• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of procbhomepageaboutsubmitalertseditorial board
Proc Biol Sci. Jun 22, 2000; 267(1449): 1213–1221.
PMCID: PMC1690654

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


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.

Full Text

The Full Text of this article is available as a PDF (180K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ayala FJ. Vagaries of the molecular clock. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7776–7783. [PMC free article] [PubMed]
  • 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. [PubMed]
  • 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. [PubMed]
  • Cao Y, Waddell PJ, 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. [PubMed]
  • Cavalier-Smith T. The origin of eukaryotic and archaebacterial cells. Ann N Y Acad Sci. 1987;503:17–54. [PubMed]
  • Embley TM, Hirt RP. Early branching eukaryotes? Curr Opin Genet Dev. 1998 Dec;8(6):624–629. [PubMed]
  • Field KG, Olsen GJ, Lane DJ, Giovannoni SJ, Ghiselin MT, Raff EC, Pace NR, Raff RA. Molecular phylogeny of the animal kingdom. Science. 1988 Feb 12;239(4841 Pt 1):748–753. [PubMed]
  • Fitch WM, 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. [PubMed]
  • 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. [PubMed]
  • Goldman N, Thorne JL, Jones DT. Assessing the impact of secondary structure and solvent accessibility on protein evolution. Genetics. 1998 May;149(1):445–458. [PMC free article] [PubMed]
  • Gray MW, Burger G, Lang BF. Mitochondrial evolution. Science. 1999 Mar 5;283(5407):1476–1481. [PubMed]
  • 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. [PubMed]
  • Hasegawa M, Hashimoto T. Ribosomal RNA trees misleading? Nature. 1993 Jan 7;361(6407):23–23. [PubMed]
  • Hirt RP, Logsdon JM, Jr, Healy B, Dorey MW, Doolittle WF, Embley TM. 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. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Knoll AH. The early evolution of eukaryotes: a geological perspective. Science. 1992 May 1;256(5057):622–627. [PubMed]
  • Leipe DD, Gunderson JH, Nerad TA, Sogin ML. 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. [PubMed]
  • Lockhart PJ, Larkum AW, Steel M, Waddell PJ, 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. [PMC free article] [PubMed]
  • Lockhart PJ, Steel MA, Barbrook AC, Huson DH, Charleston MA, Howe CJ. A covariotide model explains apparent phylogenetic structure of oxygenic photosynthetic lineages. Mol Biol Evol. 1998 Sep;15(9):1183–1188. [PubMed]
  • Loomis WF, Smith DW. Molecular phylogeny of Dictyostelium discoideum by protein sequence comparison. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9093–9097. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Miyamoto MM, Fitch WM. Testing the covarion hypothesis of molecular evolution. Mol Biol Evol. 1995 May;12(3):503–513. [PubMed]
  • Naylor GJ, Brown WM. Amphioxus mitochondrial DNA, chordate phylogeny, and the limits of inference based on comparisons of sequences. Syst Biol. 1998 Mar;47(1):61–76. [PubMed]
  • Peyretaillade E, Biderre C, Peyret P, Duffieux F, Méténier G, Gouy M, Michot B, Vivarès CP. 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. [PMC free article] [PubMed]
  • Philippe H. MUST, a computer package of Management Utilities for Sequences and Trees. Nucleic Acids Res. 1993 Nov 11;21(22):5264–5272. [PMC free article] [PubMed]
  • Philippe H. Rodent monophyly: pitfalls of molecular phylogenies. J Mol Evol. 1997 Dec;45(6):712–715. [PubMed]
  • 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. [PubMed]
  • Philippe H, Laurent J. How good are deep phylogenetic trees? Curr Opin Genet Dev. 1998 Dec;8(6):616–623. [PubMed]
  • Sogin M l. History assignment: when was the mitochondrion founded? Curr Opin Genet Dev. 1997 Dec;7(6):792–799. [PubMed]
  • Sogin ML, Silberman JD. Evolution of the protists and protistan parasites from the perspective of molecular systematics. Int J Parasitol. 1998 Jan;28(1):11–20. [PubMed]
  • Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science. 1989 Jan 6;243(4887):75–77. [PubMed]
  • Stiller JW, Hall BD. Long-branch attraction and the rDNA model of early eukaryotic evolution. Mol Biol Evol. 1999 Sep;16(9):1270–1279. [PubMed]
  • Tuffley C, Steel M. Modeling the covarion hypothesis of nucleotide substitution. Math Biosci. 1998 Jan 1;147(1):63–91. [PubMed]
  • Woese CR, Fox GE. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5088–5090. [PMC free article] [PubMed]
  • Woese CR, 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. [PubMed]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


  • MedGen
    Related information in MedGen
  • PubMed
    PubMed citations for these articles
  • Substance
    PubChem Substance links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...