Liang ZHAO, Xingtao ZHANG, Xingkui TAO, Weiwei WANG, Ming LI. Preliminary analysis of the mitochondrial genome evolutionary pattern in primates. Zoological Research, 2012, 33(E3-4): 47-56. doi: 10.3724/SP.J.1141.2012.E03-04E47
Citation: Liang ZHAO, Xingtao ZHANG, Xingkui TAO, Weiwei WANG, Ming LI. Preliminary analysis of the mitochondrial genome evolutionary pattern in primates. Zoological Research, 2012, 33(E3-4): 47-56. doi: 10.3724/SP.J.1141.2012.E03-04E47

Preliminary analysis of the mitochondrial genome evolutionary pattern in primates

doi: 10.3724/SP.J.1141.2012.E03-04E47
Funds:  This project was supported by the National Basic Research Program of China (973 Program: 2007CB411600), the Natural Science Foundation of China (30630016; 30570292)
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  • Author Bio:

    Liang ZHAO

  • Corresponding author: Ming LI
  • Received Date: 2012-01-19
  • Rev Recd Date: 2012-06-27
  • Publish Date: 2012-08-10
  • Since the birth of molecular evolutionary analysis, primates have been a central focus of study and mitochondrial DNA is well suited to these endeavors because of its unique features. Surprisingly, to date no comprehensive evaluation of the nucleotide substitution patterns has been conducted on the mitochondrial genome of primates. Here, we analyzed the evolutionary patterns and evaluated selection and recombination in the mitochondrial genomes of 44 Primates species downloaded from GenBank. The results revealed that a strong rate heterogeneity occurred among sites and genes in all comparisons. Likewise, an obvious decline in primate nucleotide diversity was noted in the subunit rRNAs and tRNAs as compared to the protein-coding genes. Within 13 protein-coding genes, the pattern of nonsynonymous divergence was similar to that of overall nucleotide divergence, while synonymous changes differed only for individual genes, indicating that the rate heterogeneity may result from the rate of change at nonsynonymous sites. Codon usage analysis revealed that there was intermediate codon usage bias in primate protein-coding genes, and supported the idea that GC mutation pressure might determine codon usage and that positive selection is not the driving force for the codon usage bias. Neutrality tests using site-specific positive selection from a Bayesian framework indicated no sites were under positive selection for any gene, consistent with near neutrality. Recombination tests based on the pairwise homoplasy test statistic supported complete linkage even for much older divergent primate species. Thus, with the exception of rate heterogeneity among mitochondrial genes, evaluating the validity assumed complete linkage and selective neutrality in primates prior to phylogenetic or phylogeographic analysis seems unnecessary.
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  • [1]
    Ballard JWO. 2000. Comparative genomics of mitochondrial DNA in Drosophila simulans [J]. J Mol Evol, 51(1): 64-75.
    Brown WM, George M Jr, Wilson AC. 1979. Rapid evolution of animal mitochondrial DNA [J]. Proc Natl Acad Sci USA, 76(4): 1967-1971.
    Brown WM, Prager EM, Wang A, Wilson AC. 1982. Mitochondrial DNA sequences of primates: tempo and mode of evolution [J]. J Mol Evol, 18(4): 225-239.
    Bruen TC, Philippe H, Bryant D. 2006. A simple and robust statistical test for detecting the presence of recombination [J]. Genetics, 172(4): 2665-2681.
    Bulmer M. 1991. The selection-mutation-drift theory of synonymous codon usage [J]. Genetics, 129(3): 897-907.
    Duret L. 2000. tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes [J]. Trends Genet, 16(7): 287-289.
    Duret L. 2002. Evolution of synonymous codon usage in metazoans [J]. Curr Opin Genet Dev, 12(6): 640-649.
    Elson JL, Turnbull DM, Howell N. 2004. Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection [J]. Am J Hum Genet, 74(2): 229-238.
    Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap [J]. Evolution, 39(4): 783-791.
    Galtier N, Enard D, Radondy Y, Bazin E, Belkhir K. 2006. Mutation hot spots in mammalian mitochondrial DNA [J]. Genome Res, 16(2): 215-222.
    García-Martínez J, Castro JA, Ramón MR, Latorre A, Moya A. 1998. Mitochondrial DNA haplotype frequencies in natural and experimental populations of Drosophila subobscura [J]. Genetics, 149(3): 1377-1382.
    Goodarzi H, Torabi N, Najafabadi HS, Archetti M. 2008. Amino acid and codon usage profiles: adaptive changes in the frequency of amino acids and codons [J]. Gene, 407(1-2): 30-41.
    Gray MW, Burger G, Lang BF. 1999. Mitochondrial evolution [J]. Science, 283(5407): 1476-1481.
    Hasegawa M, Cao Y, Yang Z. 1998. Preponderance of slightly deleterious polymorphism in mitochondrial DNA: nonsynonymous/ synonymous rate ratio is much higher within species than between species [J]. Mol Biol Evol, 15(11): 1499-1505.
    Hill WG, Robertson A. 1968. Linkage disequilibrium in finite populations [J]. Theor Appl Genet, 38(6): 226-231.
    Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees [J]. Bioinformatics, 17(8): 754-755.
    Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies [J]. Mol Biol Evol, 23(2): 254-267.
    Ihaka R, Gentleman R. 1996. R: A language for data analysis and graphics [J]. J Comput Graph Stat, 5(3): 299-314.
    Kanaya S, Yamada Y, Kinouchi M, Kudo Y, Ikemura T. 2001. Codon usage and tRNA genes in eukaryotes: correlation of codon usage diversity with translation efficiency and with CG-dinucleotide usage as assessed by multivariate analysis [J]. J Mol Evol, 53(4-5): 290-298.
    Kelly JK. 1997. A test of neutrality based on interlocus associations [J]. Genetics, 146(3): 1197-1206.
    Kumazawa Y, Azuma Y, Nishida M. 2004. Tempo of mitochondrial gene evolution: Can mitochondrial DNA be used to date old divergences? [J]. Endocytobiosis Cell Res, 15(1): 136-142.
    Marshall HD, Coulson MW, Carr SM. 2009. Near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in Atlantic Cod (Gadus morhua) and other gadine fish [J]. Mol Biol Evol, 26(3): 579-589.
    Meunier J, Duret L. 2004. Recombination drives the evolution of GC-content in the human genome [J]. Mol Biol Evol, 21(6): 984-990.
    Morton BR. 1993. Chloroplast DNA codon use: evidence for selection at the psb A locus based on tRNA availability [J]. J Mol Evol, 37(3): 273-280.
    Nachman MW, Brown WM, Stoneking M, Aquadro CF. 1996. Nonneutral mitochondrial DNA variation in humans and chimpanzees [J]. Genetics, 142(3): 953-963.
    Nei M, Kumar S. 2000. Molecular Evolution and Phylogenetics [M]. New York: Oxford University Press.
    Nielsen R, Yang Z. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene [J]. Genetics, 148(3): 929-936.
    Ohta T. 1973. Slightly deleterious mutant substitutions in evolution [J]. Nature, 246(5428): 96-98.
    Pesole G, Gissi C, De Chirico A, Saccone C. 1999. Nucleotide substitution rate of mammalian mitochondrial genomes [J]. J Mol Evol, 48(4): 427-434.
    Piganeau G, Gardner M, Eyre-Walker A. 2004. A broad survey of recombination in animal mitochondria [J]. Mol Biol Evol, 21(12): 2319-2325.
    Powell JR, Moriyama EN. 1997. Evolution of codon usage bias in Drosophila [J]. Proc Natl Acad Sci USA, 94(15): 7784-7790.
    Prat Y, Fromer M, Linial N, Linial M. 2009. Codon usage is associated with the evolutionary age of genes in metazoan genomes [J]. BMC Evol Biol, 9(1): 285.
    Rand DM, Dorfsman M, Kann LM. 1994. Neutral and non-neutral evolution of drosophila mitochondrial DNA [J]. Genetics, 138(3): 741-756.
    Ronquist F, Huelsenbeck JP. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models [J]. Bioinformatics, 19(12): 1572-1574.
    Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods [J]. Bioinformatics, 19(18): 2496-2497.
    Saccone C, Gissi C, Lanave C, Larizza A, Pesole G, Reyes A. 2000. Evolution of the mitochondrial genetic system: an overview [J]. Gene, 261(1): 153-159.
    Schierup MH, Hein J. 2000. Consequences of recombination on traditional phylogenetic analysis [J]. Genetics, 156(2): 879-891.
    Schmidt HA, Strimmer K, Vingron M, von Haeseler A. 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing [J]. Bioinformatics, 18(3): 502-504.
    Sharp PM, Averof M, Lloyd AT, Matassi G, Peden JF. 1995. DNA sequence evolution: the sounds of silence [J]. Philos Trans R Soc Lond B Biol Sci, 349(1329): 241-247.
    Subramanian S. 2008. Nearly neutrality and the evolution of codon usage bias in eukaryotic genomes [J]. Genetics, 178(4): 2429-2432.
    Swofford DL. 2002. PAUP*. Phylogenetic analysis using parsimony. (*and other methods), Version 4.0b10. Sunderland, Massachusetts: Sinauer Associates.
    Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0 [J]. Mol Biol Evol, 24(8): 1596-1599.
    Templeton AR. 1996. Contingency tests of neutrality using intra/interspecfic gene trees: the rejection of neutrality for the evolution of the mitochondrial cytochrome xidase II gene in the hominoid primates [J]. Genetics, 144(3): 1263-1270.
    Thyagarajan B, Padua RA, Campbell C. 1996. Mammalian mitochondria possess homologous DNA recombination activity [J]. J Biol Chem, 271(44): 27536-27543.
    Tsaousis AD, Martin DP, Ladoukakis ED, Posada D, Zouros E. 2005. Widespread recombination in published animal mtDNA sequences [J]. Mol Biol Evol, 22(4): 925-933.
    Wilson AC, Cann RL, Carr SM, George M, Gyllensten UB, Helm-Bychowski KM, Higuchi RG, Palumbi SR, Prager EM, Sage RD, Stoneking M. 1985. Mitochondrial DNA and two perspectives on evolutionary genetics [J]. Biol Linn Soc, 26(4): 375-400.
    Wright F. 1990. The 'effective number of codons' used in a gene [J]. Gene, 87(1): 23-29.

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