Philosophy and evolution: minding the gap between evolutionary patterns and tree-like patterns.

Ever since Darwin, the familiar genealogical pattern known as the Tree of Life (TOL) has been prominent in evolutionary thinking and has dominated not only systematics, but also the analysis of the units of evolution. However, recent findings indicate that the evolution of DNA, especially in prokaryotes and such DNA vehicles as viruses and plasmids, does not follow a unique tree-like pattern. Because evolutionary patterns track a greater range of processes than those captured in genealogies, genealogical patterns are in fact only a subset of a broader set of evolutionary patterns. This fact suggests that evolutionists who focus exclusively on genealogical patterns are blocked from providing a significant range of genuine evolutionary explanations. Consequently, we highlight challenges to tree-based approaches, and point the way toward more appropriate methods to study evolution (although we do not present them in technical detail). We argue that there is significant benefit in adopting wider range of models, evolutionary representations, and evolutionary explanations, based on an analysis of the full range of evolutionary processes. We introduce an ecosystem orientation into evolutionary thinking that highlights the importance of "type 1 coalitions" (functionally related units with genetic exchanges, aka "friends with genetic benefits"), "type 2 coalitions" (functionally related units without genetic exchanges), "communal interactions," and "emergent evolutionary properties." On this basis, we seek to promote the study of (especially prokaryotic) evolution with dynamic evolutionary networks, which are less constrained than the TOL, and to provide new ways to analyze an expanded range of evolutionary units (genetic modules, recombined genes, plasmids, phages and prokaryotic genomes, pangenomes, microbial communities) and evolutionary processes. Finally, we discuss some of the conceptual and practical questions raised by such network-based representation.

[1]  Paul Wilmes,et al.  The dynamic genetic repertoire of microbial communities , 2009, FEMS microbiology reviews.

[2]  I. Sanders,et al.  Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi , 2001, Nature.

[3]  I. Sanders,et al.  Changes in arbuscular mycorrhizal fungal phenotypes and genotypes in response to plant species identity and phosphorus concentration. , 2009, The New phytologist.

[4]  E. Delong,et al.  The Microbial Engines That Drive Earth's Biogeochemical Cycles , 2008, Science.

[5]  Richard M Burian,et al.  On microRNA and the need for exploratory experimentation in post-genomic molecular biology. , 2007, History and philosophy of the life sciences.

[6]  J. Lawrence,et al.  Selfish operons: the evolutionary impact of gene clustering in prokaryotes and eukaryotes. , 1999, Current opinion in genetics & development.

[7]  W. Martin,et al.  Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes. , 2011, Genome research.

[8]  Marc Ereshefsky Mystery of mysteries: Darwin and the species problem , 2011, Cladistics : the international journal of the Willi Hennig Society.

[9]  T. Lambert,et al.  Analysis of the Mobilization Functions of the Vancomycin Resistance Transposon Tn1549, a Member of a New Family of Conjugative Elements , 2009, Journal of bacteriology.

[10]  Symbiosis, lateral function transfer and the (many) saplings of life , 2010 .

[11]  Florent E. Angly,et al.  Comparative Metagenomics Reveals Host Specific Metavirulomes and Horizontal Gene Transfer Elements in the Chicken Cecum Microbiome , 2008, PloS one.

[12]  Tal Dagan,et al.  Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution , 2008, Proceedings of the National Academy of Sciences.

[13]  Debashish Bhattacharya,et al.  Genomic Footprints of a Cryptic Plastid Endosymbiosis in Diatoms , 2009, Science.

[14]  H. Brüssow The not so universal tree of life or the place of viruses in the living world , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[15]  C. Kurland,et al.  Horizontal gene transfer: A critical view , 2003 .

[16]  L. Hancock,et al.  Mechanism of chromosomal transfer of Enterococcus faecalis pathogenicity island, capsule, antimicrobial resistance, and other traits , 2010, Proceedings of the National Academy of Sciences.

[17]  Itai Sharon,et al.  Reconstructing a puzzle: existence of cyanophages containing both photosystem-I and photosystem-II gene suites inferred from oceanic metagenomic datasets. , 2011, Environmental microbiology.

[18]  Maureen A. O’Malley,et al.  Metagenomics and biological ontology. , 2007, Studies in history and philosophy of biological and biomedical sciences.

[19]  E. Koonin,et al.  Is evolution Darwinian or/and Lamarckian? , 2009, Biology Direct.

[20]  Eric Bapteste,et al.  On the need for integrative phylogenomics, and some steps toward its creation , 2010 .

[21]  Eric Bapteste,et al.  Network analyses structure genetic diversity in independent genetic worlds , 2009, Proceedings of the National Academy of Sciences.

[22]  Miriam Barlow,et al.  What antimicrobial resistance has taught us about horizontal gene transfer. , 2009, Methods in molecular biology.

[23]  Pietro Liò,et al.  Analysis of plasmid genes by phylogenetic profiling and visualization of homology relationships using Blast2Network , 2008, BMC Bioinformatics.

[24]  Bruno J. Strasser,et al.  GenBank--Natural History in the 21st Century? , 2008, Science.

[25]  J. Davies,et al.  Origins and Evolution of Antibiotic Resistance , 1996, Microbiology and Molecular Biology Reviews.

[26]  A. Tansley The Use and Abuse of Vegetational Concepts and Terms , 1935 .

[27]  Andrew C. Tolonen,et al.  Transfer of photosynthesis genes to and from Prochlorococcus viruses. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Jay Odenbaugh Seeing the Forest and the Trees: Realism about Communities and Ecosystems , 2007, Philosophy of Science.

[29]  James O. McInerney,et al.  The network of life: genome beginnings and evolution , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[30]  L. Melderen,et al.  Bacterial toxin-antitoxin systems: more than selfish entities? , 2009 .

[31]  Kevin C Elliott Varieties of exploratory experimentation in nanotoxicology. , 2007, History and philosophy of the life sciences.

[32]  Ruben E. Valas,et al.  Save the tree of life or get lost in the woods , 2010, Biology Direct.

[33]  C. Keel,et al.  Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi , 2010, The ISME Journal.

[34]  P. Lopez,et al.  Molecular phylogeny: reconstructing the forest. , 2009, Comptes rendus biologies.

[35]  Otto X. Cordero,et al.  Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global Vibrio cholerae Populations , 2011, mBio.

[36]  J. Overmann,et al.  Ultrastructural Characterization of the Prokaryotic Symbiosis in “Chlorochromatium aggregatum” , 2008, Journal of bacteriology.

[37]  Daniel Janies,et al.  Tracking the geographical spread of avian influenza (H5N1) with multiple phylogenetic trees , 2010, Cladistics : the international journal of the Willi Hennig Society.

[38]  Maureen A. O’Malley,et al.  Prokaryotic evolution and the tree of life are two different things , 2009, Biology Direct.

[39]  M. Kuntner,et al.  Are the linnean and phylogenetic nomenclatural systems combinable? Recommendations for biological nomenclature. , 2006, Systematic biology.

[40]  David Bryant,et al.  Genome Networks Root the Tree of Life between Prokaryotic Domains , 2010, Genome biology and evolution.

[41]  Edward F. DeLong,et al.  Life on the Thermodynamic Edge , 2007, Science.

[42]  R. O'HARA,et al.  Population thinking and tree thinking in systematics , 1997 .

[43]  N. Galtier,et al.  Dealing with incongruence in phylogenomic analyses , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  Andrés Moya,et al.  Legionella pneumophila pangenome reveals strain-specific virulence factors , 2010, BMC Genomics.

[45]  S. Ferriera,et al.  Supporting Online Material Materials and Methods Figs. S1 and S2 Tables S1 and S2 References Temporal Fragmentation of Speciation in Bacteria , 2022 .

[46]  J. Lawrence,et al.  Phylogenetic incongruence arising from fragmented speciation in enteric bacteria , 2010, Proceedings of the National Academy of Sciences.

[47]  D. Krakauer,et al.  Levels of selection in positive‐strand virus dynamics , 2003, Journal of evolutionary biology.

[48]  Olga Zhaxybayeva,et al.  On the chimeric nature, thermophilic origin, and phylogenetic placement of the Thermotogales , 2009, Proceedings of the National Academy of Sciences.

[49]  F. Bouchard Causal Processes, Fitness, and the Differential Persistence of Lineages , 2008, Philosophy of Science.

[50]  François-Joseph Lapointe,et al.  Harvesting evolutionary signals in a forest of prokaryotic gene trees. , 2011, Molecular biology and evolution.

[51]  M. Ghiselin,et al.  Species concepts, individuality, and objectivity , 1987 .

[52]  D. Lipman,et al.  A genomic perspective on protein families. , 1997, Science.

[53]  Shiraz A. Shah,et al.  CRISPR/Cas and Cmr modules, mobility and evolution of adaptive immune systems. , 2011, Research in microbiology.

[54]  J. Overmann The phototrophic consortium "Chlorochromatium aggregatum" - a model for bacterial heterologous multicellularity. , 2010, Advances in experimental medicine and biology.

[55]  François-Joseph Lapointe,et al.  Clanistics: a multi-level perspective for harvesting unrooted gene trees. , 2010, Trends in microbiology.

[56]  Tao Li,et al.  Expression-based identification of genetic determinants of the bacterial symbiosis 'Chlorochromatium aggregatum'. , 2010, Environmental microbiology.

[57]  A. Danchin,et al.  Organised Genome Dynamics in the Escherichia coli Species Results in Highly Diverse Adaptive Paths , 2009, PLoS genetics.

[58]  Victoria J. Orphan,et al.  Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics , 2008, Proceedings of the National Academy of Sciences.

[59]  W. Doolittle,et al.  Eradicating typological thinking in prokaryotic systematics and evolution. , 2009, Cold Spring Harbor symposia on quantitative biology.

[60]  George Gaylord Simpson,et al.  Principles of Animal Taxonomy , 1961 .

[61]  Matthias E. Futschik,et al.  Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution , 2007, Nature.

[62]  W. Martin,et al.  The tree of one percent , 2006, Genome Biology.

[63]  J. Overmann,et al.  Identification and analysis of four candidate symbiosis genes from 'Chlorochromatium aggregatum', a highly developed bacterial symbiosis. , 2008, Environmental microbiology.

[64]  Weizhong Li,et al.  Analysis and comparison of very large metagenomes with fast clustering and functional annotation , 2009, BMC Bioinformatics.

[65]  J. Lawrence,et al.  The interplay of homologous recombination and horizontal gene transfer in bacterial speciation. , 2009, Methods in molecular biology.

[66]  R. Knight,et al.  The convergence of carbohydrate active gene repertoires in human gut microbes , 2008, Proceedings of the National Academy of Sciences.

[67]  Gábor Csárdi,et al.  The igraph software package for complex network research , 2006 .

[68]  Pamela Lyon,et al.  From quorum to cooperation: lessons from bacterial sociality for evolutionary theory. , 2007, Studies in history and philosophy of biological and biomedical sciences.

[69]  N. Moran,et al.  Phylogenetics and the Cohesion of Bacterial Genomes , 2003, Science.

[70]  D. Janzen WHEN IS IT COEVOLUTION? , 1980, Evolution; international journal of organic evolution.

[71]  B. Brogaard,et al.  Species as individuals , 2004 .

[72]  M. Newman,et al.  Finding community structure in networks using the eigenvectors of matrices. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[73]  E. Mayr Answers to these comments , 1987 .

[74]  Rick L. Stevens,et al.  Functional metagenomic profiling of nine biomes , 2008, Nature.

[75]  B. Snel,et al.  Toward Automatic Reconstruction of a Highly Resolved Tree of Life , 2006, Science.

[76]  G. E. Hutchinson,et al.  CIRCULAR CAUSAL SYSTEMS IN ECOLOGY , 1948, Annals of the New York Academy of Sciences.

[77]  John Boyle,et al.  Cytoscape: a community-based framework for network modeling. , 2009, Methods in molecular biology.

[78]  Maureen A. O’Malley,et al.  Exploratory experimentation and scientific practice: metagenomics and the proteorhodopsin case. , 2007, History and philosophy of the life sciences.

[79]  Eric Bapteste,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:Pattern pluralism and the Tree of Life hypothesis , 2007 .

[80]  J. Archibald,et al.  The eukaryotic tree of life: endosymbiosis takes its TOL. , 2008, Trends in ecology & evolution.

[81]  F. Oehl,et al.  Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity , 2006, Molecular ecology.

[82]  Gipsi Lima-Mendez,et al.  Reticulate representation of evolutionary and functional relationships between phage genomes. , 2008, Molecular biology and evolution.

[83]  J. McInerney,et al.  Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function , 2010, Proceedings of the National Academy of Sciences.

[84]  Yan Boucher,et al.  Lateral gene transfer challenges principles of microbial systematics. , 2008, Trends in microbiology.

[85]  Vincent J. Denef,et al.  Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria , 2007, Nature.

[86]  W. Doolittle,et al.  Metagenomics and the Units of Biological Organization , 2010 .

[87]  W. Doolittle,et al.  Lateral gene transfer and the origins of prokaryotic groups. , 2003, Annual review of genetics.

[88]  K. Konstantinidis,et al.  Genomic insights that advance the species definition for prokaryotes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[89]  B. Strasser Laboratories, museums, and the comparative perspective: Alan A. Boyden's quest for objectivity in serological taxonomy, 1924-1962. , 2010, Historical studies in the natural sciences.

[90]  W. Doolittle,et al.  The Genome of Thermosipho africanus TCF52B: Lateral Genetic Connections to the Firmicutes and Archaea , 2009, Journal of bacteriology.

[91]  Michael Shmoish,et al.  Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. , 2005, Environmental microbiology.

[92]  I. Paulsen,et al.  Coastal Synechococcus metagenome reveals major roles for horizontal gene transfer and plasmids in population diversity. , 2009, Environmental microbiology.

[93]  W. Doolittle,et al.  On the origin of prokaryotic species. , 2009, Genome research.

[94]  W. Martin,et al.  Getting a better picture of microbial evolution en route to a network of genomes , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[95]  W. Martin,et al.  Seeing Green and Red in Diatom Genomes , 2009, Science.

[96]  M. Pop,et al.  Metagenomic Analysis of the Human Distal Gut Microbiome , 2006, Science.

[97]  N. Moran,et al.  From Gene Trees to Organismal Phylogeny in Prokaryotes:The Case of the γ-Proteobacteria , 2003, PLoS biology.

[98]  J. Collins,et al.  Bacterial charity work leads to population-wide resistance , 2010, Nature.

[99]  D. Wilson,et al.  Artificial ecosystem selection. , 2000, Proceedings of the National Academy of Sciences of the United States of America.