Honey bee virus causes context-dependent changes in host social behavior

Significance The increase in human population has fueled demand for pollination services; the resulting intensification and globalization of honey bee management has coincided with increased pathogen pressure. We hypothesized that Israeli acute paralysis virus (IAPV) can alter host social behavior, predicting different behavioral changes depending on social context. Using automated and manual behavioral monitoring, we find that honey bees have social immune mechanisms that may keep IAPV from spreading within a colony, but IAPV infection results in behavioral and physiological changes that could increase transmission between colonies. These results show how IAPV could take advantage of modern apiculture to increase its virulence and highlight the critical need to understand how human manipulation of managed species can lead to increased pathogen pressure. 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.