Abstract
The history of life is punctuated by evolutionary transitions which engender emergence of new levels of biological organization that involves selection acting at increasingly complex ensembles of biological entities. Major evolutionary transitions include the origin of prokaryotic and then eukaryotic cells, multicellular organisms and eusocial animals. All or nearly all cellular life forms are hosts to diverse selfish genetic elements with various levels of autonomy including plasmids, transposons and viruses. I present evidence that, at least up to and including the origin of multicellularity, evolutionary transitions are driven by the coevolution of hosts with these genetic parasites along with sharing of ‘public goods’. Selfish elements drive evolutionary transitions at two distinct levels. First, mathematical modelling of evolutionary processes, such as evolution of primitive replicator populations or unicellular organisms, indicates that only increasing organizational complexity, e.g. emergence of multicellular aggregates, can prevent the collapse of the host–parasite system under the pressure of parasites. Second, comparative genomic analysis reveals numerous cases of recruitment of genes with essential functions in cellular life forms, including those that enable evolutionary transitions.This article is part of the themed issue ‘The major synthetic evolutionary transitions’.
Highlights
As forcefully propounded by Charles Darwin [1] and solidified in the neoDarwinian synthesis [2,3], evolution in general proceeds gradually through small heritable changes
The key aspect of anti-parasite defence evolution is quite simple: the active moieties of defence systems are weapons capable of destroying genomes. These weapons can be turned against a parasite or against its host and have the potential to evolve into selfish elements in their own right
The biosphere is literally dominated by viruses and other mobile genetic elements (MGE)
Summary
As forcefully propounded by Charles Darwin [1] and solidified in the neoDarwinian synthesis [2,3], evolution in general proceeds gradually through small heritable changes (mutations, in modern parlance). Numerous environmental studies confidently indicate that viruses are the most abundant biological entities on Earth, with the number of virus particles in environments as diverse as seawater, soil and animal guts exceeding the number of cells by one to two orders of magnitude [49,50,51,52] Given this dominance of viruses in the biosphere, the invari- 3 able association of viruses and/or other selfish elements with cellular life forms (encapsulated in the virocell concept of Forterre [53,54]) and the emergence of parasites in theoretical and experimental models of replicator systems, a major role of these elements in all stages of the evolution of life appears self-evident. During the first two, arguably the most momentous evolutionary transitions in the evolution of life, coevolution of genetic parasites with their hosts caused dramatic complexification on both sides of the host – parasite divide
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