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Table 4 Major concepts in virus evolution

From: The ancient Virus World and evolution of cells

Concept Principal message References Brief critique/comment
Cell degeneration model of virus origin Viruses, at least complex ones, evolved as a result of degeneration of cells, perhaps, through a stage of intracellular parasites [40, 43, 45, 50] This route of virus evolution appears to be inconsistent with the results of viral comparative genomic, in particular, the prominence of genes without cellular counterparts in the conserved cores of viral genomes
Escaped-genes model of virus origin Viruses evolved from within cells, through autonomization of the appropriate genes, e.g., those coding for polymerases [40, 43, 45, 55] Similarly, this model lacks support from virus genome comparison
Origin of viruses from a primordial gene pool Viruses are direct descendants of primordial genetic elements [40, 43, 87] Generally, this appears to be the most plausible path for the origin of viruses. However, non-trivial conceptual development is required, given that viruses are intracellular parasites and, technically, could not precede cells during evolution
An ancient lineage of viruses spanning the three domains of cellular life The presence of JRC in a variety of groups of DNA viruses is taken as evidence of the existence of an ancient lineage of viruses infecting all three domains of cellular life [13–15] This concept capitalizes on a truly remarkable observation of the near ubiquity of JRC in viruses. However, inferring an ancient lineage of viruses on the basis of the conservation of a single protein smacks of essentialism and does little to explain the trajectories of most other virus-specific and virus hallmark genes. Besides, this concept does not specify the cellular context in which the ancient virus lineage might have emerged
Three DNA viruses to replicate genomes of RNA cells The hypothesis postulates that at least three major lineages of RNA viruses emerged by the escaped-genes route from RNA-based progenitors of archaea, bacteria and eukaryotes. These ancient RNA viruses are thought to have given rise to three independent lineages of DNA viruses that imparted DNA replication onto their cellular hosts [49, 55] This concept is based on important general notions of the ancient origin of viruses and their major role in evolution of cells. However, the specific model of Forterre appears to be critically flawed as it stems from a model of cellular evolution that appears not to be defendable (see text)