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Dynamic evolution in the key honey bee pathogen Deformed wing virus

By Eugene V Ryabov, Anna K. Childers, Dawn Lopez, Kyle Grubbs, Francisco Posada-Florez, Daniel Weaver, William Girten, Dennis vanEngelsdorp, Yanping Chen, Jay D Evans

Posted 05 Jun 2019
bioRxiv DOI: 10.1101/653543 (published DOI: 10.1371/journal.pbio.3000502)

The impacts of invertebrate RNA virus population dynamics on virulence and infection outcomes are poorly understood. Deformed wing virus (DWV), the main viral pathogen of honey bees, negatively impacts bee health which can lead to colony death. Despite previous reports on the reduction of DWV diversity following the arrival of the parasitic mite Varroa destructor, the key DWV vector, we found high genetic diversity of DWV in infested United States (US) honey bee colonies. Phylogenetic analysis showed that the divergent US DWV genotypes are of monophyletic origin, which were likely generated as a result of diversification after a genetic bottleneck. To investigate the population dynamics of this divergent DWV, we designed a series of novel infectious cDNA clones corresponding to co-existing DWV genotypes, thereby devising a reverse genetic system for an invertebrate RNA virus quasispecies. Equal replication rates were observed for all clone-derived DWV variants in single infections. Surprisingly, individual clones replicated to the same high levels as their mixtures and even the parental highly diverse natural DWV population, suggesting that complementation between genotypes was not required to replicate to high levels. Mixed clone-derived infections showed a lack of strong competitive exclusion, suggesting that the DWV genotypes were adapted to co-exist. Mutational and recombination events were observed across clone progeny providing new insights into the forces that drive and constrain virus diversification. Accordingly, herein we propose a new model of Varroa-induced DWV dynamics whereby an initial selective sweep is followed by virus diversification fueled by negative frequency-dependent selection for new genotypes. This selection likely reflects the ability of rare lineages to evade host defenses, specifically antiviral RNA interference (RNAi). In support of this, we show that RNAi induced against one DWV strain is less effective against an alternate strain from the same population.

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