Review Article

Ecological and evolutionary approaches to managing honeybee disease

  • Nature Ecology & Evolution 112501262 (2017)
  • doi:10.1038/s41559-017-0246-z
  • Download Citation
Received:
Accepted:
Published online:

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.

  • Subscribe to Nature Ecology & Evolution for full access:

    $99

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

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

  2. 2.

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

  3. 3.

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

  4. 4.

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

  5. 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).

  6. 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).

  7. 7.

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

  8. 8.

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

  9. 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).

  10. 10.

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

  11. 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).

  12. 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).

  13. 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).

  14. 14.

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

  15. 15.

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

  16. 16.

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

  17. 17.

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

  18. 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).

  19. 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).

  20. 20.

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

  21. 21.

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

  22. 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).

  23. 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).

  24. 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).

  25. 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).

  26. 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).

  27. 27.

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

  28. 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).

  29. 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).

  30. 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).

  31. 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).

  32. 32.

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

  33. 33.

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

  34. 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).

  35. 35.

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

  36. 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).

  37. 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).

  38. 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).

  39. 39.

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

  40. 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. 41.

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

  42. 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).

  43. 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).

  44. 44.

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

  45. 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).

  46. 46.

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

  47. 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).

  48. 48.

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

  49. 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).

  50. 50.

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

  51. 51.

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

  52. 52.

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

  53. 53.

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

  54. 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).

  55. 55.

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

  56. 56.

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

  57. 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).

  58. 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).

  59. 59.

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

  60. 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).

  61. 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).

  62. 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).

  63. 63.

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

  64. 64.

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

  65. 65.

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

  66. 66.

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

  67. 67.

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

  68. 68.

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

  69. 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).

  70. 70.

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

  71. 71.

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

  72. 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).

  73. 73.

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

  74. 74.

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

  75. 75.

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

  76. 76.

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

  77. 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).

  78. 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).

  79. 79.

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

  80. 80.

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

  81. 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).

  82. 82.

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

  83. 83.

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

  84. 84.

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

  85. 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).

  86. 86.

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

  87. 87.

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

  88. 88.

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

  89. 89.

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

  90. 90.

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

  91. 91.

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

  92. 92.

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

  93. 93.

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

  94. 94.

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

  95. 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).

  96. 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).

  97. 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).

  98. 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).

  99. 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).

  100. 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).

  101. 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).

  102. 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).

  103. 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).

  104. 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).

  105. 105.

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

  106. 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).

  107. 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).

  108. 108.

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

  109. 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).

  110. 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).

  111. 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).

  112. 112.

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

  113. 113.

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

  114. 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).

  115. 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).

  116. 116.

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

  117. 117.

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

  118. 118.

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

  119. 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).

  120. 120.

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

  121. 121.

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

  122. 122.

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

  123. 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).

  124. 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).

  125. 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).

  126. 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).

  127. 127.

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

  128. 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).

  129. 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).

  130. 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).

  131. 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).

  132. 132.

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

  133. 133.

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

  134. 134.

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

  135. 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).

  136. 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).

  137. 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).

  138. 138.

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

  139. 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).

  140. 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).

  141. 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).

  142. 142.

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

  143. 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).

  144. 144.

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

  145. 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).

  146. 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).

  147. 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. 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).

  149. 149.

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

  150. 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).

  151. 151.

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

  152. 152.

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

  153. 153.

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

  154. 154.

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

  155. 155.

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

  156. 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).

  157. 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).

  158. 158.

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

  159. 159.

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

  160. 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).

  161. 161.

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

  162. 162.

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

  163. 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).

  164. 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).

  165. 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).

  166. 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).

  167. 167.

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

  168. 168.

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

  169. 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).

  170. 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).

  171. 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).

  172. 172.

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

  173. 173.

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

  174. 174.

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

  175. 175.

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

  176. 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).

  177. 177.

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

  178. 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).

  179. 179.

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

  180. 180.

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

  181. 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).

  182. 182.

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

  183. 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).

  184. 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).

  185. 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).

  186. 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).

  187. 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).

  188. 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).

  189. 189.

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

  190. 190.

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

  191. 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).

  192. 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).

  193. 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).

  194. 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).

  195. 195.

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

  196. 196.

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

  197. 197.

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

  198. 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).

  199. 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).

  200. 200.

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

  201. 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).

  202. 202.

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

  203. 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).

  204. 204.

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

  205. 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).

  206. 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).

  207. 207.

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

  208. 208.

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

  209. 209.

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

  210. 210.

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

  211. 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).

  212. 212.

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

  213. 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).

  214. 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).

  215. 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).

  216. 216.

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

  217. 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).

  218. 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).

  219. 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).

  220. 220.

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

  221. 221.

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

  222. 222.

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

  223. 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).

  224. 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).

  225. 225.

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

  226. 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).

Download references

Acknowledgements

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.

Author information

Author notes

  1. Berry J. Brosi and Jacobus C. de Roode contributed equally to this work.

Affiliations

  1. Department of Environmental Sciences, Emory University, Atlanta, GA, 30322, USA

    • Berry J. Brosi
  2. Department of Entomology, University of Georgia, Athens, GA, 30602, USA

    • Keith S. Delaplane
  3. Department of Integrative Biology, University of California, Berkeley, CA, 94720, USA

    • Michael Boots
  4. Department of Biology, Emory University, Atlanta, GA, 30322, USA

    • Jacobus C. de Roode

Authors

  1. Search for Berry J. Brosi in:

  2. Search for Keith S. Delaplane in:

  3. Search for Michael Boots in:

  4. Search for Jacobus C. de Roode in:

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Berry J. Brosi or Jacobus C. de Roode.