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. 1979 Dec;93(4):997–1018. doi: 10.1093/genetics/93.4.997

Genic Heterogeneity within Electrophoretic "Alleles" and the Pattern of Variation among Loci in DROSOPHILA PSEUDOOBSCURA

Rama S Singh 1
PMCID: PMC1214126  PMID: 546677

Abstract

An investigation, similar to our previously reported xanthine dehydrogenase study, was undertaken to examine the extent of hidden genic variation at nine loci (five larval proteins, three esterases and one aldehyde oxidase) by sequential application of various electrophoretic criteria employing pH, gel concentration and buffer variation. Polymorphic loci appear to fall into two distinct groups: weakly polymorphic, including larval protein 6, 7, 8, 10 and 13 and esterase-1 and -6; and highly polymorphic, including esterase-5, Xdh and possibly Ao. Monomorphic loci may belong to a third group different from all polymorphic loci. Bogota, a geographical isolate that is reproductively isolated from the mainland population, was found to be genetically distinct at four of the ten loci examined in detail so far, including Xdh, whereas previously it was found to be genetically distinct at none. These results are discussed in the light of balancing selection, neutral and mutation-selection hypotheses of genic variation in natural populations.

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Selected References

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  1. Anderson R. P., Roth J. R. Tandem chromosomal duplications in Salmonella typhimurium: fusion of histidine genes to novel promoters. J Mol Biol. 1978 Feb 15;119(1):147–166. doi: 10.1016/0022-2836(78)90274-7. [DOI] [PubMed] [Google Scholar]
  2. Berkowitz D., Hushon J. M., Whitfield H. J., Jr, Roth J., Ames B. N. Procedure for identifying nonsense mutations. J Bacteriol. 1968 Jul;96(1):215–220. doi: 10.1128/jb.96.1.215-220.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bernstein S. C., Throckmorton L. H., Hubby J. L. Still more genetic variability in natural populations. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3928–3931. doi: 10.1073/pnas.70.12.3928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brake A. J., Fowler A. V., Zabin I., Kania J., Müller-Hill B. beta-Galactosidase chimeras: primary structure of a lac repressor-beta-galactosidase protein. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4824–4827. doi: 10.1073/pnas.75.10.4824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Christiansen F. B., Frydenberg O. Geographical patterns of four polymorphisms in Zoarces viviparus as evidence of selection. Genetics. 1974 Aug;77(4):765–770. doi: 10.1093/genetics/77.4.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cobbs G. Polymorphism for dimerizing ability at the esterase-5 locus in Drosophila pseudoobscura. Genetics. 1976 Jan;82(1):53–62. doi: 10.1093/genetics/82.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cobbs G., Prakash S. A comparative study of the esterase-5 locus in Drosophila pseudoobscura, D. persimilis and D. miranda. Genetics. 1977 Apr;85(4):697–711. doi: 10.1093/genetics/85.4.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cochrane B. J. Heat stability variants of esterase-6 in Drosophila melanogaster. Nature. 1976 Sep 9;263(5573):131–132. doi: 10.1038/263131a0. [DOI] [PubMed] [Google Scholar]
  9. Cochrane B. J., Richmond R. C. Studies of esterase 6 in Drosophila melanogaster. I. The genetics of a posttranslational modification. Biochem Genet. 1979 Feb;17(1-2):167–183. doi: 10.1007/BF00484483. [DOI] [PubMed] [Google Scholar]
  10. Courtright J. B. Polygenic control of aldehyde oxidase in Drosophila. Genetics. 1967 Sep;57(1):25–39. doi: 10.1093/genetics/57.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Coyne J. A., Eanes W. F., Lewontin R. C. The genetics of electrophoretic variation. Genetics. 1979 May;92(1):353–360. doi: 10.1093/genetics/92.1.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Coyne J. A., Felton A. A. Genic Heterogeneity at Two Alcohol Dehydrogenase Loci in DROSOPHILA PSEUDOOBSCURA and DROSOPHILA PERSIMILIS. Genetics. 1977 Oct;87(2):285–304. doi: 10.1093/genetics/87.2.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Coyne J. A., Felton A. A., Lewontin R. C. Extent of genetic variation at a highly polymorphic esterase locus in Drosophila pseudoobscura. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5090–5093. doi: 10.1073/pnas.75.10.5090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Coyne J. A. Lack of genic similarity between two sibling species of drosophila as revealed by varied techniques. Genetics. 1976 Nov;84(3):593–607. doi: 10.1093/genetics/84.3.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cuzin F., Jacob F. Mutations de l'épisome F d'Escherichia coli K 12. II. Mutants à réplication thermosensible. Ann Inst Pasteur (Paris) 1967 Apr;112(4):397–418. [PubMed] [Google Scholar]
  16. Demerec M., Adelberg E. A., Clark A. J., Hartman P. E. A proposal for a uniform nomenclature in bacterial genetics. Genetics. 1966 Jul;54(1):61–76. doi: 10.1093/genetics/54.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Faelen M., Toussaint A. Bacteriophage Mu-1: a tool to transpose and to localize bacterial genes. J Mol Biol. 1976 Jul 5;104(3):525–539. doi: 10.1016/0022-2836(76)90118-2. [DOI] [PubMed] [Google Scholar]
  18. Finnerty V., Johnson G. Post-Translational Modification as a Potential Explanation of High Levels of Enzyme Polymorphism: Xanthine Dehydrogenase and Aldehyde Oxidase in DROSOPHILA MELANOGASTER. Genetics. 1979 Apr;91(4):695–722. doi: 10.1093/genetics/91.4.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Johnson G. B. Hidden alleles at the alpha-glycerophosphate dehydrogenase locus in Colias butterflies. Genetics. 1976 May;83(1):149–167. doi: 10.1093/genetics/83.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. KOHIYAMA M., LANFROM H., BRENNER S., JACOB F. MODIFICATIONS DE FONCTIONS INDISPENSABLES CHEZ DES MUTANTS THERMOSENSIBLES D'ESCHERICHIA COLI. SUR UNE MUTATION EMP ECHANT LA R'EPLICATION DU CHROMOSOME BACT'ERIEN. C R Hebd Seances Acad Sci. 1963 Sep 23;257:1979–1981. [PubMed] [Google Scholar]
  22. Lederberg J. Detection of Fermentative Variants with Tetrazolium. J Bacteriol. 1948 Nov;56(5):695–695. doi: 10.1128/jb.56.5.695-695.1948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Milkman R. Further evidence of thermostability variation within electrophoretic mobility classes of enzymes. Biochem Genet. 1976 Apr;14(3-4):383–387. doi: 10.1007/BF00484776. [DOI] [PubMed] [Google Scholar]
  24. Milkman R., Koehler R. Isoelectric focusing of MDH and 6-PGDH from Escherichia coli of diverse natural origins. Biochem Genet. 1976 Jun;14(5-6):517–522. doi: 10.1007/BF00486131. [DOI] [PubMed] [Google Scholar]
  25. Myers J. H. Isozymes and allozymes: alternate forms of protein adaptation? Can J Genet Cytol. 1978 Jun;20(2):187–192. doi: 10.1139/g78-020. [DOI] [PubMed] [Google Scholar]
  26. Müller-Hill B., Kania J. Lac repressor can be fused to beta-galactosidase. Nature. 1974 Jun 7;249(457):561–563. doi: 10.1038/249561a0. [DOI] [PubMed] [Google Scholar]
  27. Narise S., Hubby J. L. Purification of esterase-5 from Drosophila pseudoobscura. Biochim Biophys Acta. 1966 Aug 10;122(2):281–288. doi: 10.1016/0926-6593(66)90068-3. [DOI] [PubMed] [Google Scholar]
  28. Nei M., Chakraborty R. Electrophoretically silent alleles in a finite population. J Mol Evol. 1976 Dec 30;8(4):381–385. doi: 10.1007/BF01739262. [DOI] [PubMed] [Google Scholar]
  29. Ohta T., Kimura M. A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet Res. 1973 Oct;22(2):201–204. doi: 10.1017/s0016672300012994. [DOI] [PubMed] [Google Scholar]
  30. Prakash S. Origin of reproductive isolation in the absence of apparent genic differentiation in a geographic isolate of Drosophila pseudoobscura. Genetics. 1972 Sep;72(1):143–155. doi: 10.1093/genetics/72.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schmid M., Roth J. R. Circularization of transduced fragments: a mechanism for adding segments to the bacterial chromosome. Genetics. 1980 Jan;94(1):15–29. doi: 10.1093/genetics/94.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Scott J. F., Roth J. R., Artz S. W. Regulation of histidine operon does not require hisG enzyme. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5021–5025. doi: 10.1073/pnas.72.12.5021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Singh R. S., Hubby J. L., Lewontin R. C. Molecular heterosis for heat-sensitive enzyme alleles. Proc Natl Acad Sci U S A. 1974 May;71(5):1808–1810. doi: 10.1073/pnas.71.5.1808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Singh R. S., Lewontin R. C., Felton A. A. Genetic heterogeneity within electrophoretic "alleles" of xanthine dehydrogenase in Drosophila pseudoobscura. Genetics. 1976 Nov;84(3):609–629. doi: 10.1093/genetics/84.3.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Strobeck C., Morgan K. The effect of intragenic recombination on the number of alleles in a finite population. Genetics. 1978 Apr;88(4):829–844. doi: 10.1093/genetics/88.4.829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Syvanen J. M., Roth J. R. Structural genes for ornithine transcarbamylase in Salmonella typhimurium and Escherichia coli K-12. J Bacteriol. 1972 Apr;110(1):66–70. doi: 10.1128/jb.110.1.66-70.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Thörig E. W., Schoone A. A., Scharloo W. Variation between electrophoretically identical alleles at the alcohol dehydrogenase locus in Drosophila melanogaster. Biochem Genet. 1975 Oct;13(9-10):721–731. doi: 10.1007/BF00484929. [DOI] [PubMed] [Google Scholar]
  38. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  39. Zouros E. Hybrid molecules and the superiority of the heterozygote. Nature. 1976 Jul 15;262(5565):227–229. doi: 10.1038/262227a0. [DOI] [PubMed] [Google Scholar]

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