The origins and evolution of viruses.

Early in the 20th century, three hypotheses were advanced for the origin of viruses: (1) viruses are degenerate intracellular parasites; (2) viruses are relics of precellular life; and (3) viruses are cellular genes that escaped. Research in the latter half of the 20th century revolutionized our knowledge of the physical nature of viruses, but comparable progress in understanding viral origins is conspicuously lacking. It has long been appreciated that viruses need not be a monophyletic group. Beyond that, the three classical hypotheses can be restated today, with only minor refinements.1.The degenerate parasite hypothesis currently has few supporters, ostensibly because the absence of intermediate forms and the extent of the implied degeneration render such speculation non-productive; ironically, the decline in favor of this hypothesis coincided with general acceptance of an endosymbiont origin for organelles, which presents some of the same problems.2.From the outset, the precellular life hypothesis faced the dilemma that viruses require cellular hosts and therefore could not have preceded them; a currently viable, related hypothesis is that some RNA viruses originated in the RNA world.3.Most virologists today probably view at least the larger DNA viruses as escaped cellular genes. Molecular genetics has gradually replaced the primitive concept of individual genes going out on their own with scenarios where blocks of genes (possibly from diverse cellular sources) comprise functional modules that merged with one another, giving the typical virus a chimeric ancestry 1.xSee all References, 2.xEvolution of the lambdoid phages. Campbell, A and Botstein, D. : 365–380See all References. Simplistic searches for primordial cellular modules have generally been confounded by the presence of degraded relics of viral DNA (defective proviruses) in most chromosomes 3xDefective bacteriophages and incomplete prophages. Campbell, A. : 259–328See all References3.At the dawn of the 21st century, it is gratifying that this subject is receiving renewed attention 4.xThe origins and ongoing evolution of viruses. Hendrix, R.W et al. Trends Microbiol. 2000; 8: 504–508Abstract | Full Text | Full Text PDF | PubMed | Scopus (229)See all References, 5.xEvolution on life's fringes. Balter, M. Science. 2000; 289: 1866–1867Crossref | PubMed | Scopus (27)See all References. Hendrix et al.4xThe origins and ongoing evolution of viruses. Hendrix, R.W et al. Trends Microbiol. 2000; 8: 504–508Abstract | Full Text | Full Text PDF | PubMed | Scopus (229)See all References4 postulate that the initiating event was the occurrence of the icosahedral capsid, and cite examples of cellular proteins assembling into icosahedra. There is much to recommend this idea: capsids (icosahedral or helical) are the most characteristically viral structures known and are essential for the viral lifestyle. Hendrix et al. focus on tailed double-stranded (ds) DNA bacteriophages, in which icosahedral capsids are the rule. In making capsid formation the primary event, they imply a separate origin for helical viruses.Most viral capsids are not complete delivery systems, but for some simpler viruses, such as picornaviruses, they are. Hendrix et al.4xThe origins and ongoing evolution of viruses. Hendrix, R.W et al. Trends Microbiol. 2000; 8: 504–508Abstract | Full Text | Full Text PDF | PubMed | Scopus (229)See all References4 discuss a possible role for primitive viral capsids as vehicles for the lateral transfer of host genes. The importance of this is debatable. Pre-cells might have transferred DNA rather easily, through cell fusion or transformation, with subsequent selection acting more to create barriers than to circumvent them 6xLateral gene transfer in prokaryotes. Campbell, A.M. Theoret. Pop. Biol. 2000; 57: 71–77Crossref | PubMed | Scopus (39)See all References6. At any rate, such a role is not a cornerstone of their hypothesis. They correctly state that encapsidation of DNA provides a selfish advantage to the encapsidation genes, which would at least sometimes be transferred.Another major feature of their scheme is the ongoing acquisition of small DNA segments (‘morons’) that can add to viral genomes, as extensively documented in their previous work. Extrapolating this process into the past, viral evolution probably included many such additions, as well as fusions of larger modules. Such serial acquisitions could well also be crucial to cellular evolution 7xGene transfer, speciation and the evolution of bacterial genomes. Lawrence, J.G. Curr. Opin. Microbiol. 1999; 2: 519–523Crossref | PubMed | Scopus (161)See all References7. The databases for the extent of gene transfer into viral and host genomes are not totally independent: more than one-third of the genes in Escherichia coli that were classified as alien by codon usage patterns 8xCodon usages in different gene classes of the Escherichia coli genome. Karlin, S et al. Mol. Microbiol. 1998; 29: 1341–1355Crossref | PubMed | Scopus (155)See all References8 lie within defective prophages 9xSee all References9.We can hope for a lively round of discussion by students of a wider range of viruses, some of which has already commenced 5xEvolution on life's fringes. Balter, M. Science. 2000; 289: 1866–1867Crossref | PubMed | Scopus (27)See all References5.