MBE Advance Access originally published online on December 5, 2003
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Mol. Biol. Evol. 21(3):443-453. 2004
DOI: 10.1093/molbev/msh031
© 2004 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038
Evolution of Interacting Proteins in the Mitochondrial Electron Transport System in a Marine Copepod
* Department of Biology, University of North Carolina, Chapel Hill
Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla
E-mail: willett4{at}email.unc.edu.
The extensive interaction between mitochondrial-encoded and nuclear-encoded subunits of electron transport system (ETS) enzymes in mitochondria is expected to lead to intergenomic coadaptation. Whether this coadaptation results from adaptation to the environment or from fixation of deleterious mtDNA mutations followed by compensatory nuclear gene evolution is unknown. The intertidal copepod Tigriopus californicus shows extreme divergence in mtDNA sequence and provides an excellent model system for study of intergenomic coadaptation. Here, we examine genes encoding subunits of complex III of the ETS, including the mtDNA-encoded cytochrome b (CYTB), the nuclear-encoded rieske iron-sulfur protein (RISP), and cytochrome c1 (CYC1). We compare levels of polymorphism within populations and divergence between populations in these genes to begin to untangle the selective forces that have shaped evolution in these genes. CYTB displays dramatic divergence between populations, but sequence analysis shows no evidence for positive selection driving this divergence. CYC1 and RISP have lower levels of sequence divergence between populations than CYTB, but, again, sequence analysis gives no evidence for positive selection acting on them. However, an examination of variation at cytochrome c (CYC), a nuclear-encoded protein that transfers electrons between complex III and complex IV provides evidence for selective divergence. Hence, it appears that rapid evolution in mitochondrial-encoded subunits is not always associated with rapid divergence in interacting subunits (CYC1 and RISP), but can be in some cases (CYC). Finally, a comparison of nuclear-encoded and mitochondrial-encoded genes from T. californicus suggests that substitution rates in the mitochondrial-encoded genes are dramatically increased relative to nuclear genes.
Key Words: mitochondrial DNA evolution • ubiquinol-cytochrome c reductase • cytochrome c1 • rieske iron-sulfur protein • cytochrome b • Tigriopus californicus
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