MBE Advance Access published online on October 5, 2007
Molecular Biology and Evolution, doi:10.1093/molbev/msm212
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Research Article |
Multiple Origins and Rapid Evolution of Duplicated Mitochondrial Genes in Parthenogenetic Geckos (Heteronotia binoei; Squamata, Gekkonidae)
1 Department of Integrative Biology, University of California, Berkeley, CA 94720
2 Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720
3 Joint Genome Institute and Lawrence Berkeley National Laboratory, Walnut Creek, CA 94598
4 Genome Project Solutions, Hercules, CA 94547
* Corresponding Author: Matthew K. Fujita, Museum of Vertebrate Zoology, University of California, 3101 Valley Life Sciences Building, Berkeley, CA 94720, phone: (510) 642-7928, fax: (510) 643-8238, mkfujita{at}berkeley.edu
Received for publication May 30, 2007. Revision received August 28, 2007. Revision received September 25, 2007. Accepted for publication September 26, 2007.
Accumulating evidence for alternative gene orders demonstrates that vertebrate mitochondrial genomes are more evolutionarily dynamic than previously thought. Several lineages of parthenogenetic lizards contain large, tandem duplications that include rRNA, tRNA, and protein-coding genes, as well as the control region. Such duplications are hypothesized as intermediate stages in gene rearrangement, but the early stages of their evolution have not been previously studied. To better understand the evolutionary dynamics of duplicated segments of mitochondrial DNA, we sequenced 10 mitochondrial genomes from recently-formed (
300,000 years ago) hybrid parthenogenetic geckos of the Heteronotia binoei complex, and one from a sexual form. These genomes included some with an arrangement typical of vertebrates and others with tandem duplications varying in size from 5.7 kb to 9.4 kb, each with different gene contents and duplication endpoints. These results, together with phylogenetic analyses, indicate independent and frequent origins of the duplications. Small, direct repeats at the duplication endpoints imply slipped-strand error as a mechanism generating the duplications, as opposed to a false initiation/termination of DNA replication mechanism that has been invoked to explain duplications in other lizard mitochondrial systems. Despite their recent origin, there is evidence for non-functionalization of genes due primarily to deletions, and the observed pattern of gene disruption supports the duplication-deletion model for rearrangement of mtDNA gene order. Conversely, the accumulation of mutations between these recent duplicates provides no evidence for gene conversion, as has been reported in some other systems. These results demonstrate that, despite their long term stasis in gene content and arrangement in some lineages, vertebrate mitochondrial genomes can be evolutionary dynamic even at short timescales.
Key Words: mitochondrial genome • mtDNA • molecular evolution • Heteronotia • tandem duplication • parthenogenesis
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