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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The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss

J Morris, Richard Lenski, Erik R. Zinser (2012)

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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Evolution and tinkering.

F Jacob (1977)

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Explaining microbial population genomics through phage predation.

Francisco Rodriguez-Valera, Ana-Belen Martin-Cuadrado, Beltran Rodriguez-Brito … (2009)

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:

ORCID: http://orcid.org/0000-0003-1966-1215

eric.bapteste@upmc.fr

Philippe Huneman: philippe.huneman@gmail.com

Journal

Journal ID (nlm-ta): BMC Biol

Journal ID (iso-abbrev): BMC Biol

Title: BMC Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1741-7007

Publication date (Electronic): 29 May 2018

Publication date PMC-release: 29 May 2018

Publication date Collection: 2018

Volume: 16

Electronic Location Identifier: 56

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

Author information

Eric Bapteste http://orcid.org/0000-0003-1966-1215

Article

Publisher ID: 531

DOI: 10.1186/s12915-018-0531-6

PMC ID: 5972403

PubMed ID: 29843714

SO-VID: 774a38a2-75d7-4682-ab6e-4dcf7ab06626

License:

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.

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Funding

Funded by: FundRef http://dx.doi.org/10.13039/100011199, FP7 Ideas: European Research Council;

Award ID: 615274

Award Recipient : Eric Bapteste

Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;

Award ID: ANR 13 BSH3 0007

Award Recipient : Philippe Huneman

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ScienceOpen disciplines: Life sciences

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

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ScienceOpen disciplines: Life sciences

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

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

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The Dynamic Brain

Most cited references 163

The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss

Evolution and tinkering.

Explaining microbial population genomics through phage predation.

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