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The Viruses Hidden in Our Queens

- February 1, 2021 - Alison McAfee - (excerpt)

viruses hidden in queen bees

Research in workers shows that the heat-shock response is antiviral, which is giving us clues to how queens fight viruses too

Maybe it’s because of their regal appearance. Maybe it’s their social buffer of young, healthy attendants. Maybe it’s their lack of obvious symptoms, the fact that they are (thankfully) repulsive to varroa, or that they are seldom tested for pathogens. Whatever the reason, we don’t usually think of our queens as being susceptible to disease — but they are, and it might have something to do with queen failure.

In 2019, I began a queen survey in which I collected queens from throughout the province of British Columbia. Thanks to the generosity of beekeepers, I ended that season with about 125 donated queens from different genetic lineages and colony health statuses (Figure 1a). This year, I collected a further 49 queens, this time from a smaller geographic area and with known ages. Long after their deaths, these queens are supplying a treasure trove of information about what may be causing the high failure rates we see in the field.

In the golden days, queens used to commonly live two or more years, but now, about 50% of colonies replace their queens within six months. According to a study by Dennis vanEngelsdorp in 2013, those colonies are three times more likely to perish in the following two months, without intervention, compared to colonies that didn’t replace their queens.1 Queen failure is clearly a problem, but it is frustratingly difficult to diagnose the root cause.

My mission is to figure out why our queens are failing and what can be done about it, starting by measuring everything we can think of in queens collected from the field. The survey began because the BC Bee Breeders’ Association wanted to know how their locally produced queens stacked up against imports from California and Hawaii, but it quickly turned into something much more. Our data suggest that poor quality queens tend to have higher viral infections, and there might be an easy way to help prevent that from happening.

Royal mistreatment

Several of the queen producers who participated in the survey also culled their worst queens and added them to the batch headed to our laboratory, creating a valuable data set of failed and healthy queens from a variety of locations and genetic backgrounds. We measured sperm counts, sperm viability, ovary size, and expression of thousands of specific proteins in these queens, hoping that would yield clues to their demise (Figure 1b).

Meanwhile, in the laboratory, I ran what was essentially a queen torture chamber, where I experimentally stressed other queens under controlled conditions [see “Queen Forensics,” July 2019 ABJ]. I have killed so many queens in the last two years, it is hard for me to think about, but it is for an important purpose.

The goal of the queen torturing was to identify unique molecular signatures induced by different stressors, which included heat-shock, cold-shock, and exposure to pesticides.2 These conditions can kill the queen’s stored sperm, making her unable to fertilize enough eggs and eventually leading to symptoms of queen failure [see “Long Live the Sperm,” August 2018 ABJ]. Once I defined these molecular stress signatures, I looked for them in the queens surveyed from the field to see what they may have been exposed to in the past, and couldn’t make sense of what I found.

Overall, the failed queens had lower sperm viability (Figure 2) — a finding that agrees with previous research. But when I looked at the stress signatures in the surveyed queens, I was perplexed. The failed queens had unexpectedly high levels of the molecular markers for heat-shock — unexpected because, in BC, our climate is mainly temperate, and the temperature loggers included in queen shipments indicated that they did not experience extreme heat during transit. Yet, approximately half of the failed queens I analyzed had the heat-shock signature (Figure 3). These data didn’t make sense to me, and I suspected that something else was going on.

Artificial fevers

Earlier in 2020, Alex McMenamin, a PhD candidate at Montana State University, published research showing that virus infection and heat-shock stimulate very similar stress responses in honey bee workers.3 When exposed to high temperatures, honey bees (and many other animals) produce heat-shock proteins, which are multifunctional proteins that also appear to help fight viral infection.

“We and others previously saw if you infect bees with viruses, they tend to have induced expression of heat-shock proteins,” says McMenamin. “So I just had this idea, what if we turn on heat-shock proteins by heat-shocking bees after infecting them with a virus?”

When McMenamin and his colleagues heat-shocked workers for 4 hours at 42°C (107.6°F) after injecting them with Sindbis virus, they found that those workers had lower infection levels compared