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Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster

Abstract

TWO genomic regions with unusally low recombination rates inDrosophila melanogaster have normal levels of divergence but greatly reduced nucleotide diversity1,2, apparently resulting from the fixation of advantageous mutations and the associated hitchhiking effect3,4. Here we show that for 20 gene regions from across the genome, the amount of nucleotide diversity in natural populations of D. melanogaster is positively correlated with the regional rate of recombination. This cannot be explained by variation in mutation rates and/or functional constraint, because we observe no correlation between recombination rates and DNA sequence divergence between D. melanogaster and its sibling species, D. simulans. We suggest that the correlation may result from genetic hitch-hiking associated with the fixation of advantageous mutants. Hitch-hiking thus seems to occur over a large fraction of the Drosophilagenome and may constitute a major constraint on levels of genetic variation in nature.

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References

  1. Begun, D. J. & Aquadro, C. F. Genetics 129, 1147–1158 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Berry, A. J., Ajioka, J. W. & Kreitman, M. Genetics 129, 1111–1117 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Maynard Smith, J. & Haigh, J. Genet. Res. 23, 23–35 (1974).

    Article  Google Scholar 

  4. Kaplan, N. L., Hudson, R. R. & Langley, C. H. Genetics 123, 887–899 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Nei, M. Molecular Evolutionary Genetics (Columbia Univ. Press, 1987).

    Google Scholar 

  6. Lindsley, D. L. & Sandler, L. Phil. Trans. R. Soc B. 277, 295–312 (1977).

    Article  CAS  Google Scholar 

  7. Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, 1983).

    Book  Google Scholar 

  8. Tajima, F. Genetics 125, 447–454 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Hudson, R. R. Theor. Populat. Biol. 23, 183–201 (1983).

    Article  CAS  Google Scholar 

  10. Birky, C. W. Jr & Walsh, J. B. Proc. natn. Acad. Sci. U.S.A. 85, 6414–6418 (1988).

    Article  ADS  CAS  Google Scholar 

  11. McDonald, J. H. & Kreitman, M. Nature 351, 652–654 (1991).

    Article  ADS  CAS  PubMed  Google Scholar 

  12. Aguadé, M., Miyashita, N. & Langley, C. H. Molec. Biol. Evol. 6, 123–130 (1988).

    Google Scholar 

  13. Miyashita, N. & Langley, C. H. Genetics 120, 199–212 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Schaeffer, S. W., Aquadro, C. F. & Langley, C. H. Molec. Biol. Evol. 5, 30–40 (1988).

    CAS  PubMed  Google Scholar 

  15. Langley, C. H. in Population Biology of Genes and Molecules (eds Takahata, N. & Crow, J. F.) 75–91 (Baifukan, Japan).

  16. Eanes, W. F., Ajioka, J. W., Hey, J. & Wesley, C. Molec. Biol. Evol. 6, 384–397 (1989).

    CAS  PubMed  Google Scholar 

  17. Takano, T. S., Kusakabe, S. & Mukai, T. Genetics 129, 753–761 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Langley, C. H., Montgomery, E. & Quattlebaum, W. F. Proc. natn. Acad. Sci. U.S.A. 79, 5631–5635 (1982).

    Article  ADS  CAS  Google Scholar 

  19. Aquadro, C. F., Deese, S. F., Bland, M. M., Langley, C. H. & Laurie-Ahlberg, C. C. Genetics 114, 1165–1190 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Langley, C. H. et al. Genetics 119, 619–629 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Game, A. Y. & Oakeshott, J. G. Genetics 126, 1021–1031 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Lange, B. W., Langley, C. H. & Stephan, W. Genetics 126, 921–932 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Leigh Brown, A. J. Proc. natn. Acad. Sci. U.S.A. 80, 5350–5354 (1983).

    Article  ADS  Google Scholar 

  24. Leigh Brown, A. J. & Ish-Horowitz, D. Nature 290, 677–682 (1981).

    Article  ADS  CAS  PubMed  Google Scholar 

  25. Aquadro, C. F., Lado, K. M. & Noon, W. A. Genetics 119, 875–888 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Ashburner, M. Drosophila Genetic Maps (Drosophila Information Service 69, 1991).

    Google Scholar 

  27. Lindsley, D. L. & Grell, E. H. Genetic Variations of Drosophila melanogaster (Carnegie Institute, Washington DC, 1967).

    Google Scholar 

  28. Sousa, V. Chromosome Maps of Drosophila (CRC, Boca Raton, Florida, 1988).

    Google Scholar 

  29. Merriam, J., Ashburner, M., Hartl, D. L. & Kafatos, F. C. Science 254, 221–225 (1991).

    Article  ADS  CAS  PubMed  Google Scholar 

  30. Hochman, B. in Genetics and Biology of Drosophila Vol. 1b (eds Ashburner, M. & Novitski, E.) 903–928 (Academic, New York, 1976).

    Google Scholar 

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Begun, D., Aquadro, C. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356, 519–520 (1992). https://doi.org/10.1038/356519a0

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