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  • Review Article
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Ecological and evolutionary approaches to managing honeybee disease

A Publisher Correction to this article was published on 04 December 2017

This article has been updated

Abstract

Honeybee declines are a serious threat to global agricultural security and productivity. Although multiple factors contribute to these declines, parasites are a key driver. Disease problems in honeybees have intensified in recent years, despite increasing attention to addressing them. Here we argue that we must focus on the principles of disease ecology and evolution to understand disease dynamics, assess the severity of disease threats, and control these threats via honeybee management. We cover the ecological context of honeybee disease, including both host and parasite factors driving current transmission dynamics, and then discuss evolutionary dynamics including how beekeeping management practices may drive selection for more virulent parasites. We then outline how ecological and evolutionary principles can guide disease mitigation in honeybees, including several practical management suggestions for addressing short- and long-term disease dynamics and consequences.

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Fig. 1: Honeybee colony losses.

Photo credit: K.S.D.

Fig. 2: Parasites threatening honeybees.

Photo credits: Jennifer Berry (a); Mariano Higes (b); Jamie Ellis (c); Paul Kruse at KnackbockBlog (d); Western Australian Agriculture Authority (Department of Agriculture and Food, WA (e); Ron Snyder at the Bee Informed Partnership (f); USDA (g); John Hafernik (h).

Fig. 3: Beekeeping results in high bee densities and movement.
Fig. 4: Management applications.

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Change history

  • 04 December 2017

    In the HTML version of this Review originally published, a technical error led to the images in Box 2 being swapped over. This was corrected on 28 August 2017.

References

  1. Boecking, O. & Genersch, E. Varroosis: the ongoing crisis in bee keeping. J. Consum. Protect. Food Safe. 3, 221–228 (2008).

    Article  Google Scholar 

  2. Wenner, A. M. & Bushing, W. W. Varroa mite spread in the United States. Bee Cult. 124, 342–343 (1996).

    Google Scholar 

  3. Martin, S. J. et al. Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304–1306 (2012).

    Article  PubMed  CAS  Google Scholar 

  4. Pettis, J. S. & Delaplane, K. S. Coordinated responses to honey bee decline in the USA. Apidologie 41, 256–263 (2010).

    Article  Google Scholar 

  5. vanEngelsdorp, D. & Meixner, M. D. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J. Invert. Pathol. 103, S80–S95 (2010).

    Article  Google Scholar 

  6. Lee, K. V. et al. A national survey of managed honey bee 2013–2014 annual colony losses in the USA. Apidologie 46, 292–305 (2015).

    Article  Google Scholar 

  7. Budge, G. E. et al. Pathogens as predictors of honey bee colony strength in England and Wales. PLoS ONE 10, e0133228 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Potts, S. G. et al. Declines of managed honey bees and beekeepers in Europe. J. Apicult. Res. 49, 15–22 (2015).

    Article  Google Scholar 

  9. Dedej, S. & Delaplane, K. S. Honey bee (Hymenoptera: apidae) pollination of rabbiteye blueberry Vaccinium ashei var. ‘Climax’ is pollinator density-dependent. J. Econ. Entomol. 96, 1215–1220 (2003).

    Article  PubMed  Google Scholar 

  10. Potts, S. G. et al. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353 (2010).

    Article  PubMed  Google Scholar 

  11. Smith, M. R., Singh, G. M., Arian, D. M. & Myers, S. S. Effects of decreases of animal pollinators on human nutrition and global health: a modelling analysis. Lancet 386, 1964–1972 (2015).

    Article  PubMed  Google Scholar 

  12. Gallai, N., Salles, J.-M., Settele, J. & Vaissiere, B. E. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68, 810–821 (2009).

    Article  Google Scholar 

  13. Morse, R. A. & Calderone, N. W. The value of honey bees as pollinators of U. S. crops in 2000. Bee Cult. 128, 1 (2000).

    Google Scholar 

  14. Williams, I. H. in Agricultural Zoology Reviews Vol. 6 (ed. Evans, K.) 229–257 (Intercept, Newcastle upon Tyne, 1994).

  15. Klein, A.-M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303–313 (2007).

    Article  PubMed  Google Scholar 

  16. Chaplin-Kramer, R. et al. Global malnutrition overlaps with pollinator-dependent micronutrient production. Proc. R. Soc. B 281, 20141799 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Ellis, A. M., Myers, S. S. & Ricketts, T. H. Do pollinators contribute to nutritional health? PLoS ONE 10, e114805 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Goulson, D., Nicholls, E., Botias, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015).

    Article  PubMed  CAS  Google Scholar 

  19. Otto, C. R., Roth, C. L., Carlson, B. L. & Smart, M. D. Land-use change reduces habitat suitability for supporting managed honey bee colonies in the Northern Great Plains. Proc. Natl Acad. Sci. USA 113, 10430–10435 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Core, A. et al. A new threat to honey bees, the parasitic phorid fly Apocephalus borealis. PLoS ONE 7, e29639 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Higes, M., Martín-Hernández, R. & Meana, A. Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41, 375–392 (2010).

    Article  Google Scholar 

  22. Sammataro, D., de Guzman, L., George, S., Ochoa, R. & Otis, G. Standard methods for tracheal mite research. J. Apicult. Res. http://dx.doi.org/10.3896/IBRA.1.52.4.20 (2013).

    Article  Google Scholar 

  23. Tarpy, D. R. & Seeley, T. D. Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften 93, 195–199 (2006).

    Article  PubMed  CAS  Google Scholar 

  24. Carrillo-Tripp, J., Dolezal, A. G., Goblirsch, M. J., Miller, W. A., Toth, A. L. & Bonning, B. C. In vivo and in vitro infection dynamics of honey bee viruses. Sci. Rep. 6, 22265 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L. & Neumann, P. Dead or alive: Deformed Wing Virus and Varroa destructor reduce the life span of winter honeybees. Appl. Environ. Microbiol. 78, 981–987 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Nazzi, F. et al. Synergistic parasite–pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog. 8, e1002735 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. vanEngelsdorp, D. et al. Colony Collapse Disorder: A descriptive study. PLoS ONE 4, e6481 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Le Conte, Y., Ellis, M. & Ritter, W. Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie 41, 353–363 (2010).

    Article  Google Scholar 

  29. Guzmán-Novoa, E. et al. Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie 41, 443–450 (2010).

    Article  Google Scholar 

  30. Kraus, B. & Page, R. E. Effect of Varroa jacobsoni (Mesostigmata: Varroidae) on feral Apis mellifera (Hymenoptera: Apidae) in California. Environ. Entomol. 24, 1473–1480 (1995).

    Article  Google Scholar 

  31. Kielmanowicz, M. G. et al. Prospective large-scale field study generates predictive model identifying major contributors to colony losses. PLoS Pathog. 11, e1004816 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Cox-Foster, D. L. et al. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318, 283–287 (2007).

    Article  PubMed  CAS  Google Scholar 

  33. Bromenshenk, J. J. et al. Iridovirus and microsporidian linked to honey bee colony decline. PLoS ONE 5, e13181 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Di Prisco, G. et al. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc. Natl Acad. Sci. USA 110, 18466–18471 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Alaux, C. et al. Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol. 12, 774–782 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Mullin, C. A. et al. High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5, e9754 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Berry, J. A., Hood, W. M., Pietravalle, S. & Delaplane, K. S. Field-level sublethal effects of approved bee hive chemicals on honey bees (Apis mellifera L). PLoS ONE 8, e76536 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Kermack, W. O. & McKendrick, A. G. A contribution to the mathematical theory of epidemics. Proc. R. Soc. Lon. Ser. A 115, 700–721 (1927).

    Article  Google Scholar 

  39. Anderson, R. M. & May, R. M. Infectious Diseases of Humans: Dynamics and Control (Oxford Univ. Press, Oxford, 1991).

  40. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. & Dobson, A. P. in The Ecology of Wildlife Diseases (eds Hudson, P. J. et al.) (Oxford Univ. Press, Oxford, 2002).

  41. Pandey, A. et al. Strategies for containing Ebola in West Africa. Science 346, 991–995 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Keeling, M. J., Woolhouse, M. E. J., May, R. M., Davies, G. & Grenfell, B. T. Modelling vaccination strategies against foot-and-mouth disease. Nature 421, 136–142 (2003).

    Article  PubMed  CAS  Google Scholar 

  43. Anderson, R. M., Jackson, H. C., May, R. M. & Smith, A. M. Population dynamics of fox rabies in Europe. Nature 289, 765–771 (1981).

    Article  PubMed  CAS  Google Scholar 

  44. Lloyd-Smith, J. O. et al. Should we expect population thresholds for wildlife disease? Trends Ecol. Evol. 20, 511–519 (2005).

    Article  PubMed  Google Scholar 

  45. Peel, A. J. et al. The effect of seasonal birth pulses on pathogen persistence in wild mammal populations. Proc. R. Soc. B 281, 20132962 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Bartlett, M. S. Measles periodicity and community size. J. R. Stat. Soc. Ser. A 120, 48–70 (1957).

    Article  Google Scholar 

  47. Bjørnstad, O. N., Finkenstädt, B. F. & Grenfell, B. T. Dynamics of measles epidemics: estimating scaling of transmission rates using a Time series SIR model. Ecol. Monogr. 72, 169–184 (2002).

    Article  Google Scholar 

  48. Brown, C. R. & Brown, M. B. Empirical measurement of parasite transmission between groups in a colonial bird. Ecology 85, 1619–1626 (2004).

    Article  Google Scholar 

  49. Ramsey, D. et al. The effects of reducing population density on contact rates between brushtail possums: implications for transmission of bovine tuberculosis. J. Appl. Ecol. 39, 806–818 (2002).

    Article  Google Scholar 

  50. Farrar, C. The influence of colony populations on honey production. J. Agricult. Res 54, 945–954 (1937).

    Google Scholar 

  51. Delaplane, K. S. Practical science—research helping beekeepers 2. Colony manipulations for honey production. Bee World 78, 5–11 (1997).

    Article  Google Scholar 

  52. Seeley, T. & Morse, R. The nest of the honey bee (Apis mellifera L.). Insectes Sociaux 23, 495–512 (1976).

    Article  Google Scholar 

  53. Delaplane, K. S. & Hood, W. M. Economic threshold for Varroa jacobsoni Oud. in the southeastern USA. Apidologie 30, 383–395 (1999).

    Article  Google Scholar 

  54. Loftus, J. C., Smith, M. L. & Seeley, T. D. How honey bee colonies survive in the wild: testing the importance of small nests and frequent swarming. PLoS ONE 11, e0150362 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Seeley, T. D. Honeybee Ecology (Princeton Univ. Press, Princeton, 1985).

  56. Killion, E. E. Honey in the Comb (Dadant and Sons, Hamilton, IL, 1981).

  57. Seeley, T. D., Tarpy, D. R., Griffin, S. R., Carcione, A. & Delaney, D. A. A survivor population of wild colonies of European honeybees in the northeastern United States: investigating its genetic structure. Apidologie 46, 654–666 (2015).

    Article  Google Scholar 

  58. Seeley, T. D. & Smith, M. L. Crowding honeybee colonies in apiaries can increase their vulnerability to the deadly ectoparasite Varroa destructor. Apidologie 46, 716–727 (2015).

    Article  Google Scholar 

  59. Greatti, M., Milani, N. & Nazzi, F. Reinfestation of an acaricide-treated apiary by Varroa jacobsoni Oud. Exp. Appl. Acarol. 16, 279–286 (1992).

    Article  Google Scholar 

  60. Frey, E. & Rosenkranz, P. Autumn invasion rates of Varroa destructor (Mesostigmata: Varroidae) into honey bee (Hymenoptera: Apidae) colonies and the resulting increase in mite populations. J. Econ. Entomol. 107, 508–515 (2014).

    Article  PubMed  Google Scholar 

  61. Nolan, M. P. & Delaplane, K. S. Distance between honey bee Apis mellifera colonies regulates populations of Varroa destructor at a landscape scale. Apidologie 48, 8–16 (2016).

    Article  PubMed Central  Google Scholar 

  62. Frey, E., Schnell, H. & Rosenkranz, P. Invasion of Varroa destructor mites into mite-free honey bee colonies under the controlled conditions of a military training area. J. Apicult. Res. 50, 138–144 (2011).

    Article  Google Scholar 

  63. King, K. C. & Lively, C. M. Does genetic diversity limit disease spread in natural host populations? Heredity 109, 199–203 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Keesing, F. et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647–652 (2010).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  65. Civitello, D. J. et al. Biodiversity inhibits parasites: Broad evidence for the dilution effect. Proc. Natl Acad. Sci. USA 112, 8667–8671 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Zhu, Y. Y. et al. Genetic diversity and disease control in rice. Nature 406, 718–722 (2000).

    Article  PubMed  CAS  Google Scholar 

  67. Mundt, C. C. Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 40, 381–410 (2002).

    Article  PubMed  CAS  Google Scholar 

  68. Schmid-Hempel, P. Parasites in Social Insects (Princeton Univ. Press, Princeton, 1998).

  69. Tarpy, D., Nielsen, R. & Nielsen, D. A scientific note on the revised estimates of effective paternity frequency in Apis. Insectes Sociaux 51, 203–204 (2004).

    Article  Google Scholar 

  70. Seeley, T. D. & Tarpy, D. R. Queen promiscuity lowers disease within honeybee colonies. Proc. R. Soc. B 274, 67–72 (2007).

    Article  PubMed  Google Scholar 

  71. Tarpy, D. R. Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc. R. Soc. B 270, 99–103 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Delaplane, K. S., Pietravalle, S., Brown, M. A. & Budge, G. E. Honey bee colonies headed by hyperpolyandrous queens have improved brood rearing efficiency and lower infestation rates of parasitic Varroa mites. PLoS ONE 10, e0142985 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Lochmiller, R. L. & Deerenberg, C. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98 (2000).

    Article  Google Scholar 

  74. Ayres, J. S. & Schneider, D. S. The role of anorexia in resistance and tolerance to infections in Drosophila. PLoS Biol. 7, e1000150 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Moret, Y. & Schmid-Hempel, P. Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 1166–1168 (2000).

    Article  PubMed  CAS  Google Scholar 

  76. Siva-Jothy, M. T. & Thompson, J. J. W. Short-term nutrient deprivation affects immune function. Physiol. Entomol. 27, 206–212 (2002).

    Article  Google Scholar 

  77. vanEngelsdorp, D., Hayes, J., Underwood, R. M., Pettis, J. & Gay, N. A survey of honey bee colony losses in the U. S., fall 2007 to spring 2008. PLoS ONE 3, e4071 (2008).

    Article  PubMed Central  CAS  Google Scholar 

  78. DeGrandi-Hoffman, G. et al. Honey bee colonies provided with natural forage have lower pathogen loads and higher overwinter survival than those fed protein supplements. Apidologie 47, 186–196 (2016).

    Article  CAS  Google Scholar 

  79. Alaux, C., Ducloz, F., Crauser, D. & Le Conte, Y. Diet effects on honeybee immunocompetence. Biol. Lett. 6, 562–565 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  80. de Roode, J. C., Lefèvre, T. & Hunter, M. D. Self-medication in animals. Science 340, 150–151 (2013).

    Article  PubMed  Google Scholar 

  81. Villalba, J. J., Miller, J., Ungar, E. D., Landau, S. Y. & Glendinning, J. Ruminant self-medication against gastrointestinal nematodes: evidence, mechanism, and origins. Parasite 21, 31 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  82. de Roode, J. C. & Lefèvre, T. Behavioral immunity in insects. Insects 3, 789–820 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  83. Gherman, B. I. et al. Pathogen-associated self-medication behavior in the honeybee Apis mellifera. Behav. Ecol. Sociobiol. 68, 1777–1784 (2014).

    Article  Google Scholar 

  84. Castella, G., Chapuisat, M. & Christe, P. Prophylaxis with resin in wood ants. Anim. Behav. 75, 1591–1596 (2008).

    Article  Google Scholar 

  85. Simone-Finstrom, M. D. & Spivak, M. Increased resin collection after parasite challenge: a case of self-medication in honey bees? PLoS ONE 7, e34601 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Cremer, S., Armitage, S. A. O. & Schmid-Hempel, P. Social immunity. Curr. Biol. 17, R693–R702 (2007).

    Article  PubMed  CAS  Google Scholar 

  87. López, J. H., Schuehly, W., Crailsheim, K. & Riessberger-Gallé, U. Trans-generational immune priming in honeybees. Proc. R. Soc. B. 281, 20140454 (2014).

    Article  Google Scholar 

  88. Byrd, A. L. & Segre, J. A. Adapting Koch’s postulates. Science 351, 224–226 (2016).

    Article  PubMed  CAS  Google Scholar 

  89. Johnson, P. T. J., de Roode, J. C. & Fenton, A. Why infectious disease research needs community ecology. Science 349, 1259504 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Alizon, S., de Roode, J. C. & Michalakis, Y. Multiple infections and the evolution of virulence. Ecol. Lett. 16, 556–567 (2013).

    Article  PubMed  Google Scholar 

  91. Pedersen, A. B. & Fenton, A. Emphasizing the ecology in parasite community ecology. Trends Ecol. Evol. 22, 133–139 (2007).

    Article  PubMed  Google Scholar 

  92. May, R. M. & Nowak, M. A. Coinfection and the evolution of parasite virulence. Proc. R. Soc. B 261, 209–215 (1995).

    Article  PubMed  CAS  Google Scholar 

  93. Van Baalen, M. & Sabelis, M. W. The dynamics of multiple infection and the evolution of virulence. Am. Nat. 146, 881–910 (1995).

    Article  Google Scholar 

  94. Nowak, M. A. & May, R. M. Superinfection and the evolution of parasite virulence. Proc. R. Soc. B 255, 81–89 (1994).

    Article  PubMed  CAS  Google Scholar 

  95. Blackwell, A. D., Martin, M., Kaplan, H. & Gurven, M. Antagonism between two intestinal parasites in humans: the importance of co-infection for infection risk and recovery dynamics. Proc. R. Soc. B 280, 20131671 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  96. Knowles, S. C. L. et al. Stability of within-host-parasite communities in a wild mammal system. Proc. R. Soc. B 280, 20130598 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Ezenwa, V. O. & Jolles, A. E. Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales. Science 347, 175–177 (2015).

    Article  PubMed  CAS  Google Scholar 

  98. Jolles, A. E., Ezenwa, V. O., Etienne, R. S., Turner, W. C. & Olff, H. Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology 89, 2239–2250 (2008).

    Article  PubMed  Google Scholar 

  99. Anderson, D. L. & Gibbs, A. J. Inapparent virus infections and their interactions in pupae of the honey bee (Apis mellifera Linnaeus) in Australia. J. Gen. Virol. 69, 1617–1625 (1988).

    Article  Google Scholar 

  100. Toplak, I., Jamnikar Ciglenečki, U., Aronstein, K. & Gregorc, A. Chronic bee paralysis virus and Nosema ceranae experimental co-infection of winter honey bee workers (Apis mellifera L.). Viruses 5, 2282–2297 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Antúnez, K. et al. Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ. Microbiol. 11, 2284–2290 (2009).

    Article  PubMed  CAS  Google Scholar 

  102. Chen, Y. P. et al. Multiple virus infections in the honey bee and genome divergence of honey bee viruses. J. Invert. Pathol. 87, 84–93 (2004).

    Article  CAS  Google Scholar 

  103. Delaplane, K. S., Ellis, J. D. & Hood, W. M. A test for interactions between Varroa destructor (Acari: Varroidae) and Aethina tumida (Coleoptera: Nitidulidae) in colonies of honey bees (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 103, 711–715 (2010).

    Article  Google Scholar 

  104. Downey, D. L. & Winston, M. L. Honey bee colony mortality and productivity with single and dual infestations of parasitic mite species. Apidologie 32, 567–575 (2001).

    Article  Google Scholar 

  105. Cornman, R. S. et al. Pathogen webs in collapsing honey bee colonies. PLoS ONE 7, 15 (2012).

    Article  CAS  Google Scholar 

  106. Ellis, J. D., Evans, J. D. & Pettis, J. Colony losses, managed colony population decline, and Colony Collapse Disorder in the United States. J. Apicult. Res. 49, 134–136 (2010).

    Article  Google Scholar 

  107. Mondet, F., de Miranda, J. R., Kretzschmar, A., Le Conte, Y. & Mercer, A. R. On the front line: quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor. PLoS Pathog. 10, e1004323 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  108. Wilfert, L. et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 351, 594–597 (2016).

    Article  PubMed  CAS  Google Scholar 

  109. Yang, X. L. & Cox-Foster, D. L. Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification. Proc. Natl Acad. Sci. USA 102, 7470–7475 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. Oliver, K. M., Russell, J. A., Moran, N. A. & Hunter, M. S. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl Acad. Sci. USA 100, 1803–1807 (2003).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  111. Gerardo, N. M. & Parker, B. J. Mechanisms of symbiont-conferred protection against natural enemies: an ecological and evolutionary framework. Curr. Opin. Insect Sci. 4, 8–14 (2014).

    Article  PubMed  Google Scholar 

  112. Buffie, C. G. & Pamer, E. G. Microbiota-mediated colonization resistance against intestinal pathogens. Nat. Rev. Immunol. 13, 790–801 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  113. Moran, N. A. Genomics of the honey bee microbiome. Curr. Opin. Insect Sci. 10, 22–28 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  114. Omar, M. O. M. et al. Antagonistic effect of gut bacteria in the hybrid carniolan honey bee, Apis mellifera carnica, against Ascosphaera apis, the causal organsim of chalkbrood disease. J. Apicult. Sci. 58, 17–27 (2014).

    Article  CAS  Google Scholar 

  115. Corby-Harris, V. et al. Parasaccharibacter apium, gen. nov., sp nov., improves honey bee (Hymenoptera: Apidae) resistance to Nosema. J. Econ. Entomol. 109, 537–543 (2016).

    Article  PubMed  CAS  Google Scholar 

  116. Burnet, M. & White, D. O. The Natural History of Infectious Disease (Cambridge Univ. Press, Cambridge, 1972).

  117. Anderson, R. M. & May, R. M. Coevolution of hosts and parasites. Parasitology 85, 411–426 (1982).

    Article  PubMed  Google Scholar 

  118. Bremermann, H. J. & Thieme, H. R. A competitive exclusion principle for pathogen virulence. J. Math. Biol. 27, 179–190 (1989).

    Article  PubMed  CAS  Google Scholar 

  119. May, R. M. & Anderson, R. M. Epidemiology and genetics in the coevolution of parasites and hosts. Proc. R. Soc. B 219, 281–313 (1983).

    Article  CAS  Google Scholar 

  120. Levin, S. & Pimentel, D. Selection of intermediate rates of increase in parasite-host systems. Am. Nat. 117, 308–315 (1981).

    Article  Google Scholar 

  121. Bremermann, H. J. & Pickering, J. A game-theoretical model of parasite virulence. J. Theor. Biol. 100, 411–426 (1983).

    Article  PubMed  CAS  Google Scholar 

  122. Frank, S. A. Models of parasite virulence. Quart. Rev. Biol. 71, 37–78 (1996).

    Article  PubMed  CAS  Google Scholar 

  123. Antia, R., Levin, B. R. & May, R. M. Within-host population dynamics and the evolution and maintenance of microparasite virulence. Am. Nat. 144, 457–472 (1994).

    Article  Google Scholar 

  124. Sasaki, A. & Iwasa, Y. Optimal growth schedule of pathogens within a host: switching between lytic and latent cycles. Theor. Pop. Biol. 39, 201–239 (1991).

    Article  CAS  Google Scholar 

  125. Alizon, S., Hurford, A., Mideo, N. & Van Baalen, M. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22, 245–259 (2009).

    Article  PubMed  CAS  Google Scholar 

  126. de Roode, J. C., Yates, A. J. & Altizer, S. Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc. Natl Acad. Sci. USA 105, 7489–7494 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  127. Bolker, B. M., Nanda, A. & Shah, D. Transient virulence of emerging pathogens. J. R. Soc. Lon. Interf. 7, 811–822 (2010).

    Article  Google Scholar 

  128. Jensen, K. H., Little, T. J., Skorping, A. & Ebert, D. Empirical support for optimal virulence in a castrating parasite. PLoS Biol. 4, e197 (2006).

    Article  CAS  Google Scholar 

  129. Mackinnon, M. J. & Read, A. F. Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53, 689–703 (1999).

    Article  PubMed  Google Scholar 

  130. Messenger, S. L., Molineux, I. J. & Bull, J. J. Virulence evolution in a virus obeys a trade-off. Proc. R. Soc. B 266, 397–404 (1999).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  131. Fraser, C., Hollingsworth, T. D., Chapman, R., de Wolf, F. & Hanage, W. P. Variation in HIV-1 set-point viral load: Epidemiological analysis and an evolutionary hypothesis. Proc. Natl Acad. Sci. USA 104, 17441–17446 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  132. Mackinnon, M. J. & Read, A. F. Virulence in malaria: an evolutionary viewpoint. Philos. Trans. R. Soc. Lon. Ser. B 359, 965–986 (2004).

    Article  Google Scholar 

  133. Bull, J. J., Molineux, I. J. & Rice, W. R. Selection of benevolence in a host-parasite system. Evolution 45, 875–882 (1991).

    Article  PubMed  CAS  Google Scholar 

  134. Ewald, P. W. Host-parasite relations, vectors, and the evolution of disease severity. Annu. Rev. Ecol. System 14, 465–485 (1983).

    Article  Google Scholar 

  135. de Roode, J. C. et al. Virulence and competitive ability in genetically diverse malaria infections. Proc. Natl Acad. Sci. USA 102, 7624–7628 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  136. Vojvodic, S., Jensen, A. B., Markussen, B., Eilenberg, J. & Boomsma, J. J. Genetic variation in virulence among chalkbrood strains infecting honeybees. PLoS ONE 6, e25035 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  137. McMahon, D. P. et al. Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc. R. Soc. B 283, 20160811 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Anderson, D. L. Variation in the parasitic bee mite Varroa jacobsoni Oud. Apidologie 31, 281–292 (2000).

    Article  Google Scholar 

  139. Corrêa-Marques, M. H., Medina, L. M., Martin, S. J. & De Jong, D. Comparing data on the reproduction of Varroa destructor. Genet. Mol. Res. 2, 1–6 (2003).

    PubMed  Google Scholar 

  140. De Jong, D. & Soares, A. E. E. An isolated population of Italian bees that has survived Varroa jacobsoni infestation without treatment for over 12 years. Am. Bee J. 137, 742–745 (1997).

    Google Scholar 

  141. Corrêa-Marques, M. H., de Jong, D., Rosenkranz, P. & Gonçalves, L. S. Varroa-tolerant Italian honey bees introduced from Brazil were not more efficient in defending themselves against the mite Varroa destructor than Carniolan bees in Germany. Genet. Mol. Res. 1, 153–158 (2002).

    PubMed  Google Scholar 

  142. Ritter, W., Leclercq, E. & Koch, W. Observations on bee and Varroa mite populations in infested honey bee colonies. Apidologie 15, 389–399 (1984).

    Article  Google Scholar 

  143. Martin, S. J. The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. J. Appl. Ecol. 38, 1082–1093 (2001).

    Article  Google Scholar 

  144. Fries, I. & Camazine, S. Implications of horizontal and vertical pathogen transmission for honey bee epidemiology. Apidologie 32, 199–214 (2001).

    Article  Google Scholar 

  145. Haraguchi, Y. & Sasaki, A. The evolution of parasite virulence and transmission rate in a spatially structured population. J. Theoret. Biol. 203, 85–96 (2000).

    Article  CAS  Google Scholar 

  146. Best, A., Webb, S., White, A. & Boots, M. Host resistance and coevolution in spatially structured populations. Proc. R. Soc. B 278, 2216–2222 (2011).

    Article  PubMed  Google Scholar 

  147. Van Baalen, M. in Adaptive Dynamics of Infectious Diseases: In Pursuit of Virulence Management (eds Dieckmann, U., Metz, J. A. J., Sabelis, M. W. & Sigmund, K.) 85–103 (Cambridge Univ. Press, Cambridge, 2002).

  148. Kamo, M., Sasaki, A. & Boots, M. The role of trade-off shapes in the evolution of parasites in spatial host populations: An approximate analytical approach. J. Theoret. Biol. 244, 588–596 (2007).

    Article  Google Scholar 

  149. O’Keefe, K. J. & Antonovics, J. Playing by different rules: the evolution of virulence in sterilizing pathogens. Am. Nat. 159, 597–605 (2002).

    Article  PubMed  Google Scholar 

  150. Boots, M. & Sasaki, A. ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance. Proc. R. Soc. B 266, 1933–1938 (1999).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  151. Lion, S. & Boots, M. Are parasites “prudent” in space? Ecol. Lett. 13, 1245–1255 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  152. Wild, G., Gardner, A. & West, S. A. Adaptation and the evolution of parasite virulence in a connected world. Nature 459, 983–986 (2009).

    Article  PubMed  CAS  Google Scholar 

  153. Lion, S. & van Baalen, M. Self-structuring in spatial evolutionary ecology. Ecol. Lett. 11, 277–295 (2008).

    Article  PubMed  Google Scholar 

  154. Rosenkranz, P. Honey bee (Apis mellifera L.) tolerance to Varroa jacobsoni Oud. in South America. Apidologie 30, 159–172 (1999).

    Article  Google Scholar 

  155. Dahle, B. The role of Varroa destructor for honey bee colony losses in Norway. J. Apicult. Res. 49, 124–125 (2010).

    Article  Google Scholar 

  156. Seeley, T. D. Honey bees of the Arnot Forest: a population of feral colonies persisting with Varroa destructor in the northeastern United States. Apidologie 38, 19–29 (2007).

    Article  Google Scholar 

  157. Fleming-Davies, A. E., Dukic, V., Andreasen, V. & Dwyer, G. Effects of host heterogeneity on pathogen diversity and evolution. Ecol. Lett. 18, 1252–1261 (2015).

    Article  PubMed  Google Scholar 

  158. Regoes, R. R., Nowak, M. A. & Bonhoeffer, S. Evolution of virulence in a heterogeneous host population. Evolution 54, 64–71 (2000).

    Article  PubMed  CAS  Google Scholar 

  159. Kennedy, D. A. et al. Potential drivers of virulence evolution in aquaculture. Evol. Appl. 9, 344–354 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  160. Kirchner, J. W. & Roy, B. A. Evolutionary implications of host-pathogen specificity: fitness consequences of pathogen virulence traits. Evol. Ecol. Res. 4, 27–48 (2002).

    Google Scholar 

  161. Gandon, S. & Michalakis, Y. Evolution of parasite virulence against qualitative or quantitative host resistance. Proc. R. Soc. B 267, 985–990 (2000).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  162. Gandon, S., Mackinnon, M. J., Nee, S. & Read, A. F. Imperfect vaccines and the evolution of pathogen virulence. Nature 414, 751–756 (2001).

    Article  PubMed  CAS  Google Scholar 

  163. de Roode, J. C., Lopez Fernandez de Castillejo, C., Faits, T. & Alizon, S. Virulence evolution in response to anti-infection resistance: toxic food plants can select for virulent parasites of monarch butterflies. J. Evol. Biol. 24, 712–722 (2011).

    Article  PubMed  Google Scholar 

  164. Miller, M. R., White, A. & Boots, M. The evolution of parasites in response to tolerance in their hosts: The good, the bad, and apparent commensalism. Evolution 60, 945–956 (2006).

    Article  PubMed  Google Scholar 

  165. Restif, O. & Koella, J. C. Shared control of epidemiological traits in a coevolutionary model of host-parasite interactions. Am. Nat. 161, 827–836 (2003).

    Article  PubMed  Google Scholar 

  166. Atkins, K. E. et al. Vaccination and reduced cohort duration can drive virulence evolution: Marek’s disease virus and industrialized agriculture. Evolution 67, 851–860 (2013).

    Article  PubMed  CAS  Google Scholar 

  167. Read, A. F. et al. Imperfect vaccination can enhance the transmission of highly virulent pathogens. PLoS Biol. 13, e1002198 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  168. Oldroyd, B. P. Coevolution while you wait: Varroa jacobsoni, a new parasite of western honeybees. Trends Ecol. Evol. 14, 312–315 (1999).

    Article  PubMed  CAS  Google Scholar 

  169. Klee, J. et al. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J. Invert. Pathol. 96, 1–10 (2007).

    Article  Google Scholar 

  170. Daszak, P., Cunningham, A. A. & Hyatt, A. D. Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287, 443–449 (2000).

    Article  PubMed  CAS  Google Scholar 

  171. Lenski, R. E. & May, R. M. The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. J. Theoret. Biol. 169, 253–265 (1994).

    Article  CAS  Google Scholar 

  172. Griette, Q., Raoul, G. & Gandon, S. Virulence evolution at the front line of spreading epidemics. Evolution 69, 2810–2819 (2015).

    Article  PubMed  Google Scholar 

  173. Berngruber, T. W., Froissart, R., Choisy, M. & Gandon, S. Evolution of virulence in emerging epidemics. PLoS Pathog. 9, 8 (2013).

    Article  CAS  Google Scholar 

  174. André, J. B. & Hochberg, M. E. Virulence evolution in emerging infectious diseases. Evolution 59, 1406–1412 (2005).

    Article  PubMed  Google Scholar 

  175. Hawley, D. M. et al. Parallel patterns of increased virulence in a recently emerged wildlife pathogen. PLoS Biol. 11, 11 (2013).

    Article  CAS  Google Scholar 

  176. Sternberg, E. D., Li, H., Wang, R., Gowler, C. & de Roode, J. C. Patterns of host-parasite adaptation in three populations of monarch butterflies infected with a naturally occurring protozoan disease: virulence, resistance, and tolerance. Am. Nat. 182, E235–E248 (2013).

    Article  PubMed  Google Scholar 

  177. Best, A., White, A. & Boots, M. The implications of coevolutionary dynamics to host‐parasite interactions. Am. Nat. 173, 779–791 (2009).

    Article  PubMed  Google Scholar 

  178. Boecking, O. & Ritter, W. Grooming and removal behavior of Apis mellifera intermissa in Tunisia against Varroa jacobsoni. J. Apicult. Res. 32, 127–134 (1993).

    Article  Google Scholar 

  179. Büchler, R. in New Perspectives on Varroa (ed. Matheson, A.) 12–23 (IBRA, 1994).

  180. Rath, W. Co-adaptation of Apis cerana Fabr. and Varroa jacobsoni Oud. Apidologie 30, 97–110 (1999).

    Article  Google Scholar 

  181. Higes, M., García-Palencia, P., Martín-Hernández, R. & Meana, A. Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J. Invert. Pathol. 94, 211–217 (2007).

    Article  Google Scholar 

  182. Knell, R. J. Syphilis in Renaissance Europe: rapid evolution of an introduced sexually transmitted disease? Proc. R. Soc. B 271, S174–S176 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  183. Dwyer, G., Levin, S. A. & Buttel, L. A simulation model of the population dynamics and evolution of myxomatosis. Ecol. Monogr. 60, 423–447 (1990).

    Article  Google Scholar 

  184. Tildesley, M. J., Bessell, P. R., Keeling, M. J. & Woolhouse, M. E. J. The role of pre-emptive culling in the control of foot-and-mouth disease. Proc. R. Soc. B 276, 3239–3248 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  185. Gilligan, C. A., Truscott, J. E. & Stacey, A. J. Impact of scale on the effectiveness of disease control strategies for epidemics with cryptic infection in a dynamical landscape: an example for a crop disease. J. R. Soc. Interf. 4, 925–934 (2007).

    Article  Google Scholar 

  186. Potts, S. G. et al. Summary for Policymakers of the Assessment Report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on Pollinators, Pollination and Food Production. (IPBES, Bonn, 2016).

    Google Scholar 

  187. Danka, R. G., Rinderer, T. E., Spivak, M. & Kefuss, J. Comments on: “Varroa destructor, research avenues towards sustainable control”. J. Apicult. Res. 52, 69–71 (2013).

    Article  Google Scholar 

  188. Fries, I., Imdorf, A. & Rosenkranz, P. Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate. Apidologie 37, 564–570 (2006).

    Article  Google Scholar 

  189. Le Conte, Y. et al. Honey bee colonies that have survived Varroa destructor. Apidologie 38, 566–572 (2007).

    Article  Google Scholar 

  190. Mattila, H. R. & Seeley, T. D. Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317, 362–364 (2007).

    Article  PubMed  CAS  Google Scholar 

  191. Ibrahim, A. & Spivak, M. The relationship between hygienic behavior and suppression of mite reproduction as honey bee (Apis mellifera) mechanisms of resistance to Varroa destructor. Apidologie 37, 31–40 (2006).

    Article  Google Scholar 

  192. Ibrahim, A., Reuter, G. S. & Spivak, M. Field trial of honey bee colonies bred for mechanisms of resistance against Varroa destructor. Apidologie 38, 67–76 (2007).

    Article  Google Scholar 

  193. Guzman-Novoa, E., Emsen, B., Unger, P., Espinosa-Montaño, L. G. & Petukhova, T. Genotypic variability and relationships between mite infestation levels, mite damage, grooming intensity, and removal of Varroa destructor mites in selected strains of worker honey bees (Apis mellifera L.). J. Invert. Pathol. 110, 314–320 (2012).

    Article  Google Scholar 

  194. Page, R. E. Jr & Laidlaw, H. H. Jr Closed population honeybee breeding. 2. Comparative methods of stock maintenance and selective breeding. J. Apicult. Res. 21, 38–44 (1982).

    Article  Google Scholar 

  195. Rinderer, T. E. Bee Genetics and Breeding (Academic, London, 1986).

  196. Ruttner, F. & Ruttner, H. Untersuchungen über die Flugaktivität und das Paarungsverhalten der Drohnen. V. Drohensammelplätze und Paarungsdistanz. Apidologie 3, 203–232 (1972).

    Article  Google Scholar 

  197. Status of Pollinators in North America (National Research Council, Washington DC, 2007).

  198. Simone-Finstrom, M. & Spivak, M. Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41, 295–311 (2010).

    Article  Google Scholar 

  199. Royce, L. A., Rossignol, P. A., Burgett, D. M. & Stringer, B. A. Reduction of tracheal mite parasitism of honey bees by swarming. Philos. Trans. R. Soc. Lon. Ser. B 331, 123–129 (1991).

    Article  CAS  Google Scholar 

  200. Simone, M., Evans, J. D. & Spivak, M. Resin collection and social immunity in honey bees. Evolution 63, 3016–3022 (2009).

    Article  PubMed  CAS  Google Scholar 

  201. Graystock, P., Goulson, D. & Hughes, W. O. H. Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proc. R. Soc. B 282, 20151371 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  202. Otterstatter, M. C. & Thomson, J. D. Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PLoS ONE 3, e2771 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  203. Fürst, M. A., McMahon, D. P., Osborne, J. L., Paxton, R. J. & Brown, M. J. F. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506, 364–366 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  204. Gong, H. R. et al. Evidence of Apis cerana sacbrood virus infection in Apis mellifera. Appl. Environ. Microbiol. 82, 2256–2262 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  205. Al-Khafaji, K., Tuljapurkar, S., Carey, J. R. & Page, R. E. Hierarchical demography: a general approach with an application to honey bees. Ecology 90, 556–566 (2009).

    Article  PubMed  Google Scholar 

  206. Smart, M., Pettis, J., Rice, N., Browning, Z. & Spivak, M. Linking measures of colony and individual honey bee health to survival among apiaries exposed to varying agricultural land use. PLoS ONE 11, e0152685 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  207. Johansen, C. A. Pesticides and pollinators. Annu. Rev. Entomol. 22, 177–192 (1977).

    Article  CAS  Google Scholar 

  208. Desneux, N., Decourtye, A. & Delpuech, J.-M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106 (2007).

    Article  PubMed  CAS  Google Scholar 

  209. Rundlöf, M. et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521 (2015).

  210. Stanley, D. A. et al. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528, 548–550 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  211. Seitz, N. et al. A national survey of managed honey bee 2014–2015 annual colony losses in the USA. J. Apicult. Res. 54, 292–304 (2016).

    Article  Google Scholar 

  212. Rivers, T. M. Viruses and Koch’s postulates. J. Bacteriol. 33, 1–12 (1937).

    PubMed  PubMed Central  CAS  Google Scholar 

  213. Otis, G. W. & Scott-Dupree, C. D. Effects of Acarapis woodi on overwintered colonies of honey bees (Hymenoptera, Apidae) in New York. J. Econ. Entomol. 85, 40–46 (1992).

    Article  Google Scholar 

  214. McMullan, J. B. & Brown, M. J. F. A qualitative model of mortality in honey bee (Apis mellifera) colonies infested with tracheal mites (Acarapis woodi). Exp. Appl. Acarol. 47, 225–234 (2009).

    Article  PubMed  Google Scholar 

  215. Soroker, V. et al. Evaluation of colony losses in Israel in relation to the incidence of pathogens and pests. Apidologie 42, 192–199 (2011).

    Article  Google Scholar 

  216. Higes, M. et al. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 10, 2659–2669 (2008).

    Article  PubMed  Google Scholar 

  217. Paxton, R. J., Klee, J., Korpela, S. & Fries, I. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 38, 558–565 (2007).

    Article  Google Scholar 

  218. Klinger, E. G., Vojvodic, S., DeGrandi-Hoffman, G., Welker, D. L. & James, R. R. Mixed infections reveal virulence differences between host-specific bee pathogens. J. Invert. Pathol 129, 28–35 (2015).

    Article  Google Scholar 

  219. de Miranda, J. R., Cordoni, G. & Budge, G. The Acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex. J. Invert. Pathol. 103, S30–S47 (2010).

    Article  CAS  Google Scholar 

  220. Francis, R. M., Nielsen, S. L. & Kryger, P. Varroa-virus interaction in collapsing honey bee colonies. PLoS ONE 8, e57540 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  221. Retschnig, G. et al. Sex-specific differences in pathogen susceptibility in honey bees (Apis mellifera). PLoS ONE 9, e85261 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  222. Bailey, L., Gibbs, A. J. & Woods, R. D. Sacbrood virus of the larval honey bee (Apis mellifera Linnaeus). Virology 23, 425–429 (1964).

    Article  PubMed  CAS  Google Scholar 

  223. Tokarz, R., Firth, C., Street, C., Cox-Foster, D. L. & Lipkin, W. I. Lack of evidence for an association between Iridovirus and Colony Collapse Disorder. PLoS ONE 6, e21844 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  224. Neumann, P. & Elzen, P. The biology of the small hive beetle (Aethina tumida, Coleoptera: Nitidulidae): gaps in our knowledge of an invasive species. Apidologie 35, 229–247 (2004).

    Article  Google Scholar 

  225. Anderson, R. M. & May, R. M. Population biology of infectious diseases: Part I. Nature 280, 361–367 (1979).

    Article  PubMed  CAS  Google Scholar 

  226. Mideo, N., Alizon, S. & Day, T. Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol. Evol. 23, 511–517 (2008).

    Article  PubMed  Google Scholar 

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This work was supported by the National Institute of General Medical Sciences of the National Institutes of Health under award number R01GM109501. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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Brosi, B.J., Delaplane, K.S., Boots, M. et al. Ecological and evolutionary approaches to managing honeybee disease. Nat Ecol Evol 1, 1250–1262 (2017). https://doi.org/10.1038/s41559-017-0246-z

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