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MBE Advance Access published online on October 8, 2008

Molecular Biology and Evolution, doi:10.1093/molbev/msn222
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© The Author 2008. 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

Research Article

Timing of Genome Duplications Relative to the Origin of the Vertebrates: Did Cyclostomes Diverge before, or after?

Shigehiro Kuraku1,2,§, Axel Meyer2 and Shigeru Kuratani1

1 Laboratory for Evolutionary Morphology, RIKEN Center for Developmental Biology, Kobe, Japan
2 Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, 78457 Konstanz, Germany

§ Corresponding author: Shigehiro Kuraku; tel, +49-7531-88-2763; fax, +49-7531-88-3018; email, shigehiro.kuraku{at}uni-konstanz.de

Received for publication May 26, 2008. Revision received August 23, 2008. Accepted for publication September 27, 2008.

Two rounds of whole genome duplications are thought to have played an important role in the establishment of gene repertoires in vertebrates. These events occurred during chordate evolution after the split of the urochordate and cephalochordate lineages, but before the radiation of extant gnathostomes (jawed vertebrates). During this interval, diverse agnathans (jawless fishes), including cyclostomes (hagfishes and lampreys), diverged. However, there is no solid evidence for the timing of these genome duplications in relation to the divergence of cyclostomes from the gnathostome lineage. We conducted cDNA sequencing in diverse early vertebrates for members of homeobox-containing (Dlx and ParaHox) and other gene families that would serve as landmarks for genome duplications. Including these new sequences, we performed a molecular phylogenetic census using the maximum-likelihood method for 55 gene families. In most of these gene families, we detected many more gene duplications before the cyclostome–gnathostome split, than after. Many of these gene families (for example. visual opsins, RAR, Notch) have multiple paralogs in conserved, syntenic genomic regions that must have been generated by large-scale duplication events. Taken together, this indicates that the genome duplications occurred before the cyclostome–gnathostome split. We propose that the redundancy in gene repertoires possessed by all vertebrates, including hagfishes and lampreys, were introduced primarily by genome duplications. Apart from subsequent lineage-specific modifications, these ancient genome duplication events might serve generally to distinguish vertebrates from invertebrates at the genomic level.

Key Words: hagfish • lamprey • genome duplication • 2R-hypothesis • conserved synteny


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