Abstract

Anthropogenic changes create evolutionarily novel environments that present opportunities for emerging diseases, potentially changing the balance between host and pathogen. Honey bees provide essential pollination services, but intensification and globalization of honey bee management has coincided with increased pathogen pressure, primarily due to a parasitic mite/virus complex. Here, we investigated how honey bee individual and group phenotypes are altered by a virus of concern, Israeli acute paralysis virus (IAPV). Using automated and manual behavioral monitoring of IAPV-inoculated individuals, we find evidence for pathogen manipulation of worker behavior by IAPV, and reveal that this effect depends on social context; that is, within versus between colony interactions. Experimental inoculation reduced social contacts between honey bee colony members, suggesting an adaptive host social immune response to diminish transmission. Parallel analyses with double-stranded RNA (dsRNA)-immunostimulated bees revealed these behaviors are part of a generalized social immune defensive response. Conversely, inoculated bees presented to groups of bees from other colonies experienced reduced aggression compared with dsRNA-immunostimulated bees, facilitating entry into susceptible colonies. This reduction was associated with a shift in cuticular hydrocarbons, the chemical signatures used by bees to discriminate colony members from intruders. These responses were specific to IAPV infection, suggestive of pathogen manipulation of the host. Emerging bee pathogens may thus shape host phenotypes to increase transmission, a strategy especially well-suited to the unnaturally high colony densities of modern apiculture. These findings demonstrate how anthropogenic changes could affect arms races between human-managed hosts and their pathogens to potentially affect global food security.

Citation

Geffre, A. C., Gernat, T., Harwood, G. P., Jones, B. M., Morselli Gysi, D., Hamilton, A. R., Dolezal, A. G. (2020). Honey bee virus causes context-dependent changes in host social behavior. Proceedings of the National Academy of Sciences, 202002268. https://doi.org/10.1073/pnas.2002268117

Press Coverage

Scientific Journals or similar:

• “Deadly virus turns honey bees into Trojan horses” Science, by Erik Stokstad.
• Study highlighted in the “In this Issue” section of the Proceedings of the National Academy of Sciences.
• Research Highlight in Nature Reviews Microbiology.

Audio/Radio news:

• " Viral Battle In The Honey Bee Hive” Interview for “Science Friday” on National Public Radio, with Charles Bergquist.
• “Virus-Infected Bees Practice Social Distancing”, Scientific American Podcast: 60 Second Science.
• Interview on radio show Top of the mind with Julie Rose (BYU Radio)
• “Paralyse-Virus: Social Distancing bei Bienen” Forschung aktuell on Deutschlandfunk by Joachim Budde, dubbed in German

Written articles:

• Interview with Deutsche Welle about COVID impacts on beekeeping industry + the IAPV study.
• “Honey Bee Virus Tricks Hive Guards Into Admitting Sick Intruders” Smithsonian Magazine.
• “Deadly Pathogen Alters Honey Bee Behavior to Gain Access to Foreign Hives, Researchers Find” Ecowatch
• “ Deadly Virus Helps Infected Bees Get Past The Guards Of Healthy Hives” IFL Science