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      Prokaryotic evolution and the tree of life are two different things

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          Abstract

          Background

          The concept of a tree of life is prevalent in the evolutionary literature. It stems from attempting to obtain a grand unified natural system that reflects a recurrent process of species and lineage splittings for all forms of life. Traditionally, the discipline of systematics operates in a similar hierarchy of bifurcating (sometimes multifurcating) categories. The assumption of a universal tree of life hinges upon the process of evolution being tree-like throughout all forms of life and all of biological time. In multicellular eukaryotes, the molecular mechanisms and species-level population genetics of variation do indeed mainly cause a tree-like structure over time. In prokaryotes, they do not. Prokaryotic evolution and the tree of life are two different things, and we need to treat them as such, rather than extrapolating from macroscopic life to prokaryotes. In the following we will consider this circumstance from philosophical, scientific, and epistemological perspectives, surmising that phylogeny opted for a single model as a holdover from the Modern Synthesis of evolution.

          Results

          It was far easier to envision and defend the concept of a universal tree of life before we had data from genomes. But the belief that prokaryotes are related by such a tree has now become stronger than the data to support it. The monistic concept of a single universal tree of life appears, in the face of genome data, increasingly obsolete. This traditional model to describe evolution is no longer the most scientifically productive position to hold, because of the plurality of evolutionary patterns and mechanisms involved. Forcing a single bifurcating scheme onto prokaryotic evolution disregards the non-tree-like nature of natural variation among prokaryotes and accounts for only a minority of observations from genomes.

          Conclusion

          Prokaryotic evolution and the tree of life are two different things. Hence we will briefly set out alternative models to the tree of life to study their evolution. Ultimately, the plurality of evolutionary patterns and mechanisms involved, such as the discontinuity of the process of evolution across the prokaryote-eukaryote divide, summons forth a pluralistic approach to studying evolution.

          Reviewers

          This article was reviewed by Ford Doolittle, John Logsdon and Nicolas Galtier.

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          Most cited references127

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          TESTING SIGNIFICANCE OF INCONGRUENCE

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            Neighbor-net: an agglomerative method for the construction of phylogenetic networks.

            We present Neighbor-Net, a distance based method for constructing phylogenetic networks that is based on the Neighbor-Joining (NJ) algorithm of Saitou and Nei. Neighbor-Net provides a snapshot of the data that can guide more detailed analysis. Unlike split decomposition, Neighbor-Net scales well and can quickly produce detailed and informative networks for several hundred taxa. We illustrate the method by reanalyzing three published data sets: a collection of 110 highly recombinant Salmonella multi-locus sequence typing sequences, the 135 "African Eve" human mitochondrial sequences published by Vigilant et al., and a collection of 12 Archeal chaperonin sequences demonstrating strong evidence for gene conversion. Neighbor-Net is available as part of the SplitsTree4 software package.
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              A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation.

              We previously developed a cladistic approach to identify subsets of haplotypes defined by restriction endonuclease mapping or DNA sequencing that are associated with significant phenotypic deviations. Our approach was limited to segments of DNA in which little recombination occurs. In such cases, a cladogram can be constructed from the restriction site or sequence data that represents the evolutionary steps that interrelate the observed haplotypes. The cladogram is used to define a nested statistical design to identify mutational steps associated with significant phenotypic deviations. The central assumption behind this strategy is that any undetected mutation causing a phenotypic effect is embedded within the same evolutionary history that is represented by the cladogram. The power of this approach depends upon the confidence one has in the particular cladogram used to draw inferences. In this paper, we present a strategy for estimating the set of cladograms that are consistent with a particular sample of either restriction site or nucleotide sequence data and that includes the possibility of recombination. We first evaluate the limits of parsimony in constructing cladograms. Once these limits have been determined, we construct the set of parsimonious and nonparsimonious cladograms that is consistent with these limits. Our estimation procedure also identifies haplotypes that are candidates for being products of recombination. If recombination is extensive, our algorithm subdivides the DNA region into two or more subsections, each having little or no internal recombination. We apply this estimation procedure to three data sets to illustrate varying degrees of cladogram ambiguity and recombination.
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                Author and article information

                Journal
                Biol Direct
                Biology Direct
                BioMed Central
                1745-6150
                2009
                29 September 2009
                : 4
                : 34
                Affiliations
                [1 ]UPMC, UMR CNRS 7138, 75005 Paris, France
                [2 ]ESRC Centre for Genomics in Society (Egenis), University of Exeter, Exeter, UK
                [3 ]Faculty of Computer Science, Dalhousie University, Halifax, Nova Scotia, Canada
                [4 ]Department of Philosophy, University of Calgary, Calgary, Alberta, Canada
                [5 ]Department of Molecular and Cell Biology, University of Connecticut, USA
                [6 ]Department of Philosophy, NYU, USA
                [7 ]Département de sciences biologiques, Université de Montréal, Montréal (Québec), Canada
                [8 ]Institute of Botany, University of Düsseldorf, Düsseldorf, Germany
                [9 ]Department of Civil and Environmental Engineering, MIT, Cambridge, MA, USA
                Article
                1745-6150-4-34
                10.1186/1745-6150-4-34
                2761302
                19788731
                2a23c735-ccba-463a-a788-d636d48ade72
                Copyright © 2009 Bapteste et al; 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.

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                Review

                Life sciences
                Life sciences

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