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. 2004 Apr;166(4):1783–1794. doi: 10.1534/genetics.166.4.1783

Nucleotide variation and recombination along the fourth chromosome in Drosophila simulans.

Wen Wang 1, Kevin Thornton 1, J J Emerson 1, Manyuan Long 1
PMCID: PMC1470817  PMID: 15126398

Abstract

The fourth chromosome of Drosophila melanogaster and its sister species are believed to be nonrecombining and have been a model system for testing predictions of the effects of selection on linked, neutral variation. We recently examined nucleotide variation along the chromosome of D. melanogaster and revealed that a low average level of recombination could be associated with considerably high levels of nucleotide variation. In this report, we further investigate the variation along the fourth chromosome of D. simulans. We sequenced 12 gene regions evenly distributed along the fourth chromosome for a worldwide collection of 11 isofemale lines and 5 gene regions in a local population of 10 isofemale lines from South America. In contrast to predictions for regions of very low recombination, these data reveal that the variation levels in many gene regions, including an intron region of the ci gene, vary considerably along the fourth chromosome. Nucleotide diversity ranged from 0.0010 to 0.0074 in 9 gene regions interspersed with several regions of greatly reduced variation. Tests of recombination indicate that the recombination level is not as low as previously thought, likely an order of magnitude higher than that in D. melanogaster. Finally, estimates of the recombination parameters are shown to support a crossover-plus-conversion model.

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Selected References

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  1. Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
  2. Aguade M., Miyashita N., Langley C. H. Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics. 1989 Jul;122(3):607–615. doi: 10.1093/genetics/122.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aguadé M., Meyers W., Long A. D., Langley C. H. Single-strand conformation polymorphism analysis coupled with stratified DNA sequencing reveals reduced sequence variation in the su(s) and su(wa) regions of the Drosophila melanogaster X chromosome. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4658–4662. doi: 10.1073/pnas.91.11.4658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Aguadé M., Miyashita N., Langley C. H. Restriction-map variation at the zeste-tko region in natural populations of Drosophila melanogaster. Mol Biol Evol. 1989 Mar;6(2):123–130. doi: 10.1093/oxfordjournals.molbev.a040538. [DOI] [PubMed] [Google Scholar]
  5. Andolfatto P. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 2001 Mar;18(3):279–290. doi: 10.1093/oxfordjournals.molbev.a003804. [DOI] [PubMed] [Google Scholar]
  6. Andolfatto P., Przeworski M. A genome-wide departure from the standard neutral model in natural populations of Drosophila. Genetics. 2000 Sep;156(1):257–268. doi: 10.1093/genetics/156.1.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Begun D. J., Aquadro C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. doi: 10.1038/356519a0. [DOI] [PubMed] [Google Scholar]
  8. Begun D. J., Whitley P. Reduced X-linked nucleotide polymorphism in Drosophila simulans. Proc Natl Acad Sci U S A. 2000 May 23;97(11):5960–5965. doi: 10.1073/pnas.97.11.5960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Berry A. J., Ajioka J. W., Kreitman M. Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics. 1991 Dec;129(4):1111–1117. doi: 10.1093/genetics/129.4.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Betancourt Andrea J., Presgraves Daven C. Linkage limits the power of natural selection in Drosophila. Proc Natl Acad Sci U S A. 2002 Oct 7;99(21):13616–13620. doi: 10.1073/pnas.212277199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Braverman J. M., Hudson R. R., Kaplan N. L., Langley C. H., Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. doi: 10.1093/genetics/140.2.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Charlesworth B. Background selection and patterns of genetic diversity in Drosophila melanogaster. Genet Res. 1996 Oct;68(2):131–149. doi: 10.1017/s0016672300034029. [DOI] [PubMed] [Google Scholar]
  13. Charlesworth B., Langley C. H., Sniegowski P. D. Transposable element distributions in Drosophila. Genetics. 1997 Dec;147(4):1993–1995. doi: 10.1093/genetics/147.4.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Charlesworth D., Charlesworth B., Morgan M. T. The pattern of neutral molecular variation under the background selection model. Genetics. 1995 Dec;141(4):1619–1632. doi: 10.1093/genetics/141.4.1619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dvorák J., Luo M. C., Yang Z. L. Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing aegilops species. Genetics. 1998 Jan;148(1):423–434. doi: 10.1093/genetics/148.1.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Frisse L., Hudson R. R., Bartoszewicz A., Wall J. D., Donfack J., Di Rienzo A. Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. Am J Hum Genet. 2001 Aug 29;69(4):831–843. doi: 10.1086/323612. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Grell R. F. Heat-induced exchange in the fourth chromosome of diploid females of Drosophila melanogaster. Genetics. 1971 Dec;69(4):523–527. doi: 10.1093/genetics/69.4.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hawley R. S., McKim K. S., Arbel T. Meiotic segregation in Drosophila melanogaster females: molecules, mechanisms, and myths. Annu Rev Genet. 1993;27:281–317. doi: 10.1146/annurev.ge.27.120193.001433. [DOI] [PubMed] [Google Scholar]
  19. Hilliker A. J., Harauz G., Reaume A. G., Gray M., Clark S. H., Chovnick A. Meiotic gene conversion tract length distribution within the rosy locus of Drosophila melanogaster. Genetics. 1994 Aug;137(4):1019–1026. doi: 10.1093/genetics/137.4.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hudson R. R., Kaplan N. L. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 1985 Sep;111(1):147–164. doi: 10.1093/genetics/111.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hudson R. R., Kreitman M., Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. doi: 10.1093/genetics/116.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hudson R. R. Two-locus sampling distributions and their application. Genetics. 2001 Dec;159(4):1805–1817. doi: 10.1093/genetics/159.4.1805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jensen Mark A., Charlesworth Brian, Kreitman Martin. Patterns of genetic variation at a chromosome 4 locus of Drosophila melanogaster and D. simulans. Genetics. 2002 Feb;160(2):493–507. doi: 10.1093/genetics/160.2.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kaplan N. L., Hudson R. R., Langley C. H. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. doi: 10.1093/genetics/123.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kreitman M., Hudson R. R. Inferring the evolutionary histories of the Adh and Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. Genetics. 1991 Mar;127(3):565–582. doi: 10.1093/genetics/127.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kreitman M. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature. 1983 Aug 4;304(5925):412–417. doi: 10.1038/304412a0. [DOI] [PubMed] [Google Scholar]
  27. Langley C. H., Lazzaro B. P., Phillips W., Heikkinen E., Braverman J. M. Linkage disequilibria and the site frequency spectra in the su(s) and su(w(a)) regions of the Drosophila melanogaster X chromosome. Genetics. 2000 Dec;156(4):1837–1852. doi: 10.1093/genetics/156.4.1837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Locke J., Podemski L., Aippersbach N., Kemp H., Hodgetts R. A physical map of the polytenized region (101EF-102F) of chromosome 4 in Drosophila melanogaster. Genetics. 2000 Jul;155(3):1175–1183. doi: 10.1093/genetics/155.3.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nachman M. W. Patterns of DNA variability at X-linked loci in Mus domesticus. Genetics. 1997 Nov;147(3):1303–1316. doi: 10.1093/genetics/147.3.1303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nachman M. W. Single nucleotide polymorphisms and recombination rate in humans. Trends Genet. 2001 Sep;17(9):481–485. doi: 10.1016/s0168-9525(01)02409-x. [DOI] [PubMed] [Google Scholar]
  31. Nordborg M., Charlesworth B., Charlesworth D. The effect of recombination on background selection. Genet Res. 1996 Apr;67(2):159–174. doi: 10.1017/s0016672300033619. [DOI] [PubMed] [Google Scholar]
  32. Patterson J. T., Muller H. J. Are "Progressive" Mutations Produced by X-Rays? Genetics. 1930 Nov;15(6):495–577. doi: 10.1093/genetics/15.6.495f. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Podemski L., Ferrer C., Locke J. Whole arm inversions of chromosome 4 in Drosophila species. Chromosoma. 2001 Aug;110(4):305–312. doi: 10.1007/s004120100151. [DOI] [PubMed] [Google Scholar]
  34. Rozas J., Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. doi: 10.1093/bioinformatics/15.2.174. [DOI] [PubMed] [Google Scholar]
  35. Sandler L., Szauter P. The effect of recombination-defective meiotic mutants on fourth-chromosome crossing over in Drosophila melanogaster. Genetics. 1978 Dec;90(4):699–712. doi: 10.1093/genetics/90.4.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sheldahl Lea A., Weinreich Daniel M., Rand David M. Recombination, dominance and selection on amino acid polymorphism in the Drosophila genome: contrasting patterns on the X and fourth chromosomes. Genetics. 2003 Nov;165(3):1195–1208. doi: 10.1093/genetics/165.3.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Simonsen K. L., Churchill G. A., Aquadro C. F. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics. 1995 Sep;141(1):413–429. doi: 10.1093/genetics/141.1.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  39. Sun F. L., Cuaycong M. H., Craig C. A., Wallrath L. L., Locke J., Elgin S. C. The fourth chromosome of Drosophila melanogaster: interspersed euchromatic and heterochromatic domains. Proc Natl Acad Sci U S A. 2000 May 9;97(10):5340–5345. doi: 10.1073/pnas.090530797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. True J. R., Mercer J. M., Laurie C. C. Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics. 1996 Feb;142(2):507–523. doi: 10.1093/genetics/142.2.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wall Jeffrey D., Andolfatto Peter, Przeworski Molly. Testing models of selection and demography in Drosophila simulans. Genetics. 2002 Sep;162(1):203–216. doi: 10.1093/genetics/162.1.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wang W., Zhang J., Alvarez C., Llopart A., Long M. The origin of the Jingwei gene and the complex modular structure of its parental gene, yellow emperor, in Drosophila melanogaster. Mol Biol Evol. 2000 Sep;17(9):1294–1301. doi: 10.1093/oxfordjournals.molbev.a026413. [DOI] [PubMed] [Google Scholar]
  44. Wang Wen, Brunet Frédéric G., Nevo Eviatar, Long Manyuan. Origin of sphinx, a young chimeric RNA gene in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2002 Mar 19;99(7):4448–4453. doi: 10.1073/pnas.072066399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wiuf C., Hein J. The coalescent with gene conversion. Genetics. 2000 May;155(1):451–462. doi: 10.1093/genetics/155.1.451. [DOI] [PMC free article] [PubMed] [Google Scholar]

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