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. 2001 Jul;158(3):1147–1155. doi: 10.1093/genetics/158.3.1147

DNA variation at the rp49 gene region of Drosophila simulans: evolutionary inferences from an unusual haplotype structure.

J Rozas 1, M Gullaud 1, G Blandin 1, M Aguadé 1
PMCID: PMC1461709  PMID: 11454763

Abstract

An approximately 1.3-kb region including the rp49 gene plus its 5' and 3' flanking regions was sequenced in 24 lines of Drosophila simulans (10 from Spain and 14 from Mozambique). Fifty-four nucleotide and 8 length polymorphisms were detected. All nucleotide polymorphisms were silent: 52 in noncoding regions and 2 at synonymous sites in the coding region. Estimated silent nucleotide diversity was similar in both populations (pi = 0.016, for the total sample). Nucleotide variation revealed an unusual haplotype structure showing a subset of 11 sequences with a single polymorphism. This haplotype was present at intermediate frequencies in both the European and the African samples. The presence of such a major haplotype in a highly recombining region is incompatible with the neutral equilibrium model. This haplotype structure in both a derived and a putatively ancestral population can be most parsimoniously explained by positive selection. As the rate of recombination in the rp49 region is high, the target of selection should be close to or within the region studied.

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Selected References

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  1. 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]
  2. Ballard J. W., Hatzidakis J., Karr T. L., Kreitman M. Reduced variation in Drosophila simulans mitochondrial DNA. Genetics. 1996 Dec;144(4):1519–1528. doi: 10.1093/genetics/144.4.1519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Begun D. J., Aquadro C. F. Molecular variation at the vermilion locus in geographically diverse populations of Drosophila melanogaster and D. simulans. Genetics. 1995 Jul;140(3):1019–1032. doi: 10.1093/genetics/140.3.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Depaulis F., Veuille M. Neutrality tests based on the distribution of haplotypes under an infinite-site model. Mol Biol Evol. 1998 Dec;15(12):1788–1790. doi: 10.1093/oxfordjournals.molbev.a025905. [DOI] [PubMed] [Google Scholar]
  6. Duvernell D. D., Eanes W. F. Contrasting molecular population genetics of four hexokinases in Drosophila melanogaster, D. simulans and D. yakuba. Genetics. 2000 Nov;156(3):1191–1201. doi: 10.1093/genetics/156.3.1191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eanes W. F., Kirchner M., Yoon J., Biermann C. H., Wang I. N., McCartney M. A., Verrelli B. C. Historical selection, amino acid polymorphism and lineage-specific divergence at the G6pd locus in Drosophila melanogaster and D. simulans. Genetics. 1996 Nov;144(3):1027–1041. doi: 10.1093/genetics/144.3.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ewens W. J. The sampling theory of selectively neutral alleles. Theor Popul Biol. 1972 Mar;3(1):87–112. doi: 10.1016/0040-5809(72)90035-4. [DOI] [PubMed] [Google Scholar]
  9. Fay J. C., Wu C. I. Hitchhiking under positive Darwinian selection. Genetics. 2000 Jul;155(3):1405–1413. doi: 10.1093/genetics/155.3.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fu Y. X., Li W. H. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. doi: 10.1093/genetics/133.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fu Y. X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997 Oct;147(2):915–925. doi: 10.1093/genetics/147.2.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gillespie J. H. Genetic drift in an infinite population. The pseudohitchhiking model. Genetics. 2000 Jun;155(2):909–919. doi: 10.1093/genetics/155.2.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gillespie J. H. The role of population size in molecular evolution. Theor Popul Biol. 1999 Apr;55(2):145–156. doi: 10.1006/tpbi.1998.1391. [DOI] [PubMed] [Google Scholar]
  14. Hamblin M. T., Veuille M. Population structure among African and derived populations of Drosophila simulans: evidence for ancient subdivision and recent admixture. Genetics. 1999 Sep;153(1):305–317. doi: 10.1093/genetics/153.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hasson E., Wang I. N., Zeng L. W., Kreitman M., Eanes W. F. Nucleotide variation in the triosephosphate isomerase (Tpi) locus of Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 1998 Jun;15(6):756–769. doi: 10.1093/oxfordjournals.molbev.a025979. [DOI] [PubMed] [Google Scholar]
  16. Hey J., Kliman R. M. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol Biol Evol. 1993 Jul;10(4):804–822. doi: 10.1093/oxfordjournals.molbev.a040044. [DOI] [PubMed] [Google Scholar]
  17. Hudson R. R., Bailey K., Skarecky D., Kwiatowski J., Ayala F. J. Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics. 1994 Apr;136(4):1329–1340. doi: 10.1093/genetics/136.4.1329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hudson R. R., Boos D. D., Kaplan N. L. A statistical test for detecting geographic subdivision. Mol Biol Evol. 1992 Jan;9(1):138–151. doi: 10.1093/oxfordjournals.molbev.a040703. [DOI] [PubMed] [Google Scholar]
  19. Hudson R. R. Estimating the recombination parameter of a finite population model without selection. Genet Res. 1987 Dec;50(3):245–250. doi: 10.1017/s0016672300023776. [DOI] [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. Properties of a neutral allele model with intragenic recombination. Theor Popul Biol. 1983 Apr;23(2):183–201. doi: 10.1016/0040-5809(83)90013-8. [DOI] [PubMed] [Google Scholar]
  23. Hudson R. R., Sáez A. G., Ayala F. J. DNA variation at the Sod locus of Drosophila melanogaster: an unfolding story of natural selection. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7725–7729. doi: 10.1073/pnas.94.15.7725. [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. Kelly J. K. A test of neutrality based on interlocus associations. Genetics. 1997 Jul;146(3):1197–1206. doi: 10.1093/genetics/146.3.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kim Y., Stephan W. Joint effects of genetic hitchhiking and background selection on neutral variation. Genetics. 2000 Jul;155(3):1415–1427. doi: 10.1093/genetics/155.3.1415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kliman R. M., Hey J. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics. 1993 Feb;133(2):375–387. doi: 10.1093/genetics/133.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Labate J. A., Biermann C. H., Eanes W. F. Nucleotide variation at the runt locus in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 1999 Jun;16(6):724–731. doi: 10.1093/oxfordjournals.molbev.a026157. [DOI] [PubMed] [Google Scholar]
  29. Moriyama E. N., Powell J. R. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 1996 Jan;13(1):261–277. doi: 10.1093/oxfordjournals.molbev.a025563. [DOI] [PubMed] [Google Scholar]
  30. O'Connell P. O., Rosbash M. Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res. 1984 Jul 11;12(13):5495–5513. doi: 10.1093/nar/12.13.5495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rozas J., Aguadé M. Transfer of genetic information in the rp49 region of Drosophila subobscura between different chromosomal gene arrangements. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8083–8087. doi: 10.1073/pnas.90.17.8083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Rozas J., Segarra C., Ribó G., Aguadé M. Molecular population genetics of the rp49 gene region in different chromosomal inversions of Drosophila subobscura. Genetics. 1999 Jan;151(1):189–202. doi: 10.1093/genetics/151.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  37. Strobeck C. Average number of nucleotide differences in a sample from a single subpopulation: a test for population subdivision. Genetics. 1987 Sep;117(1):149–153. doi: 10.1093/genetics/117.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]
  41. Watterson G. A. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. doi: 10.1016/0040-5809(75)90020-9. [DOI] [PubMed] [Google Scholar]

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