Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Latest Articles
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • Topics
    • Applied and Environmental Science
    • Clinical Science and Epidemiology
    • Ecological and Evolutionary Science
    • Host-Microbe Biology
    • Molecular Biology and Physiology
    • Therapeutics and Prevention
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About mBio
    • Editor in Chief
    • Board of Editors
    • AAM Fellows
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
mBio
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Latest Articles
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • Topics
    • Applied and Environmental Science
    • Clinical Science and Epidemiology
    • Ecological and Evolutionary Science
    • Host-Microbe Biology
    • Molecular Biology and Physiology
    • Therapeutics and Prevention
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About mBio
    • Editor in Chief
    • Board of Editors
    • AAM Fellows
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
Minireview

The Bee Microbiome: Impact on Bee Health and Model for Evolution and Ecology of Host-Microbe Interactions

Philipp Engel, Waldan K. Kwong, Quinn McFrederick, Kirk E. Anderson, Seth Michael Barribeau, James Angus Chandler, R. Scott Cornman, Jacques Dainat, Joachim R. de Miranda, Vincent Doublet, Olivier Emery, Jay D. Evans, Laurent Farinelli, Michelle L. Flenniken, Fredrik Granberg, Juris A. Grasis, Laurent Gauthier, Juliette Hayer, Hauke Koch, Sarah Kocher, Vincent G. Martinson, Nancy Moran, Monica Munoz-Torres, Irene Newton, Robert J. Paxton, Eli Powell, Ben M. Sadd, Paul Schmid-Hempel, Regula Schmid-Hempel, Se Jin Song, Ryan S. Schwarz, Dennis vanEngelsdorp, Benjamin Dainat
Gregory B. Hurst, Invited Editor, R. John Collier, Editor
Philipp Engel
aDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Waldan K. Kwong
bEcology and Evolutionary Biology, Yale University, New Haven, Connecticut, USA
cDepartment of Integrative Biology, University of Texas at Austin, Austin, Texas, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Quinn McFrederick
dDepartment of Entomology, University of California, Riverside, California, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Kirk E. Anderson
eUSDA, Carl Hayden Bee Research Center, Tucson, Arizona, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Seth Michael Barribeau
fDepartment of Biology, East Carolina University, Greenville, North Carolina, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
James Angus Chandler
gDepartment of Microbiology, California Academy of Sciences, San Francisco, California, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
R. Scott Cornman
hU.S. Geological Survey, Fort Collins Science Center, Fort Collins, Colorado, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jacques Dainat
iBioinformatics Infrastructure for Life Sciences (BILS), Linköpings Universitet Victoria Westling, Linköping, Sweden, and Department of Medical Biochemistry and Microbiology Uppsala University, Uppsala, Sweden
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Joachim R. de Miranda
jDepartment of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Joachim R. de Miranda
Vincent Doublet
kInstitute for Biology, Martin Luther University Halle-Wittenberg, Halle, Germany
lGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Olivier Emery
aDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jay D. Evans
mUSDA, ARS Bee Research Laboratory, Beltsville, Maryland, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Laurent Farinelli
nFasteris SA, Plan -les-Ouates, Switzerland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Michelle L. Flenniken
oDepartment of Plant Sciences and Plant Pathology, Montana State University, Bozeman, Montana, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Fredrik Granberg
pSLU, BVF, Virologi, Uppsala, Sweden
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Juris A. Grasis
qDepartment of Biology, North Life Sciences, San Diego State University, San Diego, California, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Laurent Gauthier
aDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
bEcology and Evolutionary Biology, Yale University, New Haven, Connecticut, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Juliette Hayer
rSLU, Institutionen för Husdjursgenetik, Uppsala, Sweden
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Hauke Koch
cDepartment of Integrative Biology, University of Texas at Austin, Austin, Texas, USA
sRoyal Botanic Gardens, Kew, Richmond, Surrey, United Kingdom
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sarah Kocher
tDepartment of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge , Massachusetts , USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Vincent G. Martinson
uDepartment of Biology, University of Rochester, Rochester, New York, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Nancy Moran
cDepartment of Integrative Biology, University of Texas at Austin, Austin, Texas, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Monica Munoz-Torres
vEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley , California , USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Irene Newton
wDepartment of Biology, Indiana University, Bloomington, Indiana, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Robert J. Paxton
kInstitute for Biology, Martin Luther University Halle-Wittenberg, Halle, Germany
lGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Eli Powell
cDepartment of Integrative Biology, University of Texas at Austin, Austin, Texas, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ben M. Sadd
xSchool of Biological Sciences, Illinois State University, Normal, Illinois, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Paul Schmid-Hempel
yETHZ Institut für Integrative Biologie, Zurich, Switzerland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Regula Schmid-Hempel
yETHZ Institut für Integrative Biologie, Zurich, Switzerland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Se Jin Song
zUniversity of Colorado at Boulder, Boulder, Colorado, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Se Jin Song
Ryan S. Schwarz
mUSDA, ARS Bee Research Laboratory, Beltsville, Maryland, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Dennis vanEngelsdorp
aaDepartment of Entomology, University of Maryland, College Park, Maryland, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Benjamin Dainat
abAgroscope, Swiss Bee Research Centre, Bern, Switzerland
acBee Health Extension Service, Apiservice, Bern , Switzerland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Benjamin Dainat
Gregory B. Hurst
Oak Ridge National Laboratory
Roles: Invited Editor
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
R. John Collier
Harvard Medical School
Roles: Editor
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/mBio.02164-15
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

As pollinators, bees are cornerstones for terrestrial ecosystem stability and key components in agricultural productivity. All animals, including bees, are associated with a diverse community of microbes, commonly referred to as the microbiome. The bee microbiome is likely to be a crucial factor affecting host health. However, with the exception of a few pathogens, the impacts of most members of the bee microbiome on host health are poorly understood. Further, the evolutionary and ecological forces that shape and change the microbiome are unclear. Here, we discuss recent progress in our understanding of the bee microbiome, and we present challenges associated with its investigation. We conclude that global coordination of research efforts is needed to fully understand the complex and highly dynamic nature of the interplay between the bee microbiome, its host, and the environment. High-throughput sequencing technologies are ideal for exploring complex biological systems, including host-microbe interactions. To maximize their value and to improve assessment of the factors affecting bee health, sequence data should be archived, curated, and analyzed in ways that promote the synthesis of different studies. To this end, the BeeBiome consortium aims to develop an online database which would provide reference sequences, archive metadata, and host analytical resources. The goal would be to support applied and fundamental research on bees and their associated microbes and to provide a collaborative framework for sharing primary data from different research programs, thus furthering our understanding of the bee microbiome and its impact on pollinator health.

INTRODUCTION

Bees, ranging from wild solitary species to highly social and managed species like honey bees, play key roles in natural and agricultural ecosystems worldwide (1–3). Recent losses of honey bees and wild bees have been attributed to pesticide exposure, poor nutrition, increased parasite loads, habitat degradation, and reduced genetic diversity (4, 5). While the latter cause has been challenged by genome-wide surveys of honey bee populations (6), pesticides, parasites and malnutrition have been experimentally linked to poor bee health (5, 7–11).

Bee-associated microorganisms include a diverse set of viruses, bacteria, fungi, and protists, some of which are important pathogens of bees (12). For example, the two bacterial pathogens Paenibacillus larvae and Melissococcus plutonius are the causative agents of American and European foulbrood, respectively (13, 14). They are spread easily by beekeeping practices, and if left untreated, they are usually lethal to the colony. Their treatment is correspondingly rigorous and expensive, involving the sacrifice of both the colony and hive materials, and, in some countries, quarantine procedures for the affected beekeeping operation and surrounding apiaries.

However, for many pathogens, the precise impacts on honey bee health and colony fitness remain elusive (12). For example, the respective effects on honey bee health of two common microsporidian pathogens, Nosema apis and Nosema ceranae, remain controversial. Some studies suggest that N. ceranae is more virulent than N. apis and may be in part responsible for recent colony losses (15–17). Other studies have failed to show such links, and it has been argued that additional factors might contribute to the virulence of Nosema (5, 18–22).

In addition to microsporidian pathogens, over twenty different bee viruses have been described to date (23, 24). Most can cause detrimental effects, ranging from physiological changes to gross physical deformities, behavioral alterations, and reduced longevity. The degree of pathology may differ between individual hosts, and most viruses can persist chronically and asymptomatically within bee colonies (25). There is accumulating evidence that simultaneous infection with multiple pathogens or the combined exposure to pathogens and pesticides can have synergistic negative effects on bee health (12, 26–32). Furthermore, many honey bee viral pathogens can cross-infect bumblebees, solitary bees, and wasps, suggesting that the pool of pathogens in a particular host, such as the honey bee, must be viewed in the context of a larger set of host species with overlapping geographic ranges (33, 34).

In addition to the plethora of pathogens, honey bees harbor a relatively simple but remarkably specialized and consistent intestinal microbial community, consisting of 8 to 10 bacterial species or phylotypes (i.e., bacteria with ≥97% 16S rRNA sequence identity) (35), belonging to three different phyla: Proteobacteria, Actinobacteria, and Firmicutes. The precise functions of these gut bacteria and the nature of their symbiotic relationships with the host have so far remained largely elusive. Nevertheless, analogous symbionts found in vertebrate gut communities play key roles in host health and assist the host in the face of environmental stress (36, 37). Genomic and metagenomic analyses suggest that bee gut bacteria contribute to the digestion of macromolecules, nutrient provisioning, neutralization of dietary toxins, and defense against parasites (38–40). Whether and to what extent the bacterial gut communities of bees influence pathogen loads, through modulation of the immune response, by providing barriers against invasion, or through competition for nutrients, is still unclear. However, there is evidence that some of the Firmicutes bacteria can inhibit the growth of the two principal honey bee bacterial pathogens, Paenibacillus larvae and Melissococcus plutonius (41, 42). Moreover, in bumble bees, gut communities have been associated with reduced levels of the parasite Crithidia bombi, both in experiments and wild populations (43, 44). In honey bees, a common member of the gut microbiome, Frischella perrara, is responsible for causing the widespread scab phenotype in the gut, likely due to the local induction of a melanization immune response (45). This example illustrates that microbes can be the hidden cause of host phenotypes and raises the possibility that widespread gut symbionts may be detrimental to their hosts.

In this paper, we collectively refer to the microbes associated with bees as the ‘bee microbiome,’ regardless of whether these symbionts engage in mutualistic, commensal, or parasitic relationships with the host. In the following sections, we discuss the most relevant research questions to be addressed with respect to the evolution of the bee microbiome and its relevance to the health of the host (Table 1). We argue that, to achieve these goals, standardized research methods and analyses are required, as well as communal resources that integrate information from disparate studies.

View this table:
  • View inline
  • View popup
TABLE 1 

Outstanding questions in bee microbiome research

We also propose that bees present an excellent model to study fundamental aspects of the ecology and evolution of microbe-host interactions in multispecies relationships. Bees constitute a diverse group of insects that have evolved remarkably different lifestyles and social behaviors (46, 47), and yet they share a large number of microbial commensals and pathogens (33, 48, 49). Knowing how such lifestyle differences affect microbial transmission and thereby shape the composition and ecology of the microbiome in different species will be invaluable for a better understanding of bee biology and microbiome evolution.

MICROBIOME AS A COMPONENT OF BEE HEALTH

As with the human microbiome, the bee gut microbiome likely consists of a mix of beneficial, commensal, and pathogenic microbes. The relative and absolute abundances of the community members and their interactions with one another will determine the microbiome’s overall contribution to host health. Bees may therefore be colonized by different microbial communities, depending on individual host circumstances and environmental conditions. A recent study of the gut microbiome of bumble bees supports this hypothesis. Two distinct gut microbial communities, so-called enterotypes, were found to occur in individuals of various bumble bee species in China (50). One enterotype was dominated by core bacterial species that are typical for honey bees and bumble bees, while the other was dominated by species often found to be pathogenic for insects. How these dramatic differences in microbiota occurring within host species affect host health is not known. An important future research avenue is to disentangle the various individual contributions of bee gut symbionts so as to reconstruct and understand their combined contribution to host fitness, in managed as well as wild pollinators.

The impact of most microbial parasites on bee health has likewise remained elusive. Microsporidia, trypanosomatids and viruses are frequently detected in honey bees, without any obvious detrimental effects (51–53). These asymptomatic infections render the definition of health more complex: particularly in social bees, in which individuals of different castes, ages, and genetic backgrounds (i.e., varying in relatedness due to polyandry) form a “superorganism,” it is crucial to define measurable health criteria instead of focusing on the somewhat nebulous idea of “bee health” or “bee vitality” (Table 2). For example, to study the effects of pathogen transmission or replication in host tissues, the measurable criteria for individual bees could include longevity, adult weight and the ability to collect resources for nest mates. Measurable traits at the colony level include colony growth and strength (e.g., the Liebefeld method [54] or frame counts for honey bees), honey production, queen production for bumble bees, and survival during winter. Independent pathogen-specific criteria include prevalence, abundance, replication rate, transmissibility, and infectivity. Additionally, in highly social species, such as the honey bee, it remains to be determined how individual health and infection frequency translate into colony fitness measurements.

View this table:
  • View inline
  • View popup
TABLE 2 

Major challenges for bee microbiome studies

The effects of specific microorganisms on bee health may be modulated by the context of infection, including coinfection or colonization by different microorganisms (41, 42, 55, 56). Some microbes, such as the gut symbionts in bumble bees (44), might provide protection against pathogenic agents. Others could have synergistic effects with pathogens and, thus, have negative effects even if individually they have a neutral or positive impact on bee health. Thus, interactions between microorganisms can influence the results or interpretation of infection experiments. Cocolonization studies in sterile host backgrounds are one means to initially characterize these interactions precisely and elucidate their effects on the host.

The contribution of the hosts’ genetic background has largely been ignored in bee microbiome studies. Honey bee queens typically mate with 10 to 20 male bees, whereas queens of many other bee species mate with only one male. Consequently, the genetic structure and diversity within and across colonies and between species vary substantially. This genotypic variation may modulate interactions with the microbiome, as shown for other insects (57, 58) and as indicated by reduced pathogenic pressure in polyandrous versus monandrous honey bee queens (59, 60). For example, genotypes may vary in immune response patterns that influence the susceptibility to colonization by particular microbes.

Another challenging question is the extent to which the environment contributes to bee microbiome composition and dynamics, and how this in turn affects host fitness. The honey bee and bumble bee gut microbiomes appear to be highly host specific and most likely acquired through social activity, while the microbiomes of other bees (both solitary and primitively eusocial) appear to mostly consist of environmentally acquired microbes (39, 61, 62). Therefore, environmental context may be more important to symbiont acquisition in these bee species than in Bombus and Apis species. Although little is known about microbiome host specificity in wild bees, their microbial compositions may be reflected by transmission/acquisition parameters that could include the number and species of flowers visited and the rates at which those flowers are visited by other pollinators.

Studies aimed at determining the diversity and overlap of pollinator microbes and pathogens throughout pollinator ecosystems are needed. Several recent studies demonstrate that potential pathogens are shared between different pollinator species, most likely via horizontal transmission at common floral resources (34, 49, 63).

Human activity is the major disruptive influence in many ecosystems around the world (64–67). Habitat fragmentation, agricultural intensification and monocultures, climate change, the globalization of trade, and the accidental or deliberate introduction of invasive species all conspire to threaten endemic or other valued species around the world. One open question concerns the effects of environmental anthropogenic toxins (including pesticides) on the structure and composition of the bee microbiome, especially in the gut. For honey bees, recent evidence that beekeeping practices can shape the gut microbiome is provided by the emergence of increased antibiotic resistance in honey bee gut symbionts in the United States (68). This is likely due to extensive prophylactic use of oxytetracycline to fight Paenibacillus larvae, the causative agent of American foulbrood. In addition, pesticide exposure can modulate the immune response of bees, thereby increasing susceptibility to opportunistic viral infections (69). These examples show the importance of considering environmental factors when studying microbiome-host interactions.

Relative to the studies on managed pollinator species, there are fewer in-depth studies of anthropogenic environmental influences on the microbiomes of wild pollinators, including solitary bees and bumble bees. However, the human impact may be substantial; for example, the loss of two once-common bumble bee species in North America may be due to the introduction of Nosema bombi by human activity (70). The introduction of nonnative solitary bees may also introduce disease (71). Given global trade and extended pollinator movement through accidental introductions or commercial beekeeping, the potential for the spread of microbes affecting pollinators should not be underestimated (72–74).

A comprehensive catalogue of Apis and non-Apis diseases, microbes, and supporting literature, providing an overview of most of the microorganisms known to date, can be found in the supplemental material (see Tables S1, S2, and S3 and Texts S1, S2, and S3).

Table S1 

Comprehensive overview of Apis bee diseases, including known hosts and known effects on hosts. Table S1, XLSX file, 0.02 MB.
Copyright © 2016 Engel et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

Table S2 

Comprehensive overview of Apis bee microbes. Table S2, XLSX file, 0.01 MB.
Copyright © 2016 Engel et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

Table S3 

Comprehensive overview of non-Apis bee microorganisms. Table S3, XLSX file, 0.02 MB.
Copyright © 2016 Engel et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

Text S1 

Literature support for the Apis bee diseases. Download Text S1, DOCX file, 0.02 MB.
Copyright © 2016 Engel et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

Text S2 

Literature support for the Apis bee microbes. Download Text S2, PDF file, 0.1 MB.
Copyright © 2016 Engel et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

Text S3 

Literature support for the non-Apis bee microorganisms. Download Text S3, DOCX file, 0.02 MB.
Copyright © 2016 Engel et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

THE BEE MICROBIOME AS AN EVOLUTIONARY MODEL FOR SYMBIOSIS

The multitude of microbial interactions in bees, both beneficial and parasitic, offers an excellent opportunity for investigating the evolution of different symbiotic strategies. Of particular interest is the question of how host lifestyle influences these processes. The effect of sociality on microbiome evolution and the potential reciprocal impacts on the host remain largely unstudied. Bees represent an excellent model to address such questions, because related species exhibit marked differences in the degree of sociality, ranging from solitary through facultative social to highly eusocial. We hypothesize that the transmission of microbes is facilitated by specialized social contacts among host individuals, favoring the maintenance of microbial associations. Sociality does not always correlate with host specificity (61, 75), but social transmission has been shown to be important for establishing the honey bee and bumble bee gut microbiome (76–78). Perhaps specialized behaviors like trophallaxis (transfer of food among members of a community) allow the maintenance of characteristic associations, such as those found with Apis and Bombus spp. In this respect, the gut microbiome is of particular interest.

The honey bee gut community represents a complex ecosystem involving multiple species of bacterial symbionts interacting within a dynamic host environment, but one that is nonetheless simpler than those of mammalian models (79). How stable heritable microbial gut communities arise and evolve is a central question in microbiome research, and resolving the extent to which such communities exist in different bee species will be invaluable for identifying general principles of gut microbiome evolution that are more broadly applicable across social animals.

The evolutionary forces that shape the animal microbiome remain unclear. One hypothesis is that the dominant forces driving microbiome evolution are microbe-microbe interactions, with host effects being relatively minor, consisting primarily of providing the physical substrate and raw nutrients for the development of the microbiome. Microbial cooperation and competition may give rise to traits such as resource partitioning and spatial organization. An alternative and perhaps more appealing hypothesis is that microbiome evolution is driven by coevolutionary dynamics occurring between gut microbiomes and their hosts. To date, evidence suggests that only the social corbiculate bees possess distinctive gut communities, while most other bee species and wasps possess transient or highly variable microbiomes (62, 79). This is consistent with the hypothesis that the evolution of intimate microbial associations is favored in social hosts (80, 81). Continuous close social contacts likely aid transmission of beneficial microbes from parent to offspring and between colony members (77, 78), facilitating the evolution of mutualistic interactions.

Social contacts also provide opportunities for the emergence of cheaters: symbionts that evolve to spread rapidly at the expense of the host and other gut community members, by hijacking efficient routes of social transmission. How these selfish tendencies are kept in check is mostly unknown for gut symbionts, and the bee gut is a tractable ecological system in which to examine this issue. Social contact will facilitate the spread not only of beneficial microbes but also pathogenic ones (82). The large population size of some social bee species could favor the emergence and evolutionary persistence of pathogens causing acute diseases that spread rapidly through the host population (e.g., Paenibacillus larvae or Melissococcus plutonius). Conversely, a solitary lifestyle may select for pathogens causing chronic infections, because host transmission is less frequent and persistence strategies increase the chance of pathogens being maintained, to allow their eventual transmission. The bee microbiome presents an excellent model to study such ecoevolutionary dynamics of microbe-host relationships. However, additional data on the microbiome composition, especially for wild bee species, is needed for a more comprehensive picture of these processes.

The bee immune system (83, 84) almost certainly plays a substantial role in mediating symbioses. In the gut microbiome, evidence for co-diversification (77, 85, 86) suggests that the association between the corbiculate bees and their symbionts is ancient. An understanding of how the microbiome can successfully colonize the gut without rejection by the host immune system may help to reveal the evolutionary processes responsible for the development of specialized and heritable gut communities. Host immunity may act as a mechanism of partner choice (87), permitting only certain strains to colonize, resulting in host specificity and driving divergence of the microbiomes between separate bee lineages (39, 77). The microbiome itself may be a critical component of bee immunity; there is evidence for defensive functions by some gut bacterial species and for potential pathogen-specific interactions (44, 88).

The recent discovery of high strain-level diversity within many of the gut bacterial species of honey bees is intriguing (39, 85, 89, 90). Several explanations for this fine-scale diversity have been proposed; for example, functional diversification due to niche partitioning (38) and co-divergence with, and adaptation to, host lineages (77). The pattern of diversification in the honey bee gut microbiome parallels that in mammalian gut microbiomes, in which a large number of strains have emerged from a relatively few founder lineages (91, 92). Whether such microbiome diversity benefits the host is debated (93, 94). To understand functionally relevant diversity, we need more information on how divergent functions are distributed across the members of the gut community and how they affect hosts.

The consequences of diversity for microbiome stability are also unknown. Dynamic interaction networks between gut species and strains could give rise to stable and distinct states (enterotypes) within host species (95). Identifying how different factors, such as diet, sociality, and host physiology, drive microbiome composition will be an important step forward. The effects of beekeeping practices on the bee microbiome should also be assessed. For example, routine mixing of bees from multiple colonies or the importation of nonnative (sub)species into new geographic regions may irrevocably alter gut communities in an artificial and negative manner. Even the distance between honey bee colonies may play a role in promoting the exchange of symbionts and potentially affecting the strains that replicate at the host’s expense, versus mutualistic genotypes that benefit or are benign to hosts.

PERSPECTIVE: CHALLENGES AND NOVEL APPROACHES

Measuring the effects of microbes on bee health is a challenging undertaking that requires consideration of many abiotic and biotic factors and their interactions (Table 2). Approaches to assess variation beyond the standard markers, such as the 16S rRNA gene, are needed in order to uncover intraspecific variation that may affect bee ecology. Elucidating the central processes affecting bee microbiomes will require sequencing of genomes and transcriptomes of cultured strains, as well as metagenomes and metatranscriptomes, which can provide snapshots of whole communities. These data could be used to reveal patterns of microbial gene flow within and between host species and may define microbial pangenomes, thus providing insight into microbiome evolution. Genomic characterization should not be confined to members of the gut microbiome but should also extend to other microbes, for example by targeted sequencing of virus-derived small RNAs (96) and species found on flowers and hive material (97, 98). Such broader sampling would provide a more complete picture of the microbial environment bees inhabit.

Correlative studies based on high-throughput sequencing of targeted samples can be extremely powerful for formulating hypotheses about the contributions of different factors to bee health. Sequencing data can be linked to metadata information to suggest how factors such as colony health, host genotype, season, and environmental stressors correlate with the composition of the microbiome (e.g., Cornman et al. [29]). Such correlative patterns can narrow the set of hypotheses to be tested by confirmatory experimental studies of causal relationships.

A strength of the bee microbiome system is that it is being addressed by a worldwide community of researchers using diverse approaches. However, the lack of coordination across studies also presents an obstacle. By combining data from different sequence-based studies, global patterns of bee microbiome evolution might become evident. To promote better integration, we propose the establishment of a curated online database (Fig. 1) dedicated to bee-associated microbes with the overall aims to (i) facilitate standardization, data integration, and collaboration between researchers in the field and (ii) facilitate transparent scientific exchange and communication with the public, research councils, and policy makers.

FIG 1 
  • Open in new tab
  • Download powerpoint
FIG 1 

A resource and analysis platform for bee microbiome studies. Large amounts of sequence data, metadata, and methods are being generated by different research groups around the globe. A centralized platform is needed to systematically archive such information, to make it available to other researchers in the field, to allow cross-study analyses, and to standardize approaches. The bee microbiome platform will enable more detailed analyses of available data to formulate novel hypotheses about bee health and microbiome evolution.

One planned element of the database would be an organized encyclopedia for bee-associated microbes (bees ranging from solitary bees to social bees), providing a general description of each microbe, listing relevant publications and methods for detection, and linking available genomic data. Full genome sequences for the major viruses, bacterial disease agents, fungi, and eukaryotic gut parasites are available in general public sequence repositories (e.g., GenBank and ENA) with new ones added continously to encompass the breadth of global bee microbiome species and strains. For microbes currently lacking genome assemblies, sequences of marker genes, such as the 16S rRNA gene, are available. As an example, a nonredundant sequence set from honey bee-associated microbes has been in development (99, 100). An expanded version of this could serve, alongside other datasets, in the BeeBiome database.

A second element in the database envisioned can serve as a centralized place for information from bee microbiome projects. The database can link to existing high-throughput sequencing datasets in repositories suitable for long-term storage, such as the Sequence Read Archive (at NCBI) or the European Nucleotide Archive (at EMBL-EBI). Datasets will include metadata (e.g., sample type, sampling date and location, host genotype, host age/caste, sequencing platform, sequencing depth, sample processing methods, and metagenomic assembly and analysis routines). These will enable common practices in the future and promote the discussion of what those practices should entail. Finally, as a third element we propose the development of bioinformatic processing pipelines to promote common analysis protocols. These data and pipelines could be distributed via dedicated Web portals along with public resources for genomic analysis. Existing portals that minimize technical burdens while retaining transparency and flexibility include Galaxy, Embassy Cloud, CyVerse (previously iPlant), and various cloud-based environments (e.g., Amazon-Qiime).

Gathering high-throughput sequencing projects and making them accessible from one location can aid the design of future studies so that they are compatible with, and complementary to, existing datasets, facilitating data integration and filling knowledge gaps. Finally, the database can enable the monitoring of changes in the bee microbiome across time and space, to allow detection of large-scale shifts in pathogen distributions and numbers or in genomic composition and to link such changes to variables representing the environment, climate, parasite load, or composition of the gut microbiome.

The first step toward the establishment of such a database occurred during the first bee microbiome workshop funded through the National Evolutionary Synthesis Center (NESCent), United States. A second meeting will focus on practical issues of financing and maintaining such a database, a major challenge for providing high-quality community resources. Ideally, the database should be curated by a dedicated project manager and financially supported by international public funding agencies to guarantee the continuity and stability of the resources.

CONCLUSIONS

The bee microbiome (i) is an important factor in bee health and (ii) can serve as an excellent model to study the evolution and ecology of microbial symbioses. However, a large number of important questions remain unsolved (Table 1). Co-infections of pathogens are frequent, the contribution of gut microbial communities to bee health is not yet understood, and the effects of environmental parameters on host-microbe interactions are unclear. Investigating possible synergistic and antagonistic interactions among the microbes, their environment, and the bee host will be crucial for the evaluation of host impact. This requires comprehensive characterization and systematic, functional analysis of all microbes associated with bees, i.e., the bee microbiome. High-throughput sequencing methods provide means to conduct large-scale surveys of bee microbes in nature and to identify correlations, for which causative processes can then be tested in laboratory experiments. However, formidable challenges are linked to such systematic approaches, including the sheer diversity of bee species, the variability of environmental parameters, the complex lifestyle of social bee species, and the lack of standardization of methods to allow cross-study comparison (Table 2). A number of relatively simple steps for advancements are proposed in Table 3. In addition, a database dedicated to bee microbiome research may help to overcome these challenges and allow scientists to join forces to study fundamental aspects of bee microbiome evolution, ecology and bee health. We envision such a database as providing guidelines for standard operational procedures, archiving capabilities for sequencing data and metadata information, and cross-study analysis tools. These resources will facilitate research, add transparency to data analysis, and improve the comparability of results across studies, approaches, and study systems. Such resources would evolve to keep track of new data, as well as improved analytical or laboratory techniques. A working group has been created to strive toward those objectives.

View this table:
  • View inline
  • View popup
TABLE 3 

Practical steps for advancements

ACKNOWLEDGMENTS

The manuscript arose from the discussions by the Bee Microbiome consortium at the National Evolutionary Synthesis Center (NESCent) workshop BeeBiome:Omic approaches for understanding bee-microbe relationships, held in Durham, NC, USA, from 20 to 24 October 2014.

  • Copyright © 2016 Engel et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

REFERENCES

  1. 1.↵
    1. Potts S,
    2. Biesmeijer K,
    3. Bommarco R,
    4. Breeze T,
    5. Carvalheiro L,
    6. Franzen M,
    7. Gonzalez-Varo JP,
    8. Holzschuh A,
    9. Kleijn D,
    10. Klein AM,
    11. Kunin B,
    12. Lecocq T,
    13. Lundin O,
    14. Michez D,
    15. Neumann P,
    16. Nieto A,
    17. Penev L,
    18. Rasmont P,
    19. Ratamäki O,
    20. Riedinger V,
    21. Roberts SPM,
    22. Rundlöf M,
    23. Scheper J,
    24. Sorensen P,
    25. Steffan-Dewenter I,
    26. Stoev P,
    27. Vila M,
    28. Schweiger O
    . 2015. Step: status and trends of European pollinators. Pensoft Publishers, Sofia, Bulgaria.
  2. 2.↵
    1. Gallai N,
    2. Salles J,
    3. Settele J,
    4. Vaissière BE
    . 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821. doi:10.1016/j.ecolecon.2008.06.014.
    OpenUrlCrossRefWeb of Science
  3. 3.↵
    1. Aizen MA,
    2. Garibaldi LA,
    3. Cunningham SA,
    4. Klein AM
    . 2008. Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr Biol 18:1572–1575. doi:10.1016/j.cub.2008.08.066.
    OpenUrlCrossRefPubMedWeb of Science
  4. 4.↵
    1. Potts SG,
    2. Biesmeijer JC,
    3. Kremen C,
    4. Neumann P,
    5. Schweiger O,
    6. Kunin WE
    . 2010. Global pollinator declines: impacts and drivers. Trends Ecol Evol. 25:345–353. doi:10.1016/j.tree.2010.01.007.
    OpenUrlCrossRefPubMedWeb of Science
  5. 5.↵
    1. VanEngelsdorp D,
    2. Evans JD,
    3. Saegerman C,
    4. Mullin C,
    5. Haubruge E,
    6. Nguyen BK,
    7. Frazier M,
    8. Frazier J,
    9. Cox-Foster D,
    10. Chen Y,
    11. Underwood R,
    12. Tarpy DR,
    13. Pettis JS
    . 2009. Colony collapse disorder: a descriptive study. PLoS One 4:e6481. doi:10.1371/journal.pone.0006481.
    OpenUrlCrossRefPubMed
  6. 6.↵
    1. Wallberg A,
    2. Han F,
    3. Wellhagen G,
    4. Dahle B,
    5. Kawata M,
    6. Haddad N,
    7. Simões ZL,
    8. Allsopp MH,
    9. Kandemir I,
    10. De la Rúa P,
    11. Pirk CW,
    12. Webster MT
    . 2014. A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera. Nat Genet 46:1081–1088. doi:10.1038/ng.3077.
    OpenUrlCrossRefPubMed
  7. 7.↵
    1. Dively GP,
    2. Embrey MS,
    3. Kamel A,
    4. Hawthorne DJ,
    5. Pettis JS
    . 2015. Assessment of chronic sublethal effects of imidacloprid on honey bee colony health. PLoS One 10:e0118748. doi:10.1371/journal.pone.0118748.
    OpenUrlCrossRefPubMed
  8. 8.↵
    1. Dainat B,
    2. Evans JD,
    3. Chen YP,
    4. Gauthier L,
    5. Neumann P
    . 2012. Predictive markers of honey bee colony collapse. PLoS One 7:e32151. doi:10.1371/journal.pone.0032151.
    OpenUrlCrossRefPubMed
  9. 9.↵
    1. Frias BED,
    2. Barbosa CD,
    3. Lourenço AP
    . 2016. Pollen nutrition in honey bees (Apis mellifera): impact on adult health. Apidologie 47:15–25. doi:10.1007/s13592-015-0373-y.
    OpenUrlCrossRef
  10. 10.↵
    1. Brodschneider R,
    2. Crailsheim K
    . 2010. Nutrition and health in honey bees. Apidologie 41:278–294. doi:10.1051/apido/2010012.
    OpenUrlCrossRef
  11. 11.↵
    1. Di Pasquale G,
    2. Salignon M,
    3. Le Conte Y,
    4. Belzunces LP,
    5. Decourtye A,
    6. Kretzschmar A,
    7. Suchail S,
    8. Brunet J-L,
    9. Alaux C
    . 2013. Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS One 8:e72016. doi:10.1371/journal.pone.0072016.
    OpenUrlCrossRefPubMed
  12. 12.↵
    1. Evans JD,
    2. Schwarz RS
    . 2011. Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol 19:614–620. doi:10.1016/j.tim.2011.09.003.
    OpenUrlCrossRefPubMedWeb of Science
  13. 13.↵
    1. Genersch E
    . 2010. American foulbrood in honeybees and its causative agent, Paenibacillus larvae. J Invertebr Pathol 103(Suppl 1):S10–S19. doi:10.1016/j.jip.2009.06.015.
    OpenUrlCrossRefPubMed
  14. 14.↵
    1. Forsgren E
    . 2010. European foulbrood in honey bees. J Invertebr Pathol 103(Suppl 1):S5–S9. doi:10.1016/j.jip.2009.06.016.
    OpenUrlCrossRefPubMed
  15. 15.↵
    1. Martín-Hernández R,
    2. Meana A,
    3. Prieto L,
    4. Salvador AM,
    5. Garrido-Bailón E,
    6. Higes M
    . 2007. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol 73:6331–6338. doi:10.1128/AEM.00270-07.
    OpenUrlAbstract/FREE Full Text
  16. 16.↵
    1. Botías C,
    2. Martín-Hernández R,
    3. Barrios L,
    4. Meana A,
    5. Higes M
    . 2013. Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet Res 44:25. doi:10.1186/1297-9716-44-25.
    OpenUrlCrossRefPubMed
  17. 17.↵
    1. Higes M,
    2. Martín-Hernández R,
    3. Botías C,
    4. Bailón EG,
    5. González-Porto AV,
    6. Barrios L,
    7. del Nozal MJ,
    8. Bernal JL,
    9. Jiménez JJ,
    10. Palencia PG,
    11. Meana A
    . 2008. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10:2659–2669. doi:10.1111/j.1462-2920.2008.01687.x.
    OpenUrlCrossRefPubMedWeb of Science
  18. 18.↵
    1. Cox-Foster DL,
    2. Conlan S,
    3. Holmes EC,
    4. Palacios G,
    5. Evans JD,
    6. Moran NA,
    7. Quan PL,
    8. Briese T,
    9. Hornig M,
    10. Geiser DM,
    11. Martinson V,
    12. Vanengelsdorp D,
    13. Kalkstein AL,
    14. Drysdale A,
    15. Hui J,
    16. Zhai J,
    17. Cui L,
    18. Hutchison SK,
    19. Simons JF,
    20. Egholm M,
    21. Pettis JS,
    22. Lipkin WI
    . 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318:283–287. doi:10.1126/science.1146498.
    OpenUrlAbstract/FREE Full Text
  19. 19.↵
    1. Huang WF,
    2. Solter L,
    3. Aronstein K,
    4. Huang Z
    . 2015. Infectivity and virulence of Nosema ceranae and Nosema apis in commercially available North American honey bees. J Invertebr Pathol 124:107–113. doi:10.1016/j.jip.2014.10.006.
    OpenUrlCrossRefPubMed
  20. 20.↵
    1. Milbrath MO,
    2. Van Tran T,
    3. Huang WF,
    4. Solter LF,
    5. Tarpy DR,
    6. Lawrence F,
    7. Huang ZY
    . 2015. Comparative virulence and competition between Nosema apis and Nosema ceranae in honey bees (Apis mellifera). J Invertebr Pathol 125:9–15. doi:10.1016/j.jip.2014.12.006.
    OpenUrlCrossRefPubMed
  21. 21.↵
    1. Natsopoulou ME,
    2. Doublet V,
    3. Paxton RJ
    . 2016. European isolates of the Microsporidia Nosema apis and Nosema ceranae have similar virulence in laboratory tests on European worker honey bees. Apidologie 47:57–65. doi:10.1007/s13592-015-0375-9.
    OpenUrlCrossRef
  22. 22.↵
    1. Natsopoulou ME,
    2. McMahon DP,
    3. Doublet V,
    4. Bryden J,
    5. Paxton RJ
    . 2015. Interspecific competition in honeybee intracellular gut parasites is asymmetric and favours the spread of an emerging infectious disease. Proc Biol Sci 282:20141896. doi:10.1098/rspb.2014.1896.
    OpenUrlAbstract/FREE Full Text
  23. 23.↵
    1. Chen YP,
    2. Siede R
    . 2007. Honey bee viruses. Adv Virus Res 70:33–80. doi:10.1016/S0065-3527(07)70002-7.
    OpenUrlCrossRefPubMed
  24. 24.↵
    1. McMenamin AJ,
    2. Genersch E
    . 2015. Honey bee colony losses and associated viruses. Curr Opin Insect Sci 8:121–129. doi:10.1016/j.cois.2015.01.015.
    OpenUrlCrossRef
  25. 25.↵
    1. De Miranda JR,
    2. Bailey L,
    3. Ball BV,
    4. Blanchard P,
    5. Budge GE,
    6. Chejanovsky N,
    7. Chen Y,
    8. Gauthier L,
    9. Genersch E,
    10. de Graaf DC,
    11. Ribière M,
    12. Ryabov E,
    13. De Smet L,
    14. van der Steen JJM
    . 2013. Standard methods for virus research in Apis mellifera. J Apic Res 52:1–56. doi:10.3896/IBRA.1.52.4.22.
    OpenUrlCrossRef
  26. 26.↵
    1. Dainat B,
    2. Evans JD,
    3. Chen YP,
    4. Gauthier L,
    5. Neumann P
    . 2012. Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Appl Environ Microbiol 78:981–987. doi:10.1128/AEM.06537-11.
    OpenUrlAbstract/FREE Full Text
  27. 27.↵
    1. Doublet V,
    2. Labarussias M,
    3. de Miranda JR,
    4. Moritz RF,
    5. Paxton RJ
    . 2015. Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ Microbiol 17:969–983. doi:10.1111/1462-2920.12426.
    OpenUrlCrossRefPubMed
  28. 28.↵
    1. Nazzi F,
    2. Brown SP,
    3. Annoscia D,
    4. Del Piccolo F,
    5. Di Prisco G,
    6. Varricchio P,
    7. Della Vedova G,
    8. Cattonaro F,
    9. Caprio E,
    10. Pennacchio F
    . 2012. Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 8:e1002735. doi:10.1371/journal.ppat.1002735.
    OpenUrlCrossRefPubMed
  29. 29.↵
    1. Cornman RS,
    2. Tarpy DR,
    3. Chen Y,
    4. Jeffreys L,
    5. Lopez D,
    6. Pettis JS,
    7. vanEngelsdorp D,
    8. Evans JD
    . 2012. Pathogen webs in collapsing honey bee colonies. PLoS One 7:e43562. doi:10.1371/journal.pone.0043562.
    OpenUrlCrossRefPubMed
  30. 30.↵
    1. Cavigli I,
    2. Daughenbaugh KF,
    3. Martin M,
    4. Lerch M,
    5. Banner K,
    6. Garcia E,
    7. Brutscher LM,
    8. Flenniken ML
    . 2016. Pathogen prevalence and abundance in honey bee colonies involved in almond pollination. Apidologie 47:251–266 doi:10.1007/s13592-015-0395-5:1-16.
    OpenUrlCrossRef
  31. 31.↵
    1. Daughenbaugh KF,
    2. Martin M,
    3. Brutscher LM,
    4. Cavigli I,
    5. Garcia E,
    6. Lavin M,
    7. Flenniken ML
    . 2015. Honey bee infecting Lake Sinai viruses. Viruses 7:3285–3309. doi:10.3390/v7062772.
    OpenUrlCrossRef
  32. 32.↵
    1. Vanbergen AJ, The Insect Pollinators Initiative
    . 2013. Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ 11:251–259 doi:10.1890/120126.
    OpenUrlCrossRef
  33. 33.↵
    1. McMahon DP,
    2. Fürst MA,
    3. Caspar J,
    4. Theodorou P,
    5. Brown MJ,
    6. Paxton RJ
    . 2015. A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. J Anim Ecol 84:615–624. doi:10.1111/1365-2656.12345.
    OpenUrlCrossRefPubMed
  34. 34.↵
    1. Fürst MA,
    2. McMahon DP,
    3. Osborne JL,
    4. Paxton RJ,
    5. Brown MJ
    . 2014. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–366. doi:10.1038/nature12977.
    OpenUrlCrossRefPubMedWeb of Science
  35. 35.↵
    1. Moran NA
    . 2015. Genomics of the honey bee microbiome. Curr Opin Insect Sci 10:22–28. doi:10.1016/j.cois.2015.04.003.
    OpenUrlCrossRefPubMed
  36. 36.↵
    1. Kamada N,
    2. Chen GY,
    3. Inohara N,
    4. Núñez G
    . 2013. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol 14:685–690. doi:10.1038/ni.2608.
    OpenUrlCrossRefPubMed
  37. 37.↵
    1. Stefka AT,
    2. Feehley T,
    3. Tripathi P,
    4. Qiu J,
    5. McCoy K,
    6. Mazmanian SK,
    7. Tjota MY,
    8. Seo G-Y,
    9. Cao S,
    10. Theriault BR,
    11. Antonopoulos DA,
    12. Zhou L,
    13. Chang EB,
    14. Fu Y-X,
    15. Nagler CR
    . 2014. Commensal bacteria protect against food allergen sensitization. Proc Natl Acad Sci U S A 111:13145–13150. doi:10.1073/pnas.1412008111.
    OpenUrlAbstract/FREE Full Text
  38. 38.↵
    1. Engel P,
    2. Martinson VG,
    3. Moran NA
    . 2012. Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci U S A 109:11002–11007. doi:10.1073/pnas.1202970109.
    OpenUrlAbstract/FREE Full Text
  39. 39.↵
    1. Kwong WK,
    2. Engel P,
    3. Koch H,
    4. Moran NA
    . 2014. Genomics and host specialization of honey bee and bumble bee gut symbionts. Proc Natl Acad Sci U S A 111:11509–11514. doi:10.1073/pnas.1405838111.
    OpenUrlAbstract/FREE Full Text
  40. 40.↵
    1. Lee FJ,
    2. Rusch DB,
    3. Stewart FJ,
    4. Mattila HR,
    5. Newton IL
    . 2015. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environ Microbiol 17:796–815. doi:10.1111/1462-2920.12526.
    OpenUrlCrossRef
  41. 41.↵
    1. Forsgren E,
    2. Olofsson TC,
    3. Vásquez A,
    4. Fries I
    . 2010. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41:99–108. doi:10.1051/apido/2009065.
    OpenUrlCrossRef
  42. 42.↵
    1. Vásquez A,
    2. Forsgren E,
    3. Fries I,
    4. Paxton RJ,
    5. Flaberg E,
    6. Szekely L,
    7. Olofsson TC
    . 2012. Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS One 7:e33188. doi:10.1371/journal.pone.0033188.
    OpenUrlCrossRefPubMed
  43. 43.↵
    1. Cariveau DP,
    2. Elijah Powell J,
    3. Koch H,
    4. Winfree R,
    5. Moran NA
    . 2014. Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). ISME J 8:2369–2379. doi:10.1038/ismej.2014.68.
    OpenUrlCrossRef
  44. 44.↵
    1. Koch H,
    2. Schmid-Hempel P
    . 2011. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci U S A 108:19288–19292. doi:10.1073/pnas.1110474108.
    OpenUrlAbstract/FREE Full Text
  45. 45.↵
    1. Engel P,
    2. Bartlett KD,
    3. Moran NA
    . 2015. The bacterium Frischella perrara causes scab formation in the gut of its honeybee host. mBio 6:e00193–e00115. doi:10.1128/mBio.00193-15.
    OpenUrlCrossRefPubMed
  46. 46.↵
    1. Wilson EO
    . 1972. The insect societies. Harvard University Press, Cambridge, MA.
  47. 47.↵
    1. Seeley TD
    . 1985. Honeybee ecology. A study of adaptation in social life. Princeton University Press, Princeton, NJ.
  48. 48.↵
    1. Herrera CM,
    2. Pozo MI,
    3. Medrano M
    . 2013. Yeasts in nectar of an early-blooming herb: sought by bumble bees, detrimental to plant fecundity. Ecology 94:273–279. doi:10.1890/12-0595.1.
    OpenUrlCrossRefPubMedWeb of Science
  49. 49.↵
    1. Singh R,
    2. Levitt AL,
    3. Rajotte EG,
    4. Holmes EC,
    5. Ostiguy N,
    6. vanEngelsdorp D,
    7. Lipkin WI,
    8. dePamphilis CW,
    9. Toth AL,
    10. Cox-Foster DL
    . 2010. RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS One 5:e14357. doi:10.1371/journal.pone.0014357.
    OpenUrlCrossRefPubMed
  50. 50.↵
    1. Li J,
    2. Powell JE,
    3. Guo J,
    4. Evans JD,
    5. Wu J,
    6. Williams P,
    7. Lin Q,
    8. Moran NA,
    9. Zhang Z
    . 2015. Two gut community enterotypes recur in diverse bumblebee species. Curr Biol 25:R652–R653. doi:10.1016/j.cub.2015.06.031.
    OpenUrlCrossRef
  51. 51.↵
    1. Tentcheva D,
    2. Gauthier L,
    3. Zappulla N,
    4. Dainat B,
    5. Cousserans F,
    6. Colin ME,
    7. Bergoin M
    . 2004. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl Environ Microbiol 70:7185–7191. doi:10.1128/AEM.70.12.7185-7191.2004.
    OpenUrlAbstract/FREE Full Text
  52. 52.↵
    1. Genersch E
    . 2010. Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87:87–97. doi:10.1007/s00253-010-2573-8.
    OpenUrlCrossRefPubMedWeb of Science
  53. 53.↵
    1. Runckel C,
    2. Flenniken ML,
    3. Engel JC,
    4. Ruby JG,
    5. Ganem D,
    6. Andino R,
    7. DeRisi JL
    . 2011. Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One 6:e20656. doi:10.1371/journal.pone.0020656.
    OpenUrlCrossRefPubMed
  54. 54.↵
    1. Imdorf A,
    2. Bühlmann G,
    3. Gerig L,
    4. Kilchenmann V,
    5. Wille H
    . 1987. Überprüfung der Schätzmethode zur Ermittlung der Brutfläche und der Anzahl Arbeiterinnen in freifliegenden Bienenvölkern. Apidologie 18:137–146. doi:10.1051/apido:19870204.
    OpenUrlCrossRef
  55. 55.↵
    1. Zheng HQ,
    2. Gong HR,
    3. Huang SK,
    4. Sohr A,
    5. Hu FL,
    6. Chen YP
    . 2015. Evidence of the synergistic interaction of honey bee pathogens Nosema ceranae and deformed wing virus. Vet Microbiol 177:1–6 doi:10.1016/j.vetmic.2015.02.003.
    OpenUrlCrossRef
  56. 56.↵
    1. Doublet V,
    2. Natsopoulou ME,
    3. Zschiesche L,
    4. Paxton RJ
    . 2015. Within-host competition among the honey bees pathogens Nosema ceranae and deformed wing virus is asymmetric and to the disadvantage of the virus. J Invertebr Pathol 124:31–34. doi:10.1016/j.jip.2014.10.007.
    OpenUrlCrossRefPubMed
  57. 57.↵
    1. Lazzaro BP,
    2. Sackton TB,
    3. Clark AG
    . 2006. Genetic variation in Drosophila melanogaster resistance to infection: a comparison across bacteria. Genetics 174:1539–1554. doi:10.1534/genetics.105.054593.
    OpenUrlAbstract/FREE Full Text
  58. 58.↵
    1. Dobson AJ,
    2. Chaston JM,
    3. Newell PD,
    4. Donahue L,
    5. Hermann SL,
    6. Sannino DR,
    7. Westmiller S,
    8. Wong ACN,
    9. Clark AG,
    10. Lazzaro BP,
    11. Douglas AE
    . 2015. Host genetic determinants of microbiota-dependent nutrition revealed by genome-wide analysis of Drosophila melanogaster. Nat Commun 6:6312.
    OpenUrl
  59. 59.↵
    1. Tarpy DR,
    2. Seeley TD
    . 2006. Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften 93:195–199. doi:10.1007/s00114-006-0091-4.
    OpenUrlCrossRefPubMedWeb of Science
  60. 60.↵
    1. Seeley TD,
    2. Tarpy DR
    . 2007. Queen promiscuity lowers disease within honeybee colonies. Proc Biol Sci 274:67–72. doi:10.1098/rspb.2006.3702.
    OpenUrlAbstract/FREE Full Text
  61. 61.↵
    1. McFrederick QS,
    2. Wcislo WT,
    3. Hout MC,
    4. Mueller UG
    . 2014. Host species and developmental stage, but not host social structure, affects bacterial community structure in socially polymorphic bees. FEMS Microbiol Ecol 88:398–406. doi:10.1111/1574-6941.12302.
    OpenUrlCrossRefPubMed
  62. 62.↵
    1. McFrederick QS,
    2. Wcislo WT,
    3. Taylor DR,
    4. Ishak HD,
    5. Dowd SE,
    6. Mueller UG
    . 2012. Environment or kin: whence do bees obtain acidophilic bacteria? Mol Ecol 21:1754–1768. doi:10.1111/j.1365-294X.2012.05496.x.
    OpenUrlCrossRefPubMedWeb of Science
  63. 63.↵
    1. Graystock P,
    2. Goulson D,
    3. Hughes WO
    . 2015. Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proc Biol Sci 282:20151371. doi:10.1098/rspb.2015.1371.
    OpenUrlAbstract/FREE Full Text
  64. 64.↵
    1. Vitousek PM,
    2. Mooney HA,
    3. Lubchenco J,
    4. Melillo JM
    . 1997. Human domination of Earth’s ecosystems. Science 277:494–499. doi:10.1126/science.277.5325.494.
    OpenUrlCrossRefWeb of Science
  65. 65.↵
    1. Murphy GE,
    2. Romanuk TN
    . 2014. A meta-analysis of declines in local species richness from human disturbances. Ecol Evol 4:91–103. doi:10.1002/ece3.909.
    OpenUrlCrossRefPubMed
  66. 66.↵
    1. Halpern BS,
    2. Walbridge S,
    3. Selkoe KA,
    4. Kappel CV,
    5. Micheli F,
    6. D’Agrosa C,
    7. Bruno JF,
    8. Casey KS,
    9. Ebert C,
    10. Fox HE,
    11. Fujita R,
    12. Heinemann D,
    13. Lenihan HS,
    14. Madin EM,
    15. Perry MT,
    16. Selig ER,
    17. Spalding M,
    18. Steneck R,
    19. Watson R
    . 2008. A global map of human impact on marine ecosystems. Science 319:948–952. doi:10.1126/science.1149345.
    OpenUrlAbstract/FREE Full Text
  67. 67.↵
    1. Burkle LA,
    2. Marlin JC,
    3. Knight TM
    . 2013. Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615. doi:10.1126/science.1232728.
    OpenUrlAbstract/FREE Full Text
  68. 68.↵
    1. Tian B,
    2. Fadhil NH,
    3. Powell JE,
    4. Kwong WK,
    5. Moran NA
    . 2012. Long-term exposure to antibiotics has caused accumulation of resistance determinants in the gut microbiota of honeybees. mBio 3:e00377-12. doi:10.1128/mBio.00377-12.
    OpenUrlCrossRefPubMed
  69. 69.↵
    1. Di Prisco G,
    2. Cavaliere V,
    3. Annoscia D,
    4. Varricchio P,
    5. Caprio E,
    6. Nazzi F,
    7. Gargiulo G,
    8. Pennacchio F
    . 2013. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc Natl Acad Sci U S A 110:18466–18471. doi:10.1073/pnas.1314923110.
    OpenUrlAbstract/FREE Full Text
  70. 70.↵
    1. Cameron SA,
    2. Lozier JD,
    3. Strange JP,
    4. Koch JB,
    5. Cordes N,
    6. Solter LF,
    7. Griswold TL
    . 2011. Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci U S A 108:662–667. doi:10.1073/pnas.1014743108.
    OpenUrlAbstract/FREE Full Text
  71. 71.↵
    1. Hedtke SM,
    2. Blitzer EJ,
    3. Montgomery GA,
    4. Danforth BN
    . 2015. Introduction of non-native pollinators can lead to trans-continental movement of bee-associated fungi. PLoS One 10:e0130560. doi:10.1371/journal.pone.0130560.
    OpenUrlCrossRef
  72. 72.↵
    1. Murray TE,
    2. Coffey MF,
    3. Kehoe E,
    4. Horgan FG
    . 2013. Pathogen prevalence in commercially reared bumble bees and evidence of spillover in conspecific populations. Biol Conserv 159:269–276. doi:10.1016/j.biocon.2012.10.021.
    OpenUrlCrossRef
  73. 73.↵
    1. Graystock P,
    2. Yates K,
    3. Evison SEF,
    4. Darvill B,
    5. Goulson D,
    6. Hughes WOH
    . 2013. The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies. J Appl Ecol 50:1207–1215. doi:10.1111/1365-2664.12134.
    OpenUrlCrossRef
  74. 74.↵
    1. Schmid-Hempel R,
    2. Eckhardt M,
    3. Goulson D,
    4. Heinzmann D,
    5. Lange C,
    6. Plischuk S,
    7. Escudero LR,
    8. Salathé R,
    9. Scriven JJ,
    10. Schmid-Hempel P
    . 2014. The invasion of southern South America by imported bumblebees and associated parasites. J Anim Ecol 83:823–837. doi:10.1111/1365-2656.12185.
    OpenUrlCrossRefPubMed
  75. 75.↵
    1. McFrederick QS,
    2. Cannone JJ,
    3. Gutell RR,
    4. Kellner K,
    5. Plowes RM,
    6. Mueller UG
    . 2013. Specificity between lactobacilli and hymenopteran hosts is the exception rather than the rule. Appl Environ Microbiol 79:1803–1812. doi:10.1128/AEM.03681-12.
    OpenUrlAbstract/FREE Full Text
  76. 76.↵
    1. Martinson VG,
    2. Moy J,
    3. Moran NA
    . 2012. Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol 78:2830–2840. doi:10.1128/AEM.07810-11.
    OpenUrlAbstract/FREE Full Text
  77. 77.↵
    1. Koch H,
    2. Abrol DP,
    3. Li J,
    4. Schmid-Hempel P
    . 2013. Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees. Mol Ecol 22:2028–2044. doi:10.1111/mec.12209.
    OpenUrlCrossRefPubMedWeb of Science
  78. 78.↵
    1. Powell JE,
    2. Martinson VG,
    3. Urban-Mead K,
    4. Moran NA
    . 2014. Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Appl Environ Microbiol 80:7378–7387. doi:10.1128/AEM.01861-14.
    OpenUrlAbstract/FREE Full Text
  79. 79.↵
    1. Martinson VG,
    2. Danforth BN,
    3. Minckley RL,
    4. Rueppell O,
    5. Tingek S,
    6. Moran NA
    . 2011. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol Ecol 20:619–628. doi:10.1111/j.1365-294X.2010.04959.x.
    OpenUrlCrossRefPubMedWeb of Science
  80. 80.↵
    1. Lombardo MP
    . 2008. Access to mutualistic endosymbiotic microbes: an underappreciated benefit of group living. Behav Ecol Sociobiol 62:479–497. doi:10.1007/s00265-007-0428-9.
    OpenUrlCrossRefWeb of Science
  81. 81.↵
    1. Troyer K
    . 1984. Microbes, herbivory and the evolution of social behavior. J Theor Biol 106:157–169. doi:10.1016/0022-5193(84)90016-X.
    OpenUrlCrossRef
  82. 82.↵
    1. Otterstatter MC,
    2. Thomson JD
    . 2007. Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies. Oecologia 154:411–421. doi:10.1007/s00442-007-0834-8.
    OpenUrlCrossRefPubMedWeb of Science
  83. 83.↵
    1. Brutscher LM,
    2. Daughenbaugh KF,
    3. Flenniken ML
    . 2015. Antiviral defense mechanisms in honey bees. Curr Opin Insect Sci 10:71–82. doi:10.1016/j.cois.2015.04.016.
    OpenUrlCrossRefPubMed
  84. 84.↵
    1. Evans JD,
    2. Aronstein K,
    3. Chen YP,
    4. Hetru C,
    5. Imler JL,
    6. Jiang H,
    7. Kanost M,
    8. Thompson GJ,
    9. Zou Z,
    10. Hultmark D
    . 2006. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15:645–656. doi:10.1111/j.1365-2583.2006.00682.x.
    OpenUrlCrossRefPubMedWeb of Science
  85. 85.↵
    1. Engel P,
    2. Stepanauskas R,
    3. Moran NA
    . 2014. Hidden diversity in honey bee gut symbionts detected by single-cell genomics. PLoS Genet 10:e1004596. doi:10.1371/journal.pgen.1004596.
    OpenUrlCrossRefPubMed
  86. 86.↵
    1. Kwong WK,
    2. Moran NA
    . 2015. Evolution of host specialization in gut microbes: the bee gut as a model. Gut Microbes 6:214–220. doi:10.1080/19490976.2015.1047129.
    OpenUrlCrossRefPubMed
  87. 87.↵
    1. Sachs JL,
    2. Mueller UG,
    3. Wilcox TP,
    4. Bull JJ
    . 2004. The evolution of cooperation. Q Rev Biol 79:135–160. doi:10.1086/383541.
    OpenUrlCrossRefPubMedWeb of Science
  88. 88.↵
    1. Koch H,
    2. Schmid-Hempel P
    . 2012. Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host-parasite system. Ecol Lett 15:1095–1103. doi:10.1111/j.1461-0248.2012.01831.x.
    OpenUrlCrossRefPubMed
  89. 89.↵
    1. Olofsson TC,
    2. Alsterfjord M,
    3. Nilson B,
    4. Butler E,
    5. Vásquez A
    . 2014. Lactobacillus apinorum sp. nov., Lactobacillus mellifer sp. nov., Lactobacillus mellis sp. nov., Lactobacillus melliventris sp. nov., Lactobacillus kimbladii sp. nov., Lactobacillus helsingborgensis sp. nov. and Lactobacillus kullabergensis sp. nov., isolated from the honey stomach of the honeybee Apis mellifera. Int J Syst Evol Microbiol 64:3109–3119. doi:10.1099/ijs.0.059600-0.
    OpenUrlCrossRefPubMed
  90. 90.↵
    1. Ellegaard KM,
    2. Tamarit D,
    3. Javelind E,
    4. Olofsson TC,
    5. Andersson SG,
    6. Vásquez A
    . 2015. Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut. BMC Genomics 16:284. doi:10.1186/s12864-015-1476-6.
    OpenUrlCrossRefPubMed
  91. 91.↵
    1. Dethlefsen L,
    2. McFall-Ngai M,
    3. Relman DA
    . 2007. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811–818. doi:10.1038/nature06245.
    OpenUrlCrossRefPubMedWeb of Science
  92. 92.↵
    1. Ley RE,
    2. Peterson DA,
    3. Gordon JI
    . 2006. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848. doi:10.1016/j.cell.2006.02.017.
    OpenUrlCrossRefPubMedWeb of Science
  93. 93.↵
    1. Lozupone CA,
    2. Stombaugh JI,
    3. Gordon JI,
    4. Jansson JK,
    5. Knight R
    . 2012. Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230. doi:10.1038/nature11550.
    OpenUrlCrossRefPubMedWeb of Science
  94. 94.↵
    1. Schnorr SL,
    2. Candela M,
    3. Rampelli S,
    4. Centanni M,
    5. Consolandi C,
    6. Basaglia G,
    7. Turroni S,
    8. Biagi E,
    9. Peano C,
    10. Severgnini M,
    11. Fiori J,
    12. Gotti R,
    13. De Bellis G,
    14. Luiselli D,
    15. Brigidi P,
    16. Mabulla A,
    17. Marlowe F,
    18. Henry AG,
    19. Crittenden AN
    . 2014. Gut microbiome of the Hadza hunter-gatherers. Nat Commun 5:3654. doi:10.1038/ncomms4654.
    OpenUrlCrossRefPubMed
  95. 95.↵
    1. Arumugam M,
    2. Raes J,
    3. Pelletier E,
    4. Le Paslier D,
    5. Yamada T,
    6. Mende DR,
    7. Fernandes GR,
    8. Tap J,
    9. Bruls T,
    10. Batto J-M,
    11. Bertalan M,
    12. Borruel N,
    13. Casellas F,
    14. Fernandez L,
    15. Gautier L,
    16. Hansen T,
    17. Hattori M,
    18. Hayashi T,
    19. Kleerebezem M,
    20. Kurokawa K,
    21. Leclerc M,
    22. Levenez F,
    23. Manichanh C,
    24. Nielsen HB,
    25. Nielsen T,
    26. Pons N,
    27. Poulain J,
    28. Qin J,
    29. Sicheritz-Ponten T,
    30. Tims S,
    31. Torrents D,
    32. Ugarte E,
    33. Zoetendal EG,
    34. Wang J,
    35. Guarner F,
    36. Pedersen O,
    37. de Vos WM,
    38. Brunak S,
    39. Dore J,
    40. Weissenbach J,
    41. Ehrlich SD,
    42. Bork P
    . 2011. Enterotypes of the human gut microbiome. Nature 473:174–180. doi:10.1038/nature09944.
    OpenUrlCrossRefPubMedWeb of Science
  96. 96.↵
    1. Webster CL,
    2. Waldron FM,
    3. Robertson S,
    4. Crowson D,
    5. Ferrari G,
    6. Quintana JF,
    7. Brouqui J-M,
    8. Bayne EH,
    9. Longdon B,
    10. Buck AH,
    11. Lazzaro BP,
    12. Akorli J,
    13. Haddrill PR,
    14. Obbard DJ
    . 2015. The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. PLoS Biol 13:e1002210. doi:10.1371/journal.pbio.1002210.
    OpenUrlCrossRefPubMed
  97. 97.↵
    1. Anderson KE,
    2. Sheehan TH,
    3. Mott BM,
    4. Maes P,
    5. Snyder L,
    6. Schwan MR,
    7. Walton A,
    8. Jones BM,
    9. Corby-Harris V
    . 2013. Microbial ecology of the hive and pollination landscape: bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). PLoS One 8:e83125. doi:10.1371/journal.pone.0083125.
    OpenUrlCrossRefPubMed
  98. 98.↵
    1. Anderson KE,
    2. Carroll MJ,
    3. Sheehan T,
    4. Mott BM,
    5. Maes P,
    6. Corby-Harris V
    . 2014. Hive-stored pollen of honey bees: many lines of evidence are consistent with pollen preservation, not nutrient conversion. Mol Ecol 23:5904–5917. doi:10.1111/mec.12966.
    OpenUrlCrossRef
  99. 99.↵
    1. Tozkar CÖ,
    2. Kence M,
    3. Kence A,
    4. Huang Q,
    5. Evans JD
    . 2015. Metatranscriptomic analyses of honey bee colonies. Front Genet 6:100. doi:10.3389/fgene.2015.00100.
    OpenUrlCrossRef
  100. 100.↵
    1. Schwarz RS,
    2. Huang Q,
    3. Evans JD
    . 2015. Hologenome theory and the honey bee pathosphere. Curr Opin Insect Sci 10:1–7. doi:10.1016/j.cois.2015.04.006.
    OpenUrlCrossRef
View Abstract
PreviousNext
Back to top
Download PDF
Citation Tools
The Bee Microbiome: Impact on Bee Health and Model for Evolution and Ecology of Host-Microbe Interactions
Philipp Engel, Waldan K. Kwong, Quinn McFrederick, Kirk E. Anderson, Seth Michael Barribeau, James Angus Chandler, R. Scott Cornman, Jacques Dainat, Joachim R. de Miranda, Vincent Doublet, Olivier Emery, Jay D. Evans, Laurent Farinelli, Michelle L. Flenniken, Fredrik Granberg, Juris A. Grasis, Laurent Gauthier, Juliette Hayer, Hauke Koch, Sarah Kocher, Vincent G. Martinson, Nancy Moran, Monica Munoz-Torres, Irene Newton, Robert J. Paxton, Eli Powell, Ben M. Sadd, Paul Schmid-Hempel, Regula Schmid-Hempel, Se Jin Song, Ryan S. Schwarz, Dennis vanEngelsdorp, Benjamin Dainat
mBio Apr 2016, 7 (2) e02164-15; DOI: 10.1128/mBio.02164-15

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this mBio article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
The Bee Microbiome: Impact on Bee Health and Model for Evolution and Ecology of Host-Microbe Interactions
(Your Name) has forwarded a page to you from mBio
(Your Name) thought you would be interested in this article in mBio.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
The Bee Microbiome: Impact on Bee Health and Model for Evolution and Ecology of Host-Microbe Interactions
Philipp Engel, Waldan K. Kwong, Quinn McFrederick, Kirk E. Anderson, Seth Michael Barribeau, James Angus Chandler, R. Scott Cornman, Jacques Dainat, Joachim R. de Miranda, Vincent Doublet, Olivier Emery, Jay D. Evans, Laurent Farinelli, Michelle L. Flenniken, Fredrik Granberg, Juris A. Grasis, Laurent Gauthier, Juliette Hayer, Hauke Koch, Sarah Kocher, Vincent G. Martinson, Nancy Moran, Monica Munoz-Torres, Irene Newton, Robert J. Paxton, Eli Powell, Ben M. Sadd, Paul Schmid-Hempel, Regula Schmid-Hempel, Se Jin Song, Ryan S. Schwarz, Dennis vanEngelsdorp, Benjamin Dainat
mBio Apr 2016, 7 (2) e02164-15; DOI: 10.1128/mBio.02164-15
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • INTRODUCTION
    • MICROBIOME AS A COMPONENT OF BEE HEALTH
    • THE BEE MICROBIOME AS AN EVOLUTIONARY MODEL FOR SYMBIOSIS
    • PERSPECTIVE: CHALLENGES AND NOVEL APPROACHES
    • CONCLUSIONS
    • ACKNOWLEDGMENTS
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

Related Articles

Cited By...

About

  • About mBio
  • Editor in Chief
  • Board of Editors
  • AAM Fellows
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Author Warranty
  • Article Types
  • Ethics
  • Contact Us

Follow #mBio

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

Online ISSN: 2150-7511