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MBE Advance Access published online on June 21, 2006

Molecular Biology and Evolution, doi:10.1093/molbev/msl044
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted June 15, 2006

Research Article

Phylum-Wide Analysis of SSU rDNA Reveals Deep Phylogenetic Relationships Among Nematodes and Accelerated Evolution Towards Crown Clades

Martijn Holterman 1 {dagger}, Andre van der Wurff 1 {dagger}, Sven van den Elsen 1 {dagger}, Hanny van Megen 1, Tom Bongers 1, Oleksandr Holovachov 2, Jaap Bakker 1, and Johannes Helder 1 *

1 Laboratory of Nematology, Department of Plant Sciences, Wageningen University, Binnenhaven 5, 6709 PD Wageningen, The Netherlands
2 Department of Zoology, Biology Faculty, Ivan Franko National University, Lviv, Ukraine

* To whom correspondence should be addressed.
Johannes Helder, E-mail: Hans.Helder{at}wur.nl


   Abstract

Inference of evolutionary relationships between nematodes is severely hampered by their conserved morphology, the high frequency of homoplasy, and the scarcity of phylum-wide molecular data. To study the origin of nematode radiation and to unravel the phylogenetic relationships between distantly related species, 339 nearly full length small subunit (SSU) ribosomal DNA sequences were analyzed from a diverse range of nematodes. Bayesian inference revealed a backbone comprising twelve consecutive dichotomies that subdivided the phylum Nematoda into twelve clades. The most basal clade is dominated by the subclass Enoplia, and members of the order Triplonchida occupy positions most close to the common ancestor of the nematodes. Crown clades 8-12 - a group formerly indicated as ‘Secernentea’ that includes Caenorhabditis elegans and virtually all major plant and animal parasites - show significantly higher nucleotide substitution rates than the more basal clades 1-7. Accelerated substitution rates are associated with parasitic lifestyles (clade 8 and 12) or short generation times (clade 9-11). The relatively high substitution rates in the distal clades resulted in numerous autapomorphies that allow in most cases DNA barcode-based species identification. Teratocephalus, a genus comprising terrestrial bacterivores, was shown to be most close to the starting point of ‘Secernentean’ radiation. Notably, fungal feeding nematodes were exclusively found basal to or as sister taxon next to the three groups of plant parasitic nematodes, namely Trichodoridae, Longidoridae and Tylenchomorpha. The exclusive common presence of fungivorous and plant parasitic nematodes supports a longstanding hypothesis saying that plant parasitic nematodes arose from fungivorous ancestors.

Keywords: nematode evolution; SSU rDNA; accelerated evolution.

{dagger}MH, AvdW and SvdE contributed equally to this work.


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