Journal of Molecular Evolution

, Volume 43, Issue 1, pp 32–40

On transition bias in mitochondrial genes of pocket gophers

  • Xuhua Xia
  • Mark S. Hafner
  • Philip D. Sudman
Article

Abstract

The relative contribution of mutation and purifying selection to transition bias has not been quantitatively assessed in mitochondrial protein genes. The observed transition/transversion (s/v) ratio is (μsPs)/(μvPv), where μs and μv denote mutation rate of transitions and transversions, respectively, andPs andPv denote fixation probabilities of transitions and transversions, respectively. Because selection against synonymous transitions can be assumed to be roughly equal to that against synonymous transversions,Ps/Pv ≈ 1 at fourfold degenerate sites, so that thes/v ratio at fourfold degenerate sites is approximately μsv, which is a measure of mutational contribution to transition bias. Similarly, thes/v ratio at nondegenerate sites is also an estimate of μsv if we assume that selection against nonsynonymous transitions is roughly equal to that against nonsynonymous transversions. In two mitochondrial genes, cytochrome oxidase subunit I (COI) and cytochromeb (cyt-b) in pocket gophers, thes/v ratio is about two at nondegenerate and fourfold degenerate sites for both the COI and the cyt-b genes. This implies that mutation contribution to transition bias is relatively small. In contrast, thes/v ratio is much greater at twofold degenerate sites, being 48 for COI and 40 for cyt-b. Given that the μsv ratio is about 2, thePs/Pv ratio at twofold degenerate sites must be on the order of 20 or greater. This suggests a great effect of purifying selection on transition bias in mitochondrial protein genes because transitions are synonymous and transversions are nonsynonymous at twofold degenerate sites in mammalian mitochondrial genes. We also found that nonsynonymous mutations at twofold degenerate sites are more neutral than nonsynonymous mutations at nondegenerate sites, and that the COI gene is subject to stronger purifying selection than is the cyt-b gene. A model is presented to integrate the effect of purifying selection, codon bias, DNA repair and GC content ons/v ratio of protein-coding genes.

Key words

Transition bias Mitochondrial protein gene Purifying selection Molecular evolution 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aquadro CF, Greenberg BD (1983) Human mitochondrial DNA variation and evolution: analysis of nucleotide sequences from seven individuals. Genetics 103:287–312PubMedGoogle Scholar
  2. Bechkenbach AT, Thomas WK, Homayoun S (1990) Intraspecific sequence variation in the mitochondrial genome of rainbow trout (Oncorhynchus mykiss). Genome 33:13–15Google Scholar
  3. Brown WM (1985) The mitochondrial genome of animals. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum Press, New York, p 95Google Scholar
  4. Brown GG, Simpson MV (1982) Novel features of animal mtDNA evolution as shown by sequences of two rate cytochrome oxidase subunit II genes. Proc Natl Acad Sci USA 79:3246–3250PubMedGoogle Scholar
  5. Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: the tempo and mode of evolution. J Mol Evol 18:225–239CrossRefPubMedGoogle Scholar
  6. Curtis SE, Clegg MT (1984) Molecular evolution of chloroplast DNA sequences. Mol Biol Evol 1:291–301PubMedGoogle Scholar
  7. DeSalle R Freedman T, Prager EM, Wilston AC (1987) Tempo and mode of sequence evolution in mitochondrial DNA of HawaiianDrosophila. J Mol Evol 26:157–164CrossRefPubMedGoogle Scholar
  8. DeWalt TS, Sudman PD, Hafner MS, Davis SK (1993) Phylogenetic relationship of pocket gophers (Cratogeomys andPappogeomys) based on mitochondrial DNA cytochrome b sequences. Mol Phylogen Evol 2:193–204Google Scholar
  9. Edwards SV, Wilson AC (1990) Phylogenetically informative length polymorphisms and sequence variability in mitochondrial DNA of Australian songbirds (Pomatostomus). Genetics 126:695–711PubMedGoogle Scholar
  10. Felsenstein J (1993) PHYLIP 3.5 (phylogeny inference package). Department of Genetics, University of Washington, SeattleGoogle Scholar
  11. Fitch W (1980) Estimating the total number of nucleotide substitutions since the common ancestor of a pair of homologous genes: comparison of several methods and three beta hemoglobin messenger RNAs. J Mol Evol 16:153–209CrossRefPubMedGoogle Scholar
  12. Gojobori T, Li WH, Graur D (1982) Patterns of nucleotide substitution in pseudogenes and functional genes. J Mol Evol 18:360–369PubMedGoogle Scholar
  13. Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11: 725–736PubMedGoogle Scholar
  14. Grantham R (1974) Amino acid difference formula to help explain protein evolution. Science 185:862–864PubMedGoogle Scholar
  15. Hafner MS, Sudman PD, Villablanca FX, Spradling TA, Demastes JW, Nadler SA (1994) Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265:1087–1090PubMedGoogle Scholar
  16. Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144PubMedGoogle Scholar
  17. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, CambridgeGoogle Scholar
  18. Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 31:151–160CrossRefGoogle Scholar
  19. Li WH (1993) Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36:96–99PubMedGoogle Scholar
  20. Li WH, Wu CI, Luo CH (1984) Nonrandomness of point mutation as reflected in nucleotide substitutions and its evolutionary implications. J Mol Evol 21:58–71CrossRefPubMedGoogle Scholar
  21. Li WH, Wu CI, Luo CH (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2:150–174PubMedGoogle Scholar
  22. Miyata T, Miyazawa S, Yasunaga T (1979) Two types of amino acid substitution in protein evolution. J Mol Evol 12:219–236CrossRefPubMedGoogle Scholar
  23. Myers KA, Raffhill R, O'Conner PJ (1988) Repair of alkylated purines in the hepatic DNA of mitochondria and nuclei in the rat. Carcinogenesis 9:285–292PubMedGoogle Scholar
  24. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  25. SAS Institute (1994) SAS/STAT User's guide, version 6, 4th ed, vol 1. p 222Google Scholar
  26. Satta Y, Ishiwa H, Chigusa SI (1987) Analysis of nucleotide substitutions of mitochondrial DNAs inDrosophila melanogaster and its sibling species. Mol Biol Evol 4:638–650PubMedGoogle Scholar
  27. Satoh MS, Huh N, Rajewsky MF, Turoki T (1988) Enzymatic removal of O-ethylguanine from mitochondrial DNA in rat tissues exposed to N-ethyl-N-nitrosoureain vivo. J Biol Chem 263:6854–6856PubMedGoogle Scholar
  28. Swofford DL (1993) Phylogenetic analysis using parsimony (PAUP), version 3.2. University of Illinois, ChampaignGoogle Scholar
  29. Thomas WK, Beckenbach AT (1989) Variation in Salmonid mitochondrial DNA: evolutionary constraints and mechanisms of substitution. J Mol Evol 29:233–245CrossRefPubMedGoogle Scholar
  30. Thomas WK, Wilson AC (1991) Mode and tempo of molecular evolution in the nematodeCaenorhabditis: cytochrome oxidase II and calmodulin sequences. Genetics 128:269–279PubMedGoogle Scholar
  31. Thomas WK, Maa J, Wilson AC (1989) Shifting constraints on tRNA genes during mitochondrial DNA evolution in animals. New Biol 1:93–100PubMedGoogle Scholar
  32. van Ooyen A, van den Berg J, Mantel N, Weissmann C (1979) Comparison of total sequence of a cloned rabbit β-globin gene and its flanking regions with a homologous mouse sequence. Science 206: 337–344PubMedGoogle Scholar
  33. Vogel F, Kopun M (1977) Higher frequencies of transitions among point mutations. J Mol Evol 9:159–180PubMedGoogle Scholar
  34. Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058PubMedGoogle Scholar
  35. Yang Z (1994) Maximum likelihood phlogenetic estimation from DNA sequences with variable rates over sites: approximately methods. J Mol Evol 39:306–314PubMedGoogle Scholar
  36. Yang Z (1995) Phylogenetic analysis by maximum likelihood (PAML), version 1.1. Institute of Molecular Evolutionary Genetics, The Pennsylvania State UniversityGoogle Scholar

Copyright information

© Springer-Verlag New York Inc 1996

Authors and Affiliations

  • Xuhua Xia
    • 1
  • Mark S. Hafner
    • 1
    • 2
  • Philip D. Sudman
    • 1
  1. 1.Museum of Natural ScienceLouisiana State UniversityBaton RougeUSA
  2. 2.Department of Zoology and PhysiologyLouisiana State UniversityBaton RougeUSA
  3. 3.Department of BiologyUniversity of South DakotaVermilionUSA

Personalised recommendations