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Inferring the historical patterns of biological evolution

Abstract

Phylogenetic trees describe the pattern of descent amongst a group of species. With the rapid accumulation of DNA sequence data, more and more phylogenies are being constructed based upon sequence comparisons. The combination of these phylogenies with powerful new statistical approaches for the analysis of biological evolution is challenging widely held beliefs about the history and evolution of life on Earth.

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Figure 1: Cumulative number of publications in the Science Citation Index since 1981 that cite the terms ‘molecular’ and ‘phylogeny’ in the key words or abstract.
Figure 2: A phylogeny of the artiodactyls with approximate branch lengths, adapted from ref.
Figure 3: A tree of life showing the approximate relationships among the bacteria, archaea (eurarchaea and crenarchaea) and eukaryotes, adapted from ref.
Figure 4: Peculiar cactus-like shape of two gene trees from data on the influenza virus (modified from ref.
Figure 5: The quartet method simultaneously considers two pairs of species with known times of divergence based on fossils.

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References

  1. Hillis,D. M., Moritz,C. & Mable,B. K. Molecular Systematics, 2nd edn (Sinauer, Sunderland, Massachusetts, 1996).

    Google Scholar 

  2. Pagel,M. Inferring evolutionary processes from phylogenies. Zool. Scripta 26, 331–348 (1997).

    Google Scholar 

  3. Edwards,A. W. F. Likelihood (Cambridge Univ. Press, Cambridge, 1972).

    MATH  Google Scholar 

  4. Golding,G. B. & Dean,A. M. The structural basis of molecular adaptation. Mol. Biol. Evol. 15, 355– 369 (1998).

    CAS  PubMed  Google Scholar 

  5. Ivics,Z., Hackett,P. B., Plasterk,R. H. & Izsvak,Z. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91, 501–510 (1997).

    CAS  PubMed  Google Scholar 

  6. Pagel,M. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. Lond. B 255, 37–45 (1994).

    ADS  Google Scholar 

  7. Schluter,D. Uncertainty in ancient phylogenies. Nature 377, 108–109 (1995).

    ADS  CAS  PubMed  Google Scholar 

  8. Schluter,D., Price,T., Mooers,A. Ø. & Ludwig,D. Likelihood of ancestor states in adaptive radiation. Evolution 51, 1699–1711 ( 1997).

    PubMed  Google Scholar 

  9. Yang,Z., Kumar,S. & Nei,M. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141, 1641–1650 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Koshi,J. M. & Goldstein,R. A. Probabilistic reconstruction of ancestral protein sequences. J. Mol. Evol. 42, 313–320 (1996).

    ADS  CAS  PubMed  Google Scholar 

  11. Mooers,A. Ø. & Schluter,D. Support for one and two rate models of discrete trait evolution. Syst. Biol. 48, 623–633 (1999).

    Google Scholar 

  12. Pagel,M. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst. Biol. 48, 612–622 (1999).

    Article  Google Scholar 

  13. Hillis,D. M., Bull,J. J., White,M. E., Badgett,M. R. & Molineux, I. J. Experimental phylogenetics: generation of a known phylogeny. Science 255, 589– 592 (1992).

    ADS  CAS  PubMed  Google Scholar 

  14. Collins,T. M., Wimberger,P. H. & Naylor, G. J. P. Compositional bias, character-state bias, and character-state reconstruction using parsimony. Syst. Biol. 43, 482–496 (1994).

    Google Scholar 

  15. Maddison,D. R. Phylogenetic methods for inferring the evolutionary history and process of change in discreetly valued characters. Annu. Rev. Entomol. 39, 267–292 (1994).

    Google Scholar 

  16. Tuffley,C. & Steel,M. Links between maximum likelihood and maximum parsimony under a simple model of site substitution. Bull. Math. Biol. 59, 581–607 (1997).

    CAS  PubMed  MATH  Google Scholar 

  17. Johnston,J. Econometric Methods (McGraw Hill, New York, 1963).

    Google Scholar 

  18. Martins,E. P. & Hansen,T. F. Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat. 149, 646–667 (1997).

    Google Scholar 

  19. Jermann,T. M., Opitz,J. G., Stackhouse,J. & Benner,S. A. Reconstructing the evolutionary history of the artiodactyl ribonuclease superfamily. Nature 374, 57–59 (1995).

    ADS  CAS  PubMed  Google Scholar 

  20. Li,W.-H. Molecular Evolution (Sinauer, Sunderland, Massachusetts, 1997).

    Google Scholar 

  21. Yeager,M. & Hughes,A. L. Evolution of the mammalian MHC: natural selection, recombination, and convergent evolution. Immunol. Rev. 167, 45–58 ( 1999).

    CAS  PubMed  Google Scholar 

  22. Bull,J. J. et al. Exceptional convergent evolution in a virus. Genetics 147, 1497–1507 ( 1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Roux,K. H. et al. Structural analysis of the nurse shark (new) antigen receptor (NAR): Molecular convergence of NAR and unusual mammalian immunoglobulins. Proc. Natl Acad. Sci. USA 95, 11804– 11809 (1998).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  24. Crandall,K. A., Kelsey,C. R., Imamichi,H., Lane,H. C. & Salzman,N. P. Parallel evolution of drug resistance in HIV: Failure of nonsynonymous/synonymous substitution rate ratio to detect selection. Mol. Biol. Evol. 16, 372– 382 (1999).

    CAS  PubMed  Google Scholar 

  25. Mojzsis,S. J. et al. Evidence for life on earth before 3,800 million years ago. Nature 384, 55–59 (1996).

    ADS  CAS  PubMed  Google Scholar 

  26. Woese,C. R. Bacterial evolution. Microbiol. Rev. 51, 221–271 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Pace,N. R. A molecular view of microbial diversity and the biosphere. Science 276, 734–740 ( 1997).

    CAS  PubMed  Google Scholar 

  28. Brown,J. R. & Doolittle,W. F. Archaea and the prokaryote-to-eukaryote transition. Microbiol. Mol. Biol. Rev. 61, 456–504 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Galtier,N., Tourasse,N. & Gouy,M. A nonhyperthermophilic common ancestor to extant life forms. Science 283, 220– 221 (1999).

    CAS  PubMed  Google Scholar 

  30. Fitch,W. M., Leiter,J. M. E., Li,X. & Palese,P. Positive Darwinian evolution in human influenza A viruses. Proc. Natl Acad. Sci. USA 88, 4270–4274 ( 1991).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  31. Omland,K. Character congruence between a molecular and a morphological phylogeny for dabbling ducks (Anas). Syst. Biol. 43, 369–386 (1994).

    Google Scholar 

  32. Omland,K. Correlated ratest of molecular and morphological evolution. Evolution 51, 1381–1393 ( 1997).

    PubMed  Google Scholar 

  33. Strauss,E. Can mitochondrial clocks keep time? Science 283, 1435–1438 (1999).

    CAS  PubMed  Google Scholar 

  34. Rambaut,A. & Bromham,L. Estimating divergence dates from molecular sequences. Mol. Biol. Evol. 15, 442–448 (1998).

    CAS  PubMed  Google Scholar 

  35. Bromham,L., Rambaut,A., Fortey,R., Cooper,A. & Penny,D. Testing the Cambrian explosion hypothesis by using a molecular dating technique. Proc. Natl Acad. Sci. USA 95, 12386– 12389 (1998).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  36. Fortey,R. Life: An Unauthorised Biography (HarperCollins, London, 1997).

    Google Scholar 

  37. Valentine,J. W., Erwin,D. H. & Jablonski, D. Developmental evolution of metazoan bodyplans: The fossil evidence. Dev. Biol. 173, 373– 381 (1996).

    CAS  PubMed  Google Scholar 

  38. Bowring,S. A. et al. Calibrating rates of early Cambrian evolution. Science 261, 1293–1298 ( 1993).

    ADS  CAS  PubMed  Google Scholar 

  39. Wray,G., Levinton,J. S. & Shapiro, L. H. Molecular evidence for deep precambrian divergences among the metazoan phyla. Science 274, 568 –573 (1996).

    ADS  CAS  Google Scholar 

  40. Ayala,F. J., Rzhetsky,A. & Ayala,F. J. Origin of the metazoan phyla: molecular clocks confirm paleontological estimates. Proc. Natl Acad. Sci. USA 95, 606–611 (1998).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  41. Kerr,R. A. Earliest animals growing younger? Science 284, 411–412 (1999).

    Google Scholar 

  42. Raup,D. M. Mass Extinctions: Bad Genes or Bad Luck? (Oxford Univ. Press, Oxford, 1991).

    Google Scholar 

  43. Cooper,A. & Penny,D. Mass survival of birds across the Cretaceous–Tertiary boundary: molecular evidence. Science 275, 1109–1113 (1997).

    CAS  PubMed  Google Scholar 

  44. Hedges,S. B., Parker,P. H., Sibley,C. G. & Kumar,S. Continental breakup and the ordinal diversification of birds and mammals. Nature 381, 226–229 ( 1996).

    ADS  CAS  PubMed  Google Scholar 

  45. Vilá,C. et al. Multiple and ancient origins of the domestic dog. Science 276, 1687–1689 ( 1997).

    PubMed  Google Scholar 

  46. Krings,M. et al. Neandertal DNA sequences and the origin of modern humans. Cell 90, 19–30 ( 1997).

    CAS  PubMed  Google Scholar 

  47. Darwin,C. The Origin of Species by Means of Natural Selection, 6th edn (with corrections and additions to 1872) (John Murray, London, 1888).

    Google Scholar 

  48. Bowler,P. J. Charles Darwin: The Man and His Influence (Blackwell, Oxford, 1991).

    Google Scholar 

  49. Gould,S. J. & Eldredge,N. Punctuated equilibria comes of age. Nature 366, 223–227 (1993).

    ADS  CAS  PubMed  Google Scholar 

  50. Williams,G. C. Natural Selection (Oxford Univ. Press, Oxford, 1992 ).

    Google Scholar 

  51. Hecht,M. K. & Hoffman,A. Why no neo-Darwinism: a critique of paleobiological challenges. Oxford Surv. Evol. Biol. 3, 1–47 (1986).

    Google Scholar 

  52. Foote,M. & Sepkoski,J. J. Jr Absolute measures of the completeness of the fossil record. Nature 398 , 415–417 (1999).

    ADS  CAS  PubMed  Google Scholar 

  53. Mooers,A. Ø., Vamosi,S. M. & Schluter, D. Using phylogenies to test macroevolutionary hypotheses of trait evolution. Am. Nat. 154, 249– 259 (1999).

    PubMed  Google Scholar 

  54. Harvey,P. H. & Pagel,M. The Comparative Method in Evolutionary Biology (Oxford Univ. Press, Oxford, 1991).

    Google Scholar 

  55. Pagel,M. Seeking the evolutionary regression coefficient: an analysis of what comparative methods measure. J. Theor. Biol. 164, 191 –205 (1993).

    CAS  PubMed  Google Scholar 

  56. Ridley,M. The Explanation of Organic Diversity (Oxford Univ. Press, Oxford, 1981).

    Google Scholar 

  57. Maddison,W. P. A method for testing the correlated evolutionary of two binary characters: are gains and losses concentrated on certain branches of a phylogenetic tree. Evolution 44, 539–557 (1990).

    PubMed  Google Scholar 

  58. Felsenstein,J. Phylogenies and the comparative method. Am. Nat. 125 , 1–15 (1985).

    Google Scholar 

  59. Pagel,M. A method for the analysis of comparative data. J. Theor. Biol. 156, 431–442 ( 1992).

    Google Scholar 

  60. Garland,T. Jr, Harvey,P. H. & Ives,A. R. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41, 18–32 (1992).

    Google Scholar 

  61. Martins,E. P. & Garland,T. H. Phylogenetic analyses of the correlated evolution of continuous characters: a simulation study. Evolution 45, 534–557 ( 1991).

    PubMed  Google Scholar 

  62. Purvis,A., Gittleman,J. L. & Luh, H. K. Truth or consequences—effects of phylogenetic accuracy on two comparative methods. J. Theor. Biol. 167, 293–300 (1994).

    Google Scholar 

  63. Rolland,C., Danchin,E. & de Fraipont, M. The evolution of coloniality in birds in relation to food, habitat, predation, and life-history traits: a comparative analysis. Am. Nat. 151, 514–529 (1998).

    CAS  PubMed  Google Scholar 

  64. Ricklefs,R. E. & Starck,J. M. Applications of phylogenetically independent contrasts: A mixed progress report. Oikos 77, 167–172 ( 1996).

    Google Scholar 

  65. Price,T. Correlated evolution and independent contrasts. Phil. Trans. R. Soc. Lond. B 352, 519–529 (1997).

    ADS  CAS  Google Scholar 

  66. Harvey,P. H. & Rambaut,A. Phylogenetic extinction rates and comparative methodology. Proc. R. Soc. Lond. B 265, 1691–1696 (1998).

    Google Scholar 

  67. Durham,W. Coevolution: Genes, Culture, and Human Diversity (Stanford Univ. Press, Stanford, 1991).

    Google Scholar 

  68. Holden,C. & Mace,R. A phylogenetic analysis of the evolution of lactose digestion. Hum. Biol. 69, 605 –628 (1997).

    CAS  PubMed  Google Scholar 

  69. Jerison,H. J. Evolution of the Brain and Intelligence (Academic, New York, 1973).

    Google Scholar 

  70. Martin,R. D. Relative brain size and metabolic rate in terrestrial vertebrates. Nature 293, 57–60 ( 1981).

    ADS  CAS  PubMed  Google Scholar 

  71. Pagel,M. & Harvey,P. H. Taxonomic differences in the scaling of brain on body weight in mammals. Science 244, 1589–1593 (1989).

    ADS  CAS  PubMed  Google Scholar 

  72. Arnason,U., Gullberg,A. & Janke,A. Molecular timing of primate divergences as estimated by two nonprimate calibration points. J. Mol. Evol. 47 , 718–727 (1998).

    ADS  CAS  PubMed  Google Scholar 

  73. Purvis,A. A composite estimate of primate phylogeny. Phil. Trans. R. Soc. Lond. B 348, 405–421 ( 1995).

    ADS  CAS  Google Scholar 

  74. Healy,S. D. & Krebs,J. R. Food storing and the hippocampus in Paridae. Brain Behav. Evol. 47, 195– 199 (1996).

    CAS  PubMed  Google Scholar 

  75. Wilson,I. & Balding,D. Geneaological inference from microsatellite data. Genetics 150, 499– 510 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Larget,B. & Simon,D. L. Markov chain monte carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol. Biol. Evol. 16, 750–759 ( 1999).

    CAS  Google Scholar 

  77. Ursing,B. M. & Arnason,U. Analyses of mitochondrial genomes strongly support a hippopotamus–whale clade. Proc. R. Soc. Lond. B 265, 2252–2255 ( 1998).

    Google Scholar 

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Acknowledgements

I thank D. Cox, N. Galtier, G. Laden and A. Rambaut for discussion and access to data. The Leverhulme Trust provided financial support.

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Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999). https://doi.org/10.1038/44766

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