood and (vi) an increase in the size difference between queens and workers. Because these factors appear, in general, to be under the control of the queen it is argued that parental manipulation has been an important component of social evolution in these bees. The number of worker broods and the mechanism of male production are also related to social level but are less important. Nest architecture, nest defense and polygyny seem to be unrelated to social level. Variation in nest architecture may be in response to edaphic features of the substrate. The lack of any relationship between polygyny and social level implies that the semisocial route to eusociality was not the one taken. It is likely that polygyny can only occur where the substrate is suitable for the winter hibernation of sisters in their natal nest. Multivariate methods are useful in determining the relative social level of closely related halictine species.     

Competition and cooperation: bumblebee spatial organization and division of labor may affect worker reproduction late in life

Within-group conflict may influence the degree to which individuals within a group cooperate. For example, the most dominant individuals within a group often gain access to the best resources and may be less inclined to perform risky tasks. We monitored space use and division of labor among all workers in three colonies of bumblebees, Bombus impatiens, during the ergonomic and queenless phases of their colony cycle. We then measured the two largest oocytes in each worker to estimate each individual's reproductive potential at the end of the colony cycle. We show that workers that remained farther from the queen while inside the nest and avoided risky or more energy-expensive tasks during the ergonomic phase developed larger oocytes by the end of the colony cycle. These individuals also tended to be the largest, oldest workers. After the queen died, these workers were more likely than their nestmates to increase brood incubation. Our results suggest that inactive bumblebees may be storing fat reserves to later develop reproductive organs and that the spatial organization of workers inside the nest, particularly the distance workers maintain from the queen, may predict which individuals will later have the greatest reproductive potential in the colony.     

Role of Propagule Size in the Success of Incipient Colonies of the Invasive Argentine Ant

Abstract: Factors that contribute to the successful establishment of invasive species are often poorly understood. Propagule size is considered a key determinant of establishment success, but experimental tests of its importance are rare. We used experimental colonies of the invasive Argentine ant (   Linepithema humile ) that differed both in worker and queen number to test how these attributes influence the survivorship and growth of incipient colonies. All propagules without workers experienced queen mortality, in contrast to only 6% of propagules with workers. In small propagules (10–1,000 workers), brood production increased with worker number but not queen number. In contrast, per capita measures of colony growth decreased with worker number over these colony sizes. In larger propagules ( 1,000–11,000 workers), brood production also increased with increasing worker number, but per capita brood production appeared independent of colony size. Our results suggest that queens need workers to establish successfully but that propagules with as few as 10 workers can grow quickly. Given the requirements for propagule success in Argentine ants, it is not surprising how easily they spread via human commerce.     

Genetic relatedness and evolution of insect sociality

Summary Genetic relatedness is a vital concept in the study of the evolution of social behaviour because it can be used to predict gene transmission into future generations. Any models using genetic relatedness to predict the course of social evolution have to take into account that this relatedness, when defined as genotypic regression, is affected by selection and that the evolution also depends on specific assumptions concerning the cost/benefit ratios. In this paper these problems are shown to exist in recent studies examining the evolution of worker behaviour in insects; these studies are reanalysed using allele frequency models, and the results compared with those from other models.It is shown that cyclic inbreeding (alternating outbred and inbred generations) can favour worker evolution in diploid populations but is a necessary condition only within a very limited range of the cost/benefit ratio.Male-haploid models show that both female and male workers evolve more easily if they can manipulate the brood produced by the queen by biassing the brood sex ratio in favour of females (the optimal proportion of females is ca. 0.75). The threshold for female workers to evolve is also lowered if they are allowed to produce some of the colony's male offspring (which arise from unfertilized eggs), in which case the optimal brood sex ratio becomes closer to 1:1. It is apparent that the two factors — sex-ratio bias and worker-produced males — are also important in the comparison of worker evolution in male-haploid and diploid insects.     

Retinue attraction and ovary activation: responses of wild type and anarchistic honey bees (Apis mellifera) to queen and brood pheromones

In most social insect colonies, workers do not attempt to lay eggs in the presence of a queen. However, in the honey bee (Apis mellifera), a rare phenotype occurs in which workers activate their ovaries and lay large numbers of male eggs despite the presence of a fecund queen. We examined the proximate mechanisms by which this ‘anarchistic’ behaviour is expressed. We tested the effects of brood and queen pheromones on retinue attraction and worker ovary activation using caged worker bees. We found no difference between the anarchistic and wild type queen pheromones in the retinue response elicited in either wild type or anarchistic workers. Further, we found that anarchistic queens produce a pheromone blend that is as effective at inhibiting ovary activation as the wild type queen pheromone. However, anarchistic workers are less inhibited by queen pheromones than their wild type counterparts, in a dose-dependent manner. These results show that the anarchistic phenomenon is not due to changes in the production of queen pheromones, but rather is due in part to a shift in the worker response to these queen-produced signals. In addition, we demonstrate the dose-dependent nature of the effect of queen pheromones on honey bee worker ovary activation.     

Do these eggs smell funny to you?: an experimental study of egg discrimination by hosts of the social parasite Polyergus breviceps (Hymenoptera: Formicidae)

Social parasites exploit the behaviours of other social species. Infiltration of host systems involves a variety of mechanisms depending on the conditions within the host society and the needs of the social parasite. For many species of socially parasitic ants, colony establishment entails the usurpation of colonies of other species. This frequently involves the eviction or death of the host colony queen and the subsequent adoption of the invading queen. The social parasite queen achieves host worker acceptance by either manipulating the nest-mate recognition processes of the host or undergoing chemical modification. Little is known, however, about how host workers respond to social parasite eggs or whether host species defend against brood parasitism during parasite invasions. Host species are believed to adopt social parasite offspring because the recent common ancestry between many social parasites and their hosts may grant the sharing of certain characteristics such as chemical cues. Use of multiple host species, however, suggests other processes are needed for the social bond between host and parasite young to form. This study reports the findings of adoption bioassays in which eggs from a slave-maker ant, Polyergus breviceps, were offered to workers of two of its host species from unparasitised or newly parasitised nests to determine whether P. breviceps eggs generally elicit rearing behaviours from multiple host species. Comparisons of parasite egg survival until adulthood with conspecific egg survival reveal that workers of both host species, free-living or newly enslaved, do not typically accept slave-maker eggs. Both host species thus have sufficient discriminatory power to reject social parasite eggs although our hydrocarbon analysis indicates parasite eggs may be adapted to their local host species. Combined these results suggest that host rearing of P. breviceps eggs may reflect an evolutionary equilibrium that is maintained by probability and cost of recognition errors.Communicated by L. Sundström     

Relatedness and sex ratio in a primitively eusocial halictine bee

Lasioglossum laevissimum was studied in Calgary, Alberta, where it is eusocial with one worker brood. Estimates of relatedness were obtained among various categories of nestmate based upon four polymorphic enzyme loci, two of which exhibited significant levels of linkage disequilibrium. Relatedness estimates among workers and among reproductive brood females were very close to the expected 0.75 value that obtains when nests are headed by one, singly mated queen. However, relatedness between workers and the reproductive brood females they reared was significantly lower than 0.75. A low frequency of orphaning with subsequent monopolisation of oviposition by one worker brood female in orphaned nests may explain these results. Workers were significantly more and queens significantly less closely related to male reproductives than expected if all males were to have resulted from queen-laid eggs. Orphaning and worker-produced males contribute to this result. The sex investment ratio was 1:2.2 in favour of females, in excellent agreement with the predictions based upon relative relatednesses between workers and reproductive brood males and females. Adaptive intercolony variation in investment ratios was detected: the sex ratio was more heavily female-biased in nests in which the relative relatedness asymmetry between workers and reproductive brood was more female-biased. The study species is the most weakly eusocial hymenopteran for which relatedness estimates and sex ratio data are available. With high relatedness among nestmates and a strongly female-biased sex ratio, this study suggests the importance of indirect fitness contributions in the early stages of social evolution. Correspondence to: L. Packer     

How the social parasitic bumblebee <Emphasis Type="Italic">Bombus bohemicus</Emphasis> sneaks into power of reproduction

Social parasitism is widespread in many groups of social living hymenopteran species and has also evolved in the genus Bombus. Cuckoo bumblebees (subgenus Psithyrus) are obligate brood parasites in nests of other bumblebee species. After nest usurpation and the killing of the host queen, the parasite female has to control worker reproduction in order to accomplish and maintain reproductive dominance and to ensure her reproductive success. The aim of our study was to examine whether the generalist parasitic bumblebee Bombus bohemicus monopolizes and prevents worker reproduction by physical or chemical means and to identify possible odor compounds involved therein. We performed bioassays with callow workers of the host Bombus terrestris and have shown that B. bohemicus females are able to suppress host worker ovarian development, when these host workers are under the direct influence of the parasite female. Furthermore, by chemical analyses, we have demonstrated that the parasite females adjust to the odor profiles of their host queens in order to maintain the level of fertility signaling inside the host colony although the host queen is absent. We also found that host workers change their odor profile after nest usurpation by the parasite female and consequently, we suggest that the host and parasite are caught up in a chemical arms race.     

Differential reproduction in multiple-queen colonies of the fire ant Solenopsis invicta (Hymenoptera: Formicidae)

Summary The contribution to maternity of workers and female sexuals over time by queens in six multiple-queen laboratory colonies of Solenopsis invicta was directly assessed by use of enzyme genetic markers. Queens contributed more equally to the worker pool than to the pool of sexuals in virtually all samples (Fig. 1), and individuals producing a substantial proportion of the workers often had low or no representation of their daughters in the pool of sexuals. Signficant disparity among queens in their relative production of sexual daughters was often evident, with dominance in production of sexuals by a given queen commonly occurring in association with a pronounced loss of weight followed shortly by her death. The results suggest that significant variability in short-as well as long-term reproductive success may occur among the distantly related queens associating in natural polygyne S. invicta nests. Variance in apportionment of maternity of sexuals did not appear to be simply related to varying levels of fecundity, suggesting that the common presumption that reproductive success can be equated with fecundity in polygyne social Hymenoptera may not be well founded. The observed variance also did not appear to result from a simple mechanism of kin recognition and discrimination by workers in the process of brood rearing. Rather, this variance may have largely resulted from either, 1) recognition of certain queens and their progeny coupled with preferential sexualization of these immatures by nurse workers, or, 2) queen biasing of eggs toward development as sexuals. The frequent association of weight loss and death of mother queens with high levels of sexual daughter production may be best explained by the latter mechanism.     

Worker discrimination among queens in newly founded colonies of the fire ant Solenopsis invicta

Although colonies of the fire ant Solenopsis invicta are often founded by small groups of queens, all but one of the queens are soon eliminated due to worker attacks and queen fighting. The elimination of supernumerary queens provides an important context for tests of discrimination by the workers, since the outcome of these interactions strongly affects the workers' inclusive fitness. To test whether workers in newly founded colonies discriminate among nestmate queens, paired cofoundresses were narrowly separated by metal screens that prevented direct fighting, but through which the workers could easily pass. Soon after the first workers completed development, they often attacked one of the queens; these attacks were strongly associated with queen mortality. When one queen's brood was discarded, so that the adult workers were all the daughters of just one queen, the workers were significantly less likely to bite their mother than the unrelated queen; however, this tendency was comparatively weak. Queens kept temporarily at a higher temperature to increase their rate of investment in brood-rearing lost weight more rapidly than paired queens and were subsequently more likely to be attacked and killed by workers. Workers were more likely to bite queens that had been temporarily isolated than queens that remained close to brood and workers. When queens were not separated by screens, the presence of workers stimulated queen fights. These results show that workers discriminate strongly among equally familiar queens and that discrimination is based more on the queens' condition and recent social environment than on kinship. Received: 9 June 1998 / Accepted after revision: 10 October 1998     

Control of reproduction in social insect colonies: individual and collective relatedness preferences in the paper wasp, Polistes annularis

Social insect colonies often have one or a few queens. How these queens maintain their reproductive monopoly, when other colony members could gain by sharing in the reproduction, is not generally known. DNA microsatellite genotyping is used to determine reproductive interests of various classes of colony members in the paper wasp, Polistes annularis. The relatedness estimates show that the best outcome for most individuals is to be the reproductive egg-layer. For workers, this depends on the sex of offspring: they should prefer to lay their own male eggs, but are indifferent if the queen lays the female eggs. The next-best choice is usually to support the current queen. As a rule, subordinates and workers should prefer the current queen to reproduce over other candidates (though subordinates have no strong preference for the queen over other subordinates, and workers may prefer other workers as a source of male eggs). This result supports the theory that reproductive monopoly stems from the collective preferences of non-reproductives, who suppress each other in favor of the queen. However, we reject the general hypothesis of collective worker control in this species because its predictions about who should succeed after the death of the present queen are not upheld. The first successor is a subordinate foundress even though workers should generally prefer a worker successor. If all foundresses have died, an older worker succeeds as queen, in spite of a collective worker preference for a young worker. The results support the previous suggestion that age serves as a conventional cue serving to reduce conflict over queen succession. Received: 3 May 1996 / Accepted after revision: 22 September 1996     

Queen and worker policing in the tree wasp Dolichovespula sylvestris

Insect societies are sometimes exploited by workers who reproduce selfishly rather than help to rear the queens offspring. This causes a conflict-of-interest with the mother queen and, frequently, with the non-reproductive workers as well. One mechanism that can reduce conflict is policing, whereby either the queen or other workers aggress egg-laying workers or destroy worker-laid eggs. Here we present the first direct observations of queen and worker policing in natural, unmanipulated colonies of a social insect, the tree wasp Dolichovespula sylvestris. Worker reproduction was common, with workers producing 50% of all male eggs. However, most worker-laid eggs, 91%, were policed within 1 day, whereas most queen-laid eggs, 96%, remained unharmed. The workers were responsible for 51% of all policing events and the queen for 49%. The workers and mother queen also commonly aggressed ovipositing workers, and successfully prevented them from depositing eggs in 14% and 6% of all attempted ovipositions. Hence, both queen policing and worker policing occur and policing acts via two distinct mechanisms: selective destruction of worker-laid eggs and aggression of ovipositing workers. At a general level, our study shows that both centralized and decentralized control can act together to suppress conflict within social groups.Communicated by R. Page     

Reversible royalty in worker honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis>) under the queen influence

In most social insects, worker sterility is reversible, and in the absence of the queen, at least some workers develop ovaries and lay male-destined eggs. In the honeybee, reproductive workers also produce queen-characteristic mandibular and Dufour’s pheromones. The evolution of worker sterility is still under debate as to whether it is caused by queen manipulation (queen-control hypothesis) or represents worker fitness maximization (worker-control hypothesis). In this study, we investigated whether worker fertility and royal pheromone production are reversible under the queen influence. To that effect, we induced ovary activation and queen pheromone production in workers by rearing them as queenless (QL) groups. These workers were subsequently reintroduced into queenright (QR) microcolonies for 1 week, and their ovary status and queen pheromone levels were monitored. Workers reintroduced into QR, but not QL colonies, showed a clear regression in ovary development and levels of the queen pheromones. This is the first demonstration that worker sterility and/or fertility is reversible and is influenced by the queen. These results also emphasize the robustness of the coupling between ovary activation and royal pheromone production, as well as lending credence to the queen-control hypothesis. The dynamics of queen pheromone production in QL workers supports the role of Dufour’s gland pheromone as a fertility signal and that of the mandibular gland pheromone in dominance hierarchies.The two authors, Osnat Malka and Shiri Shnieor, contributed equally to this work.     

Egg-laying,egg-removal,and ovary development by workers in queenright honey bee colonies

Summary The study investigates whether worker policing via the selective removal of worker-laid male eggs occurs in normal honey bee colonies with a queen. Queenright honey bee colonies were set up with the queen below a queen excluder. Frames of worker brood and drone comb were placed above the queen excluder. Daily inspections of the drone frames revealed the presence of a few eggs, presumably laid by workers, at a rate of 1 egg per 16000 drone cells. 85% of these eggs were removed within 1 day and only 2% hatched. Dissections of workers revealed that about 1 worker in 10000 had a fully developed egg in her body. These data show that worker egg-laying and worker policing are both normal, though rare, in queenright honey bee colonies, and provide further confirmation of the worker policing hypothesis.     

Almost royal: incomplete suppression of host worker ovarian development by a social parasite wasp

Insect social parasites, like other parasites, may benefit from inhibiting their host from reproducing (complete or partial parasitic castration) because they can then exploit more of the host’s resources for their own reproduction. In particular, social parasites that kill or expel the host queen need to prevent host workers from reproducing; this is a common worker response to the absence of their queen. Indeed, host workers would benefit from detecting the presence of the parasite and investing in direct and indirect fitness. Studying whether and how social parasites control host worker reproduction can provide information about the degree of integration of the parasite in the host colony and help identify factors regulating workers’ reproductive decisions in social insects. We investigated whether the paper wasp social parasite, Polistes sulcifer, suppresses Polistes dominula (host) worker reproduction as efficiently as the dominant host female does in queen-right colonies by comparing worker reproductive efforts in parasitized and non-parasitized (control) colonies. Our results show that 6 weeks after usurpation of their colony by the social parasite, parasitized workers (1) had more developed ovaries than control workers and (2) laid more eggs as soon as the opportunity arose. This reproductive readiness of parasitized workers was not apparent 2 weeks after colony usurpation. This suggests that P. dominula workers have evolved means to react to social parasitism, as occurs in some ants, and that the parasite has only limited control over host reproduction.     

Social parasitism of queens and workers in the Cape honeybee (<Emphasis Type="Italic">Apis mellifera capensis</Emphasis>)

Workers of a queenless honeybee colony can requeen the colony by raising a new queen from a young worker brood laid by the old queen. If this process fails, the colony becomes hopelessly queenless and workers activate their ovaries to lay eggs themselves. Laying Cape honeybee workers (Apis mellifera capensis) produce female offspring as an additional pathway for requeening. We tested the frequency of successful requeening in ten hopelessly queenless colonies. DNA genotyping revealed that only 8% of all queens reared in hopelessly queenless colonies were the offspring of native laying worker offspring. The vast majority of queens resulted from parasitic takeovers by foreign queens (27%) and invading parasitic workers (19%). This shows that hopelessly queenless colonies typically die due to parasitic takeovers and that the parasitic laying workers are an important life history strategy more frequently used than in providing a native queen to rescue the colony. Parasitism by foreign queens, which might enter colonies alone or accompanied by only a small worker force is much more frequent than previously considered and constitutes an additional life history strategy in Cape honeybees.     

A genetic component to size in queens of the ant,<Emphasis Type="Italic"> Formica truncorum</Emphasis>

The genetic basis of morphological traits in social insects remains largely unexplored. This is even true for individual body size, a key life-history trait. In the social insects, the size of reproductive individuals affects dispersal decisions, so that small size in queens is often associated with reduced dispersal, and large size with long-range dispersal and independent colony founding. Worker size is connected to division of labour when workers specialize in certain tasks according to their size. In many species, variation in worker size has been shown to increase colony performance. In this study, we present the first evidence of an additive genetic component to queen size in ants, using maternal half sib analysis. We also compared intra-colony size variation in colonies with high (queen doubly mated) versus low (queen singly mated) genetic variability. We found a high and significant heritability (h²=0.51) for queen size in one of the two study years, but not in the other. Size variation among queens was greater in colonies headed by a doubly mated queen in one of the study years, but not in the other. This indicates that genetic factors can influence queen size, but that environmental factors may override these under some circumstances. The heritability for worker size was low (h²=0.09) and non-significant. Increased genetic diversity did not increase worker size variation in the colonies. Worker size appeared largely environmentally determined, potentially allowing colonies to adjust worker size ratios to current conditions.Communicated by J. Heinze