Researchers Find Bee Virus Spreads by Altering Honey Bees’ Social Distancing Behavior

Many bees on honeycomb
Honey bees on honeycomb, showing two worker bees (center) engaging in trophallaxis to share food. Photo by Amy Toth. 

AMES, Iowa — A new study conducted by researchers at Iowa State University and the University of Illinois suggests a deadly virus attacking honey bees alters their behavior and physiology in ways that boost the virus’ ability to spread.

The research, reported in the current issue of the "Proceedings of the National Academy of Sciences," found  the Israeli Acute Paralysis Virus, known as IAPV, seems to change bee behavior in ways that overcome some of bees’ natural defenses against disease pathogens. 

“This research expands our understanding of how a disease can evolve rapidly to take advantage of changing conditions. In this case, the high-density placement of hives used in many areas to pollinate agricultural crops appears to make bees more susceptible to infection,” said Amy Toth, professor of ecology, evolution, and organismal biology at Iowa State.

Toth was part of the study’s collaborative research team that included Adam Dolezal, University of Illinois entomology professor and one of the lead authors, who performed the work while a postdoctoral researcher at Iowa State.

“Our research shows the IAPV infection increases the likelihood that infected bees are accepted by foreign colonies,” Dolezal said. “Somehow, it makes the infected bees better able to circumvent the guards of foreign, uninfected colonies.”

To capture the behavior of individual bees, researchers tagged each one with the equivalent of a tiny QR code and continuously monitored their interactions. The scientists were able to simultaneously track the behaviors of as many as 900 bees, using this automated system to study how IAPV infection might affect the bees’ social behavior, including trophallaxis, a process by which honey bees exchange regurgitated food and other liquids.

“Honey bees ‘trophallax,’ or share food with each other by mouth. In the process, they are transferring social signaling molecules that  give their trophallaxis partner information about their home colony, social status and health, among other things.” said Amy Geffre, the other leading co-author of the study, who conducted much of the direct observation of the bees while a master’s student in ecology, evolution, and organismal biology at Iowa State. “Trophallaxis is an important behavior to consider in these studies, as current research indicates that many diseases can be transmitted through saliva, particularly during food sharing.”

Geffre studied the bees in a lab environment and apiary settings. “In both cases, we found the infected bees changed their behavior and social signals dramatically,” she said. 

In their own hives, IAPV-infected bees – and bees that had had their immune systems stimulated to mimic infection – engaged in less trophallaxis than their healthy counterparts. This type of “social distancing” response is well-known in bees and is thought to protect hive mates from getting infected with the disease.

Conversely, when the scientists placed honey bee workers in cages with guard bees from foreign colonies, the infected bees engaged in more trophallaxis with the guard bees. Also, when infected bees were placed at the entrance of foreign hives, the guards at were twice as likely to admit them than to let in healthy bees or bees whose immune systems had been stimulated. The changed behavior seemed to be specific to the IAPV infection, which meant something about the infected bees must be different.

To test if the difference was based on odor, the researchers analyzed the chemistry of the hydrocarbons, many of which act as key social signals, that coat the bees’ exoskeletons. They discovered certain hydrocarbons varied among healthy bees, IAPV-infected bees and immuno-stimulated bees.

“The virus seems to change how the bees smell. The infected bees also may be behaving in a way meant to appease the guards from noninfected hives by trophallaxing more,” Dolezal said. Another change in the bees’ behavior that contributes to the spread of infection was found in a previous study, which showed pathogen-infected honey bees lose their way more often than healthy ones when returning home from foraging trips. This may make the diseased bees more likely to spread the virus to uninfected hives, especially where commercial beekeeping operations stack hives much closer together than what is common in the wild.

“Our findings suggest that the IAPV virus has been able to manipulate the behavior of its host to increase transmission between hives,” Toth said. “This is happening in ways that may not have been possible without novel human-created environments in modern agriculture.”

“Bee health is a huge challenge right now,” she said. “One practical implication of this research is to suggest that spacing colonies farther apart might help fight spread of the IAPV virus or other diseases within an apiary.”

Sources of support for this research include the Iowa State Horticulture Research Station, the University of Illinois School of Life Sciences, the Christopher Family Foundation, National Academies Keck Futures Initiative, the North American Pollinator Protection Campaign and the U.S. Department of Agriculture National Institute of Food and Agriculture.

Other study co-authors are Bryony C. Bonning, entomology and nematology, University of Florida at Gainesville; Gene Robinson, Tim Gernat and Adam R. Hamilton, at the Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana–Champaign;  Gyan P. Harwood, entomology, University of Illinois at Urbana-Champaign;  Beryl M. Jones, ecology, evolution, and conservation biology, University of Illinois at Urbana-Champaign; Deisy Morselli Gysic, computer science, University of Leipzig, Germany.

This article was developed in cooperation with Diana Yates, University of Illinois News Bureau.