Apis mellifera filamentous virus (AmFV) is a large double-stranded DNA virus of uncertain phylogenetic position that commonly infects honey bees. Little is known about AmFV evolution or molecular aspects of infection. This study scanned public data sets of the National Center for Biotechnology Information (NCBI) to identify AmFV in RNA and DNA accessions of Apis mellifera. At least three distinct evolutionary lineages of AmFV were identified. Clade 1 predominates in Europe but in the Americas and Africa it is replaced by the other two clades as infection level increases in hosts. Only clade 3 occurred at high relative abundance in hosts with African ancestry, whereas all clades achieved high relative abundance in bees of non-African ancestry. Clade 2 was generally detected only in low-level infections in Europe but was dominant in some North American samples. The geographic distribution of clade 3 was consistent with an introduction to the Americas with ‘Africanized’ honey bees in the 1950s. Localized genomic regions of very high nucleotide divergence in individual isolates suggest recombination with additional, unknown AmFV lineages. A set of 155 ORFs was annotated based on evolutionary conservation in six AmFV genome sequences representative of the three clades. Several genes were identified as candidates for diversifying selection. Transcriptome assembly often yielded contigs exceeding 50 kb containing ORFs in both orientations, with termini associated with tandem repeats. A distinct set of ORFs had minimal to no detectable expression in brain tissue. These results expand our understanding of an enigmatic pathogen.
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