Evolutionarily diverse origins of deformed wing viruses in western honey bees

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 120; no. 26; p. e2301258120
• Main Authors: Hasegawa, Nonno, Techer, Maeva A., Adjlane, Noureddine, al-Hissnawi, Muntasser Sabah, Antúnez, Karina, Beaurepaire, Alexis, Christmon, Krisztina, Delatte, Helene, Dukku, Usman H., Eliash, Nurit, El-Niweiri, Mogbel A. A., Esnault, Olivier, Evans, Jay D., Haddad, Nizar J., Locke, Barbara, Muñoz, Irene, Noël, Grégoire, Panziera, Delphine, Roberts, John M. K., De la Rúa, Pilar, Shebl, Mohamed A., Stanimirovic, Zoran, Rasmussen, David A., Mikheyev, Alexander S.
• Format: Journal Article Web Resource
• Language: English
• Published: United States National Academy of Sciences 27.06.2023; Proceedings of the National Academy of Sciences
• Subjects: Animal biology; Animals; apis; Apis mellifera; Bees; Biodiversity; Biological Evolution; Biological Sciences; Deformation; Demography; Disease transmission; Epidemiology; Evolutionary Biology; Evolutionsbiologi; Food security; Genomes; Globalization; Honey; Host Microbial Interactions; Infectious diseases; Life Sciences; Multidisciplinary; Origins; Pandemics; Phylogeography; Population number; RNA viruses; RNA Viruses - genetics; Sciences du vivant; single-stranded RNA viruses; varroa; Varroidae; Veterinary medicine and animal Health; Virulence; Viruses; Zoologie; Zoology; East Asia; apis; varroa; single-stranded RNA viruses; phylogeography; virus des animaux; Apis mellifera; Varroa; ectoparasite; vecteur de maladie; virus des ailes déformées; transmission des maladies
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.2301258120

Novel transmission routes can allow infectious diseases to spread, often with devastating consequences. Ectoparasitic varroa mites vector a diversity of RNA viruses, 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 East 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 East Asia and appears absent from 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 globalization poses urgent threats to biodiversity and food security.