Skip to main content
Genetics logoLink to Genetics
. 2000 Apr;154(4):1681–1691. doi: 10.1093/genetics/154.4.1681

Molecular variation at the In(2L)t proximal breakpoint site in natural populations of Drosophila melanogaster and D. simulans.

P Andolfatto 1, M Kreitman 1
PMCID: PMC1461028  PMID: 10747062

Abstract

A previous study of nucleotide polymorphism in a Costa Rican population of Drosophila melanogaster found evidence for a nonneutral deficiency in the number of haplotypes near the proximal breakpoint of In(2L)t, a common inversion polymorphism in this species. Another striking feature of the data was a window of unusually high nucleotide diversity spanning the breakpoint site. To distinguish between selective and neutral demographic explanations for the observed patterns in the data, we sample alleles from three additional populations of D. melanogaster and one population of D. simulans. We find that the strength of associations among sites found at the breakpoint varies between populations of D. melanogaster. In D. simulans, analysis of the homologous region reveals unusually elevated levels of nucleotide polymorphism spanning the breakpoint site. As with American populations of D. melanogaster, our D. simulans sample shows a marked reduction in the number of haplotypes but not in nucleotide diversity. Haplotype tests reveal a significant deficiency in the number of haplotypes relative to the neutral expectation in the D. simulans sample and some populations of D. melanogaster. At the breakpoint site, the level of divergence between haplotype classes is comparable to interspecific divergence. The observation of interspecific polymorphisms that differentiate major haplotype classes in both species suggests that haplotype classes at this locus are considerably old. When considered in the context of other studies on patterns of variation within and between populations of D. melanogaster and D. simulans, our data appear more consistent with the operation of selection than with simple demographic explanations.

Full Text

The Full Text of this article is available as a PDF (197.9 KB).

Selected References

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

  1. Aguadé M. Different forces drive the evolution of the Acp26Aa and Acp26Ab accessory gland genes in the Drosophila melanogaster species complex. Genetics. 1998 Nov;150(3):1079–1089. doi: 10.1093/genetics/150.3.1079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aguadé M. Positive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila. Genetics. 1999 Jun;152(2):543–551. doi: 10.1093/genetics/152.2.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Alvarez G., Zapata C. Conditions for protected inversion polymorphism under supergene selection. Genetics. 1997 Jun;146(2):717–722. doi: 10.1093/genetics/146.2.717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Andolfatto P., Nordborg M. The effect of gene conversion on intralocus associations. Genetics. 1998 Mar;148(3):1397–1399. doi: 10.1093/genetics/148.3.1397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Andolfatto P., Wall J. D., Kreitman M. Unusual haplotype structure at the proximal breakpoint of In(2L)t in a natural population of Drosophila melanogaster. Genetics. 1999 Nov;153(3):1297–1311. doi: 10.1093/genetics/153.3.1297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Begun D. J., Aquadro C. F. African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature. 1993 Oct 7;365(6446):548–550. doi: 10.1038/365548a0. [DOI] [PubMed] [Google Scholar]
  7. Begun D. J., Aquadro C. F. Evolutionary inferences from DNA variation at the 6-phosphogluconate dehydrogenase locus in natural populations of drosophila: selection and geographic differentiation. Genetics. 1994 Jan;136(1):155–171. doi: 10.1093/genetics/136.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Bénassi V., Aulard S., Mazeau S., Veuille M. Molecular variation of Adh and P6 genes in an African population of Drosophila melanogaster and its relation to chromosomal inversions. Genetics. 1993 Jul;134(3):789–799. doi: 10.1093/genetics/134.3.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Bénassi V., Depaulis F., Meghlaoui G. K., Veuille M. Partial sweeping of variation at the Fbp2 locus in a west African population of Drosophila melanogaster. Mol Biol Evol. 1999 Mar;16(3):347–353. doi: 10.1093/oxfordjournals.molbev.a026115. [DOI] [PubMed] [Google Scholar]
  12. Comeron J. M., Kreitman M., Aguadé M. Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics. 1999 Jan;151(1):239–249. doi: 10.1093/genetics/151.1.239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. David J. R., Capy P. Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 1988 Apr;4(4):106–111. doi: 10.1016/0168-9525(88)90098-4. [DOI] [PubMed] [Google Scholar]
  14. Depaulis F., Brazier L., Veuille M. Selective sweep at the Drosophila melanogaster Suppressor of Hairless locus and its association with the In(2L)t inversion polymorphism. Genetics. 1999 Jul;152(3):1017–1024. doi: 10.1093/genetics/152.3.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fu Y. X. New statistical tests of neutrality for DNA samples from a population. Genetics. 1996 May;143(1):557–570. doi: 10.1093/genetics/143.1.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hamblin M. T., Aquadro C. F. Contrasting patterns of nucleotide sequence variation at the glucose dehydrogenase (Gld) locus in different populations of Drosophila melanogaster. Genetics. 1997 Apr;145(4):1053–1062. doi: 10.1093/genetics/145.4.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hamblin M. T., Aquadro C. F. High nucleotide sequence variation in a region of low recombination in Drosophila simulans is consistent with the background selection model. Mol Biol Evol. 1996 Oct;13(8):1133–1140. doi: 10.1093/oxfordjournals.molbev.a025676. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Harada K., Kusakabe S., Yamazaki T., Mukai T. Spontaneous mutation rates in null and band-morph mutations of enzyme loci in Drosophila melanogaster. Jpn J Genet. 1993 Dec;68(6):605–616. doi: 10.1266/jjg.68.605. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. 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]
  23. 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]
  24. Hudson R. R., Kaplan N. L. The coalescent process in models with selection and recombination. Genetics. 1988 Nov;120(3):831–840. doi: 10.1093/genetics/120.3.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Hudson R. R., Slatkin M., Maddison W. P. Estimation of levels of gene flow from DNA sequence data. Genetics. 1992 Oct;132(2):583–589. doi: 10.1093/genetics/132.2.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Irvin S. D., Wetterstrand K. A., Hutter C. M., Aquadro C. F. Genetic variation and differentiation at microsatellite loci in Drosophila simulans. Evidence for founder effects in new world populations. Genetics. 1998 Oct;150(2):777–790. doi: 10.1093/genetics/150.2.777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kaplan N., Hudson R. R., Iizuka M. The coalescent process in models with selection, recombination and geographic subdivision. Genet Res. 1991 Feb;57(1):83–91. doi: 10.1017/s0016672300029074. [DOI] [PubMed] [Google Scholar]
  30. Kirby D. A., Stephan W. Multi-locus selection and the structure of variation at the white gene of Drosophila melanogaster. Genetics. 1996 Oct;144(2):635–645. doi: 10.1093/genetics/144.2.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. 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]
  34. 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]
  35. Nordborg M. Structured coalescent processes on different time scales. Genetics. 1997 Aug;146(4):1501–1514. doi: 10.1093/genetics/146.4.1501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Slatkin M., Wiehe T. Genetic hitch-hiking in a subdivided population. Genet Res. 1998 Apr;71(2):155–160. doi: 10.1017/s001667239800319x. [DOI] [PubMed] [Google Scholar]
  37. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  38. 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]
  39. Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics. 1983 Oct;105(2):437–460. doi: 10.1093/genetics/105.2.437. [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. Tsaur S. C., Ting C. T., Wu C. I. Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism. Mol Biol Evol. 1998 Aug;15(8):1040–1046. doi: 10.1093/oxfordjournals.molbev.a026002. [DOI] [PubMed] [Google Scholar]
  42. Wasserman M. Recombination-induced chromosomal heterosis. Genetics. 1968 Jan;58(1):125–139. doi: 10.1093/genetics/58.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES