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. 1999 Oct;153(2):871–889. doi: 10.1093/genetics/153.2.871

The relationship between allozyme and chromosomal polymorphism inferred from nucleotide variation at the Acph-1 gene region of Drosophila subobscura.

A Navarro-Sabaté 1, M Aguadé 1, C Segarra 1
PMCID: PMC1460765  PMID: 10511564

Abstract

The Acph-1 gene region was sequenced in 51 lines of Drosophila subobscura. Lines differ in their chromosomal arrangement for segment I of the O chromosome (O(st) and O(3+4)) and in the Acph-1 electrophoretic allele (Acph-1(100), Acph-1(054), and Acph-1(>100)). The ACPH-1 protein exhibits much more variation than previously detected by electrophoresis. The amino acid replacements responsible for the Acph-1(054) and Acph-1(>100) electrophoretic variants are different within O(st) and within O(3+4), which invalidates all previous studies on linkage disequilibrium between chromosomal and allozyme polymorphisms at this locus. The Acph-1(>100) allele within O(3+4) has a recent origin, while both Acph-1(054) alleles are rather old. Levels of nucleotide variation are higher within the O(3+4) than within the O(st) arrangement except for nonsynonymous sites. The McDonald and Kreitman test shows a significant excess of nonsynonymous polymorphisms within O(st) when D. guanche is used as the outgroup. According to the nearly neutral model of molecular evolution, this excess is consistent with a smaller effective size of O(st) relative to O(3+4) arrangements. A smaller population size, a lower recombination, and a more recent bottleneck might be contributing to the smaller effective size of O(st).

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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. Ballard J. W., Kreitman M. Unraveling selection in the mitochondrial genome of Drosophila. Genetics. 1994 Nov;138(3):757–772. doi: 10.1093/genetics/138.3.757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Betrán E., Rozas J., Navarro A., Barbadilla A. The estimation of the number and the length distribution of gene conversion tracts from population DNA sequence data. Genetics. 1997 May;146(1):89–99. doi: 10.1093/genetics/146.1.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Charlesworth B. The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet Res. 1994 Jun;63(3):213–227. doi: 10.1017/s0016672300032365. [DOI] [PubMed] [Google Scholar]
  8. Chung H. J., Shaffer C., MacIntyre R. Molecular characterization of the lysosomal acid phosphatase from Drosophila melanogaster. Mol Gen Genet. 1996 Mar 20;250(5):635–646. doi: 10.1007/BF02174451. [DOI] [PubMed] [Google Scholar]
  9. Cirera S., Aguadé M. Molecular evolution of a duplication: the sex-peptide (Acp70A) gene region of Drosophila subobscura and Drosophila madeirensis. Mol Biol Evol. 1998 Aug;15(8):988–996. doi: 10.1093/oxfordjournals.molbev.a026014. [DOI] [PubMed] [Google Scholar]
  10. Fontdevila A., Zapata C., Alvarez G., Sanchez L., Méndez J., Enriquez I. Genetic Coadaptation in the Chromosomal Polymorphism of DROSOPHILA SUBOBSCURA. I. Seasonal Changes of Gametic Disequilibrium in a Natural Population. Genetics. 1983 Dec;105(4):935–955. doi: 10.1093/genetics/105.4.935. [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. 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]
  13. 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]
  14. Harpending H. C. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol. 1994 Aug;66(4):591–600. [PubMed] [Google Scholar]
  15. Hasson E., Eanes W. F. Contrasting histories of three gene regions associated with In(3L)Payne of Drosophila melanogaster. Genetics. 1996 Dec;144(4):1565–1575. doi: 10.1093/genetics/144.4.1565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  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., 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]
  20. 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]
  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. KUNZE-MUHL E., MULLER E. Weitere Untersuchungen über die chromosomale Struktur und die natürlichen Strukturtypen von Drosophila subobscura Coll. Chromosoma. 1958;9(6):559–570. [PubMed] [Google Scholar]
  23. Kaneko M., Satta Y., Matsuura E. T., Chigusa S. I. Evolution of the mitochondrial ATPase 6 gene in Drosophila: unusually high level of polymorphism in D. melanogaster. Genet Res. 1993 Jun;61(3):195–204. doi: 10.1017/s0016672300031360. [DOI] [PubMed] [Google Scholar]
  24. Kirby D. A., Muse S. V., Stephan W. Maintenance of pre-mRNA secondary structure by epistatic selection. Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9047–9051. doi: 10.1073/pnas.92.20.9047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kliman R. M., Hey J. Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol Biol Evol. 1993 Nov;10(6):1239–1258. doi: 10.1093/oxfordjournals.molbev.a040074. [DOI] [PubMed] [Google Scholar]
  26. Kreitman M., Aguadé M. Genetic uniformity in two populations of Drosophila melanogaster as revealed by filter hybridization of four-nucleotide-recognizing restriction enzyme digests. Proc Natl Acad Sci U S A. 1986 May;83(10):3562–3566. doi: 10.1073/pnas.83.10.3562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Loukas M., Krimbas C. B., Morgan K. The Genetics of DROSOPHILA SUBOBSCURA Populations. Xiv. Further Data on Linkage Disequilibria. Genetics. 1980 Jul;95(3):757–768. doi: 10.1093/genetics/95.3.757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Loukas M., Krimbas C. B., Vergini Y. The genetics of Drosophila subobscura populations. IX. Studies on linkage disequilibrium in four natural populations. Genetics. 1979 Oct;93(2):497–523. doi: 10.1093/genetics/93.2.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. MacIntyre R. J., Dean M. R., Batt G. Evolution of acid phosphatase-1 in the genus Drosophilia. Immunological studies. J Mol Evol. 1978 Dec 29;12(2):121–142. doi: 10.1007/BF01733263. [DOI] [PubMed] [Google Scholar]
  31. McDonald J. H. Detecting non-neutral heterogeneity across a region of DNA sequence in the ratio of polymorphism to divergence. Mol Biol Evol. 1996 Jan;13(1):253–260. doi: 10.1093/oxfordjournals.molbev.a025562. [DOI] [PubMed] [Google Scholar]
  32. Miyashita N. T., Innan H., Terauchi R. Intra- and interspecific variation of the alcohol dehydrogenase locus region in wild plants Arabis gemmifera and Arabidopsis thaliana. Mol Biol Evol. 1996 Feb;13(2):433–436. doi: 10.1093/oxfordjournals.molbev.a025603. [DOI] [PubMed] [Google Scholar]
  33. Nachman M. W., Brown W. M., Stoneking M., Aquadro C. F. Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics. 1996 Mar;142(3):953–963. doi: 10.1093/genetics/142.3.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Navarro-Sabaté A., Aguadé M., Segarra C. The acid phosphatase-1 gene region in the Drosophila species of the subobscura cluster. Hereditas. 1999;130(1):65–75. doi: 10.1111/j.1601-5223.1999.00065.x. [DOI] [PubMed] [Google Scholar]
  35. Popadić A., Anderson W. W. Evidence for gene conversion in the amylase multigene family of Drosophila pseudoobscura. Mol Biol Evol. 1995 Jul;12(4):564–572. doi: 10.1093/oxfordjournals.molbev.a040236. [DOI] [PubMed] [Google Scholar]
  36. Popadić A., Anderson W. W. The history of a genetic system. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6819–6823. doi: 10.1073/pnas.91.15.6819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Popadić A., Norman R. A., Doanet W. W., Anderson W. W. The evolutionary history of the amylase multigene family in Drosophila pseudoobscura. Mol Biol Evol. 1996 Jul;13(6):883–888. doi: 10.1093/oxfordjournals.molbev.a025648. [DOI] [PubMed] [Google Scholar]
  38. Prevosti A., Ribo G., Serra L., Aguade M., Balaña J., Monclus M., Mestres F. Colonization of America by Drosophila subobscura: Experiment in natural populations that supports the adaptive role of chromosomal-inversion polymorphism. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5597–5600. doi: 10.1073/pnas.85.15.5597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ramos-Onsins S., Segarra C., Rozas J., Aguadé M. Molecular and chromosomal phylogeny in the obscura group of Drosophila inferred from sequences of the rp49 gene region. Mol Phylogenet Evol. 1998 Feb;9(1):33–41. doi: 10.1006/mpev.1997.0438. [DOI] [PubMed] [Google Scholar]
  40. Rand D. M., Dorfsman M., Kann L. M. Neutral and non-neutral evolution of Drosophila mitochondrial DNA. Genetics. 1994 Nov;138(3):741–756. doi: 10.1093/genetics/138.3.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Rand D. M., Kann L. M. Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol Biol Evol. 1996 Jul;13(6):735–748. doi: 10.1093/oxfordjournals.molbev.a025634. [DOI] [PubMed] [Google Scholar]
  42. Rodríguez-Trelles F., Alvarez G., Zapata C. Time-series analysis of seasonal changes of the O inversion polymorphism of Drosophila subobscura. Genetics. 1996 Jan;142(1):179–187. doi: 10.1093/genetics/142.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. 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]
  45. Rozas J., Rozas R. DnaSP version 2.0: a novel software package for extensive molecular population genetics analysis. Comput Appl Biosci. 1997 Jun;13(3):307–311. [PubMed] [Google Scholar]
  46. 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]
  47. 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]
  48. 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]
  49. Segarra C., Ribó G., Aguadé M. Differentiation of Muller's chromosomal elements D and E in the obscura group of Drosophila. Genetics. 1996 Sep;144(1):139–146. doi: 10.1093/genetics/144.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Simmons G. M., Kwok W., Matulonis P., Venkatesh T. Polymorphism and divergence at the prune locus in Drosophila melanogaster and D. simulans. Mol Biol Evol. 1994 Jul;11(4):666–671. doi: 10.1093/oxfordjournals.molbev.a040145. [DOI] [PubMed] [Google Scholar]
  51. Sperlich D., Feuerbach-Mravlag H., Lange P., Michaelidis A., Pentzos-Daponte A. Genetic Load and Viability Distribution in Central and Marginal Populations of DROSOPHILA SUBOBSCURA. Genetics. 1977 Aug;86(4):835–848. doi: 10.1093/genetics/86.4.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Staden R. Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Res. 1982 Aug 11;10(15):4731–4751. doi: 10.1093/nar/10.15.4731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. 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]
  54. Terauchi R., Terachi T., Miyashita N. T. DNA polymorphism at the Pgi locus of a wild yam, Dioscorea tokoro. Genetics. 1997 Dec;147(4):1899–1914. doi: 10.1093/genetics/147.4.1899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Zeng L. W., Comeron J. M., Chen B., Kreitman M. The molecular clock revisited: the rate of synonymous vs. replacement change in Drosophila. Genetica. 1998;102-103(1-6):369–382. [PubMed] [Google Scholar]

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