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. 1996 Dec;144(4):1565–1575. doi: 10.1093/genetics/144.4.1565

Contrasting Histories of Three Gene Regions Associated with In(3l)payne of Drosophila Melanogaster

E Hasson 1, W F Eanes 1
PMCID: PMC1207709  PMID: 8978045

Abstract

In the present report, we studied nucleotide variation in three gene regions of Drosophila melanogaster, spanning >5 kb and showing different degrees of association with the cosmopolitan inversion In(3-L)Payne. The analysis of sequence variation in the regions surrounding the breakpoints and the heat shock 83 (Hsp83) gene locus, located close to the distal breakpoint, revealed the absence of shared polymorphisms and the presence of a number of fixed differences between arrangements, indicating absence of genetic exchange. In contrast, for the esterase-6 gene region, located in the center of the inversion, we observed the presence of shared polymorphisms between arrangements suggesting genetic exchange. In the regions close to the breakpoints, the common St arrangement is 10 times more polymorphic than inverted chromosomes. We propose that the lack of recombination between arrangements in these regions coupled with genetic hitchhiking is the best explanation for the low heterozygosity observed in inverted lines. Using the data for the breakpoints, we estimate that this inversion polymorphism is around 0.36 million yr old. Although it is widely accepted that inversions are examples of balanced polymorphisms, none of the current neutrality tests including our Monte Carlo simulations showed significant departure from neutral expectations.

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Selected References

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  1. Aguade M. Restriction map variation at the adh locus of Drosophila melanogaster in inverted and noninverted chromosomes. Genetics. 1988 May;119(1):135–140. doi: 10.1093/genetics/119.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aquadro C. F., Weaver A. L., Schaeffer S. W., Anderson W. W. Molecular evolution of inversions in Drosophila pseudoobscura: the amylase gene region. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):305–309. doi: 10.1073/pnas.88.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Babcock C. S., Anderson W. W. Molecular evolution of the Sex-Ratio inversion complex in Drosophila pseudoobscura: analysis of the Esterase-5 gene region. Mol Biol Evol. 1996 Feb;13(2):297–308. doi: 10.1093/oxfordjournals.molbev.a025589. [DOI] [PubMed] [Google Scholar]
  4. Blackman R. K., Meselson M. Interspecific nucleotide sequence comparisons used to identify regulatory and structural features of the Drosophila hsp82 gene. J Mol Biol. 1986 Apr 20;188(4):499–515. doi: 10.1016/s0022-2836(86)80001-8. [DOI] [PubMed] [Google Scholar]
  5. Charlesworth B., Morgan M. T., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. doi: 10.1093/genetics/134.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chovnick A. Gene conversion and transfer of genetic information within the inverted region of inversion heterozygotes. Genetics. 1973 Sep;75(1):123–131. doi: 10.1093/genetics/75.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Collet C., Nielsen K. M., Russell R. J., Karl M., Oakeshott J. G., Richmond R. C. Molecular analysis of duplicated esterase genes in Drosophila melanogaster. Mol Biol Evol. 1990 Jan;7(1):9–28. doi: 10.1093/oxfordjournals.molbev.a040582. [DOI] [PubMed] [Google Scholar]
  8. Cooke P. H., Oakeshott J. G. Amino acid polymorphisms for esterase-6 in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1426–1430. doi: 10.1073/pnas.86.4.1426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Eanes W. F., Kirchner M., Yoon J. Evidence for adaptive evolution of the G6pd gene in the Drosophila melanogaster and Drosophila simulans lineages. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7475–7479. doi: 10.1073/pnas.90.16.7475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Higuchi R. G., Ochman H. Production of single-stranded DNA templates by exonuclease digestion following the polymerase chain reaction. Nucleic Acids Res. 1989 Jul 25;17(14):5865–5865. doi: 10.1093/nar/17.14.5865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hudson R. R., Kaplan N. L. Deleterious background selection with recombination. Genetics. 1995 Dec;141(4):1605–1617. doi: 10.1093/genetics/141.4.1605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. KIMURA M., CROW J. F. THE NUMBER OF ALLELES THAT CAN BE MAINTAINED IN A FINITE POPULATION. Genetics. 1964 Apr;49:725–738. doi: 10.1093/genetics/49.4.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kaplan N. L., Darden T., Hudson R. R. The coalescent process in models with selection. Genetics. 1988 Nov;120(3):819–829. doi: 10.1093/genetics/120.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Karotam J., Boyce T. M., Oakeshott J. G. Nucleotide variation at the hypervariable esterase 6 isozyme locus of Drosophila simulans. Mol Biol Evol. 1995 Jan;12(1):113–122. doi: 10.1093/oxfordjournals.molbev.a040180. [DOI] [PubMed] [Google Scholar]
  21. Karotam J., Delves A. C., Oakeshott J. G. Conservation and change in structural and 5' flanking sequences of esterase 6 in sibling Drosophila species. Genetica. 1993;88(1):11–28. doi: 10.1007/BF02424448. [DOI] [PubMed] [Google Scholar]
  22. Knibb W. R., Oakeshott J. G., Gibson J. B. Chromosome Inversion Polymorphisms in DROSOPHILA MELANOGASTER. I. Latitudinal Clines and Associations between Inversions in Australasian Populations. Genetics. 1981 Aug;98(4):833–847. doi: 10.1093/genetics/98.4.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Langley C. H., Tobari Y. N., Kojima K. I. Linkage disequilibrium in natural populations of Drosophila melanogaster. Genetics. 1974 Nov;78(3):921–936. doi: 10.1093/genetics/78.3.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Nei M., Li W. H. Non-random association between electromorphs and inversion chromosomes in finite populations. Genet Res. 1980 Feb;35(1):65–83. doi: 10.1017/s001667230001394x. [DOI] [PubMed] [Google Scholar]
  26. Payne F. Crossover Modifiers in the Third Chromosome of DROSOPHILA MELANOGASTER. Genetics. 1924 Jul;9(4):327–342. doi: 10.1093/genetics/9.4.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Popadić A., Popadić D., Anderson W. W. Interchromosomal exchange of genetic information between gene arrangements on the third chromosome of Drosophila pseudoobscura. Mol Biol Evol. 1995 Sep;12(5):938–943. doi: 10.1093/oxfordjournals.molbev.a040271. [DOI] [PubMed] [Google Scholar]
  28. Rozas J., Aguadé M. Evidence of extensive genetic exchange in the rp49 region among polymorphic chromosome inversions in Drosophila subobscura. Genetics. 1990 Oct;126(2):417–426. doi: 10.1093/genetics/126.2.417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rozas J., Aguadé M. Gene conversion is involved in the transfer of genetic information between naturally occurring inversions of Drosophila. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11517–11521. doi: 10.1073/pnas.91.24.11517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Strobeck C. Expected linkage disequilibrium for a neutral locus linked to a chromosomal arrangement. Genetics. 1983 Mar;103(3):545–555. doi: 10.1093/genetics/103.3.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Wesley C. S., Eanes W. F. Isolation and analysis of the breakpoint sequences of chromosome inversion In(3L)Payne in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3132–3136. doi: 10.1073/pnas.91.8.3132. [DOI] [PMC free article] [PubMed] [Google Scholar]

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