Evolutionarily diverse origins of deformed wing viruses in western honey bees

Authors: HASEGAWA, NONNO - Okinawa Institute Of Science And Technology; TECHER, MAEVA - Texas A&M University; ANTUNEZ, KARINA - Biological Research Institute, Clemente Estable (IIBCE); BEAUREPAIRE, ALEX - Inland Northwest Research Alliance, Inra; CHRISTMON, KRISZTINA - Department Of Agriculture Government Of Sri Lanka; Evans, Jay; LOCKE, BARBARA - Swedish University Of Agricultural Sciences; ROBERTS, JOHN - Commonwealth Scientific And Industrial Research Organisation (CSIRO); DE LA RUA, PILAR - Universidad De Murcia; RASMUSSEN, DAVID - North Carolina State University; MIKHEYEV, ALEXANDER S - The Australian National University

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/5/2023
Publication Date: 6/20/2023
Citation: Hasegawa, N., Techer, M., Antunez, K., Beaurepaire, A., Christmon, K., Evans, J.D., Locke, B., Roberts, J., De La Rua, P., Rasmussen, D., Mikheyev, A. 2023. Evolutionarily diverse origins of deformed wing viruses in western honey bees. Proceedings of the National Academy of Sciences (PNAS). 120(26):Article e2301258120. https://doi.org/10.1073/pnas.2301258120.
DOI: https://doi.org/10.1073/pnas.2301258120

Interpretive Summary: RNA viruses adapt rapidly, sometimes switching hosts when given the opportunity. We show that two closely related honey bee Deformed Wing Virus (DWV) strains, transmitted by ectoparasitic varroa mites, show different patterns of spread. DWV-A was present in varroa's ancestral host in Asia and spread worldwide post-switch. By contrast, DWV-B was most likely absent in the original host and was acquired later, replacing the original strain in many regions. DWV illustrate the dynamic nature of viral adaptation and competition, as well as the risks posed by globalisation.

Technical Abstract: Novel transmission routes can allow infectious diseases to spread, often with devastating consequences. Ectoparasitic varroa mites vector a diversity of RNA viruses and, having switched hosts from the eastern to western honey bees (Apis cerana to Apis mellifera). They provide an opportunity to explore how novel transmission routes shape disease epidemiology. As the principal driver of the spread of Deformed Wing Viruses (mainly DWV-A and DWV-B), varroa infestation has also driven global honey bee health declines. The more virulent DWV-B strain has been replacing the original DWV-A strain in many regions over the past two decades. Yet, how these viruses originated and spread remains poorly understood. Here we use a phylogeographic analysis based on whole genome data to reconstruct the origins and demography of DWV spread. We found that, rather than reemerging in western honey bees after varroa switched hosts, as suggested by previous work, DWV-A most likely originated in Asia and spread in the mid-20th century. It also showed a massive population size expansion following the varroa host switch. By contrast, DWV-B was most likely acquired more recently from a source outside Asia, and appears absent from eastern honey bees, the original varroa host. These results highlight the dynamic nature of viral adaptation, whereby a vector’s host switch can give rise to competing and increasingly virulent disease pandemics. The evolutionary novelty and rapid global spread of these host-virus interactions, together with observed spillover into other species, illustrate how increasing globalisation poses urgent threats to biodiversity and food security.