Abstract

BackgroundThe ascovirus, DpAV4a (family Ascoviridae), is a symbiotic virus that markedly increases the fitness of its vector, the parasitic ichneumonid wasp, Diadromus puchellus, by increasing survival of wasp eggs and larvae in their lepidopteran host, Acrolepiopsis assectella. Previous phylogenetic studies have indicated that DpAV4a is related to the pathogenic ascoviruses, such as the Spodoptera frugiperda ascovirus 1a (SfAV1a) and the lepidopteran iridovirus (family Iridoviridae), Chilo iridescent virus (CIV), and is also likely related to the ancestral source of certain ichnoviruses (family Polydnaviridae).Methodology/Principal FindingsTo clarify the evolutionary relationships of these large double-stranded DNA viruses, we sequenced the genome of DpAV4a and undertook phylogenetic analyses of the above viruses and others, including iridoviruses pathogenic to vertebrates. The DpAV4a genome consisted of 119,343 bp and contained at least 119 open reading frames (ORFs), the analysis of which confirmed the relatedness of this virus to iridoviruses and other ascoviruses.ConclusionsAnalyses of core DpAV4a genes confirmed that ascoviruses and iridoviruses are evolutionary related. Nevertheless, our results suggested that the symbiotic DpAV4a had a separate origin in the iridoviruses from the pathogenic ascoviruses, and that these two types shared parallel evolutionary paths, which converged with respect to virion structure (icosahedral to bacilliform), genome configuration (linear to circular), and cytopathology (plasmalemma blebbing to virion-containing vesicles). Our analyses also revealed that DpAV4a shared more core genes with CIV than with other ascoviruses and iridoviruses, providing additional evidence that DpAV4a represents a separate lineage. Given the differences in the biology of the various iridoviruses and ascoviruses studied, these results provide an interesting model for how viruses of different families evolved from one another.

Highlights

  • Despite advances in understanding the evolutionary history of organisms made possible by molecular phylogenetics, the origins of most viruses and their radiation during evolution remain very poorly understood

  • Analyses of core Diadromus puchellus ascovirus 4a (DpAV4a) genes confirmed that ascoviruses and iridoviruses are evolutionary related

  • Our results suggested that the symbiotic DpAV4a had a separate origin in the iridoviruses from the pathogenic ascoviruses, and that these two types shared parallel evolutionary paths, which converged with respect to virion structure, genome configuration, and cytopathology

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Summary

Introduction

Despite advances in understanding the evolutionary history of organisms made possible by molecular phylogenetics, the origins of most viruses and their radiation during evolution remain very poorly understood. This is due to the enormous diversity of virus types, ranging from those that produce very small virions, less than 20 nm in diameter consisting of a single-stranded genome of 2 kbp and protein coat, to those with large and complex enveloped virions, 300 to greater than 1,000 nm in diameter, containing fifty or more proteins with double-stranded DNA genomes ranging from 200 to greater than 1,000 kbp [1]. Previous phylogenetic studies have indicated that DpAV4a is related to the pathogenic ascoviruses, such as the Spodoptera frugiperda ascovirus 1a (SfAV1a) and the lepidopteran iridovirus (family Iridoviridae), Chilo iridescent virus (CIV), and is likely related to the ancestral source of certain ichnoviruses (family Polydnaviridae)

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