The influence of social hunger on food distribution and its implications for disease transmission in a honeybee colony

Social insect colonies are characterized by extensive interactions among individuals, exchanges that can also potentially transmit pathogens. The large majority of these social interactions in a honeybee colony result from food transfer among individuals. Since colony hunger is likely to have a significant influence on these interactions, we investigated its effect on the distribution of food within the colony. By pulsing two colonies having different amounts of stored food with a radioactive label, we found that a starved colony sent out a larger number of foragers, brought in more food, and stored more of it than the satiated colony. We also found that the food brought into a starved colony was distributed more uniformly within each age class than that in the satiated colony. The queen and the young individuals received the lowest exposure to the label even though the label entered different regions of the colony at the same rate. The satiation level of the colony did not influence the relative exposures of different age groups to the label but a higher amount of it was stored in the hungry colony. We discuss the significance of these results in terms of the role played by the organizational structure of the honeybee colony on the transmission dynamics of an infectious disease.     

Estimating the genetic variance of group characters: social behaviour of honeybees (Apis mellifera L.)

Summary A new approach is presented to estimate the genetic variance of social behaviour of groups. Honeybees (Apis mellifera L.) are used as an example for highly social organisms. Most characters of economic importance strongly rely on collective group characters of honeybee colonies. The average relatedness between small groups of workers of one honeybee colony can be estimated using a discrete multinomial distribution. The genetic variance of a social behaviour (alarm behaviour) of groups of honeybee workers is estimated with the intraclass correlation between groups within a colony. In two populations tested, the coefficient of genetic determination was high (0.96–0.98) indicating that the metabolic bio-assay used was only weakly affected by environmental effects.     

Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth

Multiple mating by social insect queens increases the genetic diversity among colony members, thereby reducing intracolony relatedness and lowering the potential inclusive fitness gains of altruistic workers. Increased genetic diversity may be adaptive, however, by reducing the prevalence of disease within a nest. Honeybees, whose queens have the highest levels of multiple mating among social insects, were investigated to determine whether genetic variation helps to prevent chronic infections. I instrumentally inseminated honeybee queens with semen that was either genetically similar (from one male) or genetically diverse (from multiple males), and then inoculated their colonies with spores of Ascosphaera apis, a fungal pathogen that kills developing brood. I show that genetically diverse colonies had a lower variance in disease prevalence than genetically similar colonies, which suggests that genetic diversity may benefit colonies by preventing severe infections.     

Social parasitism by Cape honeybee workers in colonies of their own subspecies (Apis mellifera capensis Esch.)

Social parasitism is widespread in the eusocial insects. Although social parasites often show a reduced worker caste, unmated workers can also parasitize colonies. Cape honeybee workers, Apis mellifera capensis, can establish themselves as social parasites in host colonies of other honeybee subspecies. However, it is unknown whether social parasitism by laying workers also occurs among Cape honeybee colonies. In order to address this question we genotyped worker offspring of six queenless A. m. capensis colonies and determined the maternity of the reproducing workers. We found that three non-nestmate workers dominated reproduction in a host colony and produced 62.5% of the progeny. Our results show that social parasitism by laying workers is a naturally occurring part of the biology of Cape honeybees. However, such social parasitism is not frequently found (6.41% of the total worker offspring) probably due to co-evolutionary processes among A. m. capensis resulting in an equilibrium between selection for reproductive dominance in workers, colony maintenance and queen adaptation. Received 28 July 2005; revised 19 September and 11 November 2005; accepted 16 November 2005.     

Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera)

Global pollinators, like honeybees, are declining in abundance and diversity, which can adversely affect natural ecosystems and agriculture. Therefore, we tested the current hypotheses describing honeybee losses as a multifactorial syndrome, by investigating integrative effects of an infectious organism and an insecticide on honeybee health. We demonstrated that the interaction between the microsporidia Nosema and a neonicotinoid (imidacloprid) significantly weakened honeybees. In the short term, the combination of both agents caused the highest individual mortality rates and energetic stress. By quantifying the strength of immunity at both the individual and social levels, we showed that neither the haemocyte number nor the phenoloxidase activity of individuals was affected by the different treatments. However, the activity of glucose oxidase, enabling bees to sterilize colony and brood food, was significantly decreased only by the combination of both factors compared with control, Nosema or imidacloprid groups, suggesting a synergistic interaction and in the long term a higher susceptibility of the colony to pathogens. This provides the first evidences that interaction between an infectious organism and a chemical can also threaten pollinators, interactions that are widely used to eliminate insect pests in integrative pest management.     

The prevalence of the honeybee brood pathogens Ascosphaera apis,Paenibacillus larvae and Melissococcus plutonius in Spanish apiaries determined with a new multiplex PCR assay

The microorganisms Ascosphaera apis, Paenibacillus larvae and Melissococcus plutonius are the three most important pathogens that affect honeybee brood. The aim of the present study was to evaluate the prevalence of these pathogens in honeybee colonies and to elucidate their role in the honeybee colony losses in Spain. In order to get it, a multiplex polymerase chain reaction (PCR) assay was developed to simultaneously amplify the16S ribosomal ribonucleic acid (rRNA) gene of P. larvae and M. plutonius, and the 5.8S rRNA gene of A. apis. The multiplex PCR assay provides a quick and specific tool that successfully detected the three infectious pathogens (P. larvae, M. plutonius and A. apis) in brood and adult honeybee samples without the need for microbiological culture. This technique was then used to evaluate the prevalence of these pathogens in Spanish honeybee colonies in 2006 and 2007, revealing our results a low prevalence of these pathogens in most of the geographic areas studied.     

Quantitative comparison of caste differences in honeybee hemolymph

The honeybee, Apis mellifera, is an invaluable partner in agriculture around the world both for its production of honey and, more importantly, for its role in pollination. Honeybees are largely unexplored at the molecular level despite a long and distinguished career as a model organism for understanding social behavior. Like other eusocial insects, honeybees can be divided into several castes: the queen (fertile female), workers (sterile females), and drones (males). Each caste has different energetic and metabolic requirements, and each differs in its susceptibility to pathogens, many of which have evolved to take advantage of the close social network inside a colony. Hemolymph, arthropods' equivalent to blood, distributes nutrients throughout the bee, and the immune components contained within it form one of the primary lines of defense against invading microorganisms. In this study we have applied qualitative and quantitative proteomics to gain a better understanding of honeybee hemolymph and how it varies among the castes and during development. We found large differences in hemolymph protein composition, especially between larval and adult stage bees and between male and female castes but even between adult workers and queens. We also provide experimental evidence for the expression of several unannotated honeybee genes and for the detection of biomarkers of a viral infection. Our data provide an initial molecular picture of honeybee hemolymph, to a greater depth than previous studies in other insects, and will pave the way for future biochemical studies of innate immunity in this animal.     

East learns from West: Asiatic honeybees can understand dance language of European honeybees

The honeybee waggle dance, through which foragers advertise the existence and location of a food source to their hive mates, is acknowledged as the only known form of symbolic communication in an invertebrate. However, the suggestion, that different species of honeybee might possess distinct 'dialects' of the waggle dance, remains controversial. Furthermore, it remains unclear whether different species of honeybee can learn from and communicate with each other. This study reports experiments using a mixed-species colony that is composed of the Asiatic bee Apis cerana cerana (Acc), and the European bee Apis mellifera ligustica (Aml). Using video recordings made at an observation hive, we first confirm that Acc and Aml have significantly different dance dialects, even when made to forage in identical environments. When reared in the same colony, these two species are able to communicate with each other: Acc foragers could decode the dances of Aml to successfully locate an indicated food source. We believe that this is the first report of successful symbolic communication between two honeybee species; our study hints at the possibility of social learning between the two honeybee species, and at the existence of a learning component in the honeybee dance language.     

Queen promiscuity lowers disease within honeybee colonies

Most species of social insects have singly mated queens, but in some species each queen mates with numerous males to create a colony with a genetically diverse worker force. The adaptive significance of polyandry by social insect queens remains an evolutionary puzzle. Using the honeybee (Apis mellifera), we tested the hypothesis that polyandry improves a colony's resistance to disease. We established colonies headed by queens that had been artificially inseminated by either one or 10 drones. Later, we inoculated these colonies with spores of Paenibacillus larvae, the bacterium that causes a highly virulent disease of honeybee larvae (American foulbrood). We found that, on average, colonies headed by multiple-drone inseminated queens had markedly lower disease intensity and higher colony strength at the end of the summer relative to colonies headed by single-drone inseminated queens. These findings support the hypothesis that polyandry by social insect queens is an adaptation to counter disease within their colonies.     

Intracolonial genetic variability in honeybee larval resistance to the chalkbrood and American foulbrood parasites

The origin of multiple mating of queens in social Hymenoptera is a widely debated topic in evolutionary biology. One of the hypotheses is that genetic variability would benefit the colony by increasing its resistance to parasites through various mechanisms. One among the predictions of this hypothesis is that the resistance of different patrilines within a colony to parasites of different species should be independent, as a result of independent gene-for-gene interactions with each parasite. To test this aspect of the hypothesis, two honeybee colonies (Apis mellifera) were infected with the fungus Ascosphaera apis and two colonies with both A. apis and the American foulbrood bacterium Paenibacillus larvae. Patrilines were found to vary in resistance of larvae to A. apis in all four colonies, but similar variation in resistance was not found to P. larvae. Common resistance to both pathogens was not detected. This study supports the hypothesis that polyandry in social insects could have originated as an adaptation to decrease the impact of diseases.     

Inter-individual variation in nutrient balancing in the honeybee (Apis mellifera)

The Geometric Framework approach in nutritional ecology postulates that animals attempt to balance the consumption of different nutrients rather than simply maximizing energetic gain. The intake target with respect to each nutrient maximizes fitness in a specific dimension and any difference between individuals in intake target therefore represents alternative behavioral and fitness maximization strategies. Nutritional interactions are a central component of all social groups and any inter-individual variation in intake target should therefore have a significant influence on social dynamics. Using the honeybee colony as an experimental model, we quantified differences in the carbohydrate intake target of individual foragers using a capillary feeder (CAFE) assay. Our results show that the bees did not simply maximize their net energetic gain, but combined sugar and water in their diet in a way that brought them to an intake target equivalent to a 33% sucrose solution. Although the mean intake target with respect to the nutrients sucrose and water was the same under different food choice regimens, there was significant inter-individual variation in intake target and the manner in which individuals reached this target, a variation which suggests different levels of tolerance to nutrient imbalance. We discuss our results in the context of how colony performance may be influenced by the different nutrient balancing strategies of individual members and how such nutritional constraints could have contributed to the evolution of sociality.     

The spread of fecally transmitted parasites in socially-structured populations

Mammals are infected by a wide array of gastrointestinal parasites, including parasites that also infect humans and domesticated animals. Many of these parasites are acquired through contact with infectious stages present in soil, feces or vegetation, suggesting that ranging behavior will have a major impact on their spread. We developed an individual-based spatial simulation model to investigate how range use intensity, home range overlap, and defecation rate impact the spread of fecally transmitted parasites in a population composed of social groups (i.e., a socially structured population). We also investigated the effects of epidemiological parameters involving host and parasite mortality rates, transmissibility, disease-related mortality, and group size. The model was spatially explicit and involved the spillover of a gastrointestinal parasite from a reservoir population along the edge of a simulated reserve, which was designed to mimic the introduction pathogens into protected areas. Animals ranged randomly within a "core" area, with biased movement toward the range center when outside the core. We systematically varied model parameters using a Latin hypercube sampling design. Analyses of simulation output revealed a strong positive association between range use intensity and the prevalence of infection. Moreover, the effects of range use intensity were similar in magnitude to effects of group size, mortality rates, and the per-contact probability of transmission. Defecation rate covaried positively with gastrointestinal parasite prevalence. Greater home range overlap had no positive effects on prevalence, with a smaller core resulting in less range overlap yet more intensive use of the home range and higher prevalence. Collectively, our results reveal that parasites with fecal-oral transmission spread effectively in socially structured populations. Future application should focus on parameterizing the model with empirically derived ranging behavior for different species or populations and data on transmission characteristics of different infectious organisms.     

Within‐group relatedness is correlated with colony‐level social structure and reproductive sharing in a social fish

In group‐living species, the degree of relatedness among group members often governs the extent of reproductive sharing, cooperation and conflict within a group. Kinship among group members can be shaped by the presence and location of neighbouring groups, as these provide dispersal or mating opportunities that can dilute kinship among current group members. Here, we assessed how within‐group relatedness varies with the density and position of neighbouring social groups in Neolamprologus pulcher, a colonial and group‐living cichlid fish. We used restriction site‐associated DNA sequencing (RADseq) methods to generate thousands of polymorphic SNPs. Relative to microsatellite data, RADseq data provided much tighter confidence intervals around our relatedness estimates. These data allowed us to document novel patterns of relatedness in relation to colony‐level social structure. First, the density of neighbouring groups was negatively correlated with relatedness between subordinates and dominant females within a group, but no such patterns were observed between subordinates and dominant males. Second, subordinates at the colony edge were less related to dominant males in their group than subordinates in the colony centre, suggesting a shorter breeding tenure for dominant males at the colony edge. Finally, subordinates who were closely related to their same‐sex dominant were more likely to reproduce, supporting some restraint models of reproductive skew. Collectively, these results demonstrate that within‐group relatedness is influenced by the broader social context, and variation between groups in the degree of relatedness between dominants and subordinates can be explained by both patterns of reproductive sharing and the nature of the social landscape.     

Effect of Flumethrin on Survival and Olfactory Learning in Honeybees

Flumethrin has been widely used as an acaricide for the control of Varroa mites in commercial honeybee keeping throughout the world for many years. Here we test the mortality of the Asian honeybee Apis cerana cerana after treatment with flumethrin. We also ask (1) how bees react to the odor of flumethrin, (2) whether its odor induces an innate avoidance response, (3) whether its taste transmits an aversive reinforcing component in olfactory learning, and (4) whether its odor or taste can be associated with reward in classical conditioning. Our results show that flumethrin has a negative effect on Apis ceranàs lifespan, induces an innate avoidance response, acts as a punishing reinforcer in olfactory learning, and interferes with the association of an appetitive conditioned stimulus. Furthermore flumethrin uptake within the colony reduces olfactory learning over an extended period of time.     

High recombination frequency creates genotypic diversity in colonies of the leaf-cutting ant Acromyrmex echinatior

Honeybees are known to have genetically diverse colonies because queens mate with many males and the recombination rate is extremely high. Genetic diversity among social insect workers has been hypothesized to improve general performance of large and complex colonies, but this idea has not been tested in other social insects. Here, we present a linkage map and an estimate of the recombination rate for Acromyrmex echinatior, a leaf-cutting ant that resembles the honeybee in having multiple mating of queens and colonies of approximately the same size. A map of 145 AFLP markers in 22 linkage groups yielded a total recombinational size of 2076 cM and an inferred recombination rate of 161 kb cM(-1) (or 6.2 cM Mb(-1)). This estimate is lower than in the honeybee but, as far as the mapping criteria can be compared, higher than in any other insect mapped so far. Earlier studies on A. echinatior have demonstrated that variation in division of labour and pathogen resistance has a genetic component and that genotypic diversity among workers may thus give colonies of this leaf-cutting ant a functional advantage. The present result is therefore consistent with the hypothesis that complex social life can select for an increased recombination rate through effects on genotypic diversity and colony performance.     

Subfamily‐dependent alternative reproductive strategies in worker honeybees

Functional worker sterility is the defining feature of insect societies. Yet, workers are sometimes found reproducing in their own or foreign colonies. The proximate mechanisms underlying these alternative reproductive phenotypes are keys to understanding how reproductive altruism and selfishness are balanced in eusocial insects. In this study, we show that in honeybee (Apis mellifera) colonies, the social environment of a worker, that is, the presence and relatedness of the queens in a worker's natal colony and in surrounding colonies, significantly influences her fertility and drifting behaviour. Furthermore, subfamilies vary in the frequency of worker ovarian activation, propensity to drift and the kind of host colony that is targeted for reproductive parasitism. Our results show that there is an interplay between a worker's subfamily, reproductive state and social environment that substantially affects her reproductive phenotype. Our study further indicates that honeybee populations show substantial genetic variance for worker reproductive strategies, suggesting that no one strategy is optimal under all the circumstances that a typical worker may encounter.     

Diurnal and Seasonal Changes in Thermal Preference of Single,Isolated Bees and Small Groups of Bees (Apis mellifera L.)

The aim of the present study was: to compare thermoregulatory behaviour of single honeybee workers and groups of 3–15 bees over their annual activity period and to check out whether the annual fluctuations of ambient temperature selection are correlated with phases of the colony development. Thermal behaviour of both single workers and groups of bees was recorded, using a video camera, in a thermal gradient system. Thermal preferences of the insects were tested seasonally in spring (May/June), summer (July/August) and autumn (September–November). Both single bees and small groups of bees changed their thermal behaviour in daily cycle. The season of the year had distinct effect on temperature preferences of both single honeybee workers or small groups of bees. In single honeybee workers the lowest ambient temperatures were preferred in late spring (the swarming phase) while the highest temperatures were selected during the summer (the colony growing phase). There were significant seasonal changes in ambient temperature selected by groups of honeybee workers. Groups of honeybee workers tended to prefer the lowest temperatures in late spring and the highest temperatures were selected during the summer. The day-night differences exhibited by small groups of bees in our experiments are likely to represent behavioural responses of the honeybee colony. In our experiments we proved an influence of the season of the year on the honeybees’ thermal behaviour, which might be connected with seasonal shifts of temperature regulated by the honeybee colony.     

蜜蜂上颚腺及其分泌物研究进展

上颚腺是蜜蜂重要的外分泌腺体,其分泌物是维系蜂群社会性结构的重要物质。蜂王和工蜂上颚腺分泌物合成均以硬脂酸为合成前体,但在脂肪酸的β-氧化过程中表现出级型差异性,导致分泌物组分比例不同。蜂王上颚腺分泌物以9-羰基-2癸烯酸(9-ODA)为主,有吸引工蜂和雄蜂、抑制工蜂卵巢发育等作用;工蜂上颚腺分泌物以10-羟基-2癸烯酸(10-HDA)和10-羟基癸酸(10-HDAA)为主,是蜂王浆的重要组成部分。同时,这种具备典型级型差异的分泌物组成又具有级型间可塑性,在不同蜂种间也存在区别。近年来在转录水平和蛋白水平的一些研究进一步揭示了级型间差异的分子基础。针对蜜蜂上颚腺及其分泌物的研究在蜜蜂生物学、行为学和蜂产品质量控制等方面具有重要的意义。本文通过总结国内外相关研究进展,旨在为上颚腺分泌物的作用机制、生物合成机制等领域的进一步深入研究提供借鉴。