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      Genome reduction as the dominant mode of evolution

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          Abstract

          A common belief is that evolution generally proceeds towards greater complexity at both the organismal and the genomic level, numerous examples of reductive evolution of parasites and symbionts notwithstanding. However, recent evolutionary reconstructions challenge this notion. Two notable examples are the reconstruction of the complex archaeal ancestor and the intron-rich ancestor of eukaryotes. In both cases, evolution in most of the lineages was apparently dominated by extensive loss of genes and introns, respectively. These and many other cases of reductive evolution are consistent with a general model composed of two distinct evolutionary phases: the short, explosive, innovation phase that leads to an abrupt increase in genome complexity, followed by a much longer reductive phase, which encompasses either a neutral ratchet of genetic material loss or adaptive genome streamlining. Quantitatively, the evolution of genomes appears to be dominated by reduction and simplification, punctuated by episodes of complexification.

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          Most cited references88

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          The origins of genome complexity.

          Complete genomic sequences from diverse phylogenetic lineages reveal notable increases in genome complexity from prokaryotes to multicellular eukaryotes. The changes include gradual increases in gene number, resulting from the retention of duplicate genes, and more abrupt increases in the abundance of spliceosomal introns and mobile genetic elements. We argue that many of these modifications emerged passively in response to the long-term population-size reductions that accompanied increases in organism size. According to this model, much of the restructuring of eukaryotic genomes was initiated by nonadaptive processes, and this in turn provided novel substrates for the secondary evolution of phenotypic complexity by natural selection. The enormous long-term effective population sizes of prokaryotes may impose a substantial barrier to the evolution of complex genomes and morphologies.
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            Extreme genome reduction in symbiotic bacteria.

            Since 2006, numerous cases of bacterial symbionts with extraordinarily small genomes have been reported. These organisms represent independent lineages from diverse bacterial groups. They have diminutive gene sets that rival some mitochondria and chloroplasts in terms of gene numbers and lack genes that are considered to be essential in other bacteria. These symbionts have numerous features in common, such as extraordinarily fast protein evolution and a high abundance of chaperones. Together, these features point to highly degenerate genomes that retain only the most essential functions, often including a considerable fraction of genes that serve the hosts. These discoveries have implications for the concept of minimal genomes, the origins of cellular organelles, and studies of symbiosis and host-associated microbiota.
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              The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss

              ABSTRACT Reductive genomic evolution, driven by genetic drift, is common in endosymbiotic bacteria. Genome reduction is less common in free-living organisms, but it has occurred in the numerically dominant open-ocean bacterioplankton Prochlorococcus and “Candidatus Pelagibacter,” and in these cases the reduction appears to be driven by natural selection rather than drift. Gene loss in free-living organisms may leave them dependent on cooccurring microbes for lost metabolic functions. We present the Black Queen Hypothesis (BQH), a novel theory of reductive evolution that explains how selection leads to such dependencies; its name refers to the queen of spades in the game Hearts, where the usual strategy is to avoid taking this card. Gene loss can provide a selective advantage by conserving an organism’s limiting resources, provided the gene’s function is dispensable. Many vital genetic functions are leaky, thereby unavoidably producing public goods that are available to the entire community. Such leaky functions are thus dispensable for individuals, provided they are not lost entirely from the community. The BQH predicts that the loss of a costly, leaky function is selectively favored at the individual level and will proceed until the production of public goods is just sufficient to support the equilibrium community; at that point, the benefit of any further loss would be offset by the cost. Evolution in accordance with the BQH thus generates “beneficiaries” of reduced genomic content that are dependent on leaky “helpers,” and it may explain the observed nonuniversality of prototrophy, stress resistance, and other cellular functions in the microbial world.
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                Author and article information

                Journal
                Bioessays
                Bioessays
                bies
                Bioessays
                WILEY Periodicals
                0265-9247
                1521-1878
                September 2013
                25 June 2013
                : 35
                : 9
                : 829-837
                Affiliations
                National Center for Biotechnology Information, NLM, National Institutes of Health Bethesda, MA, USA
                Author notes
                * Corresponding author:, Yuri I. Wolf, E-mail: wolf@ 123456ncbi.nlm.nih.gov
                Article
                10.1002/bies.201300037
                3840695
                23801028
                11cd39a3-2aa5-45ee-902e-0a5be355c7f6
                © 2013 WILEY Periodicals, Inc.

                Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

                History
                : 05 March 2013
                : 21 May 2013
                Categories
                Prospects & Overviews

                Cell biology
                ancestral reconstruction,archaea,genome complexification,genome reduction,horizontal gene transfer,orthologs

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