[en] 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.
Disciplines :
Zoology
Author, co-author :
Hasegawa, Nonno; Okinawa Institute of Science and Technology, Okinawa 904-0495, Japan
Techer, Maeva A ; Okinawa Institute of Science and Technology, Okinawa 904-0495, Japan ; Department of Entomology, Texas A&M University, College Station, TX 77483 ; Behavioral Plasticity Research Institute, NSF-BII, College Station, TX 77483
Adjlane, Noureddine ; Department of Agronomy, Faculty of Science, University M'hamed Bougara, Boumerdes 35000, Algeria
Al-Hissnawi, Muntasser Sabah; Ministry of Education, General Directorate of Education in Najaf Governorat, Najaf-Kufa 54003, Iraq
Antúnez, Karina; Departamento de Microbiología, Instituto de Investigaciones Biológicas Clemente Estable, 11600 Montevideo, Uruguay
Beaurepaire, Alexis ; Swiss Bee Research Center, Agroscope, 3003 Bern, Switzerland ; Institute of Bee Health, University of Bern, 3003 Bern, Switzerland
Christmon, Krisztina; United States Department of Agriculture, Agricultural Research Service, Bee Research Lab, Beltsville, MD 20705
Delatte, Helene; Centre de coopération internationale en recherche agronomique pour le développement, UMR Unité Mixte de Recherche Peuplements Végétaux et Bioagresseurs en Milieu Tropical, F-97410 Saint-Pierre, La Réunion, France
Dukku, Usman H ; Department of Biological Sciences, Abubakar Tafawa Balewa University, Bauchi 740211, Nigeria
Eliash, Nurit; Okinawa Institute of Science and Technology, Okinawa 904-0495, Japan ; Shamir Research Institute, Haifa University, Haifa 3498838, Israel
El-Niweiri, Mogbel A A ; Department of Bee Research, Environment, Natural Resources and Desertification Research Institute, National Centre for Research, Khartoum, Sudan
Esnault, Olivier; Groupement de Défense Sanitaire, Réunion, La plaine des Cafres 97418, La Réunion, France
Evans, Jay D ; United States Department of Agriculture, Agricultural Research Service, Bee Research Lab, Beltsville, MD 20705
Haddad, Nizar J; Bee Research Department, National Agricultural Research Center, 19381 Baqa', Jordan
Locke, Barbara ; Department of Ecology, Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden
Muñoz, Irene ; Department of Zoology and Physical Anthropology, Faculty of Veterinary, University of Murcia, 30100 Murcia, Spain
Noël, Grégoire ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs
Panziera, Delphine; Wageningen University & Research, 6708 PB Wageningen, The Netherlands
Roberts, John M K ; Commonwealth Scientific and Industrial Research Organisation, Canberra, ACT 2601, Australia
De la Rúa, Pilar ; Department of Zoology and Physical Anthropology, Faculty of Veterinary, University of Murcia, 30100 Murcia, Spain
Shebl, Mohamed A ; Department of Plant Protection, Faculty of Agriculture, Suez Canal University, 41522 Ismailia, Egypt
Stanimirovic, Zoran ; Department of Biology, Faculty of Veterinary Medicine, University of Belgrade, 11000 Belgrade, Serbia
Rasmussen, David A ; Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC 27695 ; Bioinformatics Research Center, North Carolina State University, Raleigh, NC 27695
Mikheyev, Alexander S ; Research School of Biology, Australian National University, Canberra, ACT 2601, Australia
D. M. Morens, G. K. Folkers, A. S. Fauci, The challenge of emerging and re-emerging infectious diseases. Nature 430, 242–249 (2004).
J. S. Weitz et al., Phage-bacteria infection networks. Trends Microbiol. 21, 82–91 (2013).
S. Binder, A. M. Levitt, J. J. Sacks, J. M. Hughes, Emerging infectious diseases: Public health issues for the 21st century. Science 284, 1311–1313 (1999).
M. E. J. Woolhouse, S. Gowtage-Sequeria, Host range and emerging and reemerging pathogens. Emerg. Infect. Dis. 11, 1842–1847 (2005).
E. C. Holmes, The Evolution and Emergence of RNA Viruses (Oxford University Press, 2009).
M. E. J. Woolhouse, K. Adair, L. Brierley, RNA viruses: A case study of the biology of emerging infectious diseases. Microbiol. Spectr. 1, 10.1128/microbiolspec.OH-0001-2012 (2013).
M. A. Kulkarni, C. Duguay, K. Ost, Charting the evidence for climate change impacts on the global spread of malaria and dengue and adaptive responses: A scoping review of reviews. Global. Health 18, 1 (2022).
S. C. Weaver, M. Lecuit, Chikungunya virus and the global spread of a mosquito-borne disease. N. Engl. J. Med. 372, 1231–1239 (2015).
R. A. C. Jones, Disease pandemics and major epidemics arising from new encounters between indigenous viruses and introduced crops. Viruses 12, 1388 (2020).
C. R. Fisher, D. G. Streicker, M. J. Schnell, The spread and evolution of rabies virus: Conquering new frontiers. Nat. Rev. Microbiol. 16, 241–255 (2018).
K. S. Traynor et al., Varroa destructor: A complex parasite, crippling honey bees worldwide. Trends Parasitol. 36, 592–606 (2020).
A. Beaurepaire et al., Diversity and global distribution of viruses of the Western honey bee, Apis mellifera. Insects 11, 239 (2020).
C. Chen et al., Population genomics provide insights into the evolution and adaptation of the Eastern honey bee (Apis cerana). Mol. Biol. Evol. 35, 2260–2271 (2018).
M. A. Techer, J. M. K. Roberts, R. A. Cartwright, A. S. Mikheyev, The first steps toward a global pandemic: Reconstructing the demographic history of parasite host switches in its native range. Mol. Ecol. 31, 1358–1374 (2020).
J. M. K. Roberts, D. L. Anderson, W. T. Tay, Multiple host shifts by the emerging honeybee parasite, Varroa jacobsoni. Mol. Ecol. 24, 2379–2391 (2015).
N. Eliash, A. Mikheyev, Varroa mite evolution: A neglected aspect of worldwide bee collapses? Curr. Opin. Insect Sci. 39, 21–26 (2020).
G. J. Mordecai, L. Wilfert, S. J. Martin, I. M. Jones, D. C. Schroeder, Diversity in a honey bee pathogen: First report of a third master variant of the Deformed Wing Virus quasispecies. ISME J. 10, 1264–1273 (2016).
L. Wilfert et al., Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 351, 594–597 (2016).
R. J. Paxton et al., Epidemiology of a major honey bee pathogen, deformed wing virus: Potential worldwide replacement of genotype A by genotype B. Int. J. Parasitol. Parasites Wildl. 18, 157–171 (2022).
A. M. Norton et al., Adaptation to vector-based transmission in a honeybee virus. J. Anim. Ecol. 90, 2254–2267 (2021).
N. Eliash, M. Suenaga, A. S. Mikheyev, Vector-virus interaction affects viral loads and co-occurrence. BMC Biol. 20, 284 (2022).
S. Gisder, E. Genersch, Direct evidence for infection of Varroa destructor Mites with the bee-pathogenic deformed wing virus variant B–but not variant A–via fluorescence-in situ-hybridization analysis. J. Virol. 95, e01786-20 (2021).
F. Posada-Florez et al., Deformed wing virus type A, a major honey bee pathogen, is vectored by the mite Varroa destructor in a non-propagative manner. Sci. Rep. 9, 12445 (2019).
D. P. McMahon et al., Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc. R. Soc. 283, 20160811 (2016).
N. Hasegawa, M. Techer, A. S. Mikheyev, A toolkit for studying Varroa genomics and transcriptomics: Preservation, extraction, and sequencing library preparation. BMC Genomics 22, 54 (2021).
M. A. Techer et al., Divergent evolutionary trajectories following speciation in two ectoparasitic honey bee mites. Commun. Biol. 2, 357 (2019).
B. Langmead, S. L. Salzberg, Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
J. Wala, C.-Z. Zhang, M. Meyerson, R. Beroukhim, VariantBam: Filtering and profiling of next-generational sequencing data using region-specific rules. Bioinformatics 32, 2029–2031 (2016).
P. Danecek et al., Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021).
D. C. Koboldt et al., VarScan: Variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics 25, 2283–2285 (2009).
P. Danecek et al., The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).
N. L. Bray, H. Pimentel, P. Melsted, L. Pachter, Erratum: Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 888 (2016).
J. Aitchison, The statistical analysis of compositional data. J. R. Stat. Soc. 44, 139–160 (1982).
B. H. McArdle, M. J. Anderson, Fitting multivariate models to community data: A comment on distance–based redundancy analysis. Ecology 82, 290–297 (2021), 10.1890/0012-9658(2001)082[ 0290:FMMTCD]2.0.CO;2.
P. Dixon, VEGAN, A package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).
E. V. Ryabov et al., Recent spread of Varroa destructor virus-1, a honey bee pathogen, in the United States. Sci. Rep. 7, 17447 (2017).
J. Moore et al., Recombinants between Deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies. J. Gen. Virol. 92, 156–161 (2011).
E. V. Ryabov et al., A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro transmission. PLoS Pathog. 10, e1004230 (2014).
D. P. Martin, B. Murrell, M. Golden, A. Khoosal, B. Muhire, RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 1, vev003 (2015).
R. Bouckaert et al., BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 15, e1006650 (2019).
P. Lemey, A. Rambaut, A. J. Drummond, M. A. Suchard, Bayesian phylogeography finds its roots. PLoS Comput. Biol. 5, e1000520 (2009).
A. J. Drummond, Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 22, 1185–1192 (2005).
S. Wang et al., Occurrence of multiple honeybee viruses in the ectoparasitic mites Varroa spp. in Apis cerana colonies. J. Invertebr. Pathol. 166, 107225 (2019).
Y. Deng et al., An investigation of honey bee virus prevalence in managed honey bees (Apis mellifera and Apis cerana) undergone colony losses: A case study in China. Res. Square (2020), 10.21203/rs.3.rs-48932/v1.
O. Yañez et al., Potential for virus transfer between the honey bees Apis mellifera and A. cerana. J. Apic. Res. 54, 179–191 (2015).
I. Grindrod, J. L. Kevill, E. M. Villalobos, D. C. Schroeder, S. J. Martin, Ten years of deformed wing virus (DWV) in Hawaiian honey bees (Apis mellifera), the dominant DWV-A variant is potentially being replaced by variants with a DWV-B coding sequence. Viruses 13, 969 (2021).
M. Pérez-Losada, M. Arenas, J. C. Galán, F. Palero, F. González-Candelas, Recombination in viruses: Mechanisms, methods of study, and evolutionary consequences. Infect. Genet. Evol. 30, 296–307 (2015).
J. M. K. Roberts, D. L. Anderson, P. A. Durr, Metagenomic analysis of Varroa-free Australian honey bees (Apis mellifera) shows a diverse Picornavirales virome. J. Gen. Virol. 99, 818–826 (2018).
S. J. Martin et al., Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304–1306 (2012).
V. Kowallik, A. S. Mikheyev, Honey bee larval and adult microbiome life stages are effectively decoupled with vertical transmission overcoming early life perturbations. MBio 12, e0296621 (2021).
J. R. Ongus et al., Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J. Gen. Virol. 85, 3747–3755 (2004).
L. E. Brettell, D. C. Schroeder, S. J. Martin, RNAseq of deformed wing virus and other honey bee-associated viruses in eight insect taxa with or without Varroa infestation. Viruses 12, 1229 (2020).
R. Manley et al., Knock-on community impacts of a novel vector: Spillover of emerging DWV-B from Varroa-infested honeybees to wild bumblebees. Ecol. Lett. 22, 1306–1315 (2019).
J. L. Kevill, K. C. Stainton, D. C. Schroeder, S. J. Martin, Deformed wing virus variant shift from 2010 to 2016 in managed and feral UK honey bee colonies. Arch. Virol. 166, 2693–2702 (2021).
N. De Maio, C.-H. Wu, K. M. O’Reilly, D. Wilson, New routes to phylogeography: A bayesian structured coalescent approximation. PLoS Genet. 11, e1005421 (2015).
N. Hasegawa, et al., Evolutionarily diverse origins of honey bee deformed wing viruses, National Library of Medicine Bioproject PRJDB14940, https://www.ncbi.nlm.nih.gov/bioproject/923870. Accessed 31 May 2023.
