The bee microbiome: Impact on bee health and model for evolution and ecology of host-microbe interactions

mBio

Volumn 7, Issue 2, 2016, Pages

  Engel, Philipp ^a   Kwong, Waldan K ^b,c   McFrederick, Quinn ^d   Anderson, Kirk E ^e   Barribeau, Seth Michael ^f   Chandler, James Angus ^g,ac   Cornman, R Scott ^h   Dainat, Jacques ^i,ab   De Miranda, Joachim R ^j   Doublet, Vincent ^k,l   Emery, Olivier ^a   Evans, Jay D ^m   Farinelli, Laurent ⁿ   Flenniken, Michelle L ^o   Granberg, Fredrik ^j   Grasis, Juris A ^p   Gauthier, Laurent ^a,b   Hayer, Juliette ^j   Koch, Hauke ^c,q   Kocher, Sarah ^r   Martinson, Vincent G ^s   Moran, Nancy ^c   Munoz Torres, Monica ^t   Newton, Irene ^u   Paxton, Robert J ^k,l   Powell, Eli ^c   Sadd, Ben M ^v   Schmid Hempel, Paul ^w   Schmid Hempel, Regula ^w   Song, Se Jin ^x   Schwarz, Ryan S ^m   van Engelsdorp, Dennis ^y   Dainat, Benjamin ^z,aa   more..

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b YALE UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e CARL HAYDEN BEE RESEARCH CENTER   (United States)

^f EAST CAROLINA UNIVERSITY   (United States)

^g CALIFORNIA ACADEMY OF SCIENCES   (United States)

^h FORT COLLINS SCIENCE CENTER   (United States)

ⁱ LINKÖPING UNIVERSITY   (Sweden)

^j SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^k MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^l GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

^m U S DEPARTMENT OF AGRICULTURE   (United States)

ⁿ FASTERIS SA   (Switzerland)

^o MONTANA STATE UNIVERSITY   (United States)

^p SAN DIEGO STATE UNIVERSITY   (United States)

^q ROYAL BOTANIC GARDENS   (United Kingdom)

^r HARVARD UNIVERSITY   (United States)

^s UNIVERSITY OF ROCHESTER   (United States)

^t LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^u INDIANA UNIVERSITY   (United States)

^v ILLINOIS STATE UNIVERSITY   (United States)

^w ETH ZURICH   (Switzerland)

^x UNIVERSITY OF COLORADO   (United States)

^y University of Maryland   (United States)

^z Agroscope Liebefeld Posieux ALP   (Switzerland)

^aa Apiservice   (Switzerland)

^ab UPPSALA UNIVERSITY   (Sweden)

^ac UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

16SRRNA GENE; ARTICLE; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BEE MICROBIOME; FRISCHELLA PERRARA; GENE SEQUENCE; HIGH THROUGHPUT SEQUENCING; HOST PARASITE INTERACTION; HUMAN; MELISSOCOCCUS PLUTONIUS; MICROBIAL COMMUNITY; MICROBIOME; MOLECULAR ECOLOGY; NONHUMAN; NOSEMA; NOSEMA APIS; NOSEMA BOMBI; NOSEMA CERANAE; PAENIBACILLACEAE; PAENIBACILLUS LARVAE; PHENOTYPE; POLLINATOR; PRIORITY JOURNAL; SYMBIOSIS; SYNTHESIS; ANIMAL; BACTERIUM; BEE; CLASSIFICATION; EVOLUTION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; POLLINATION;

ANIMALS; BACTERIA; BEES; BIOLOGICAL EVOLUTION; MICROBIOTA; POLLINATION; SYMBIOSIS;

EID: 84965157449     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02164-15     Document Type: Article

References (100)

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