Common viral infections inhibit egg laying in honey bee queens and are linked to premature supersedure

Authors: CHAPMAN, ABIGAIL - University Of British Columbia; MCAFEE, ALISON - University Of British Columbia; TARPY, DAVID - North Carolina State University; Fine, Julia; REMPEL, ZOE - University Of Manitoba; PETERS, KIRA - University Of Manitoba; CURRIE, ROB - University Of Manitoba; FOSTER, LEONARD - University Of British Columbia

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/1/2024
Publication Date: 9/27/2024
Citation: Chapman, A., McAfee, A., Tarpy, D., Fine, J.D., Rempel, Z., Peters, K., Currie, R., Foster, L. 2024. Common viral infections inhibit egg laying in honey bee queens and are linked to premature supersedure. Scientific Reports. 14. Article 17285. https://doi.org/10.1038/s41598-024-66286-5.
DOI: https://doi.org/10.1038/s41598-024-66286-5

Interpretive Summary: Understanding what factors impact reproduction in honey bee queens is of great interest to beekeepers attempting to maximize the productivity of their colonies. We previously found that natural virus infection was tied to beekeeper-identified “failing” queens and established a causal relationship between virus infection and reduced ovary size. Here, we examine the impact of infection with a combination of black queen cell virus (BQCV) and deformed-wing virus B (DWV-B) in realistic settings over long periods of time, and while examining reproductive metrics beyond just ovary mass. We also investigate the role of a potential reproduction-immunity trade-off by injecting queens with inactivated virus to isolate the effects of immune activation versus pathogenicity. After one week, queens injected with infectious virus had significantly smaller ovaries and were less likely to begin laying again after injection while queens injected with inactivated virus had marginally smaller ovaries and no difference in egg laying. In a field experiment, we found that queen virus infection was negatively associated with ovary mass and was a significant predictor of whether supersedure cells were observed in the colony. Proteomics analysis of hemolymph showed that injection with inactivated virus stimulated a similar immune response to the live virus infection, and several of these proteins were shared with proteins negatively associated with ovary mass in the field experiment. This work solidifies the relationship between virus infection and symptoms associated with queen failure and suggests that a reproductive-immunity trade-off is partially, but not wholly responsible for these effects.

Technical Abstract: Understanding what factors impact the reproductive output of honey bee queens is of great interest to beekeepers attempting to maximize the productivity of their colonies. We previously found that natural virus infection was tied to beekeeper-identified “failing” queens and established a causal relationship between virus infection and reduced ovary size. Here, we examine the impact of experimental infections with a combination black queen cell virus (BQCV) and deformed-wing virus B (DWV-B) in more realistic settings, on a longer timescale, and while examining reproductive metrics beyond just ovary mass. We also investigate the role of a potential reproduction-immunity trade-off by injecting queens with inactivated virus to isolate the effects of immune activation versus pathogenicity. After one week, queens injected with infectious virus had significantly smaller ovaries and were less likely to begin laying again after injection while queens injected with inactivated virus had marginally smaller ovaries and no difference in egg laying. In a field experiment, we found that queen virus infection was negatively associated with ovary mass and was a significant predictor of whether supersedure cells were observed in the colony. Proteomics analysis of hemolymph showed that injection with inactivated virus stimulated a similar immune response to the live virus infection, and several of these proteins were shared with proteins negatively associated with ovary mass in the field experiment. This work solidifies the relationship between virus infection and symptoms associated with queen failure and suggests that a reproductive-immunity trade-off is partially, but not wholly responsible for these effects.