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MBE Advance Access published online on March 19, 2004
Molecular Biology and Evolution, doi:10.1093/molbev/msh130
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved
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Accepted February 27, 2004
© 2004 Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved.

Original Articles

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

Yuji Inagaki 1*, Edward Susko 2, Naomi M. Fast 3, and Andrew J. Roger 1

1 Program in Evolutionary Biology, Canadian Institute for Advanced Research and Genome Atlantic, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia, B3H 1X5, Canada
2 Department of Mathematics and Statistics and Genome Atlantic, Dalhousie University, Halifax, Nova Scotia, B3H 3J5, Canada
3 Department of Botany, University of British Colombia, Vancouver, British Colombia, V6T 1Z4, Canada

* To whom correspondence should be addressed. 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. Since 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 rates between the eukaryotic and archaebacterial sub-trees. 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 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 orthologues may have lost some eukaryotic EF-1{alpha}-specific non-translational 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


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