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Abstract

From comparative analyses of the nucleotide sequences of genes encoding ribosomal RNAs and several proteins, molecular phylogeneticists have constructed a “universal tree of life,” taking it as the basis for a “natural” hierarchical classification of all living things. Although confidence in some of the tree's early branches has recently been shaken, new approaches could still resolve many methodological uncertainties. More challenging is evidence that most archaeal and bacterial genomes (and the inferred ancestral eukaryotic nuclear genome) contain genes from multiple sources. If “chimerism” or “lateral gene transfer” cannot be dismissed as trivial in extent or limited to special categories of genes, then no hierarchical universal classification can be taken as natural. Molecular phylogeneticists will have failed to find the “true tree,” not because their methods are inadequate or because they have chosen the wrong genes, but because the history of life cannot properly be represented as a tree. However, taxonomies based on molecular sequences will remain indispensable, and understanding of the evolutionary process will ultimately be enriched, not impoverished.
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REFERENCES AND NOTES

1
E. Mayr, The Growth of Biological Thought (Belknap Press, Cambridge, MA, 1982).
2
A. L. Panchen, Classification, Evolution and the Nature of Biology (Cambridge Univ. Press, Cambridge, 1992); M. T. Ghiselin, Metaphysics and the Origin of Species (State Univ. of New York Press, Albany, NY, 1997).
3
C. Darwin, The Origin of Species by Means of Natural Selection (Murray, London, 1859).
4
E. Zuckerkandl and L. Pauling, in Evolving Genes and Proteins, V. Bryson and H. J. Vogel, Eds. (Academic Press, New York, 1965), pp. 97–166; J. Theor. Biol. 8, 357 (1965).
5
Woese C. R., Kandler O., Wheelis M. L., Proc. Natl. Acad. Sci. U.S.A. 87, 4576 (1990);
Doolittle W. F., Brown J. R., ibid. 91, 6721 (1994);
; R. F. Doolittle, ibid.92, 2421 (1995);
Pace N. R., Science 276, 734 (1997).
6
Schwartz R. M., Dayhoff M. O., Science 199, 395 (1978).
7
Woese C. R., Microbiol. Rev. 51, 221 (1987).
8
Green R., Noller H. F., Annu. Rev. Biochem. 66, 679 (1997).
9
Gogarten P. J., et al., Proc. Natl. Acad. Sci. U.S.A. 86, 6661 (1989);
; N. Iwabe, K. Kuma, M. Hasegawa, S. Osawa, T. Miyata, ibid., p. 9355; J. R. Brown and W. F. Doolittle, ibid. 92, 2441 (1995); S. L. Baldauf, J. D. Palmer, W. F. Doolittle, ibid. 93, 7749 (1996);
Lawson F. S., Charlebois R. L., Dillon J. A., Mol. Biol. Evol. 13, 970 (1996);
. Organisms in all major groups bear genes encoding elongation factors EF-1α (EF-Tu) and EF-2 (bacterial EF-G). These homologous (more precisely, paralogous) genes thus must be products of a gene duplication that had already occurred before the time of the last common ancestor of all organisms alive today. A tree made of EF-1α and EF-2 sequences should comprise two subtrees (one for each of these paralogs), each of which (barring LGT or artifacts) should have the topology of the true universal organismal tree. The point at which each subtree attaches to the other will be its root and will correspond to the last common organismal ancestor. Neither subtree is rootable without the other. Because rRNA genes all seem to be orthologous (derived from a single ancestral gene in the last common ancestor), such a rooting is not possible with rRNA sequences alone.
10
M. J. Kates, D. J. Kushner, A. T. Matheson, Eds., The Biochemistry of Archaea (Archaeobacteria) (Elsevier Science, Amsterdam, 1993); W. F. Doolittle, in Evolution of Microbial Life, D. M. Roberts, P. Sharp, G. Alderson, M. Collins, Eds. (Cambridge Univ. Press, Cambridge, 1996), pp. 1–21.
11
Olsen G. J., Woese C. R., Cell 89, 991 (1997);
; D. E. Edgell and W. F. Doolittle, ibid., p. 995; J. N. Reeve, K. Sandman, C. J. Daniels, ibid., p. 999; P. P. Dennis, ibid., p. 1007;
Soppa J., Mol. Microbiol. 31, 1295 (1997).
12
Philippe H., Curr. Opin. Genet. Dev. 8, 616 (1998);
; H. Phillippe and A. Adoutte, in Evolutionary Relationships Among Protozoa, G. H. Coombs, K. Vickerman, M. A. Sleigh, A. Warren, Eds. (Systematics Association, London, 1998), pp. 25–26;
Moreira D., LeGuyader H., Philippe H., Mol. Biol. Evol. 16, 234 (1999).
13
Prominent among sources of error or uncertainty in establishing branching patterns are mutational saturation, “long-branch attraction,” and “among-site rate variation.” Mutationally saturated sequences are maximally diverged, so that further changes are as likely to make them more similar as they are to make them more different, and tree topology is based on noise. Long-branch attraction [
Felsenstein J., Syst. Zool. 27, 401 (1978);
] occurs when rates of sequence change differ substantially between taxa (even without saturation). Lineages with higher rates of sequence change artifactually associate with each other and with out-groups, except with maximum likelihood methods. Even with these methods [
Yang Z., J. Mol. Evol. 42, 294 (1996);
; Trends Ecol. Evol. 11, 367 (1996)], long-branch attraction occurs when there is a substantial rate variation among different sites in a gene.
14
Hirt R. P., et al., Proc. Natl. Acad. Sci. U.S.A. 96, 580 (1999);
Stiller J. W., Duffield E. C., Hall B. D., ibid. 95, 11769 (1998).
15
P. J. Gogarten, E. Hilario, L. Olenzenski, in Evolution of Microbial Life, D. M. Roberts, P. Sharp, G. Alderson, M. Collins, Eds. (Cambridge Univ. Press, Cambridge, 1996), pp. 267–292.
16
Martin W., BioEssays 21, 99 (1999).
17
Cavalier-Smith T., Nature 326, 332 (1987);
; Biol. Rev. Camb. Philos. Soc. 73, 203 (1998).
18
Vossbrinck C. R., et al., Nature 326, 411 (1987);
Sogin M. L., Gunderson J. H., Elwood H. J., Alonso R. A., Peattie D. A., Science 243, 75 (1989);
Leipe D. D., Gunderson J. H., Nerad T. A., Sogin M. L., Mol. Biochem. Parasitol. 59, 41 (1993).
19
Embley T. M., Hirt R. P., Curr. Opin. Genet. Dev. 8, 629 (1998);
Roger A. J., Sandblom O., Doolittle W. F., Philippe H., Mol. Biol. Evol. 16, 218 (1999);
Keeling P. J., McFadden G. I., Trends Microbiol. 6, 19 (1998).
20
Miyamoto M. M., Fitch W. M., Mol. Biol. Evol. 12, 513 (1995).
21
Gray M. W., Burger G., Lang B. F., Science 283, 1476 (1999).
22
Brown J. R., Doolittle W. F., Microbiol. Mol. Biol. Rev. 61, 456 (1997);
Feng D.-F., Cho G., Doolittle R. F., Proc. Natl. Acad. Sci. U.S.A. 94, 13028 (1997) ;
Ragan M., Gaasterland T., J. Microb. Comp. Genomics 3, 219 (1998);
Rivera M. C., Jain R., Moore F. F., Lake J. A., Proc. Natl. Acad. Sci. U.S.A. 95, 6239 (1998).
23
Doolittle W. F., Trends Genet. 14, 307 (1998);
Martin W., Muller M., Nature 392, 37 (1998).
24
Lawrence J. G., Ochman H., Proc. Natl. Acad. Sci. U.S.A. 95, 9413 (1998).
25
Klenk H.-P., et al., Nature 390, 364 (1997).
26
Doolittle W. F., Logsdon J. M., Curr. Biol. 8, R209 (1998);
Ibba M., Bono J. L., Rosa P. A., Soll D., Proc. Natl. Acad. Sci. U.S.A. 94, 14383 (1997).
27
Jain R., Rivera M. C., Lake J. A., Proc. Natl. Acad. Sci. U.S.A. 96, 3801 (1999).
28
Hilario E., Gogarten J. P., Biosystems 31, 111 (1993).
29
Sonea S., Paniset M., Rev. Can. Biol. 35, 103 (1976);
; D. C. Reanney, in Aspects of Genetic Action and Evolution, suppl. 8 of International Review of Cytology, G. H. Bourne, J. F. Danielli, K. W. Jeon, Eds. (Academic Press, New York, 1978), pp. 1–67.
30
Cermakian N., et al., J. Mol. Evol. 46, 671 (1997).
31
S. A. Baldauf and W. F. Doolittle, in preparation.
32
D. M. O'Neil,
Baron L., Sypherd P., J. Bacteriol. 99, 242 (1969).
33
Doolittle R. F., Handy J. F., Curr. Opin. Genet. Dev. 8, 630 (1998).
34
Nomura M., Proc. Natl. Acad. Sci. U.S.A. 96, 1820 (1999).
35
___, Traub P., Bechmann H., Nature 219, 793 (1968).
36
Noller H. F., Woese C. R., Science 212, 403 (1981).
37
Asai T., Zaprojets D., Squires C., Squires C. L., Proc. Natl. Acad. Sci. U.S.A. 96, 1971 (1999).
38
Gupta R. S., Microbiol. Mol. Biol. Rev. 62, 1435 (1998).
39
Brown J. R., Zhang J., Hodgson J. E., Curr. Biol. 8, R365 (1998).
40
Ueda K., Kido Y., Yoshida T., Kataoka M., J. Bacteriol. 181, 78 (1999).
41
Woese C. R., Proc. Natl. Acad. Sci. U.S.A. 95, 6854 (1998).
42
J. Xiong, K. Inoue, C. C. Bauer, ibid., p. 14851.
43
Aravind L., et al., Trends Genet. 14, 442 (1998).
44
I thank J. Logsdon, A. Roger, D. Faguy, O. Feeley, and Y. Inagaki for critical discussions and the Medical Research Council of Canada and the Canadian Institute for Advanced Research for support. I am indebted to J. P. Gogarten and W. Martin for persuading me of the importance of LGT.

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Volume 284Issue 542325 June 1999
Pages: 2124 - 2128

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W. Ford Doolittle
Canadian Institute for Advanced Research, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia B3H 4H7, Canada. E-mail: [email protected]

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