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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2000 Jun 22;267(1449):1213–1221. doi: 10.1098/rspb.2000.1130

Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions.

H Philippe 1, P Lopez 1, H Brinkmann 1, K Budin 1, A Germot 1, J Laurent 1, D Moreira 1, M Müller 1, H Le Guyader 1
PMCID: PMC1690654  PMID: 10902687

Abstract

The current paradigm of eukaryotic evolution is based primarily on comparative analysis of ribosomal RNA sequences. It shows several early-emerging lineages, mostly amitochondriate, which might be living relics of a progressive assembly of the eukaryotic cell. However, the analysis of slow-evolving positions, carried out with the newly developed slow-fast method, reveals that these lineages are, in terms of nucleotide substitution, fast-evolving ones, misplaced at the base of the tree by a long branch attraction artefact. Since the fast-evolving groups are not always the same, depending on which macromolecule is used as a marker, this explains most of the observed incongruent phylogenies. The current paradigm of eukaryotic evolution thus has to be seriously re-examined as the eukaryotic phylogeny is presently best summarized by a multifurcation. This is consistent with the Big Bang hypothesis that all extant eukaryotic lineages are the result of multiple cladogeneses within a relatively brief period, although insufficiency of data is also a possible explanation for the lack of resolution. For further resolution, rare evolutionary events such as shared insertions and/or deletions or gene fusions might be helpful.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ayala F. J. Vagaries of the molecular clock. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7776–7783. doi: 10.1073/pnas.94.15.7776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brinkmann H., Philippe H. Archaea sister group of Bacteria? Indications from tree reconstruction artifacts in ancient phylogenies. Mol Biol Evol. 1999 Jun;16(6):817–825. doi: 10.1093/oxfordjournals.molbev.a026166. [DOI] [PubMed] [Google Scholar]
  3. Budin K., Philippe H. New insights into the phylogeny of eukaryotes based on ciliate Hsp70 sequences. Mol Biol Evol. 1998 Aug;15(8):943–956. doi: 10.1093/oxfordjournals.molbev.a026010. [DOI] [PubMed] [Google Scholar]
  4. Cao Y., Waddell P. J., Okada N., Hasegawa M. The complete mitochondrial DNA sequence of the shark Mustelus manazo: evaluating rooting contradictions to living bony vertebrates. Mol Biol Evol. 1998 Dec;15(12):1637–1646. doi: 10.1093/oxfordjournals.molbev.a025891. [DOI] [PubMed] [Google Scholar]
  5. Cavalier-Smith T. The origin of eukaryotic and archaebacterial cells. Ann N Y Acad Sci. 1987;503:17–54. doi: 10.1111/j.1749-6632.1987.tb40596.x. [DOI] [PubMed] [Google Scholar]
  6. Embley T. M., Hirt R. P. Early branching eukaryotes? Curr Opin Genet Dev. 1998 Dec;8(6):624–629. doi: 10.1016/s0959-437x(98)80029-4. [DOI] [PubMed] [Google Scholar]
  7. Field K. G., Olsen G. J., Lane D. J., Giovannoni S. J., Ghiselin M. T., Raff E. C., Pace N. R., Raff R. A. Molecular phylogeny of the animal kingdom. Science. 1988 Feb 12;239(4841 Pt 1):748–753. doi: 10.1126/science.3277277. [DOI] [PubMed] [Google Scholar]
  8. Fitch W. M., Markowitz E. An improved method for determining codon variability in a gene and its application to the rate of fixation of mutations in evolution. Biochem Genet. 1970 Oct;4(5):579–593. doi: 10.1007/BF00486096. [DOI] [PubMed] [Google Scholar]
  9. Germot A., Philippe H. Critical analysis of eukaryotic phylogeny: a case study based on the HSP70 family. J Eukaryot Microbiol. 1999 Mar-Apr;46(2):116–124. doi: 10.1111/j.1550-7408.1999.tb04594.x. [DOI] [PubMed] [Google Scholar]
  10. Goldman N., Thorne J. L., Jones D. T. Assessing the impact of secondary structure and solvent accessibility on protein evolution. Genetics. 1998 May;149(1):445–458. doi: 10.1093/genetics/149.1.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gray M. W., Burger G., Lang B. F. Mitochondrial evolution. Science. 1999 Mar 5;283(5407):1476–1481. doi: 10.1126/science.283.5407.1476. [DOI] [PubMed] [Google Scholar]
  12. Hasegawa M., Fujiwara M. Relative efficiencies of the maximum likelihood, maximum parsimony, and neighbor-joining methods for estimating protein phylogeny. Mol Phylogenet Evol. 1993 Mar;2(1):1–5. doi: 10.1006/mpev.1993.1001. [DOI] [PubMed] [Google Scholar]
  13. Hasegawa M., Hashimoto T. Ribosomal RNA trees misleading? Nature. 1993 Jan 7;361(6407):23–23. doi: 10.1038/361023b0. [DOI] [PubMed] [Google Scholar]
  14. Hirt R. P., Logsdon J. M., Jr, Healy B., Dorey M. W., Doolittle W. F., Embley T. M. Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc Natl Acad Sci U S A. 1999 Jan 19;96(2):580–585. doi: 10.1073/pnas.96.2.580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kamaishi T., Hashimoto T., Nakamura Y., Masuda Y., Nakamura F., Okamoto K., Shimizu M., Hasegawa M. Complete nucleotide sequences of the genes encoding translation elongation factors 1 alpha and 2 from a microsporidian parasite, Glugea plecoglossi: implications for the deepest branching of eukaryotes. J Biochem. 1996 Dec;120(6):1095–1103. doi: 10.1093/oxfordjournals.jbchem.a021527. [DOI] [PubMed] [Google Scholar]
  16. Knoll A. H. The early evolution of eukaryotes: a geological perspective. Science. 1992 May 1;256(5057):622–627. doi: 10.1126/science.1585174. [DOI] [PubMed] [Google Scholar]
  17. Leipe D. D., Gunderson J. H., Nerad T. A., Sogin M. L. Small subunit ribosomal RNA+ of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol Biochem Parasitol. 1993 May;59(1):41–48. doi: 10.1016/0166-6851(93)90005-i. [DOI] [PubMed] [Google Scholar]
  18. Lockhart P. J., Larkum A. W., Steel M., Waddell P. J., Penny D. Evolution of chlorophyll and bacteriochlorophyll: the problem of invariant sites in sequence analysis. Proc Natl Acad Sci U S A. 1996 Mar 5;93(5):1930–1934. doi: 10.1073/pnas.93.5.1930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lockhart P. J., Steel M. A., Barbrook A. C., Huson D. H., Charleston M. A., Howe C. J. A covariotide model explains apparent phylogenetic structure of oxygenic photosynthetic lineages. Mol Biol Evol. 1998 Sep;15(9):1183–1188. doi: 10.1093/oxfordjournals.molbev.a026025. [DOI] [PubMed] [Google Scholar]
  20. Loomis W. F., Smith D. W. Molecular phylogeny of Dictyostelium discoideum by protein sequence comparison. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9093–9097. doi: 10.1073/pnas.87.23.9093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lopez P., Forterre P., Philippe H. The root of the tree of life in the light of the covarion model. J Mol Evol. 1999 Oct;49(4):496–508. doi: 10.1007/pl00006572. [DOI] [PubMed] [Google Scholar]
  22. Miyamoto M. M., Fitch W. M. Testing the covarion hypothesis of molecular evolution. Mol Biol Evol. 1995 May;12(3):503–513. doi: 10.1093/oxfordjournals.molbev.a040224. [DOI] [PubMed] [Google Scholar]
  23. Naylor G. J., Brown W. M. Amphioxus mitochondrial DNA, chordate phylogeny, and the limits of inference based on comparisons of sequences. Syst Biol. 1998 Mar;47(1):61–76. doi: 10.1080/106351598261030. [DOI] [PubMed] [Google Scholar]
  24. Peyretaillade E., Biderre C., Peyret P., Duffieux F., Méténier G., Gouy M., Michot B., Vivarès C. P. Microsporidian Encephalitozoon cuniculi, a unicellular eukaryote with an unusual chromosomal dispersion of ribosomal genes and a LSU rRNA reduced to the universal core. Nucleic Acids Res. 1998 Aug 1;26(15):3513–3520. doi: 10.1093/nar/26.15.3513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Philippe H., Germot A. Phylogeny of eukaryotes based on ribosomal RNA: long-branch attraction and models of sequence evolution. Mol Biol Evol. 2000 May;17(5):830–834. doi: 10.1093/oxfordjournals.molbev.a026362. [DOI] [PubMed] [Google Scholar]
  26. Philippe H., Laurent J. How good are deep phylogenetic trees? Curr Opin Genet Dev. 1998 Dec;8(6):616–623. doi: 10.1016/s0959-437x(98)80028-2. [DOI] [PubMed] [Google Scholar]
  27. Philippe H. MUST, a computer package of Management Utilities for Sequences and Trees. Nucleic Acids Res. 1993 Nov 11;21(22):5264–5272. doi: 10.1093/nar/21.22.5264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Philippe H. Rodent monophyly: pitfalls of molecular phylogenies. J Mol Evol. 1997 Dec;45(6):712–715. [PubMed] [Google Scholar]
  29. Sogin M. L., Gunderson J. H., Elwood H. J., Alonso R. A., Peattie D. A. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science. 1989 Jan 6;243(4887):75–77. doi: 10.1126/science.2911720. [DOI] [PubMed] [Google Scholar]
  30. Sogin M. L., Silberman J. D. Evolution of the protists and protistan parasites from the perspective of molecular systematics. Int J Parasitol. 1998 Jan;28(1):11–20. doi: 10.1016/s0020-7519(97)00181-1. [DOI] [PubMed] [Google Scholar]
  31. Sogin M. l. History assignment: when was the mitochondrion founded? Curr Opin Genet Dev. 1997 Dec;7(6):792–799. doi: 10.1016/s0959-437x(97)80042-1. [DOI] [PubMed] [Google Scholar]
  32. Stiller J. W., Hall B. D. Long-branch attraction and the rDNA model of early eukaryotic evolution. Mol Biol Evol. 1999 Sep;16(9):1270–1279. doi: 10.1093/oxfordjournals.molbev.a026217. [DOI] [PubMed] [Google Scholar]
  33. Tuffley C., Steel M. Modeling the covarion hypothesis of nucleotide substitution. Math Biosci. 1998 Jan 1;147(1):63–91. doi: 10.1016/s0025-5564(97)00081-3. [DOI] [PubMed] [Google Scholar]
  34. Woese C. R., Achenbach L., Rouviere P., Mandelco L. Archaeal phylogeny: reexamination of the phylogenetic position of Archaeoglobus fulgidus in light of certain composition-induced artifacts. Syst Appl Microbiol. 1991;14(4):364–371. doi: 10.1016/s0723-2020(11)80311-5. [DOI] [PubMed] [Google Scholar]
  35. Woese C. R., Fox G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5088–5090. doi: 10.1073/pnas.74.11.5088. [DOI] [PMC free article] [PubMed] [Google Scholar]

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