A virocentric perspective on the evolution of life

Highlights

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  We present an overview of the evolution of the virus world and its multifaceted, complex interaction with cellular life forms.

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  Several viral hallmark genes that encode essential proteins are shared by extremely diverse groups of viruses.

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  The existence of hallmark genes implies that viruses and related selfish elements evolved from the primordial gene pool.

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  The emergence of selfish elements is theoretically inevitable in any ensemble of evolving replicators.

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  Virus–host arms races and cooperation were among the decisive factors in the evolution of all life forms.

Abstract

Viruses and/or virus-like selfish elements are associated with all cellular life forms and are the most abundant biological entities on Earth, with the number of virus particles in many environments exceeding the number of cells by one to two orders of magnitude. The genetic diversity of viruses is commensurately enormous and might substantially exceed the diversity of cellular organisms. Unlike cellular organisms with their uniform replication-expression scheme, viruses possess either RNA or DNA genomes and exploit all conceivable replication-expression strategies. Although viruses extensively exchange genes with their hosts, there exists a set of viral hallmark genes that are shared by extremely diverse groups of viruses to the exclusion of cellular life forms. Coevolution of viruses and host defense systems is a key aspect in the evolution of both viruses and cells, and viral genes are often recruited for cellular functions. Together with the fundamental inevitability of the emergence of genomic parasites in any evolving replicator system, these multiple lines of evidence reveal the central role of viruses in the entire evolution of life.