Bees guarding healthy hives regularly grant entrance to foreign intruders infected with the Israeli acute paralysis virus, a deadly pathogen linked with colony collapse disorder, according to a new study.

In fact, bees infected with IAPV were more likely to gain entrance to foreign hives than healthy would-be intruders.

The research, published Monday in the journal PNAS, suggests the virus alters the behavior and physiology of infected bees in a way that helps them spread the pathogen to other hives.

"The most important finding of our study is that IAPV infection increases the likelihood that infected bees are accepted by foreign colonies," lead researcher Adam Dolezal, a professor of entomology at the University of Illinois at Urbana-Champaign, said in a news release. "Somehow, the infected bees are able to circumvent the guards of foreign colonies, which they shouldn't be able to do."

Previous studies have shown IAPV-infected honey bees are more likely to get lost traveling to and from the hive and nearby food sources. The latest research suggests lost bees with IAPV are readily accepted by foreign hives.

To study the spread of IAPV, scientists used precise tracking technology to follow the movements of individual bees and their interactions with one another. Each bee was tagged with the equivalent of a QR code. The method was originally developed to study the movements and interactions of individual bees during trophallaxis, the process through which honey bees swap regurgitated food and other liquids.

"Honey bees use trophallaxis to share food with each other, as well as hormones and other signaling molecules that can affect their physiology and behavior," said Illinois entomologist Gene Robinson. "They do it in pairs by touching their mouth parts and antennae, and each bee does this with hundreds of partners a day."

"Trophallaxis is essential to the spread of information and nutrition throughout the hive, but unfortunately, a behavior performed with such close social contact also allows viral infections to be transmitted through a hive," Robinson said.

Inside their own hives, IAPV infection inspires more cautious behavior. Though equally mobile, infected bees are less likely to participate in trophallaxis than their healthy peers. Scientists also artificially stimulated an immune response in some uninfected bees, but failed to observe the same kind of social distancing.

Outside their own hive, sick bees were less cautious. When scientists placed IAPV-infected bees near the entrance of foreign hives, they readily engaged in trophallaxis with the guards. The gate guards regularly allowed entrance to infected bees while declining access to healthy bees or bees whose immune systems had been stimulated.

When scientists studied the chemical makeup of the odors emitted by sick, healthy and immuno-stimulated bees, they found each featured distinct hydrocarbon profiles.

"Something about them must be different," Dolezal said. "It seems that the virus is changing how the bees smell, and perhaps the infected bees also are behaving in a way that is meant to appease the guards by engaging more in trophallaxus."

The latest research suggests IAPV has evolved to augment bee behavior in a way that encourages the pathogen's spread.

"If you're a virus, it's much more valuable to get transmitted to a new family group, like traveling from one city to a new city," Dolezal said. "And so how do you get there? You increase the chances that the sick bees leaving colony A are more likely to get into colony B."

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