• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Mar 1985; 82(6): 1741–1745.
PMCID: PMC397348

Evidence for higher rates of nucleotide substitution in rodents than in man.

Abstract

When the coding regions of 11 genes from rodents (mouse or rat) and man are compared with those from another mammalian species (usually bovine), it is found that rodents evolve significantly faster than man. The ratio of the number of nucleotide substitutions in the rodent lineage to that in the human lineage since their divergence is 2.0 for synonymous substitutions and 1.3 for nonsynonymous substitutions. Rodents also evolve faster in the 5' and 3' untranslated regions of five different mRNAs; the ratios are 2.6 and 3.1, respectively. The numbers of nucleotide substitutions between members of the beta-globin gene family that were duplicated before the man-mouse split are also higher in mouse than in man. The difference is, again, greater for synonymous substitutions than for nonsynonymous substitutions. This tendency is more consistent with the neutralist view of molecular evolution than with the selectionist view. A simple explanation for the higher rates in rodents is that rodents have shorter generation times and, thus, higher mutation rates. The implication of our findings for the study of molecular phylogeny is discussed.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.0M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Wilson AC, Carlson SS, White TJ. Biochemical evolution. Annu Rev Biochem. 1977;46:573–639. [PubMed]
  • Sarich VM, Wilson AC. Immunological time scale for hominid evolution. Science. 1967 Dec 1;158(3805):1200–1203. [PubMed]
  • Laird CD, McConaughy BL, McCarthy BJ. Rate of fixation of nucleotide substitutions in evolution. Nature. 1969 Oct 11;224(5215):149–154. [PubMed]
  • Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. [PubMed]
  • Bell GI, Pictet RL, Rutter WJ, Cordell B, Tischer E, Goodman HM. Sequence of the human insulin gene. Nature. 1980 Mar 6;284(5751):26–32. [PubMed]
  • Lomedico P, Rosenthal N, Efstratidadis A, Gilbert W, Kolodner R, Tizard R. The structure and evolution of the two nonallelic rat preproinsulin genes. Cell. 1979 Oct;18(2):545–558. [PubMed]
  • Kwok SC, Chan SJ, Steiner DF. Cloning and nucleotide sequence analysis of the dog insulin gene. Coded amino acid sequence of canine preproinsulin predicts an additional C-peptide fragment. J Biol Chem. 1983 Feb 25;258(4):2357–2363. [PubMed]
  • Hanauer A, Levin M, Heilig R, Daegelen D, Kahn A, Mandel JL. Isolation and characterization of cDNA clones for human skeletal muscle alpha actin. Nucleic Acids Res. 1983 Jun 11;11(11):3503–3516. [PMC free article] [PubMed]
  • Zakut R, Shani M, Givol D, Neuman S, Yaffe D, Nudel U. Nucleotide sequence of the rat skeletal muscle actin gene. Nature. 1982 Aug 26;298(5877):857–859. [PubMed]
  • Putney SD, Herlihy WC, Schimmel P. A new troponin T and cDNA clones for 13 different muscle proteins, found by shotgun sequencing. Nature. 1983 Apr 21;302(5910):718–721. [PubMed]
  • Miller WL, Eberhardt NL. Structure and evolution of the growth hormone gene family. Endocr Rev. 1983 Spring;4(2):97–130. [PubMed]
  • Fiddes JC, Goodman HM. The gene encoding the common alpha subunit of the four human glycoprotein hormones. J Mol Appl Genet. 1981;1(1):3–18. [PubMed]
  • Godine JE, Chin WW, Habener JF. alpha Subunit of rat pituitary glycoprotein hormones. Primary structure of the precursor determined from the nucleotide sequence of cloned cDNAs. J Biol Chem. 1982 Jul 25;257(14):8368–8371. [PubMed]
  • Nilson JH, Thomason AR, Cserbak MT, Moncman CL, Woychik RP. Nucleotide sequence of a cDNA for the common alpha subunit of the bovine pituitary glycoprotein hormones. Conservation of nucleotides in the 3'-untranslated region of bovine and human pre-alpha subunit mRNAs. J Biol Chem. 1983 Apr 25;258(8):4679–4682. [PubMed]
  • Hudson P, Haley J, John M, Cronk M, Crawford R, Haralambidis J, Tregear G, Shine J, Niall H. Structure of a genomic clone encoding biologically active human relaxin. Nature. 1983 Feb 17;301(5901):628–631. [PubMed]
  • Hudson P, Haley J, Cronk M, Shine J, Niall H. Molecular cloning and characterization of cDNA sequences coding for rat relaxin. Nature. 1981 May 14;291(5811):127–131. [PubMed]
  • Haley J, Hudson P, Scanlon D, John M, Cronk M, Shine J, Tregear G, Niall H. Porcine relaxin: molecular cloning and cDNA structure. DNA. 1982;1(2):155–162. [PubMed]
  • Takahashi H, Hakamata Y, Watanabe Y, Kikuno R, Miyata T, Numa S. Complete nucleotide sequence of the human corticotropin-beta-lipotropin precursor gene. Nucleic Acids Res. 1983 Oct 11;11(19):6847–6858. [PMC free article] [PubMed]
  • Chang AC, Cochet M, Cohen SN. Structural organization of human genomic DNA encoding the pro-opiomelanocortin peptide. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4890–4894. [PMC free article] [PubMed]
  • Uhler M, Herbert E. Complete amino acid sequence of mouse pro-opiomelanocortin derived from the nucleotide sequence of pro-opiomelanocortin cDNA. J Biol Chem. 1983 Jan 10;258(1):257–261. [PubMed]
  • Ellison JW, Berson BJ, Hood LE. The nucleotide sequence of a human immunoglobulin C gamma1 gene. Nucleic Acids Res. 1982 Jul 10;10(13):4071–4079. [PMC free article] [PubMed]
  • Hieter PA, Max EE, Seidman JG, Maizel JV, Jr, Leder P. Cloned human and mouse kappa immunoglobulin constant and J region genes conserve homology in functional segments. Cell. 1980 Nov;22(1 Pt 1):197–207. [PubMed]
  • Honjo T, Obata M, Yamawaki-Katoaka Y, Kataoka T, Kawakami T, Takahashi N, Mano Y. Cloning and complete nucleotide sequence of mouse immunoglobulin gamma 1 chain gene. Cell. 1979 Oct;18(2):559–568. [PubMed]
  • Heidmann O, Rougeon F. Molecular cloning of rabbit gamma heavy chain mRNA. Nucleic Acids Res. 1982 Mar 11;10(5):1535–1545. [PMC free article] [PubMed]
  • Emorine L, Dreher K, Kindt TJ, Max EE. Rabbit immunoglobulin kappa genes: structure of a germline b4 allotype J-C locus and evidence for several b4-related sequences in the rabbit genome. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5709–5713. [PMC free article] [PubMed]
  • Liebhaber SA, Goossens MJ, Kan YW. Cloning and complete nucleotide sequence of human 5'-alpha-globin gene. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7054–7058. [PMC free article] [PubMed]
  • Lawn RM, Efstratiadis A, O'Connell C, Maniatis T. The nucleotide sequence of the human beta-globin gene. Cell. 1980 Oct;21(3):647–651. [PubMed]
  • Nishioka Y, Leder P. The complete sequence of a chromosomal mouse alpha--globin gene reveals elements conserved throughout vertebrate evolution. Cell. 1979 Nov;18(3):875–882. [PubMed]
  • Konkel DA, Maizel JV, Jr, Leder P. The evolution and sequence comparison of two recently diverged mouse chromosomal beta--globin genes. Cell. 1979 Nov;18(3):865–873. [PubMed]
  • Schon EA, Wernke SM, Lingrel JB. Gene conversion of two functional goat alpha-globin genes preserves only minimal flanking sequences. J Biol Chem. 1982 Jun 25;257(12):6825–6835. [PubMed]
  • Schon EA, Cleary ML, Haynes JR, Lingrel JB. Structure and evolution of goat gamma-, beta C- and beta A-globin genes: three developmentally regulated genes contain inserted elements. Cell. 1981 Dec;27(2 Pt 1):359–369. [PubMed]
  • Notake M, Tobimatsu T, Watanabe Y, Takahashi H, Mishina M, Numa S. Isolation and characterization of the mouse corticotropin-beta-lipotropin precursor gene and a related pseudogene. FEBS Lett. 1983 May 30;156(1):67–71. [PubMed]
  • Nakanishi S, Teranishi Y, Watanabe Y, Notake M, Noda M, Kakidani H, Jingami H, Numa S. Isolation and characterization of the bovine corticotropin/beta-lipotropin precursor gene. Eur J Biochem. 1981 Apr;115(3):429–438. [PubMed]
  • Hendy GN, Kronenberg HM, Potts JT, Jr, Rich A. Nucleotide sequence of cloned cDNAs encoding human preproparathyroid hormone. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7365–7369. [PMC free article] [PubMed]
  • Heinrich G, Kronenberg HM, Potts JT, Jr, Habener JF. Gene encoding parathyroid hormone. Nucleotide sequence of the rat gene and deduced amino acid sequence of rat preproparathyroid hormone. J Biol Chem. 1984 Mar 10;259(5):3320–3329. [PubMed]
  • Spritz RA, DeRiel JK, Forget BG, Weissman SM. Complete nucleotide sequence of the human delta-globin gene. Cell. 1980 Oct;21(3):639–646. [PubMed]
  • Slightom JL, Blechl AE, Smithies O. Human fetal G gamma- and A gamma-globin genes: complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes. Cell. 1980 Oct;21(3):627–638. [PubMed]
  • Hansen JN, Konkel DA, Leder P. The sequence of a mouse embryonic beta-globin gene. Evolution of the gene and its signal region. J Biol Chem. 1982 Jan 25;257(2):1048–1052. [PubMed]
  • Baralle FE, Shoulders CC, Proudfoot NJ. The primary structure of the human epsilon-globin gene. Cell. 1980 Oct;21(3):621–626. [PubMed]
  • Hill A, Hardies SC, Phillips SJ, Davis MG, Hutchison CA, 3rd, Edgell MH. Two mouse early embryonic beta-globin gene sequences. Evolution of the nonadult beta-globins. J Biol Chem. 1984 Mar 25;259(6):3739–3747. [PubMed]
  • Efstratiadis A, Posakony JW, Maniatis T, Lawn RM, O'Connell C, Spritz RA, DeRiel JK, Forget BG, Weissman SM, Slightom JL, et al. The structure and evolution of the human beta-globin gene family. Cell. 1980 Oct;21(3):653–668. [PubMed]
  • Czelusniak J, Goodman M, Hewett-Emmett D, Weiss ML, Venta PJ, Tashian RE. Phylogenetic origins and adaptive evolution of avian and mammalian haemoglobin genes. Nature. 1982 Jul 15;298(5871):297–300. [PubMed]
  • Hardison RC. Comparison of the beta-like globin gene families of rabbits and humans indicates that the gene cluster 5'-epsilon-gamma-delta-beta-3' predates the mammalian radiation. Mol Biol Evol. 1984 Sep;1(5):390–410. [PubMed]
  • Fitch WM. 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 RNA's. J Mol Evol. 1980 Dec;16(3-4):153–209. [PubMed]
  • Winter RM, Tuddenham EG, Goldman E, Matthews KB. A maximum likelihood estimate of the sex ratio of mutation rates in haemophilia A. Hum Genet. 1983;64(2):156–159. [PubMed]
  • Miyata T, Yasunaga T, Nishida T. Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7328–7332. [PMC free article] [PubMed]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • Cited in Books
    Cited in Books
    PubMed Central articles cited in books
  • PubMed
    PubMed
    PubMed citations for these articles
  • Substance
    Substance
    PubChem Substance links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...