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Comparative Genomics of Drosophila mtDNA: Novel Features of Conservation and Change Across Functional Domains and Lineages

Abstract

To gain insight on mitochondrial DNA (mtDNA) evolution, we assembled and analyzed the mitochondrial genomes of Drosophila erecta, D. ananassae, D. persimilis, D. willistoni, D. mojavensis, D. virilis and D. grimshawi together with the sequenced mtDNAs of the melanogaster subgroup. Genomic comparisons across the well-defined Drosophila phylogeny impart power for detecting conserved mtDNA regions that maintain metabolic function and regions that evolve uniquely on lineages. Evolutionary rate varies across intergenic regions of the mtDNA. Rapidly evolving intergenic regions harbor the majority of mitochondrial indel divergence. In contrast, patterns of nearly perfect conservation within intergenic regions reveal a refined set of nucleotides underlying the binding of transcription termination factors. Sequencing of 5′ cDNA ends indicates that cytochrome C oxidase I (CoI) has a novel (T/C)CG start codon and that perfectly conserved regions upstream of two NADH dehydrogenase (ND) genes are transcribed and likely extend these protein sequences. Substitutions at synonymous sites in the Drosophila mitochondrial proteomes reflect a mutation process that is biased toward A and T nucleotides and differs between mtDNA strands. Differences in codon usage bias across genes reveal that weak selection at silent sites may offset the mutation bias. The mutation-selection balance at synonymous sites has also diverged between the Drosophila and Sophophora lineages. Rates of evolution are highly heterogeneous across the mitochondrial proteome, with ND accumulating many more amino acid substitutions than CO. These oxidative phosphorylation complex-specific rates of evolution vary across lineages and may reflect physiological and ecological change across the Drosophila phylogeny.

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Acknowledgments

The authors gratefully acknowledge constructive discussion with the fly genomics community at large, as well as specific input from Brian Bettencourt, Rob Haney, Rob Kulathinal and Colin Meiklejohn and helpful comments from anonymous reviewers. The shotgun sequence data reported in this manuscript were generated by the Drosophila 12 Genomes Consortium. This work was supported by National Institutes of Health grants GM067862 to DMR and GM076812 to KLM and a Summer Research Fellowship to DMR in the Bay Paul Center for Comparative Molecular Biology and Evolution at the Marine Biological Laboratories.

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Correspondence to Kristi L. Montooth.

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Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. EU189427-189434 and TPA: BK006335-006341.

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Montooth, K.L., Abt, D.N., Hofmann, J.W. et al. Comparative Genomics of Drosophila mtDNA: Novel Features of Conservation and Change Across Functional Domains and Lineages. J Mol Evol 69, 94 (2009). https://doi.org/10.1007/s00239-009-9255-0

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Keywords

  • Comparative genomics
  • Codon bias
  • Drosophila
  • mtDNA
  • Oxidative phosphorylation
  • tRNA evolution