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Here we report the genome sequence of the honeybee Apis mellifera, a key model for social behaviour and essential to global ecology through pollination. Compared with other sequenced insect genomes, the A. mellifera genome has high A+T and CpG contents, lacks major transposon families, evolves more slowly, and is more similar to vertebrates for circadian rhythm, RNA interference and DNA methylation genes, among others. Furthermore, A. mellifera has fewer genes for innate immunity, detoxification enzymes, cuticle-forming proteins and gustatory receptors, more genes for odorant receptors, and novel genes for nectar and pollen utilization, consistent with its ecology and social organization. Compared to Drosophila, genes in early developmental pathways differ in Apis, whereas similarities exist for functions that differ markedly, such as sex determination, brain function and behaviour. Population genetics suggests a novel African origin for the species A. mellifera and insights into whether Africanized bees spread throughout the New World via hybridization or displacement.

Key Points A distinctive microbial community of approximately nine bacterial species clusters inhabits the bee gut. These bacteria are host-adapted, and each species cluster occupies particular niches and spatial locations in the bee. The gut microbial community of the bee is transmitted through social contact, similar to the mode of transmission in mammals. The characteristic microbial community of the bee gut can be perturbed and invaded by opportunistic microorganisms, which resembles disease states in humans. There is substantial strain-level diversity in the bee gut microbiota, with individual strains harbouring unique sets of genes with distinct functional capabilities. How this diversity arises and is maintained is not well understood. Metabolically, most members of the microbial community in the bee gut are fermentative, breaking down the carbohydrate-rich diet of bees into products, such as lactic acid and acetate. Although not yet well-established, these fermentative microorganisms may have a role in contributing to the nutrition of hosts. The normal bee gut microbiota has been associated with lower levels of infection with pathogens, which may indicate a beneficial role of the microbiota for the host bee. The bee gut microbiota can be cultured in vitro , and gnotobiotic bees can be easily produced, which makes bees a tractable model for the study of the symbiosis of gut microorganisms. The gut of honey bees is inhabited by a small group of highly host-adapted bacteria. In this Review, Kwong and Moran detail the composition and functions of the microbiota of honey bees and highlight similarities and differences to the human microbiota. The gut microbiota can have profound effects on hosts, but the study of these relationships in humans is challenging. The specialized gut microbial community of honey bees is similar to the mammalian microbiota, as both are mostly composed of host-adapted, facultatively anaerobic and microaerophilic bacteria. However, the microbial community of the bee gut is far simpler than the mammalian microbiota, being dominated by only nine bacterial species clusters that are specific to bees and that are transmitted through social interactions between individuals. Recent developments, which include the discovery of extensive strain-level variation, evidence of protective and nutritional functions, and reports of eco-physiological or disease-associated perturbations to the microbial community, have drawn attention to the role of the microbiota in bee health and its potential as a model for studying the ecology and evolution of gut symbionts.

Wild and managed pollinators provide a wide range of benefits to society in terms of contributions to food security, farmer and beekeeper livelihoods, social and cultural values, as well as the maintenance of wider biodiversity and ecosystem stability. Pollinators face numerous threats, including changes in land-use and management intensity, climate change, pesticides and genetically modified crops, pollinator management and pathogens, and invasive alien species. There are well-documented declines in some wild and managed pollinators in several regions of the world. However, many effective policy and management responses can be implemented to safeguard pollinators and sustain pollination services. Wild and managed pollinators are threatened by pressures such as environmental changes and pesticides, leading to risks for pollinator-dependent crop production, meaning more research and better policies are needed to safeguard pollinators and their services. Take care of the pollinators Pollinators provide numerous goods and services to society, and help to maintain ecosystem health and function, but their numbers are in decline in several parts of the world. In this Review, Simon Potts et al . synthesize data on the current status of pollinators, outline the main drivers of their decline, and discuss the policy and management intervention that can help to safeguard their survival.

Social bees harbor a simple and specialized microbiota that is spatially organized into different gut compartments. Recent results on the potential involvement of bee gut communities in pathogen protection and nutritional function have drawn attention to the impact of the microbiota on bee health. However, the contributions of gut microbiota to host physiology have yet to be investigated. Here we show that the gut microbiota promotes weight gain of both whole body and the gut in individual honey bees. This effect is likely mediated by changes in host vitellogenin, insulin signaling, and gustatory response. We found that microbial metabolism markedly reduces gut pH and redox potential through the production of shortchain fatty acids and that the bacteria adjacent to the gut wall form an oxygen gradient within the intestine. The short-chain fatty acid profile contributed by dominant gut species was confirmed in vitro. Furthermore, metabolomic analyses revealed that the gut community has striking impacts on the metabolic profiles of the gut compartments and the hemolymph, suggesting that gut bacteria degrade plant polymers from pollen and that the resulting metabolites contribute to host nutrition. Our results demonstrate how microbial metabolism affects bee growth, hormonal signaling, behavior, and gut physicochemical conditions. These findings indicate that the bee gut microbiota has basic roles similar to those found in some other animals and thus provides a model in studies of host–microbe interactions.

The western honey bee (Apis mellifera) is the most frequent floral visitor of crops worldwide, but quantitative knowledge of its role as a pollinator outside of managed habitats is largely lacking. Here we use a global dataset of 80 published plant–pollinator interaction networks as well as pollinator effectiveness measures from 34 plant species to assess the importance of A. mellifera in natural habitats. Apis mellifera is the most frequent floral visitor in natural habitats worldwide, averaging 13% of floral visits across all networks (range 0–85%), with 5% of plant species recorded as being exclusively visited by A. mellifera. For 33% of the networks and 49% of plant species, however, A. mellifera visitation was never observed, illustrating that many flowering plant taxa and assemblages remain dependent on non-A. mellifera visitors for pollination. Apis mellifera visitation was higher in warmer, less variable climates and on mainland rather than island sites, but did not differ between its native and introduced ranges. With respect to single-visit pollination effectiveness, A. mellifera did not differ from the average non-A. mellifera floral visitor, though it was generally less effective than the most effective non-A. mellifera visitor. Our results argue for a deeper understanding of how A. mellifera, and potential future changes in its range and abundance, shape the ecology, evolution, and conservation of plants, pollinators, and their interactions in natural habitats.

Despite substantial evidence that neonicotinoid pesticides can have negative effects on bees, there have been no reports that this leads to problems with pollination; here bumblebee colonies exposed to a neonicotinoid are shown to provide reduced pollination services to apple trees, leading to a reduction in seed number. Reduced pollination by neonicotinoid-exposed bees There is now substantial evidence that neonicotinoid pesticides can have negative effects on bees. However, it has not been shown that this leads to problems with the ecosystem service that bees provide, pollination. These authors show, in field tests involving 100 apple trees, that bumblebees exposed to a neonicotinoid provide less efficient pollination, leading to a reduction in seed number. Recent concern over global pollinator declines has led to considerable research on the effects of pesticides on bees 1 , 2 , 3 , 4 , 5 . Although pesticides are typically not encountered at lethal levels in the field, there is growing evidence indicating that exposure to field-realistic levels can have sublethal effects on bees, affecting their foraging behaviour 1 , 6 , 7 , homing ability 8 , 9 and reproductive success 2 , 5 . Bees are essential for the pollination of a wide variety of crops and the majority of wild flowering plants 10 , 11 , 12 , but until now research on pesticide effects has been limited to direct effects on bees themselves and not on the pollination services they provide. Here we show the first evidence to our knowledge that pesticide exposure can reduce the pollination services bumblebees deliver to apples, a crop of global economic importance. Bumblebee colonies exposed to a neonicotinoid pesticide provided lower visitation rates to apple trees and collected pollen less often. Most importantly, these pesticide-exposed colonies produced apples containing fewer seeds, demonstrating a reduced delivery of pollination services. Our results also indicate that reduced pollination service delivery is not due to pesticide-induced changes in individual bee behaviour, but most likely due to effects at the colony level. These findings show that pesticide exposure can impair the ability of bees to provide pollination services, with important implications for both the sustained delivery of stable crop yields and the functioning of natural ecosystems.

Wild and managed bees are well documented as effective pollinators of global crops of economic importance. However, the contributions by pollinators other than bees have been little explored despite their potential to contribute to crop production and stability in the face of environmental change. Non-bee pollinators include flies, beetles, moths, butterflies, wasps, ants, birds, and bats, among others. Here we focus on non-bee insects and synthesize 39 field studies from five continents that directly measured the crop pollination services provided by non-bees, honey bees, and other bees to compare the relative contributions of these taxa. Non-bees performed 25–50% of the total number of flower visits. Although non-bees were less effective pollinators than bees per flower visit, they made more visits; thus these two factors compensated for each other, resulting in pollination services rendered by non-bees that were similar to those provided by bees. In the subset of studies that measured fruit set, fruit set increased with non-bee insect visits independently of bee visitation rates, indicating that non-bee insects provide a unique benefit that is not provided by bees. We also show that non-bee insects are not as reliant as bees on the presence of remnant natural or seminatural habitat in the surrounding landscape. These results strongly suggest that non-bee insect pollinators play a significant role in global crop production and respond differently than bees to landscape structure, probably making their crop pollination services more robust to changes in land use. Non-bee insects provide a valuable service and provide potential insurance against bee population declines.

Urbanisation is an important global driver of biodiversity change, negatively impacting some species groups whilst providing opportunities for others. Yet its impact on ecosystem services is poorly investigated. Here, using a replicated experimental design, we test how Central European cities impact flying insects and the ecosystem service of pollination. City sites have lower insect species richness, particularly of Diptera and Lepidoptera, than neighbouring rural sites. In contrast, Hymenoptera, especially bees, show higher species richness and flower visitation rates in cities, where our experimentally derived measure of pollination is correspondingly higher. As well as revealing facets of biodiversity (e.g. phylogenetic diversity) that correlate well with pollination, we also find that ecotones in insect-friendly green cover surrounding both urban and rural sites boost pollination. Appropriately managed cities could enhance the conservation of Hymenoptera and thereby act as hotspots for pollination services that bees provide to wild flowers and crops grown in urban settings. Pollinators can persist in urban areas despite little natural habitat. Here the authors compare insect pollinators and pollination inside and outside of German cities, showing that urban areas have high diversity of bees but not other insects, and high pollination provisioning, relative to rural sites.

Laboratory infection experiments and field data show that emerging infectious diseases of honeybees are widespread infectious agents within the pollinator assemblage; the prevalence of deformed wing virus (DWV) and the parasite Nosema ceranae in honeybees and bumblebees is linked, and sympatric bumblebees and honeybees are infected by the same DWV strains, indicating ongoing disease transmission. Honeybee diseases threaten wild pollinators Efficient pollination is vital for both crop production and ecosystem sustainability, and there is evidence to suggest that emerging infectious diseases are contributing to a decline in populations of some important insect pollinators. This study combines laboratory infection experiments and field studies to demonstrate infectivity of two serious honeybee ( Apis mellifera ) pathogens in a wild pollinator, the bumblebee ( Bombus terrestris ). Data from across the United Kingdom show that there is co-localization of deformed wing virus (DWV) and the microsporidian parasite Nosema ceranae in the two types of pollinator, and that the honeybee disease can be infectious in bumblebees. This work indicates that wild pollinator populations may be at risk, and unlike managed populations of Apis , they are not protected by intervention from beekeepers. Such a loss of wild pollinators would significantly decrease crop pollination efficiency. Emerging infectious diseases (EIDs) pose a risk to human welfare, both directly 1 and indirectly, by affecting managed livestock and wildlife that provide valuable resources and ecosystem services, such as the pollination of crops 2 . Honeybees ( Apis mellifera ), the prevailing managed insect crop pollinator, suffer from a range of emerging and exotic high-impact pathogens 3 , 4 , and population maintenance requires active management by beekeepers to control them. Wild pollinators such as bumblebees ( Bombus spp.) are in global decline 5 , 6 , one cause of which may be pathogen spillover from managed pollinators like honeybees 7 , 8 or commercial colonies of bumblebees 9 . Here we use a combination of infection experiments and landscape-scale field data to show that honeybee EIDs are indeed widespread infectious agents within the pollinator assemblage. The prevalence of deformed wing virus (DWV) and the exotic parasite Nosema ceranae in honeybees and bumblebees is linked; as honeybees have higher DWV prevalence, and sympatric bumblebees and honeybees are infected by the same DWV strains, Apis is the likely source of at least one major EID in wild pollinators. Lessons learned from vertebrates 10 , 11 highlight the need for increased pathogen control in managed bee species to maintain wild pollinators, as declines in native pollinators may be caused by interspecies pathogen transmission originating from managed pollinators.

Bees acquire carbohydrates from nectar and lipids; and amino acids from pollen, which also contains polysaccharides including cellulose, hemicellulose, and pectin. These potential energy sources could be degraded and fermented through microbial enzymatic activity, resulting in short chain fatty acids available to hosts. However, the contributions of individual microbiota members to polysaccharide digestion have remained unclear. Through analysis of bacterial isolate genomes and a metagenome of the honey bee gut microbiota, we identify that Bifidobacterium and Gilliamella are the principal degraders of hemicellulose and pectin. Both Bifidobacterium and Gilliamella show extensive strain-level diversity in gene repertoires linked to polysaccharide digestion. Strains from honey bees possess more such genes than strains from bumble bees. In Bifidobacterium, genes encoding carbohydrate-active enzymes are colocated within loci devoted to polysaccharide utilization, as in Bacteroides from the human gut. Carbohydrate-active enzyme-encoding gene expressions are up-regulated in response to particular hemicelluloses both in vitro and in vivo. Metabolomic analyses document that bees experimentally colonized by different strains generate distinctive gut metabolomic profiles, with enrichment for specific monosaccharides, corresponding to predictions from genomic data. The other 3 core gut species clusters (Snodgrassella and 2 Lactobacillus clusters) possess few or no genes for polysaccharide digestion. Together, these findings indicate that strain composition within individual hosts determines the metabolic capabilities and potentially affects host nutrition. Furthermore, the niche specialization revealed by our study may promote overall community stability in the gut microbiomes of bees.