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MBE Advance Access published online on November 10, 2004
Molecular Biology and Evolution, doi:10.1093/molbev/msi047
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved
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Accepted November 2, 2004

Research Article

Evolution of Duplicate Control Regions in the Mitochondrial Genomes of Metazoa: A Case Study with Australasian Ixodes Ticks

Renfu Shao 1*, Stephen C. Barker 2 *, Harumi Mitani 3, Yayoi Aoki 3, and Masahito Fukunaga 3 *

1 Department of Microbiology and Parasitology, and Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, 4072, Australia; Faculty of Pharmacy and Pharmaceutical Sciences, Fukuyama University, Fukuyama, Hiroshima 729-0292, Japan
2 Department of Microbiology and Parasitology, and Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, 4072, Australia
3 Faculty of Pharmacy and Pharmaceutical Sciences, Fukuyama University, Fukuyama, Hiroshima 729-0292, Japan

* To whom correspondence should be addressed.
Renfu Shao, E-mail: r.shao{at}uq.edu.au


  Abstract

To investigate the evolution pattern and phylogenetic utility of duplicate control regions (CRs) in mitochondrial (mt) genomes, we sequenced the entire mt genomes of three Ixodes species and part of the mt genomes of another 11 species. All the species from the Australasian lineage have duplicate CRs whereas the other species have one CR. Sequence analyses indicate that the two CRs of the Australasian Ixodes ticks have evolved in concert in each species. In addition to the Australasian Ixodes ticks, species from seven other lineages of metazoa also have mt genomes with duplicate CRs. Accumulated mtDNA sequence data from these metazoans and two recent experiments on replication of mt genomes in human cell lines with duplicate CRs allowed us to re-examine four intriguing questions about the presence of duplicate CRs in the mt genomes of metazoa: (1) why do some mt genomes, but not others, have duplicate CRs; (2) how did mt genomes with duplicate CRs evolve; (3) how could the nucleotide sequences of duplicate CRs remain identical or very similar over evolutionary time; and (4) are duplicate CRs phylogenetic markers? It appears that mt genomes with duplicate CRs have a selective advantage in replication over mt genomes with one CR. Tandem duplication followed by deletion of genes is the most plausible mechanism for the generation of mt genomes with duplicate CRs. Once duplicate CRs occur in a mt genome, they tend to evolve in concert, probably by gene conversion. However, there are lineages where gene conversion may not always occur and thus the two CRs may evolve independently in these lineages. Duplicate CRs have much potential as phylogenetic markers at low taxonomic levels such as within genera, within families or among families, but not at high taxonomic levels such as among orders.

Keywords: concerted evolution; duplicate control regions; gene rearrangement; Ixodes ticks.

*These authors contributed equally.


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