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      The role of duplications in the evolution of genomes highlights the need for evolutionary-based approaches in comparative genomics

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      1 , 2 , , 3 ,
      Biology Direct
      BioMed Central

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          Abstract

          Understanding the evolutionary plasticity of the genome requires a global, comparative approach in which genetic events are considered both in a phylogenetic framework and with regard to population genetics and environmental variables. In the mechanisms that generate adaptive and non-adaptive changes in genomes, segmental duplications (duplication of individual genes or genomic regions) and polyploidization (whole genome duplications) are well-known driving forces. The probability of fixation and maintenance of duplicates depends on many variables, including population sizes and selection regimes experienced by the corresponding genes: a combination of stochastic and adaptive mechanisms has shaped all genomes. A survey of experimental work shows that the distinction made between fixation and maintenance of duplicates still needs to be conceptualized and mathematically modeled. Here we review the mechanisms that increase or decrease the probability of fixation or maintenance of duplicated genes, and examine the outcome of these events on the adaptation of the organisms.

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          This article was reviewed by Dr. Etienne Joly, Dr. Lutz Walter and Dr. W. Ford Doolittle.

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          Most cited references51

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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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            Concerted and birth-and-death evolution of multigene families.

            Until around 1990, most multigene families were thought to be subject to concerted evolution, in which all member genes of a family evolve as a unit in concert. However, phylogenetic analysis of MHC and other immune system genes showed a quite different evolutionary pattern, and a new model called birth-and-death evolution was proposed. In this model, new genes are created by gene duplication and some duplicate genes stay in the genome for a long time, whereas others are inactivated or deleted from the genome. Later investigations have shown that most non-rRNA genes including highly conserved histone or ubiquitin genes are subject to this type of evolution. However, the controversy over the two models is still continuing because the distinction between the two models becomes difficult when sequence differences are small. Unlike concerted evolution, the model of birth-and-death evolution can give some insights into the origins of new genetic systems or new phenotypic characters.
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              Recent segmental duplications in the human genome.

              Primate-specific segmental duplications are considered important in human disease and evolution. The inability to distinguish between allelic and duplication sequence overlap has hampered their characterization as well as assembly and annotation of our genome. We developed a method whereby each public sequence is analyzed at the clone level for overrepresentation within a whole-genome shotgun sequence. This test has the ability to detect duplications larger than 15 kilobases irrespective of copy number, location, or high sequence similarity. We mapped 169 large regions flanked by highly similar duplications. Twenty-four of these hot spots of genomic instability have been associated with genetic disease. Our analysis indicates a highly nonrandom chromosomal and genic distribution of recent segmental duplications, with a likely role in expanding protein diversity.
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                Author and article information

                Journal
                Biol Direct
                Biology Direct
                BioMed Central
                1745-6150
                2011
                18 February 2011
                : 6
                : 11
                Affiliations
                [1 ]INRA, UMR1163 de Biotechnologie des Champignons Filamenteux, IFR86-BAIM. Universités de Provence et de la Méditerranée, ESIL, 163 avenue de Luminy, CP 925, 13288 Marseille Cedex 09, France
                [2 ]Universités Aix-Marseille 1 et 2, UMR1163, 163 avenue de Luminy, CP925, 13288 Marseille Cedex 09, France
                [3 ]Evolution Biologique et Modélisation.: UMR6632 CNRS, Université Aix-Marseille 1, 3 place V. Hugo, 13331 Marseille, France
                Article
                1745-6150-6-11
                10.1186/1745-6150-6-11
                3052240
                21333002
                53f69798-c507-439d-862e-b0387bdd7b52
                Copyright ©2011 Levasseur and Pontarotti; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 28 September 2010
                : 18 February 2011
                Categories
                Review

                Life sciences
                Life sciences

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