Skip Navigation


MBE Advance Access originally published online on March 19, 2004
This Article
Right arrow Full Text Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow Supplementary Material
Right arrow All Versions of this Article:
21/7/1340    most recent
msh130v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (45)
Right arrowRequest Permissions
Google Scholar
Right arrow Articles by Inagaki, Y.
Right arrow Articles by Roger, A. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Inagaki, Y.
Right arrow Articles by Roger, A. J.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

Mol. Biol. Evol. 21(7):1340-1349. 2004
DOI: 10.1093/molbev/msh130
© 2004 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038

Research Article

Covarion Shifts Cause a Long-Branch Attraction Artifact That Unites Microsporidia and Archaebacteria in EF-1{alpha} Phylogenies

Yuji Inagaki*,{ddagger}, Edward Susko{dagger},{ddagger}, Naomi M. Fast{ddagger},§ and Andrew J. Roger*

* Program in Evolutionary Biology, Canadian Institute for Advanced Research and Genome Atlantic, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia, Canada
{dagger} Department of Bioscience, Nagahama Institute of Bioscience and Technology, 1266 Tamura, Nagahama, Shiga 526-0829, Japan
{ddagger} Department ofMathematics and Statistics and Genome Atlantic, Dalhousie University, Halifax, Nova Scotia, Canada
§ Departmentof Botany, University of British Columbia, Vancouver, British Columbia, Canada

E-mail: yinagai{at}dal.ca.

Abstract

Microsporidia branch at the base of eukaryotic phylogenies inferred from translation elongation factor 1{alpha} (EF-1{alpha}) sequences. Because these parasitic eukaryotes are fungi (or close relatives of fungi), it is widely accepted that fast-evolving microsporidian sequences are artifactually "attracted" to the long branch leading to the archaebacterial (outgroup) sequences ("long-branch attraction," or "LBA"). However, no previous studies have explicitly determined the reason(s) why the artifactual allegiance of microsporidia and archaebacteria ("M + A") is recovered by all phylogenetic methods, including maximum likelihood, a method that is supposed to be resistant to classical LBA. Here we show that the M + A affinity can be attributed to those alignment sites associated with large differences in evolutionary site rates between the eukaryotic and archaebacterial subtrees. Therefore, failure to model the significant evolutionary rate distribution differences (covarion shifts) between the ingroup and outgroup sequences is apparently responsible for the artifactual basal position of microsporidia in phylogenetic analyses of EF-1{alpha} sequences. Currently, no evolutionary model that accounts for discrete changes in the site rate distribution on particular branches is available for either protein or nucleotide level phylogenetic analysis, so the same artifacts may affect many other "deep" phylogenies. Furthermore, given the relative similarity of the site rate patterns of microsporidian and archaebacterial EF-1{alpha} proteins ("parallel site rate variation"), we suggest that the microsporidian orthologs may have lost some eukaryotic EF-1{alpha}–specific nontranslational functions, exemplifying the extreme degree of reduction in this parasitic lineage.

Key Words: phylogenetic artifact • long-branch attraction • EF-1{alpha} • microsporidia • covarion model • parallel site rate variation


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 Proc. Natl. Acad. Sci. USAHome page
C. J. Cox, P. G. Foster, R. P. Hirt, S. R. Harris, and T. M. Embley
The archaebacterial origin of eukaryotes
PNAS, December 23, 2008; 105(51): 20356 - 20361.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
N. Gruenheit, P. J. Lockhart, M. Steel, and W. Martin
Difficulties in Testing for Covarion-Like Properties of Sequences under the Confounding Influence of Changing Proportions of Variable Sites
Mol. Biol. Evol., July 1, 2008; 25(7): 1512 - 1520.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
B. Kolaczkowski and J. W. Thornton
A Mixed Branch Length Model of Heterotachy Improves Phylogenetic Accuracy
Mol. Biol. Evol., June 1, 2008; 25(6): 1054 - 1066.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
D. E. Wildman, M. Uddin, J. C. Opazo, G. Liu, V. Lefort, S. Guindon, O. Gascuel, L. I. Grossman, R. Romero, and M. Goodman
Genomics, biogeography, and the diversification of placental mammals
PNAS, September 4, 2007; 104(36): 14395 - 14400.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
L. M. F. Merlo, M. Lunzer, and A. M. Dean
An empirical test of the concomitantly variable codon hypothesis
PNAS, June 26, 2007; 104(26): 10938 - 10943.
[Abstract] [Full Text] [PDF]

Home page
 Syst BiolHome page
V. Ruano-Rubio and M. A. Fares
Artifactual Phylogenies Caused by Correlated Distribution of Substitution Rates among Sites and Lineages: The Good, the Bad, and the Ugly
Syst Biol, February 1, 2007; 56(1): 68 - 82.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
H.-C. Wang, M. Spencer, E. Susko, and A. J. Roger
Testing for Covarion-like Evolution in Protein Sequences
Mol. Biol. Evol., January 1, 2007; 24(1): 294 - 305.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
K. Shalchian-Tabrizi, M. Skanseng, F. Ronquist, D. Klaveness, T. R. Bachvaroff, C. F. Delwiche, A. Botnen, T. Tengs, and K. S. Jakobsen
Heterotachy Processes in Rhodophyte-Derived Secondhand Plastid Genes: Implications for Addressing the Origin and Evolution of Dinoflagellate Plastids
Mol. Biol. Evol., August 1, 2006; 23(8): 1504 - 1515.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
G. Baele, J. Raes, Y. Van de Peer, and S. Vansteelandt
An Improved Statistical Method for Detecting Heterotachy in Nucleotide Sequences
Mol. Biol. Evol., July 1, 2006; 23(7): 1397 - 1405.
[Abstract] [Full Text] [PDF]

Home page
 Phil Trans R Soc BHome page
T Martin Embley
Multiple secondary origins of the anaerobic lifestyle in eukaryotes
Phil Trans R Soc B, June 29, 2006; 361(1470): 1055 - 1067.
[Abstract] [Full Text] [PDF]

Home page
 Phil Trans R Soc BHome page
A. J Roger and L. A Hug
The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation
Phil Trans R Soc B, June 29, 2006; 361(1470): 1039 - 1054.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
A. G. B. Simpson, Y. Inagaki, and A. J. Roger
Comprehensive Multigene Phylogenies of Excavate Protists Reveal the Evolutionary Positions of "Primitive" Eukaryotes
Mol. Biol. Evol., March 1, 2006; 23(3): 615 - 625.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
P. Lockhart, P. Novis, B. G. Milligan, J. Riden, A. Rambaut, and T. Larkum
Heterotachy and Tree Building: A Case Study with Plastids and Eubacteria
Mol. Biol. Evol., January 1, 2006; 23(1): 40 - 45.
[Abstract] [Full Text] [PDF]

Home page
 Syst BiolHome page
P. Lockhart and M. Steel
A Tale of Two Processes
Syst Biol, December 1, 2005; 54(6): 948 - 951.
[Full Text] [PDF]

Home page
 Mol Biol EvolHome page
S. R. Gadagkar and S. Kumar
Maximum Likelihood Outperforms Maximum Parsimony Even When Evolutionary Rates Are Heterotachous
Mol. Biol. Evol., November 1, 2005; 22(11): 2139 - 2141.
[Abstract] [Full Text] [PDF]

Home page
 Syst BiolHome page
H. Brinkmann, M. van der Giezen, Y. Zhou, G. P. de Raucourt, and H. Philippe
An Empirical Assessment of Long-Branch Attraction Artefacts in Deep Eukaryotic Phylogenomics
Syst Biol, October 1, 2005; 54(5): 743 - 757.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
M. J. Buck and W. R. Atchley
Networks of Coevolving Sites in Structural and Functional Domains of Serpin Proteins
Mol. Biol. Evol., July 1, 2005; 22(7): 1627 - 1634.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
E. Belda, A. Moya, and F. J. Silva
Genome Rearrangement Distances and Gene Order Phylogeny in {gamma}-Proteobacteria
Mol. Biol. Evol., June 1, 2005; 22(6): 1456 - 1467.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
H. Philippe, N. Lartillot, and H. Brinkmann
Multigene Analyses of Bilaterian Animals Corroborate the Monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia
Mol. Biol. Evol., May 1, 2005; 22(5): 1246 - 1253.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
M. Spencer, E. Susko, and A. J. Roger
Likelihood, Parsimony, and Heterogeneous Evolution
Mol. Biol. Evol., May 1, 2005; 22(5): 1161 - 1164.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
N. Arisue, M. Hasegawa, and T. Hashimoto
Root of the Eukaryota Tree as Inferred from Combined Maximum Likelihood Analyses of Multiple Molecular Sequence Data
Mol. Biol. Evol., March 1, 2005; 22(3): 409 - 420.
[Abstract] [Full Text] [PDF]

Home page
 Syst BiolHome page
K. Roelants and F. Bossuyt
Archaeobatrachian Paraphyly and Pangaean Diversification of Crown-Group Frogs
Syst Biol, February 1, 2005; 54(1): 111 - 126.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
P. J. Keeling and Y. Inagaki
A class of eukaryotic GTPase with a punctate distribution suggesting multiple functional replacements of translation elongation factor 1{alpha}
PNAS, October 26, 2004; 101(43): 15380 - 15385.
[Abstract] [Full Text] [PDF]


Disclaimer: Please note that abstracts for content published before 1996 were created through digital scanning and may therefore not exactly replicate the text of the original print issues. All efforts have been made to ensure accuracy, but the Publisher will not be held responsible for any remaining inaccuracies. If you require any further clarification, please contact our Customer Services Department.