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Honey bee colonies are highly dependent upon the availability of floral resources from which they get the nutrients (notably pollen) necessary to their development and survival. However, foraging areas are currently affected by the intensification of agriculture and landscape alteration. Bees are therefore confronted to disparities in time and space of floral resource abundance, type and diversity, which might provide inadequate nutrition and endanger colonies. The beneficial influence of pollen availability on bee health is well-established but whether quality and diversity of pollen diets can modify bee health remains largely unknown. We therefore tested the influence of pollen diet quality (different monofloral pollens) and diversity (polyfloral pollen diet) on the physiology of young nurse bees, which have a distinct nutritional physiology (e.g. hypopharyngeal gland development and vitellogenin level), and on the tolerance to the microsporidian parasite Nosemaceranae by measuring bee survival and the activity of different enzymes potentially involved in bee health and defense response (glutathione-S-transferase (detoxification), phenoloxidase (immunity) and alkaline phosphatase (metabolism)). We found that both nurse bee physiology and the tolerance to the parasite were affected by pollen quality. Pollen diet diversity had no effect on the nurse bee physiology and the survival of healthy bees. However, when parasitized, bees fed with the polyfloral blend lived longer than bees fed with monofloral pollens, excepted for the protein-richest monofloral pollen. Furthermore, the survival was positively correlated to alkaline phosphatase activity in healthy bees and to phenoloxydase activities in infected bees. Our results support the idea that both the quality and diversity (in a specific context) of pollen can shape bee physiology and might help to better understand the influence of agriculture and land-use intensification on bee nutrition and health.

Background Malnutrition is a major factor affecting animal health, resistance to disease and survival. In honey bees ( Apis mellifera ), pollen, which is the main dietary source of proteins, amino acids and lipids, is essential to adult bee physiological development while reducing their susceptibility to parasites and pathogens. However, the molecular mechanisms underlying pollen's nutritive impact on honey bee health remained to be determined. For that purpose, we investigated the influence of pollen nutrients on the transcriptome of worker bees parasitized by the mite Varroa destructor , known for suppressing immunity and decreasing lifespan. The 4 experimental groups (control bees without a pollen diet, control bees fed with pollen, varroa-parasitized bees without a pollen diet and varroa-parasitized bees fed with pollen) were analyzed by performing a digital gene expression (DGE) analysis on bee abdomens. Results Around 36, 000 unique tags were generated per DGE-tag library, which matched about 8, 000 genes (60% of the genes in the honey bee genome). Comparing the transcriptome of bees fed with pollen and sugar and bees restricted to a sugar diet, we found that pollen activates nutrient-sensing and metabolic pathways. In addition, those nutrients had a positive influence on genes affecting longevity and the production of some antimicrobial peptides. However, varroa parasitism caused the development of viral populations and a decrease in metabolism, specifically by inhibiting protein metabolism essential to bee health. This harmful effect was not reversed by pollen intake. Conclusions The DGE-tag profiling methods used in this study proved to be a powerful means for analyzing transcriptome variation related to nutrient intake in honey bees. Ultimately, with such an approach, applying genomics tools to nutrition research, nutrigenomics promises to offer a better understanding of how nutrition influences body homeostasis and may help reduce the susceptibility of bees to (less virulent) pathogens.

A prominent theory states that animal phenotypes arise by evolutionary changes in gene regulation, but the extent to which this theory holds true for behavioral evolution is not known. Because \"nature and nurture\" are now understood to involve hereditary and environmental influences on gene expression, we studied whether environmental influences on a behavioral phenotype, i.e., aggression, could have evolved into inherited differences via changes in gene expression. Here, with microarray analysis of honey bees, we show that aggression-related genes with inherited patterns of brain expression are also environmentally regulated. There were expression differences in the brain for hundreds of genes between the highly aggressive Africanized honey bee compared with European honey bee (EHB) subspecies. Similar results were obtained for EHB in response to exposure to alarm pheromone (which provokes aggression) and when comparing old and young bees (aggressive tendencies increase with age). There was significant overlap of the gene lists generated from these three microarray experiments. Moreover, there was statistical enrichment of several of the same cis regulatory motifs in promoters of genes on all three gene lists. Aggression shows a remarkably robust brain molecular signature regardless of whether it occurs because of inherited, age-related, or environmental (social) factors. It appears that one element in the evolution of different degrees of aggressive behavior in honey bees involved changes in regulation of genes that mediate the response to alarm pheromone.

In honey bees, Varroa sensitive hygiene (VSH) behaviour, which involves the detection and removal of brood parasitised by the mite Varroa destructor , can actively participate in the survival of colonies facing Varroa outbreaks. This study investigated the mechanisms of VSH behaviour, by comparing the antennal transcriptomes of bees that do and do not perform VSH behaviour. Results indicate that antennae likely play a key role in the expression of VSH behaviour. Comparisons with the antennal transcriptome of nurse and forager bees suggest that VSH profile is more similar to that of nurse bees than foragers. Enhanced detection of certain odorants in VSH bees may be predicted from transcriptional patterns, as well as a higher metabolism and antennal motor activity. Interestingly, Deformed wing virus/ Varroa destructor virus infections were detected in the antennae, with higher level in non-VSH bees; a putative negative impact of viral infection on bees’ ability to display VSH behaviour is proposed. These results bring new perspectives to the understanding of VSH behaviour and the evolution of collective defence by focusing attention on the importance of the peripheral nervous system. In addition, such data might be useful for promoting marker-assisted selection of honey bees that can survive Varroa infestations.

Primer and releaser pheromones are molecules used for communication that induce species-specific responses. In contrast to primer pheromones, it is not known whether the quicker-acting releaser pheromones can affect brain gene expression. We show here that isopentyl acetate (IPA), a releaser pheromone that communicates alarm in honey bees, not only provokes a quick defensive response but also influences behavior for a longer period of time and affects brain gene expression. Exposure to IPA affected behavioral responsiveness to subsequent exposures to IPA and induced the expression of the immediate early gene and transcription factor c-Jun in the antennal lobes. Our findings blur the long-standing distinction between primer and releaser pheromone and highlight the pervasiveness of environmental regulation of brain gene expression.

Intensive agricultural systems often expose honey bees (Apis mellifera L.) to large temporal variations in the availability (quantity, quality and diversity) of nutritional resources. Such nutritional irregularity is expected to affect honey bee health. We therefore tested under laboratory conditions the effect of such variation in pollen availability on honey bee health (survival and nursing physiology-hypopharyngeal gland development and vitellogenin expression). We fed honey bees with different diets composed of pollen pellets collected by honey bees in an agricultural landscape of western France. Slight drops (5-10%) in the availability of oilseed rape (Brassica napus L.) pollen resulted in significant reductions of all tested variables. Despite some variations in taxonomic diversity and nutritional quality, the pollen mixes harvested over the season had a similar positive influence on honey bee health, except for the one collected in late July that induced poor survival and nursing physiology. This period coincided with the mass-flowering of maize (Zea mays L.), an anemophilous crop which produces poor-quality pollen. Therefore, changes in bee health were not connected to variations in pollen diversity but rather to variations in pollen depletion and quality, such as can be encountered in an intensive agricultural system of western France. Finally, even though pollen can be available ad libitum during the mass-flowering of some crops (e.g. maize), it can fail to provide bees with diet adequate for their development.

Honey bees are highly important pollinators in agroecosystems, but they are currently under growing environmental pressures (e.g., from pesticides, poor nutrition, and parasites). Due to the multiplicity of environmental stress factors, their protection requires diverse and integrative approaches. Among those is the development of immunomodulatory tools, as immunosuppression is often observed in stressed bees. Toward this goal, the use of exogenous bacteria with immunomodulatory potential has recently been investigated, but knowledge about the potential of honey bee endogenous bacteria is limited. We therefore tested the influence of single strains of five species of endogenous lactic acid bacteria strains on the bee immune system during the larval stage. We measured the expression level of seven immune-related genes and the gene encoding the storage protein Hexamerin 70b. Two of the strains induced an immune stimulation, but this was limited to the antimicrobial peptide Apidaecin1. Upregulation of Apidaecin1 was associated to the downregulation of Hexamerin 70b. Those results suggest that the bee response to endogenous bacteria is specific both at the species and immune levels. As immune responses are costly, this specificity may be adaptive for saving energy and avoiding any negative side effects on the host development or survival. Further screening of bacteria immunomodulatory potential is needed, but associated immune cost needs to be taken into account for improving honey bee resilience to environmental stress.

Understanding how anthropogenic landscape alteration affects populations of ecologically- and economically-important insect pollinators has never been more pressing. In this context, the assessment of landscape quality typically relies on spatial distribution studies, but, whether habitatrestoration techniques actually improve the health of targeted pollinator populations remains obscure. This gap could be filled by a comprehensive understanding of how gradients of landscape quality influence pollinator physiology. We therefore used this approach for honey bees (Apis mellifera) to test whether landscape patterns can shape bee health. We focused on the pre-wintering period since abnormally high winter colony losses have often been observed. By exposing colonies to differentlandscapes, enriched in melliferous catch crops and surrounded by semi-natural habitats, we found that bee physiology (i.e. fat body mass and level of vitellogenin) was significantly improved by the presence of flowering catch crops. Catch crop presence was associated with a significant increase in pollen diet diversity. The influence of semi-natural habitats on bee health was even stronger. Vitellogenin level was in turn significantly linked to higher overwintering survival. Therefore, our experimental study, combining landscape ecology and bee physiology, offers an exciting proof-of-concept for directly identifying stressful or suitable landscapes and promoting efficient pollinator conservation.

Honeybee colonies are increasingly exposed to environmental stress factors, which can lead to their decline or failure. However, there are major gaps in stressor risk assessment due to the difficulty of assessing the honeybee colony state and detecting abnormal events. Since stress factors usually induce a demographic disturbance in the colony (e.g. loss of foragers, early transition from nurse to forager state), we suggest that disturbances could be revealed indirectly by measuring the age- and task-related physiological state of bees, which can be referred to as biological age (an indicator of the changes in physiological state that occur throughout an individual lifespan). We therefore estimated the biological age of bees from the relationship between age and biomarkers of task specialization (vitellogenin and the adipokinetic hormone receptor). This relationship was determined from a calibrated sample set of known-age bees and mathematically modelled for biological age prediction. Then, we determined throughout the foraging season the evolution of the biological age of bees from colonies with low (conventional apiary) or high Varroa destructor infestation rates (organic apiary). We found that the biological age of bees from the conventional apiary progressively decreased from the spring (17 days) to the fall (6 days). However, in colonies from the organic apiary, the population aged from spring (13 days) to summer (18.5 days) and then rejuvenated in the fall (13 days) after Varroa treatment. Biological age was positively correlated with the amount of brood (open and closed cells) in the apiary with low Varroa pressure, and negatively correlated with Varroa infestation level in the apiary with high Varroa pressure. Altogether, these results show that the estimation of biological age is a useful and effective method for assessing colony demographic state and likely detrimental effects of stress factors.

Background In social insects, the queen is essential to the functioning and homeostasis of the colony. This influence has been demonstrated to be mediated through pheromone communication. However, the only social insect for which any queen pheromone has been identified is the honey bee ( Apis mellifera ) with its well-known queen mandibular pheromone (QMP). Although pleiotropic effects on colony regulation are accredited to the QMP, this pheromone does not trigger the full behavioral and physiological response observed in the presence of the queen, suggesting the presence of additional compounds. We tested the hypothesis of a pheromone redundancy in honey bee queens by comparing the influence of queens with and without mandibular glands on worker behavior and physiology. Results Demandibulated queens had no detectable (E)-9-oxodec-2-enoic acid (9-ODA), the major compound in QMP, yet they controlled worker behavior (cell construction and queen retinue) and physiology (ovary inhibition) as efficiently as intact queens. Conclusions We demonstrated that the queen uses other pheromones as powerful as QMP to control the colony. It follows that queens appear to have multiple active compounds with similar functions in the colony (pheromone redundancy). Our findings support two hypotheses in the biology of social insects: (1) that multiple semiochemicals with synonymous meaning exist in the honey bee, (2) that this extensive semiochemical vocabulary exists because it confers an evolutionary advantage to the colony.