A Secreted RNA Binding Protein Forms RNA-Stabilizing Granules in the Honeybee Royal Jelly.

RNA flow between organisms has been documented within and among different kingdoms of life. Recently, we demonstrated horizontal RNA transfer between honeybees involving secretion and ingestion of worker and royal jellies. However, how the jelly facilitates transfer of RNA is still unknown. Here, we show that worker and royal jellies harbor robust RNA-binding activity. We report that a highly abundant jelly component, major royal jelly protein 3 (MRJP-3), acts as an extracellular non-sequence-specific RNA-aggregating factor. Multivalent RNA binding stimulates higher-order assembly of MRJP-3 into extracellular ribonucleoprotein granules that protect RNA from degradation and enhance RNA bioavailability. These findings reveal that honeybees have evolved a secreted dietary RNA-binding factor to concentrate, stabilize, and share RNA among individuals. Our work identifies high-order ribonucleoprotein assemblies with functions outside cells and organisms.

The expansion of agriculture has shaped the recent evolutionary history of a specialized squash pollinator.

The expansion of agriculture is responsible for the mass conversion of biologically diverse natural environments into managed agroecosystems dominated by a handful of genetically homogeneous crop species. Agricultural ecosystems typically have very different abiotic and ecological conditions from those they replaced and create potential niches for those species that are able to exploit the abundant resources offered by crop plants. While there are well-studied examples of crop pests that have adapted into novel agricultural niches, the impact of agricultural intensification on the evolution of crop mutualists such as pollinators is poorly understood. We combined genealogical inference from genomic data with archaeological records to demonstrate that the Holocene demographic history of a wild specialist pollinator of Cucurbita (pumpkins, squashes, and gourds) has been profoundly impacted by the history of agricultural expansion in North America. Populations of the squash bee Eucera pruinosa experienced rapid growth in areas where agriculture intensified within the past 1,000 y, suggesting that the cultivation of Cucurbita in North America has increased the amount of floral resources available to these bees. In addition, we found that roughly 20% of this bee species' genome shows signatures of recent selective sweeps. These signatures are overwhelmingly concentrated in populations from eastern North America where squash bees were historically able to colonize novel environments due to human cultivation of Cucurbita pepo and now exclusively inhabit agricultural niches. These results suggest that the widespread cultivation of crops can prompt adaptation in wild pollinators through the distinct ecological conditions imposed by agricultural environments.

Diverse communication strategies in bees as a window into adaptations to an unpredictable world.

Communication is a fundamental feature of animal societies and helps their members to solve the challenges they encounter, from exploiting food sources to fighting enemies or finding a new home. Eusocial bees inhabit a wide range of environments and they have evolved a multitude of communication signals that help them exploit resources in their environment efficiently. We highlight recent advances in our understanding of bee communication strategies and discuss how variation in social biology, such as colony size or nesting habits, and ecological conditions are important drivers of variation in communication strategies. Anthropogenic factors, such as habitat conversion, climate change, or the use of agrochemicals, are changing the world bees inhabit, and it is becoming clear that this affects communication both directly and indirectly, for example by affecting food source availability, social interactions among nestmates, and cognitive functions. Whether and how bees adapt their foraging and communication strategies to these changes represents a new frontier in bee behavioral and conservation research.

Recent and future declines of a historically widespread pollinator linked to climate, land cover, and pesticides.

The acute decline in global biodiversity includes not only the loss of rare species, but also the rapid collapse of common species across many different taxa. The loss of pollinating insects is of particular concern because of the ecological and economic values these species provide. The western bumble bee (Bombus occidentalis) was once common in western North America, but this species has become increasingly rare through much of its range. To understand potential mechanisms driving these declines, we used Bayesian occupancy models to investigate the effects of climate and land cover from 1998 to 2020, pesticide use from 2008 to 2014, and projected expected occupancy under three future scenarios. Using 14,457 surveys across 2.8 million km2 in the western United States, we found strong negative relationships between increasing temperature and drought on occupancy and identified neonicotinoids as the pesticides of greatest negative influence across our study region. The mean predicted occupancy declined by 57% from 1998 to 2020, ranging from 15 to 83% declines across 16 ecoregions. Even under the most optimistic scenario, we found continued declines in nearly half of the ecoregions by the 2050s and mean declines of 93% under the most severe scenario across all ecoregions. This assessment underscores the tenuous future of B. occidentalis and demonstrates the scale of stressors likely contributing to rapid loss of related pollinator species throughout the globe. Scaled-up, international species-monitoring schemes and improved integration of data from formal surveys and community science will substantively improve the understanding of stressors and bumble bee population trends.

Biodiversity and pollination benefits trade off against profit in an intensive farming system.

Agricultural expansion and intensification have boosted global food production but have come at the cost of environmental degradation and biodiversity loss. Biodiversity-friendly farming that boosts ecosystem services, such as pollination and natural pest control, is widely being advocated to maintain and improve agricultural productivity while safeguarding biodiversity. A vast body of evidence showing the agronomic benefits of enhanced ecosystem service delivery represent important incentives to adopt practices enhancing biodiversity. However, the costs of biodiversity-friendly management are rarely taken into account and may represent a major barrier impeding uptake by farmers. Whether and how biodiversity conservation, ecosystem service delivery, and farm profit can go hand in hand is unknown. Here, we quantify the ecological, agronomic, and net economic benefits of biodiversity-friendly farming in an intensive grassland-sunflower system in Southwest France. We found that reducing land-use intensity on agricultural grasslands drastically enhances flower availability and wild bee diversity, including rare species. Biodiversity-friendly management on grasslands furthermore resulted in an up to 17% higher revenue on neighboring sunflower fields through positive effects on pollination service delivery. However, the opportunity costs of reduced grassland forage yields consistently exceeded the economic benefits of enhanced sunflower pollination. Our results highlight that profitability is often a key constraint hampering adoption of biodiversity-based farming and uptake critically depends on society's willingness to pay for associated delivery of public goods such as biodiversity.

Repeated shifts in sociality are associated with fine-tuning of highly conserved and lineage-specific enhancers in a socially flexible bee.

Comparative genomic studies of social insects suggest that changes in gene regulation are associated with evolutionary transitions in social behavior, but the activity of predicted regulatory regions has not been tested empirically. We used STARR-seq, a high-throughput enhancer discovery tool, to identify and measure the activity of enhancers in the socially variable sweat bee, Lasioglossum albipes. We identified over 36,000 enhancers in the L. albipes genome from three social and three solitary populations. Many enhancers were identified in only a subset of L. albipes populations, revealing rapid divergence in regulatory regions within this species. Population-specific enhancers were often proximal to the same genes across populations, suggesting compensatory gains and losses of regulatory regions may preserve gene activity. We also identified 1182 enhancers with significant differences in activity between social and solitary populations, some of which are conserved regulatory regions across species of bees. These results indicate that social trait variation in L. albipes is associated with the fine-tuning of ancient enhancers as well as lineage-specific regulatory changes. Combining enhancer activity with population genetic data revealed variants associated with differences in enhancer activity and identified a subset of differential enhancers with signatures of selection associated with social behavior. Together, these results provide the first empirical map of enhancers in a socially flexible bee and highlight links between cis-regulatory variation and the evolution of social behavior.

Crystallography of honeycomb formation under geometric frustration.

As honeybees build their nests in preexisting tree cavities, they must deal with the presence of geometric constraints, resulting in nonregular hexagons and topological defects in the comb. In this work, we study how bees adapt to their environment in order to regulate the comb structure. Specifically, we identify the irregularities in honeycomb structure in the presence of various geometric frustrations. We 3D-print experimental frames with a variety of constraints imposed on the imprinted foundations. The combs constructed by the bees show clear evidence of recurring patterns in response to specific geometric frustrations on these starter frames. Furthermore, using an experimental-modeling framework, we demonstrate that these patterns can be successfully modeled and replicated through a simulated annealing process, in which the minimized potential is a variation of the Lennard-Jones potential that considers only first-neighbor interactions according to a Delaunay triangulation. Our simulation results not only confirm the connection between honeycomb structures and other crystal systems such as graphene, but also show that irregularities in the honeycomb structure can be explained as the result of analogous interactions between cells and their immediate surroundings, leading to emergent global order. Additionally, our computational model can be used as a first step to describe specific strategies that bees use to effectively solve geometric mismatches while minimizing cost of comb building.

An insect brain organizes numbers on a left-to-right mental number line.

The "mental number line" (MNL) is a form of spatial numeric representation that associates small and large numbers with the left and right spaces, respectively. This spatio-numeric organization can be found in adult humans and has been related to cultural factors such as writing and reading habits. Yet, both human newborns and birds order numbers consistently with an MNL, thus raising the question of whether culture is a main explanation for MNL. Here, we explored the numeric sense of honey bees and show that after being trained to associate numbers with a sucrose reward, they order numbers not previously experienced from left to right according to their magnitude. Importantly, the location of a number on that scale varies with the reference number previously trained and does not depend on low-level cues present on numeric stimuli. We provide a series of neural explanations for this effect based on the extensive knowledge accumulated on the neural underpinnings of visual processing in honey bees and conclude that the MNL is a form of numeric representation that is evolutionarily conserved across nervous systems endowed with a sense of number, irrespective of their neural complexity.

What proteomics has taught us about honey bee (Apis mellifera) health and disease.

The Western honey bee, Apis mellifera, is currently navigating a gauntlet of environmental pressures, including the persistent threat of parasites, pathogens, and climate change - all of which compromise the vitality of honey bee colonies. The repercussions of their declining health extend beyond the immediate concerns of apiarists, potentially imposing economic burdens on society through diminished agricultural productivity. Hence, there is an imperative to devise innovative monitoring techniques for assessing the health of honey bee populations. Proteomics, recognized for its proficiency in biomarker identification and protein-protein interactions, is poised to play a pivotal role in this regard. It offers a promising avenue for monitoring and enhancing the resilience of honey bee colonies, thereby contributing to the stability of global food supplies. This review delves into the recent proteomic studies of A. mellifera, highlighting specific proteins of interest and envisioning the potential of proteomics to improve sustainable beekeeping practices amidst the challenges of a changing planet.

Insights from Melipona bicolor hybrid genome assembly: a stingless bee genome with chromosome-level scaffold.

BACKGROUND: The highly eusocial stingless bees are crucial pollinators of native and agricultural ecosystems. Nevertheless, genomic studies within this bee tribe remain scarce. We present the genome assembly of the stingless bee Melipona bicolor. This bee is a remarkable exception to the typical single-queen colony structure, since in this species, multiple queens may coexist and share reproductive duties, resulting in genetically diverse colonies with weak kinship connections. As the only known genuinely polygynous bee, M. bicolor's genome provides a valuable resource for investigating sociality beyond kin selection. RESULTS: The genome was assembled employing a hybrid approach combining short and long reads, resulting in 241 contigs spanning 259 Mb (N50 of 6.2 Mb and 97.5% complete BUSCOs). Comparative analyses shed light on some evolutionary aspects of stingless bee genomics, including multiple chromosomal rearrangements in Melipona. Additionally, we explored the evolution of venom genes in M. bicolor and other stingless bees, revealing that, apart from two genes, the conserved repertoire of venom components remains under purifying selection in this clade. CONCLUSION: This study advances our understanding of stingless bee genomics, contributing to the conservation efforts of these vital pollinators and offering insights into the evolutionary mechanisms driving their unique adaptations.

Genetic Modification of a Hox Locus Drives Mimetic Color Pattern Variation in a Highly Polymorphic Bumble Bee.

Müllerian mimicry provides natural replicates ideal for exploring mechanisms underlying adaptive phenotypic divergence and convergence, yet the genetic mechanisms underlying mimetic variation remain largely unknown. The current study investigates the genetic basis of mimetic color pattern variation in a highly polymorphic bumble bee, Bombus breviceps (Hymenoptera, Apidae). In South Asia, this species and multiple comimetic species converge onto local Müllerian mimicry patterns by shifting the abdominal setal color from orange to black. Genetic crossing between the orange and black phenotypes suggested the color dimorphism being controlled by a single Mendelian locus, with the orange allele being dominant over black. Genome-wide association suggests that a locus at the intergenic region between 2 abdominal fate-determining Hox genes, abd-A and Abd-B, is associated with the color change. This locus is therefore in the same intergenic region but not the same exact locus as found to drive red black midabdominal variation in a distantly related bumble bee species, Bombus melanopygus. Gene expression analysis and RNA interferences suggest that differential expression of an intergenic long noncoding RNA between abd-A and Abd-B at the onset setal color differentiation may drive the orange black color variation by causing a homeotic shift late in development. Analysis of this same color locus in comimetic species reveals no sequence association with the same color shift, suggesting that mimetic convergence is achieved through distinct genetic routes. Our study establishes Hox regions as genomic hotspots for color pattern evolution in bumble bees and demonstrates how pleiotropic developmental loci can drive adaptive radiations in nature.

Pesticides and pollinator brain: How do neonicotinoids affect the central nervous system of bees?

Neonicotinoids represent over a quarter of the global pesticide market. Research on their environmental impact has revealed their adverse effect on the cognitive functions of pollinators, in particular of bees. Cognitive impairments, mostly revealed by behavioural studies, are the phenotypic expression of an alteration in the underlying neural circuits, a matter deserving greater attention. Here, we reviewed studies on the impact of field-relevant doses of neonicotinoids on the neurophysiology and neurodevelopment of bees. In particular, we focus on their olfactory system as much knowledge has been gained on the different brain areas that participate in odour processing. Recent studies have revealed the detrimental effects of neonicotinoids at multiple levels of the olfactory system, including modulation of odorant-induced activity in olfactory sensory neurons, diminished neural responses in the antennal lobe (the first olfactory processing centre) and abnormal development of the neural connectivity within the mushroom bodies (central neuropils involved in multisensory integration, learning and memory storage, among others). Given the importance of olfactory perception for multiple aspects of bee biology, the reported disruption of the olfactory circuit, which can occur even upon exposure to sublethal doses of neonicotinoids, has severe consequences at both individual and colony levels. Moreover, the effects reported for a multimodal structure such as the mushroom bodies indicate that neonicotinoids' impact translates to other sensory domains. Assessing the impact of field-relevant doses of pesticides on bee neurophysiology is crucial for understanding how neonicotinoids influence their behaviour in ecological contexts and for defining effective and sustainable agricultural practices.

Extreme heat exposure of host plants indirectly reduces solitary bee fecundity and survival.

Extreme heat poses a major threat to plants and pollinators, yet the indirect consequences of heat stress are not well understood, particularly for native solitary bees. To determine how brief exposure of extreme heat to flowering plants affects bee behaviour, fecundity, development and survival we conducted a no-choice field cage experiment in which Osmia lignaria were provided blueberry (Vaccinium corymbosum), phacelia (Phacelia tanacetifolia) and white clover (Trifolium repens) that had been previously exposed to either extreme heat (37.5°C) or normal temperatures (25°C) for 4 h during early bloom. Despite a similar number of open flowers and floral visitation frequency between the two treatments, female bees provided with heat-stressed plants laid approximately 70% fewer eggs than females provided with non-stressed plants. Their progeny received similar quantities of pollen provisions between the two treatments, yet larvae consuming pollen from heat-stressed plants had significantly lower survival as larvae and adults. We also observed trends for delayed emergence and reduced adult longevity when larvae consumed heat-stressed pollen. This study is the first to document how short, field-realistic bursts of extreme heat exposure to flowering host plants can indirectly affect bee pollinators and their offspring, with important implications for crop pollination and native bee populations.

Investigating trade-offs between ovary activation and immune protein expression in bumble bee (Bombus impatiens) workers and queens.

Evidence for a trade-off between reproduction and immunity has manifested in many animal species, including social insects. However, investigations in social insect queens present a conundrum: new gynes of many social hymenopterans, such as bumble bees and ants, must first mate, then transition from being solitary to social as they establish their nests, thus experiencing confounding shifts in environmental conditions. Worker bumble bees offer an opportunity to investigate patterns of immune protein expression associated with ovary activation while minimizing extraneous environmental factors and genetic differences. Here, we use proteomics to interrogate the patterns of immune protein expression of female bumble bees (Bombus impatiens) by (i) sampling queens at different stages of their life cycle, then (ii) by sampling workers with different degrees of ovary activation. Patterns of immune protein expression in the haemolymph of queens are consistent with a reproduction-immunity trade-off, but equivalent samples from workers are not. This brings into question whether queen bumble bees really experience a reproduction-immunity trade-off, or if patterns of immune protein expression may actually be due to the selective pressure of the different environmental conditions they are exposed to during their life cycle.

Extensive loss of forage diversity in social bees owing to flower constancy in simulated environments.

Many bees visit just one flower species during a foraging trip, i.e. they show flower constancy. Flower constancy is important for plant reproduction but it could lead to an unbalanced diet, especially in biodiversity-depleted landscapes. It is assumed that flower constancy does not reduce dietary diversity in social bees, such as honeybees or bumblebees, but this has not yet been tested. We used computer simulations to investigate the effects of flower constancy on colony diet in plant species-rich and species-poor landscapes. We also explored if communication about food sources, which is used by many social bees, further reduces forage diversity. Our simulations reveal an extensive loss of forage diversity owing to flower constancy in both species-rich and species-poor environments. Small flower-constant colonies often discovered only 30-50% of all available plant species, thereby increasing the risk of nutritional deficiencies. Communication often interacted with flower constancy to reduce forage diversity further. Finally, we found that food source clustering, but not habitat fragmentation impaired dietary diversity. These findings highlight the nutritional challenges flower-constant bees face in different landscapes and they can aid in the design of measures to increase forage diversity and improve bee nutrition in human-modified landscapes.

Comparability of comparative toxicity: insect sensitivity to imidacloprid reveals huge variations across species but also within species.

Pesticides have been identified as major drivers of insect biodiversity loss. Thus, the study of their effects on non-pest insect species has attracted a lot of attention in recent decades. In general toxicology, the 'gold standard' to assess the toxicity of a substance is to measure mass-specific LD50 (i.e. median lethal dose per unit body mass). In entomology, reviews attempting to compare these data across all available studies are lacking. To fill this gap in knowledge, we performed a systematic review of the lethality of imidacloprid for adult insects. Imidacloprid is possibly the most extensively studied insecticide in recent times, yet we found that little is comparable across studies, owing to both methodological divergence and missing estimates of body mass. By accounting for body mass whenever possible, we show how imidacloprid sensitivity spans across an apparent range of approximately six orders of magnitude across insect species. Very high variability within species can also be observed owing to differences in exposure methods and observation time. We suggest that a more comparable and comprehensive approach has both biological and economic relevance. Ultimately, this would help to identify differences that could direct research towards preventing non-target species from being negatively affected.

Pollen chemical and mechanical defences restrict host-plant use by bees.

Plants produce an array of chemical and mechanical defences that provide protection against many herbivores and pathogens. Putatively defensive compounds and structures can even occur in floral rewards: for example, the pollen of some plant taxa contains toxic compounds or possesses conspicuous spines. Yet little is known about whether pollen defences restrict host-plant use by bees. In other words, do bees, like other insect herbivores, tolerate the defences of their specific host plants while being harmed by non-host defences? To answer this question, we compared the effects of a chemical defence from Lupinus (Fabaceae) pollen and a putative mechanical defence (pollen spines) from Asteraceae pollen on larval survival of nine bee species in the tribe Osmiini (Megachilidae) varying in their pollen-host use. We found that both types of pollen defences reduce larval survival rate in some bee species. These detrimental effects were, however, mediated by host-plant associations, with bees being more tolerant of the pollen defences of their hosts, relative to the defences of plant taxa exploited by other species. This pattern strongly suggests that bees are adapted to the pollen defences of their hosts, and that host-plant use by bees is constrained by their ability to tolerate such defences.

Single and combined exposure to 'bee safe' pesticides alter behaviour and offspring production in a ground-nesting solitary bee (Xenoglossa pruinosa).

Mounting evidence supporting the negative impacts of exposure to neonicotinoids on bees has prompted the registration of novel 'bee-friendly' insecticides for agricultural use. Flupyradifurone (FPF) is a butenolide insecticide that shares the same mode of action as neonicotinoids and has been assessed to be 'practically non-toxic to adult honeybees' using current risk assessment procedures. However, these assessments overlook some routes of exposure specific to wild bees, such as contact with residues in soil for ground-nesters. Co-exposure with other pesticides may also lead to detrimental synergistic effects. In a fully crossed experiment, we assessed the possible lethal and sublethal effects of chronic exposure to two pesticides used on Cucurbita crops, the insecticide Sivanto Prime (FPF) and the fungicide Quadris Top (azoxystrobin and difenoconazole), alone or combined, on solitary ground-nesting squash bees (Xenoglossa pruinosa). Squash bees exposed to Quadris Top collected less pollen per flower visit, while Sivanto-exposed bees produced larger offspring. Pesticide co-exposure induced hyperactivity in female squash bees relative to both the control and single pesticide exposure, and reduced the number of emerging offspring per nest compared to individual pesticide treatments. This study demonstrates that 'low-toxicity' pesticides can adversely affect squash bees under field-realistic exposure, alone or in combination.

Glyphosate effects on growth and biofilm formation in bee gut symbionts and diverse associated bacteria.

Biofilm formation is a common adaptation enabling bacteria to thrive in various environments and withstand external pressures. In the context of host-microbe interactions, biofilms play vital roles in establishing microbiomes associated with animals and plants and are used by opportunistic microbes to facilitate survival within hosts. Investigating biofilm dynamics, composition, and responses to environmental stressors is crucial for understanding microbial community assembly and biofilm regulation in health and disease. In this study, we explore in vivo colonization and in vitro biofilm formation abilities of core members of the honey bee (Apis mellifera) gut microbiota. Additionally, we assess the impact of glyphosate, a widely used herbicide with antimicrobial properties, and a glyphosate-based herbicide formulation on growth and biofilm formation in bee gut symbionts as well as in other biofilm-forming bacteria associated with diverse animals and plants. Our results demonstrate that several strains of core bee gut bacterial species can colonize the bee gut, which probably depends on their ability to form biofilms. Furthermore, glyphosate exposure elicits variable effects on bacterial growth and biofilm formation. In some instances, the effects correlate with the bacteria's ability to encode a susceptible or tolerant version of the enzyme inhibited by glyphosate in the shikimate pathway. However, in other instances, no such correlation is observed. Testing the herbicide formulation further complicates comparisons, as results often diverge from glyphosate exposure alone, suggesting that co-formulants influence bacterial growth and biofilm formation. These findings highlight the nuanced impacts of environmental stressors on microbial biofilms, with both ecological and host health-related implications. IMPORTANCE: Biofilms are essential for microbial communities to establish and thrive in diverse environments. In the honey bee gut, the core microbiota member Snodgrassella alvi forms biofilms, potentially aiding the establishment of other members and promoting interactions with the host. In this study, we show that specific strains of other core members, including Bifidobacterium, Bombilactobacillus, Gilliamella, and Lactobacillus, also form biofilms in vitro. We then examine the impact of glyphosate, a widely used herbicide that can disrupt the bee microbiota, on bacterial growth and biofilm formation. Our findings demonstrate the diverse effects of glyphosate on biofilm formation, ranging from inhibition to enhancement, reflecting observations in other beneficial or pathogenic bacteria associated with animals and plants. Thus, glyphosate exposure may influence bacterial growth and biofilm formation, potentially shaping microbial establishment on host surfaces and impacting health outcomes.

Queen bee gut microbiota extends honeybee lifespan by inhibiting insulin signaling.

Queen and worker bees are natural models for aging research, as their lifespans vary considerably independent of genetic variation. Investigating the reasons why queens live longer than workers is of great significance for research on the universal processes of aging in animals. The gut microbiome has received attention as a vital regulator of host health, while its precise role in honeybee aging needs further investigation. The effects and mechanisms behind the relationship between gut microbiota and worker lifespan were measured by transplanting queen bee gut bacteria (QG) and worker bee gut bacteria (WG) into microbiota-free (MF) workers. The transplantation of QG to MF bees significantly extended the workers' lifespans compared with MF and WG bees. Untargeted metabolomics identified 49 lifespan-related differential metabolites, and Kyoto Encyclopedia of Genes and Genomes analysis of these revealed three lifespan-related metabolic pathways: insulin/insulin-like growth factor signaling, immune, and ketone body metabolism pathways. Further verification showed that QG inhibited the expression of insulin-like peptides (ILPs), and the expression of ILPs was lower in natural queens than in natural workers. QG transplantation also stimulated the expression of antioxidant genes and lowered oxidative damage products in natural queen bees. However, gut microbiota transplantation failed to mimic the immune properties and ketone body metabolism profiles of natural queens and workers. Concisely, QG could increase the antioxidant capacity to extend lifespan by inhibiting insulin signaling. These findings may help determine the mechanisms behind queen longevity and provide further insights into the role of gut symbionts. IMPORTANCE: Queen and worker bees share the same genetic background but have vastly different lifespans. The gut microbiome regulates host health, suggesting that differences in lifespan between queen and worker bees could be related to gut bacteria. Herein, we used an innovative method to transplant gut microbiota from adult queen or worker bees to microbiota-free bees. The transplantation of queen gut microbiota to microbiota-free bees extended their lifespan. Insulin/insulin-like growth factor signaling, a highly conserved metabolic pathway related to lifespan, displayed identical expression profiles in natural queen bees and microbiota-free bees transplanted with queen microbiota. This finding significantly expands our understanding of the relationships between intestinal bacteria, host health, and the biology of aging.