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      Towards a Dynamic Interaction Network of Life to unify and expand the evolutionary theory

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          Abstract

          The classic Darwinian theory and the Synthetic evolutionary theory and their linear models, while invaluable to study the origins and evolution of species, are not primarily designed to model the evolution of organisations, typically that of ecosystems, nor that of processes. How could evolutionary theory better explain the evolution of biological complexity and diversity? Inclusive network-based analyses of dynamic systems could retrace interactions between (related or unrelated) components. This theoretical shift from a Tree of Life to a Dynamic Interaction Network of Life, which is supported by diverse molecular, cellular, microbiological, organismal, ecological and evolutionary studies, would further unify evolutionary biology.

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          Most cited references 163

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          Evolution and tinkering.

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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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              Explaining microbial population genomics through phage predation.

              The remarkable differences that have been detected by metagenomics in the genomes of strains of the same bacterial species are difficult to reconcile with the widely accepted paradigm that periodic selection within bacterial populations will regularly purge genomic diversity by clonal replacement. We have found that many of the genes that differ between strains affect regions that are potential phage recognition targets. We therefore propose the constant-diversity dynamics model, in which the diversity of prokaryotic populations is preserved by phage predation. We provide supporting evidence for this model from metagenomics, mathematical analysis and computer simulations. Periodic selection and phage predation dynamics are not mutually exclusive; we compare their predictions to shed light on the ecological circumstances under which each type of dynamics could predominate.
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                Author and article information

                Contributors
                eric.bapteste@upmc.fr
                philippe.huneman@gmail.com
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                29 May 2018
                29 May 2018
                2018
                : 16
                Affiliations
                [1 ]ISNI 0000 0001 1955 3500, GRID grid.5805.8, Sorbonne Universités, UPMC Université Paris 06, Institut de Biologie Paris-Seine (IBPS), ; F-75005 Paris, France
                [2 ]ISNI 0000 0001 2112 9282, GRID grid.4444.0, CNRS, UMR7138, Institut de Biologie Paris-Seine, ; F-75005 Paris, France
                [3 ]ISNI 0000 0001 2324 4719, GRID grid.462114.4, Institut d’Histoire et de Philosophie des Sciences et des Techniques (CNRS / Paris I Sorbonne), ; F-75006 Paris, France
                Article
                531
                10.1186/s12915-018-0531-6
                5972403
                29843714
                © Bapteste et al. 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100011199, FP7 Ideas: European Research Council;
                Award ID: 615274
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR 13 BSH3 0007
                Award Recipient :
                Categories
                Opinion
                Custom metadata
                © The Author(s) 2018

                Life sciences

                evolutionary biology, web of life, tree of life, theoretical biology, interactions

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