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Biology and Philosophy

, Volume 14, Issue 3, pp 331–348 | Cite as

The Concept of Monophyly: A Speculative Essay

  • Malcolm S. Gordon
Article

Abstract

The concept of monophyly is central to much of modern biology. Despite many efforts over many years, important questions remain unanswered that relate both to the concept itself and to its various applications. This essay focuses primarily on four of these: i) Is it possible to define monophyly operationally, specifically with respect to both the structures of genomes and at the levels of the highest phylogenetic categories (kingdoms, phyla, classes)? ii) May the mosaic and chimeric structures of genomes be sufficiently important factors in phylogeny that situations exist in which the concept may not be applicable? iii) In the history of life on earth were there important groups of organisms that probably had polyphyletic, rather than monophyletic, origins? iv) Does the near universal search for monophyletic origins of clades lead, on occasion, to both undesirable narrowing of acceptable options for development of evolutionary scenarios and sometimes actual omission from consideration of less conventional types of both data and modes of thought, possibly at the expense of biological understanding? Three sections in the essay consider possible answers to these questions: i) A reassessment is made of major features of both the concept and some of its applications. Recent research results make it seem improbable that there could have been single basal forms for many of the highest categories of evolutionary differentiation (kingdoms, phyla, classes). The universal tree of life probably had many roots. Facts contributing to this perception include the phylogenetically widespread occurrences of: horizontal transfers of plasmids, viral genomes, and transposons; multiple genomic duplications; the existence and properties of large numbers of gene families and protein families; multiple symbioses; broad-scale hybridizations; and multiple homoplasys. Next, justifications are reassessed for the application of monophyletic frameworks to two major evolutionary developments usually interpreted as having been monophyletic: ii) the origins of life; and iii) the origins of the vertebrate tetrapods. For both cases polyphyletic hypotheses are suggested as more probable than monophyletic hypotheses. Major conclusions are, as answers to the four questions posed above: probably not, yes, yes, and yes.

cladistics evolutionary genomics monophyly origins of life origins of tetrapods phylogeny systematics 

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References

  1. Ahlberg, P.E. and Milner, A.R.: 1994, ‘The Origin and Early Diversification of Tetrapods’, Nature (London) 368, 507-514.Google Scholar
  2. Ahlberg, P.E.: 1995, ‘Elginerpeton pancheni and the Earliest Tetrapod Clade’, Nature (London) 373, 420-425.Google Scholar
  3. Baldauf, S.L., Palmer, J.D. and Doolittle, W.F.: 1996, ‘The Root of the Universal Tree and the Origin of Eukaryotes Based on Elongation Factor Phylogeny’, Proceedings of the National Academy of Sciences of the United States of America 93, 7749-7754.Google Scholar
  4. Belfort, M. and Weiner, A.: 1997, ‘Another Bridge Between Kingdoms: tRNA Splicing in Archaea and Eukaryotes’, Cell 89, 1003-1006.Google Scholar
  5. Benton, M.J.: 1995, ‘Diversification and Extinction in the History of Life’, Science 268, 52-58.Google Scholar
  6. Biebricher, C.K. and Gardiner, W.C.: 1997, ‘Molecular Evolution of RNA in vitro,’ Biophysical Chemistry 66, 179-192.Google Scholar
  7. Bloch, K.: 1995, Blondes in Venetian Paintings, the Nine-Banded Armadillo, and Other Essays in Biochemistry, Yale University Press, New Haven.Google Scholar
  8. Bock, G.R. and Goode, J.A. (eds.): 1996. Evolution of Hydrothermal Ecosystems on Earth (and Mars?), Wiley, New York.Google Scholar
  9. Bult, C.J. and 39 co-authors: 1996, ‘Complete Genome Sequence of the Methanogenic Archaeon, Methanococcus jannaschii’, Science 273, 1058-1073.Google Scholar
  10. Carroll, R.L.: 1995, ‘Problems of the Phylogenetic Analysis of Paleozoic Choanates’, Bulletin du Museum National d'Histoire Naturelle, Section C: Sciences de la Terre, Paleontologie, Geologie, Mineralogie 17, 389-445.Google Scholar
  11. Carroll, R.L.: 1997, Patterns and Processes of Vertebrate Evolution, Cambridge University Press, Cambridge, UK.Google Scholar
  12. Chela-Flores, J. and Raulin, F. (eds.): 1996, Chemical Evolution: Physics of the Origin and Evolution of Life, Kluwer, Dordrecht.Google Scholar
  13. Clack, J.A. and Coates, M.I.: 1995, ‘Acanthostega gunnari, a Primitive, Aquatic Tetrapod?’, Bulletin du Museum National d'Histoire Naturelle, Section C: Sciences de la Terre, Paleontologie, Geologie, Mineralogie 17, 359-372.Google Scholar
  14. Cloutier, R. and Ahlberg, P.E.: 1996, ‘Morphology, Characters, and the Interrelationships of Basal Sarcopterygians’, in Stiassny, M.L.J., Parenti, L.R. and Johnson, G.D. (eds.), Interrelationships of Fishes, Academic Press, San Diego, pp. 445-479.Google Scholar
  15. Coates, M.I. and Clack, J.A.: 1995, ‘Romer's Gap: Tetrapod Origins and Terrestriality’, Bulletin du Museum National d'Histoire Naturelle, Section C: Sciences de la Terre, Paleontologie, Geologie, Mineralogie 17, 373-388.Google Scholar
  16. Coates, M.I., 1996: ‘The Devonian Tetrapod Acanthostega gunnari Jarvik: Postcranial Anatomy, Basal Tetrapod Interrelationships and Patterns of Skeletal Evolution’, Transactions of the Royal Society of Edinburgh, Earth Sciences 87, 363-421.Google Scholar
  17. Conrad, R.C., Symensma, T.L. and Ellington, A.D.: 1997, ‘Natural and Unnatural Answers to Evolutionary Questions’, Proceedings of the National Academy of Sciences of the United States of America 94, 7126-7128.Google Scholar
  18. Crabtree, R.H.: 1997, ‘Where Smokers Rule’, Science 276, 222.Google Scholar
  19. Crisp, M.D. and Chandler, G.T.: 1996, ‘Paraphyletic Species’, Telopea 6, 813-844.Google Scholar
  20. Ding, P.Z., Kawamura, K. and Ferris, J.P.: 1996, ‘Oligomerization of Uridine Phosphorimidazolides on Montmorillonite: A Model for the Prebiotic Synthesis of RNA on Minerals’, Origins of Life and Evolution of the Biosphere 26, 151-171.Google Scholar
  21. Domingo, E. and 7 co-authors: 1996, ‘Basic Concepts in RNA Virus Evolution’, FASEB Journal 10, 859-864.Google Scholar
  22. Doolittle, R.F., Feng, D., Tsang, S. Cho, G. and Little, E.: 1996, ‘Determining Divergence Times of the Major Kingdoms of Living Organisms with a Protein Clock’, Science 271, 470-477.Google Scholar
  23. Eigen, M. and Winkler-Oswatitsch, R.: 1992, Steps Toward Life: a Perspective on Evolution, Oxford University Press, Oxford.Google Scholar
  24. Ferraris, J.D. and Palumbi, S.R. (eds.): 1996, Molecular Zoology: Advances, Strategies and Protocols, Wiley-Liss, New York.Google Scholar
  25. Ferris, J.P., Hill, A.R., Jr., Liu, R. and Orgel, L.E.: 1996. ‘Synthesis of Long Prebiotic Oligomers on Mineral Surfaces’, Nature (London) 381, 59-61.Google Scholar
  26. Figueroa, F., Ono, H., Tichy, H., O'Huigin, C. and Klein, J.: 1995, ‘Evidence for Insertion of a New Intron into an Mhc Gene of Perch-like Fish’, Proceedings of the Royal Society of London, Series B: Biological Sciences 259, 325-330.Google Scholar
  27. Fitch, W.M. and Ayala, F.J. (eds.): 1995, Tempo and Mode in Evolution: Genetics and Paleontology 50 Years after Simpson, National Academy Press, Washington, D. C.Google Scholar
  28. Forey, P.L., Humphries, C.J., Kitching, I.J., Scotland, R.W., Siebert, D.J. and Williams, D.M.: 1992, Cladistics: A Practical Course in Systematics, Clarendon Press, Oxford, pp. 9-11.Google Scholar
  29. Gibson, R.N.: 1993, ‘Intertidal Teleosts: Life in a Fluctuating Environment’, in Pitcher, T.J. (ed.), Behaviour of Teleost Fishes, 2nd edn, Chapman and Hall, London, pp. 513-536.Google Scholar
  30. Gordon, M.S.: 1998, ‘African Amphibious Fishes and the Invasion of the Land by the Tetrapods’, South African Journal of Zoology 33 (in press).Google Scholar
  31. Gordon, M.S. and Olson, E.C.: 1995, Invasions of the Land: The Transitions of Organisms from Aquatic to Terrestrial Life, Columbia University Press, New York.Google Scholar
  32. Graham, J.B.: 1997, Air-breathing Fishes: Evolution, Diversity, and Adaptation, Academic Press, San Diego.Google Scholar
  33. Gray, M.W., Lang, B.F., Cedergren, R., Golding, G. B., Lemieux, C. and 6 others.: 1998, ‘Genome Structure and Gene Content in Protist Mitochondrial DNAs’, Nucleic Acids Research 26, 865-878.Google Scholar
  34. Gueiros-Filho, F.J. and Beverley, S.M.: 1997, ‘Trans-Kingdom Transposition of the Drosophila Element mariner Within the Protozoan Leishmania’, Science 276, 1716-1719.Google Scholar
  35. Hartl, D.L.: 1997, ‘Mariner Sails into Leishmania’, Science 276, 1659-1660.Google Scholar
  36. Henikoff, S., Greene, E.A., Pietrokovski, S., Bork, P., Attwood, T.K. and Hood, L.: 1997, ‘Gene Families: The Taxonomy of Protein Paralogs and Chimeras’, Science 278, 609-614.Google Scholar
  37. Hilario, E. and Gogarten, J.P.: 1993, ‘Horizontal Transfer of ATPase Genes: the Tree of Life Becomes a Net of Life’, Biosystems 31, 111-119.Google Scholar
  38. Hillis, D.M.: 1997, ‘Biology Recapitulates Phylogeny’, Science 276, 218-219.Google Scholar
  39. Hirabayashi, J.: 1996, ‘On the Origin of Elementary Hexoses’, Quarterly Reviews of Biology 71, 365-380.Google Scholar
  40. Huber, C. and Wächtershäuser, G.: 1997, ‘Activated Acetic Acid by Carbon Fixation on (Fe,Ni)S Under Primordial Conditions’, Science 276, 245-247.Google Scholar
  41. Huelsenbeck, J.P., Bull, J.J. and Cunningham, C.W.: 1996, ‘Combining Data in Phylogenetic Analysis’, Trends in Ecology and Evolution 11, 152-158.Google Scholar
  42. Huelsenbeck, J.P. and Rannala, B.: 1997, ‘Phylogenetic Methods Come of Age: Testing Hypotheses in an Evolutionary Context’, Science 276, 227-232.Google Scholar
  43. Jablonski, D., Erwin, D.H. and Lipps, J.H. (eds.): 1996, Evolutionary Paleobiology, University of Chicago Press, Chicago.Google Scholar
  44. Janvier, P.: 1996, Early Vertebrates, Clarendon Press, Oxford, U.K.Google Scholar
  45. Jeffares, D.C., Poole, A.M. and Penny, D.: 1998, ‘Relics from the RNA World’, Journal of Molecular Evolution 46, 18-36.Google Scholar
  46. Kasting, J.F. and Chang, S.: 1992, ‘Formation of the Earth and the Origin of Life’, in Schopf, J.W. and Klein, C. (eds.), The Proterozoic Biosphere: A Multidisciplinary Study, Cambridge University Press, Cambridge, U.K., pp. 9-12.Google Scholar
  47. Kenrick, P. and Crane, P.R.: 1997, The Origin and Early Diversification of Land Plants: A Cladistic Study, Smithsonian Institution Press, Washington, D.C.Google Scholar
  48. Koehler, S., Delwiche, C.F., Denny, P.W., Tilney, L.G., Webster, P., Wilson, R.J.M., Palmer, J.D. and Roos, D.S.: 1997, ‘A Plastid of Probable Green Algal Origin in Apicomplexan Parasites’, Science 275, 1485-1489.Google Scholar
  49. Krupp, G.: 1996, ‘From Primordial RNA to DNA’, News Physiol. Sci. 11, 53-54.Google Scholar
  50. Landweber, L.F. and Gilbert, W.: 1994, ‘Phylogenetic Analysis of RNA Editing: A Primitive Genetic Phenomenon’, Proceedings of the National Academy of Sciences of the United States of America 91, 918-921.Google Scholar
  51. Lang, B.F., Burger, G., O'Kelly, C.J., Cedergren, R., Golding, G.B., Lemieux, C., Sankoff, D., Turmel, M. and Gray, M.W.: 1997, ‘An Ancestral Mitochondrial DNA Resembling a Eubacterial Genome in Miniature’, Nature (London) 387, 493-497.Google Scholar
  52. Long, J.A.: 1995, The Rise of Fishes: 500 Million Years of Evolution, Johns Hopkins University Press, Baltimore.Google Scholar
  53. Loukeris, T.G., Livadaras, I., Arca, B., Zabalou, S. and Savakis, C.: 1995, ‘Gene Transfer into the Medfly, Ceratitis capitata, with a Drosophila hydei transposable element’, Science 270, 2002-2005.Google Scholar
  54. Maley, L.E. and Marshall, C.R.: 1998, ‘The Coming of Age of Molecular Systematics’, Science 279, 505-506.Google Scholar
  55. Margulis, L.: 1993, Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons, 2nd edn., W. H. Freeman and Co., New York.Google Scholar
  56. Martin, J., Herniou, E., Cook, J., O'Neill, R.W. and Tristem, M.: 1997, ‘Human Endogenous Retrovirus Type I-related Viruses have an Apparently Widespread Distribution Within Vertebrates’, Journal of Virology 71, 437-443.Google Scholar
  57. Martin, K.L.M.: 1995, ‘Time and Tide Wait for No Fish: Intertidal Fishes Out of Water’, Environmental Biology of Fishes 44, 165-181.Google Scholar
  58. Martin, W. and Mueller, M.: 1998, ‘The Hydrogen Hypothesis for the First Eukaryote’, Nature (London) 392, 37-41.Google Scholar
  59. Mazel, D., Dychinco, B., Webb, V.A. and Davies, J.: 1998, ‘A Distinctive Class of Integron in the Vibrio cholerae Genome’, Science 280, 605-608.Google Scholar
  60. McDonald, J.F.: 1998, ‘Transposable Elements, Gene Silencing and Macroevolution’, Trends in Ecology & Evolution 13, 94-95.Google Scholar
  61. Meyer, A. and Dolven, S.I.: 1992, ‘Molecules, Fossils, and the Origin of Tetrapods’, Journal of Molecular Evolution 35, 102-113.Google Scholar
  62. Myers, N.: 1997, ‘Mass Extinction and Evolution’, Science 278, 597-598.Google Scholar
  63. Nee, S. and May, R.M.: 1997, ‘Extinction and the Loss of Evolutionary History’, Science 278, 692-694.Google Scholar
  64. Nielsen, C.: 1995, Animal Evolution: Interrelationships of the Living Phyla, Oxford University Press, Oxford, pp. 1-8.Google Scholar
  65. Palmer, J.D.: 1997, ‘Organelle Genomes: Going, Going, Gone!’, Science 275, 790-791.Google Scholar
  66. Panchen, A.L.: 1992, Classification, Evolution and the Nature of Biology, Cambridge University Press, Cambridge, U.K., pp. 30-61.Google Scholar
  67. Pennisi, E.: 1998a, ‘Versatile Gene Uptake System Found in Cholera Bacterium’, Science 280, 521-522.Google Scholar
  68. Pennisi, E.: 1998b, ‘Genome Data Shake Tree of Life’, Science 280, 672-674.Google Scholar
  69. Pereira, S.L., Grayling, R.A., Luirz, R. and Reeve, J.N.: 1997, ‘Archaeal Nucleosomes’, Proceedings of the National Academy of Sciences of the United States of America 94, 12633-12637.Google Scholar
  70. Poole, A.M., Jeffares, D.C. and Penny, D.: 1998, ‘The Path from the RNA World’, Journal of Molecular Evolution 46, 1-17.Google Scholar
  71. Reeve, J.N., Sandman, K. and Daniels, C.J.: 1997, ‘Archaeal Histones, Nucleosomes, and Transcription Initiation’, Cell 89, 999-1002.Google Scholar
  72. Romano, S.L. and Palumbi, S.R.: 1996, ‘Evolution of Scleractinian Corals Inferred from Molecular Systematics’, Science 271, 640-642.Google Scholar
  73. Runnegar, B.N.: 1992, ‘The Tree of Life’, in Schopf, J.W. and Klein, C. (eds.), The Proterozoic Biosphere: a Multidisciplinary Study, Cambridge University Press, Cambridge, U.K., pp. 471-475.Google Scholar
  74. Russo, V.E.A., Martienssen, R.A. and Riggs, A.D. (eds.): 1996, Epigenetic Mechanisms of Gene Regulation, Cold Spring Harbor Laboratory Press, Cold Spring Harbor.Google Scholar
  75. Sanderson, M.J. and Hufford, L. (eds.): 1996, Homoplasy: the Recurrence of Similarity in Evolution, Academic Press, San Diego.Google Scholar
  76. Schopf, J.W.: 1993, ‘Microfossils of the Early Archaean Apex Chert: New Evidence of the Antiquity of Life’, Science 260, 640-646.Google Scholar
  77. Schultze, H.-P.: 1994, ‘Comparison of Hypotheses on the Relationships of Sarcopterygians’, Systematic Biology 43, 155-173.Google Scholar
  78. Smith, J.M. and Szathmary, E.: 1995, The Major Transitions in Evolution, W.H. Freeman, Palo Alto.Google Scholar
  79. Sogin, M.L.: 1997, ‘Organelle Origins: Energy-producing Symbionts in Early Eukaryotes?’, Current Biology 7, R315-R317.Google Scholar
  80. Tatusov, R.L., Koonin, E.V. and Lipman, D.J.: 1997, ‘A Genomic Perspective on Protein Families’, Science 278, 631-637.Google Scholar
  81. Tristem, M., Herniou, E., Summers, K. and Cook, J.: 1996, ‘Three Retroviral Sequences in Amphibians are Distinct From Those in Mammals and Birds’, Journal of Virology 70, 4864-4870.Google Scholar
  82. Ultsch, G.R.: 1996, ‘Gas Exchange, Hypercarbia and Acid-Base Balance, Paleoecology, and the Evolutionary Transition from Water-Breathing to Air-Breathing Among Vertebrates’, Palaeogeography, Palaeoclimatology, Palaeoecology 123, 1-27.Google Scholar
  83. Veron, J.E.N.: 1995, Corals in Space and Time: the Biogeography and Evolution of the Scleractinia, Comstock (Cornell University Press), Ithaca.Google Scholar
  84. Vogel, G.: 1997, ‘Parasites Shed Light on Cellular Evolution’, Science 275, 1422.Google Scholar
  85. Welch, M., Majerfeld, I. and Yarus, M.: 1997, ‘23S rRNA Similarity from Selection for Peptidyl Transferase Mimicry’, Biochemistry 36, 6614-6623.Google Scholar
  86. Wray, G.A., Levinton, J.S. and Shapiro, L.H.: 1996, ‘Molecular Evidence for Deep Precambrian Divergences among Metazoan Phyla’, Science 274, 568-573.Google Scholar
  87. Yokobori, S.I., Hasegawa, M., Ueda, T., Okada, N., Nishikawa, K. and Watanabe, K.: 1994, ‘Relationships Among Coelacanths, Lungfishes and Tetrapods: A Phylogenetic Analysis Based on Mitochondrial Cytochrome Oxidase I Gene Sequences’, Journal of Molecular Evolution 38, 602-609.Google Scholar
  88. Zardoya, R. and Meyer, A.: 1996a, ‘The Complete Nucleotide Sequence of the Mitochondrial Genome of the Lungfish (Protopterus dolloi) Supports its Phylogenetic Position as a Close Relative of Land Vertebrates’, Genetics 142, 1249-1263.Google Scholar
  89. Zardoya, R. and Meyer, A.: 1996b, ‘Evolutionary Relationships of the Coelacanth, Lungfishes, and Tetrapods Based on the 28S Ribosomal RNA Gene’, Proceedings of the National Academy of Sciences of the United States of America, 93, 5449-5454.Google Scholar
  90. Zardoya, R. and Meyer, A.: 1997. ‘The Complete DNA Sequence of the Mitochondrial Genome of a “Living Fossil”, the Coelacanth (Latimeria chalumnae)’, Genetics 146, 995-1010.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Malcolm S. Gordon
    • 1
  1. 1.Department of BiologyUniversity of CaliforniaLos AngelesU.S.A

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