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Molecular Evolution of Cytochrome c Oxidase in High-Performance Fish (Teleostei: Scombroidei)

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Abstract

The 13 peptides encoded by vertebrate mitochondrial DNA (mtDNA) are essential subunits of oxidative phosphorylation (OXPHOS) enzymes. These genes normally experience purifying selection and also coevolve with nuclear-encoded subunits of OXPHOS complexes. However, the role of positive selection on mtDNA evolution is still unclear, as most examples of intergenomic coevolution appear to be the result of compensation by nuclear-encoded genes for mildly deleterious mtDNA mutations, and not simultaneous positive selection in both genomes. Organisms that have experienced strong selective pressures to increase aerobic capacity or adapt to changes in thermal environment may be better candidates in which to examine the impact of positively selected changes on mtDNA evolution. The tuna (suborder Scombroidei, family Scombridae) and billfish (suborder Scombroidei, families Xiphiidae and Istiophoridae) are highly aerobic fish with multiple specializations in muscle energetics, including a high mitochondrial content and regional endothermy. We examined the role of positively selected mtDNA substitutions in the production of these unique phenotypes. Focusing on a catalytic subunit of cytochrome c oxidase (COX II), we found that the rate ratio of nonsynonymous (d N ; amino acid changing)-to-synonymous (d S ; silent) substitutions was not increased in lineages leading to the tuna but was significantly increased in the lineage preceding the billfish. Furthermore, there are a number of individual positively selected sites that, when mapped onto the COX crystal structure, appear to interact with other COX subunits and may affect OXPHOS function and regulation in billfish.

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Notes

  1. All residues are numbered according to bovine COX and positively selected sites detected by PAML are identified by the amino acid present in billfish.

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Acknowledgments

We thank N. Fragoso, R. Brill (NMFS), M. Musyl (JIMAR), and Dr. T. M. Orrell of the NMFS/NOAA Systematics Laboratory (Smithsonian Institution, Washington, DC) for their assistance in providing samples and Dr. M. Miya for advice on compatible primer pairs. This work was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant (C.D.M.) and postgraduate scholarship (A.C.D.) and made possible by a research program funded by the Pelagic Fisheries Research Program (PFRP).

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  1. Department of Biology, Queen’s University, Kingston, Ontario, K7L 3N6, Canada

    Anne C. Dalziel, Christopher D. Moyes, Emma Fredriksson & Stephen C. Lougheed

  2. Department of Zoology, 6270 University Boulevard, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    Anne C. Dalziel

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  1. Anne C. Dalziel
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Correspondence to Anne C. Dalziel.

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Dalziel, A.C., Moyes, C.D., Fredriksson, E. et al. Molecular Evolution of Cytochrome c Oxidase in High-Performance Fish (Teleostei: Scombroidei). J Mol Evol 62, 319–331 (2006). https://doi.org/10.1007/s00239-005-0110-7

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