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Genetics. Apr 2001; 157(4): 1649–1663.
PMCID: PMC1461594

Clinal variation for amino acid polymorphisms at the Pgm locus in Drosophila melanogaster.

Abstract

Clinal variation is common for enzymes in the glycolytic pathway for Drosophila melanogaster and is generally accepted as an adaptive response to different climates. Although the enzyme phosphoglucomutase (PGM) possesses several allozyme polymorphisms, it is unique in that it had been reported to show no clinal variation. Our recent DNA sequence investigation of Pgm found extensive cryptic amino acid polymorphism segregating with the allozyme alleles. In this study, we characterize the geographic variation of Pgm amino acid polymorphisms at the nucleotide level along a latitudinal cline in the eastern United States. A survey of 15 SNPs across the Pgm gene finds significant clinal differentiation for the allozyme polymorphisms as well as for many of the cryptic amino acid polymorphisms. A test of independence shows that pervasive linkage disequilibrium across this gene region can explain many of the amino acid clines. A single Pgm haplotype defined by two amino acid polymorphisms shows the strongest correlation with latitude and the steepest change in allele frequency across the cline. We propose that clinal selection at Pgm may in part explain the extensive amino acid polymorphism at this locus and is consistent with a multilocus response to selection in the glycolytic pathway.

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Selected References

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  • Andolfatto P, Wall JD, 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. [PMC free article] [PubMed]
  • Argos P, Rossman MG, Grau UM, Zuber H, Frank G, Tratschin JD. Thermal stability and protein structure. Biochemistry. 1979 Dec 11;18(25):5698–5703. [PubMed]
  • Ballard JW, Kreitman M. Unraveling selection in the mitochondrial genome of Drosophila. Genetics. 1994 Nov;138(3):757–772. [PMC free article] [PubMed]
  • Berry A, Kreitman M. Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the east coast of North America. Genetics. 1993 Jul;134(3):869–893. [PMC free article] [PubMed]
  • Braverman JM, Hudson RR, Kaplan NL, Langley CH, Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. [PMC free article] [PubMed]
  • Kreitman M, Hudson RR. 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. [PMC free article] [PubMed]
  • Labate J, Eanes WF. Direct measurement of in vivo flux differences between electrophoretic variants of G6PD from Drosophila melanogaster. Genetics. 1992 Nov;132(3):783–787. [PMC free article] [PubMed]
  • Coyne JA, Beecham E. Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics. 1987 Dec;117(4):727–737. [PMC free article] [PubMed]
  • David JR, Bocquet C. Similarities and differences in latitudinal adaptation of two Drosophila sibling species. Nature. 1975 Oct 16;257(5527):588–590. [PubMed]
  • McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. [PubMed]
  • McDonald JH, Verrelli BC, Geyer LB. Lack of geographic variation in anonymous nuclear polymorphisms in the American oyster, Crassostrea virginica. Mol Biol Evol. 1996 Oct;13(8):1114–1118. [PubMed]
  • Dykhuizen DE, Dean AM, Hartl DL. Metabolic flux and fitness. Genetics. 1987 Jan;115(1):25–31. [PMC free article] [PubMed]
  • McDonald JH, Grasso AM, Rejto LK. Patterns of temperature adaptation in proteins from Methanococcus and Bacillus. Mol Biol Evol. 1999 Dec;16(12):1785–1790. [PubMed]
  • Mettler LE, Voelker RA, Mukai T. Inversion Clines in Populations of DROSOPHILA MELANOGASTER. Genetics. 1977 Sep;87(1):169–176. [PMC free article] [PubMed]
  • Moriyama EN, Powell JR. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 1996 Jan;13(1):261–277. [PubMed]
  • Nachman MW, Brown WM, Stoneking M, Aquadro CF. Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics. 1996 Mar;142(3):953–963. [PMC free article] [PubMed]
  • Gillespie JH. Junk ain't what junk does: neutral alleles in a selected context. Gene. 1997 Dec 31;205(1-2):291–299. [PubMed]
  • Nielsen R, Weinreich DM. The age of nonsynonymous and synonymous mutations in animal mtDNA and implications for the mildly deleterious theory. Genetics. 1999 Sep;153(1):497–506. [PMC free article] [PubMed]
  • Oakeshott JG, Chambers GK, Gibson JB, Willcocks DA. Latitudinal relationships of esterase-6 and phosphoglucomutase gene frequencies in Drosophila melanogaster. Heredity (Edinb) 1981 Dec;47(Pt 3):385–396. [PubMed]
  • Hasegawa M, Cao Y, Yang Z. Preponderance of slightly deleterious polymorphism in mitochondrial DNA: nonsynonymous/synonymous rate ratio is much higher within species than between species. Mol Biol Evol. 1998 Nov;15(11):1499–1505. [PubMed]
  • Hasson E, Wang IN, Zeng LW, Kreitman M, Eanes WF. Nucleotide variation in the triosephosphate isomerase (Tpi) locus of Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 1998 Jun;15(6):756–769. [PubMed]
  • Oakeshott JG, Chambers GK, Gibson JB, Eanes WF, Willcocks DA. Geographic variation in G6pd and Pgd allele frequencies in Drosophila melanogaster. Heredity (Edinb) 1983 Feb;50(Pt 1):67–72. [PubMed]
  • Hjorth JP. A phosphoglucomutase locus in Drosophila melanogaster. Hereditas. 1970;64(1):146–148. [PubMed]
  • Hudson RR. Estimating the recombination parameter of a finite population model without selection. Genet Res. 1987 Dec;50(3):245–250. [PubMed]
  • Hudson RR, Kaplan NL. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 1985 Sep;111(1):147–164. [PMC free article] [PubMed]
  • Ohta T. The current significance and standing of neutral and neutral theories. Bioessays. 1996 Aug;18(8):673–683. [PubMed]
  • Pogson GH, Mesa KA, Boutilier RG. Genetic population structure and gene flow in the Atlantic cod Gadus morhua: a comparison of allozyme and nuclear RFLP loci. Genetics. 1995 Jan;139(1):375–385. [PMC free article] [PubMed]
  • Hudson RR, Bailey K, Skarecky D, Kwiatowski J, Ayala FJ. Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics. 1994 Apr;136(4):1329–1340. [PMC free article] [PubMed]
  • James AC, Azevedo RB, Partridge L. Cellular basis and developmental timing in a size cline of Drosophila melanogaster. Genetics. 1995 Jun;140(2):659–666. [PMC free article] [PubMed]
  • Salamon H, Klitz W, Easteal S, Gao X, Erlich HA, Fernandez-Viña M, Trachtenberg EA, McWeeney SK, Nelson MP, Thomson G. Evolution of HLA class II molecules: Allelic and amino acid site variability across populations. Genetics. 1999 May;152(1):393–400. [PMC free article] [PubMed]
  • Kennedy P, Nachman MW. Deleterious mutations at the mitochondrial ND3 gene in South American marsh rats (Holochilus). Genetics. 1998 Sep;150(1):359–368. [PMC free article] [PubMed]
  • Singh RS, Rhomberg LR. A Comprehensive Study of Genic Variation in Natural Populations of Drosophila melanogaster. II. Estimates of Heterozygosity and Patterns of Geographic Differentiation. Genetics. 1987 Oct;117(2):255–271. [PMC free article] [PubMed]
  • Kirby DA, Stephan W. Haplotype test reveals departure from neutrality in a segment of the white gene of Drosophila melanogaster. Genetics. 1995 Dec;141(4):1483–1490. [PMC free article] [PubMed]
  • Takahata N, Satta Y, Klein J. Polymorphism and balancing selection at major histocompatibility complex loci. Genetics. 1992 Apr;130(4):925–938. [PMC free article] [PubMed]
  • Verrelli BC, Eanes WF. Extensive amino acid polymorphism at the pgm locus is consistent with adaptive protein evolution in Drosophila melanogaster. Genetics. 2000 Dec;156(4):1737–1752. [PMC free article] [PubMed]
  • Terauchi R, Terachi T, Miyashita NT. DNA polymorphism at the Pgi locus of a wild yam, Dioscorea tokoro. Genetics. 1997 Dec;147(4):1899–1914. [PMC free article] [PubMed]
  • Wayne ML, Contamine D, Kreitman M. Molecular population genetics of ref(2)P, a locus which confers viral resistance in Drosophila. Mol Biol Evol. 1996 Jan;13(1):191–199. [PubMed]
  • Trippa G, Loverre A, Catamo A. Thermostability studies for investigating non-electrophoretic polymorphic alleles in Drosophila melanogaster. Nature. 1976 Mar 4;260(5546):42–44. [PubMed]
  • Winnepenninckx B, Backeljau T, De Wachter R. Extraction of high molecular weight DNA from molluscs. Trends Genet. 1993 Dec;9(12):407–407. [PubMed]

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