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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Jan 18;91(2):827–831. doi: 10.1073/pnas.91.2.827

Weak male-driven molecular evolution in rodents.

B H Chang 1, L C Shimmin 1, S K Shyue 1, D Hewett-Emmett 1, W H Li 1
PMCID: PMC43042  PMID: 8290607

Abstract

In humans and rodents the male-to-female ratio of mutation rate (alpha m) has been suggested to be extremely large, so that the process of nucleotide substitution is almost completely male-driven. However, our sequence data from the last intron of the X chromosome-linked (Zfx) and Y chromosome-linked (Zfy) zinc finger protein genes suggest that alpha m is only approximately 2 in rodents with a 95% confidence interval from 1 to 3. Moreover, from published data on oogenesis and spermatogenesis we estimate the male-to-female ratio of the number of germ cell divisions per generation to be approximately 2 in rodents, confirming our estimate of alpha m and suggesting that errors in DNA replication are the primary source of mutation. As the estimated alpha m for rodents is only one-third of our previous estimate of approximately 6 for higher primates, there appear to be generation-time effects--i.e., alpha m decreases with decreasing generation time.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bulmer M. Neighboring base effects on substitution rates in pseudogenes. Mol Biol Evol. 1986 Jul;3(4):322–329. doi: 10.1093/oxfordjournals.molbev.a040401. [DOI] [PubMed] [Google Scholar]
  2. Clermont Y. Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev. 1972 Jan;52(1):198–236. doi: 10.1152/physrev.1972.52.1.198. [DOI] [PubMed] [Google Scholar]
  3. Ellsworth D. L., Rittenhouse K. D., Honeycutt R. L. Artifactual variation in randomly amplified polymorphic DNA banding patterns. Biotechniques. 1993 Feb;14(2):214–217. [PubMed] [Google Scholar]
  4. Hayashida H., Kuma K., Miyata T. Interchromosomal gene conversion as a possible mechanism for explaining divergence patterns of ZFY-related genes. J Mol Evol. 1992 Aug;35(2):181–183. doi: 10.1007/BF00183228. [DOI] [PubMed] [Google Scholar]
  5. Huckins C. The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat Rec. 1971 Mar;169(3):533–557. doi: 10.1002/ar.1091690306. [DOI] [PubMed] [Google Scholar]
  6. Li W. H., Tanimura M., Sharp P. M. An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol. 1987;25(4):330–342. doi: 10.1007/BF02603118. [DOI] [PubMed] [Google Scholar]
  7. Li W. H., Wu C. I., Luo C. C. Nonrandomness of point mutation as reflected in nucleotide substitutions in pseudogenes and its evolutionary implications. J Mol Evol. 1984;21(1):58–71. doi: 10.1007/BF02100628. [DOI] [PubMed] [Google Scholar]
  8. Mardon G., Luoh S. W., Simpson E. M., Gill G., Brown L. G., Page D. C. Mouse Zfx protein is similar to Zfy-2: each contains an acidic activating domain and 13 zinc fingers. Mol Cell Biol. 1990 Feb;10(2):681–688. doi: 10.1128/mcb.10.2.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Mardon G., Mosher R., Disteche C. M., Nishioka Y., McLaren A., Page D. C. Duplication, deletion, and polymorphism in the sex-determining region of the mouse Y chromosome. Science. 1989 Jan 6;243(4887):78–80. doi: 10.1126/science.2563173. [DOI] [PubMed] [Google Scholar]
  10. Mardon G., Page D. C. The sex-determining region of the mouse Y chromosome encodes a protein with a highly acidic domain and 13 zinc fingers. Cell. 1989 Mar 10;56(5):765–770. doi: 10.1016/0092-8674(89)90680-6. [DOI] [PubMed] [Google Scholar]
  11. 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. doi: 10.1101/sqb.1987.052.01.094. [DOI] [PubMed] [Google Scholar]
  12. Pamilo P., Bianchi N. O. Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol Biol Evol. 1993 Mar;10(2):271–281. doi: 10.1093/oxfordjournals.molbev.a040003. [DOI] [PubMed] [Google Scholar]
  13. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  14. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Shimmin L. C., Chang B. H., Hewett-Emmett D., Li W. H. Potential problems in estimating the male-to-female mutation rate ratio from DNA sequence data. J Mol Evol. 1993 Aug;37(2):160–166. doi: 10.1007/BF02407351. [DOI] [PubMed] [Google Scholar]
  16. Shimmin L. C., Chang B. H., Li W. H. Male-driven evolution of DNA sequences. Nature. 1993 Apr 22;362(6422):745–747. doi: 10.1038/362745a0. [DOI] [PubMed] [Google Scholar]
  17. Tajima F., Nei M. Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol. 1984 Apr;1(3):269–285. doi: 10.1093/oxfordjournals.molbev.a040317. [DOI] [PubMed] [Google Scholar]
  18. Vogel F., Rathenberg R. Spontaneous mutation in man. Adv Hum Genet. 1975;5:223–318. doi: 10.1007/978-1-4615-9068-2_4. [DOI] [PubMed] [Google Scholar]
  19. Winter R. M., Tuddenham E. G., Goldman E., Matthews K. B. A maximum likelihood estimate of the sex ratio of mutation rates in haemophilia A. Hum Genet. 1983;64(2):156–159. doi: 10.1007/BF00327115. [DOI] [PubMed] [Google Scholar]
  20. Wolfe K. H., Sharp P. M., Li W. H. Mutation rates differ among regions of the mammalian genome. Nature. 1989 Jan 19;337(6204):283–285. doi: 10.1038/337283a0. [DOI] [PubMed] [Google Scholar]
  21. Wu C. I., Li W. H. Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1741–1745. doi: 10.1073/pnas.82.6.1741. [DOI] [PMC free article] [PubMed] [Google Scholar]

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