• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. May 2003; 164(1): 259–268.
PMCID: PMC1462550

Is the rate of insertion and deletion mutation male biased?: Molecular evolutionary analysis of avian and primate sex chromosome sequences.

Abstract

The rate of mutation for nucleotide substitution is generally higher among males than among females, likely owing to the larger number of DNA replications in spermatogenesis than in oogenesis. For insertion and deletion (indel) mutations, data from a few human genetic disease loci indicate that the two sexes may mutate at similar rates, possibly because such mutations arise in connection with meiotic crossing over. To address origin- and sex-specific rates of indel mutation we have conducted the first large-scale molecular evolutionary analysis of indels in noncoding DNA sequences from sex chromosomes. The rates are similar on the X and Y chromosomes of primates but about twice as high on the avian Z chromosome as on the W chromosome. The fact that indels are not uncommon on the nonrecombining Y and W chromosomes excludes meiotic crossing over as the main cause of indel mutation. On the other hand, the similar rates on X and Y indicate that the number of DNA replications (higher for Y than for X) is also not the main factor. Our observations are therefore consistent with a role of both DNA replication and recombination in the generation of short insertion and deletion mutations. A significant excess of deletion compared to insertion events is observed on the avian W chromosome, consistent with gradual DNA loss on a nonrecombining chromosome.

Full Text

The Full Text of this article is available as a PDF (91K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Baumer A, Dutly F, Balmer D, Riegel M, Tükel T, Krajewska-Walasek M, Schinzel AA. High level of unequal meiotic crossovers at the origin of the 22q11. 2 and 7q11.23 deletions. Hum Mol Genet. 1998 May;7(5):887–894. [PubMed]
  • Bohossian HB, Skaletsky H, Page DC. Unexpectedly similar rates of nucleotide substitution found in male and female hominids. Nature. 2000 Aug 10;406(6796):622–625. [PubMed]
  • Carmichael AN, Fridolfsson AK, Halverson J, Ellegren H. Male-biased mutation rates revealed from Z and W chromosome-linked ATP synthase alpha-subunit (ATP5A1) sequences in birds. J Mol Evol. 2000 May;50(5):443–447. [PubMed]
  • Comeron JM, Kreitman M. The correlation between intron length and recombination in drosophila. Dynamic equilibrium between mutational and selective forces. Genetics. 2000 Nov;156(3):1175–1190. [PMC free article] [PubMed]
  • Crow JF. The high spontaneous mutation rate: is it a health risk? Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8380–8386. [PMC free article] [PubMed]
  • Crow JF. A new study challenges the current belief of a high human male:female mutation ratio. Trends Genet. 2000 Dec;16(12):525–526. [PubMed]
  • Crow JF. The origins, patterns and implications of human spontaneous mutation. Nat Rev Genet. 2000 Oct;1(1):40–47. [PubMed]
  • Ebersberger Ingo, Metzler Dirk, Schwarz Carsten, Päbo Svante. Genomewide comparison of DNA sequences between humans and chimpanzees. Am J Hum Genet. 2002 Jun;70(6):1490–1497. [PMC free article] [PubMed]
  • Ellegren Hans. Human mutation--blame (mostly) men. Nat Genet. 2002 May;31(1):9–10. [PubMed]
  • Ellegren H, Fridolfsson AK. Male-driven evolution of DNA sequences in birds. Nat Genet. 1997 Oct;17(2):182–184. [PubMed]
  • Graur D, Shuali Y, Li WH. Deletions in processed pseudogenes accumulate faster in rodents than in humans. J Mol Evol. 1989 Apr;28(4):279–285. [PubMed]
  • Grimm T, Meng G, Liechti-Gallati S, Bettecken T, Müller CR, Müller B. On the origin of deletions and point mutations in Duchenne muscular dystrophy: most deletions arise in oogenesis and most point mutations result from events in spermatogenesis. J Med Genet. 1994 Mar;31(3):183–186. [PMC free article] [PubMed]
  • Hurst LD, Ellegren H. Sex biases in the mutation rate. Trends Genet. 1998 Nov;14(11):446–452. [PubMed]
  • Kahn NW, Quinn TW. Male-driven evolution among Eoaves? A test of the replicative division hypothesis in a heterogametic female (ZW) system. J Mol Evol. 1999 Dec;49(6):750–759. [PubMed]
  • Ketterling RP, Vielhaber EL, Lind TJ, Thorland EC, Sommer SS. The rates and patterns of deletions in the human factor IX gene. Am J Hum Genet. 1994 Feb;54(2):201–213. [PMC free article] [PubMed]
  • Kumar S, Tamura K, Jakobsen IB, Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics. 2001 Dec;17(12):1244–1245. [PubMed]
  • Kunkel TA. Misalignment-mediated DNA synthesis errors. Biochemistry. 1990 Sep 4;29(35):8003–8011. [PubMed]
  • Kunkel TA, Bebenek K. DNA replication fidelity. Annu Rev Biochem. 2000;69:497–529. [PubMed]
  • Kunkel TA, Soni A. Mutagenesis by transient misalignment. J Biol Chem. 1988 Oct 15;263(29):14784–14789. [PubMed]
  • Lázaro C, Gaona A, Ainsworth P, Tenconi R, Vidaud D, Kruyer H, Ars E, Volpini V, Estivill X. Sex differences in mutational rate and mutational mechanism in the NF1 gene in neurofibromatosis type 1 patients. Hum Genet. 1996 Dec;98(6):696–699. [PubMed]
  • Petrov DA. Evolution of genome size: new approaches to an old problem. Trends Genet. 2001 Jan;17(1):23–28. [PubMed]
  • Petrov DA, Hartl DL. High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. Mol Biol Evol. 1998 Mar;15(3):293–302. [PubMed]
  • López Correa C, Brems H, Lázaro C, Marynen P, Legius E. Unequal meiotic crossover: a frequent cause of NF1 microdeletions. Am J Hum Genet. 2000 Jun;66(6):1969–1974. [PMC free article] [PubMed]
  • Petrov DA, Hartl DL. Patterns of nucleotide substitution in Drosophila and mammalian genomes. Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1475–1479. [PMC free article] [PubMed]
  • Makova Kateryna D, Li Wen-Hsiung. Strong male-driven evolution of DNA sequences in humans and apes. Nature. 2002 Apr 11;416(6881):624–626. [PubMed]
  • Petrov DA, Sangster TA, Johnston JS, Hartl DL, Shaw KL. Evidence for DNA loss as a determinant of genome size. Science. 2000 Feb 11;287(5455):1060–1062. [PubMed]
  • Miyata T, Hayashida H, Kuma K, Mitsuyasu K, Yasunaga T. Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harb Symp Quant Biol. 1987;52:863–867. [PubMed]
  • Saitou N, Ueda S. Evolutionary rates of insertion and deletion in noncoding nucleotide sequences of primates. Mol Biol Evol. 1994 May;11(3):504–512. [PubMed]
  • Montell H, Fridolfsson AK, Ellegren H. Contrasting levels of nucleotide diversity on the avian Z and W sex chromosomes. Mol Biol Evol. 2001 Nov;18(11):2010–2016. [PubMed]
  • Shimmin LC, Chang BH, Li WH. Male-driven evolution of DNA sequences. Nature. 1993 Apr 22;362(6422):745–747. [PubMed]
  • Mol MJ, Stuyt PM, Stalenhoef AF. Effectiviteit en veiligheid van simvastatine, een nieuw cholesterolverlagend geneesmiddel. Ned Tijdschr Geneeskd. 1989 Feb 18;133(7):362–366. [PubMed]
  • Nachman MW, Crowell SL. Estimate of the mutation rate per nucleotide in humans. Genetics. 2000 Sep;156(1):297–304. [PMC free article] [PubMed]
  • Osheroff WP, Beard WA, Yin S, Wilson SH, Kunkel TA. Minor groove interactions at the DNA polymerase beta active site modulate single-base deletion error rates. J Biol Chem. 2000 Sep 8;275(36):28033–28038. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • MedGen
    MedGen
    Related information in MedGen
  • Nucleotide
    Nucleotide
    Published Nucleotide sequences
  • PubMed
    PubMed
    PubMed citations for these articles

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...