Abstract
We studied nucleotide sequence variation at the gene coding for dopa decarboxylase (Ddc) in seven populations of Drosophila melanogaster. Strength and pattern of linkage disequilibrium are somewhat distinct in the extensively sampled Spanish and Raleigh populations. In the Spanish population, a few sites are in strong positive association, whereas a large number of sites in the Raleigh population are associated nonrandomly but the association is not strong. Linkage disequilibrium analysis shows presence of two groups of haplotypes in the populations, each of which is fairly diverged, suggesting epistasis or inversion polymorphism. There is evidence of two forms of natural selection acting on Ddc. The McDonald-Kreitman test indicates a deficit of fixed amino acid differences between D. melanogaster and D. simulans, which may be due to negative selection. An excess of derived alleles at high frequency, significant according to the H-test, is consistent with the effect of hitchhiking. The hitchhiking may have been caused by directional selection downstream of the locus studied, as suggested by a gradual decrease of the polymorphism-to-divergence ratio. Altogether, the Ddc locus exhibits a complicated pattern of variation apparently due to several evolutionary forces. Such a complex pattern may be a result of an unusually high density of functionally important genes.
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References
Aguadé M. 1998 Different forces drive the evolution of the Acp26Aa and Acp26Ab accessory gland genes in the D. melanogaster species complex. Genetics 150, 1079–1089.
Andolfatto P. and Kreitman M. 2000 Molecular variation at the In(2L)t proximal breakpoint site in natural populations of D. melanogaster and D. simulans. Genetics 154, 1681–1691.
Andolfatto P. and Przeworski M. 2001 Regions of lower crossing over harbor more rare variants in African populations of D. melanogaster. Genetics 158, 657–865.
Aquadro C. F., Jennings R. M. Jr, Bland M. M., Laurie C. C. and Langley C. H. 1992 Patterns of naturally occurring restriction map variation, dopa decarboxylase activity variation and linkage disequilibrium in the Ddc gene region of Drosophila melanogaster. Genetics 132, 443–452.
Aquadro C. F., DuMont V. B. and Reed F. A. 2001 Genome-wide variation in the human and fruitfly: a comparison. Curr. Opin. Genet. Dev. 11, 627–634.
Begun D. J. and Aquadro C. F. 1992 Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356, 519–520.
Begun D. J. and Aquadro C. F. 1993 African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature 365, 548–550.
Begun D. J. and Aquadro C. F. 1995 Molecular variation at the vermilion locus in geographically diverse populations of Drosophila melanogaster and D. simulans. Genetics 140, 1019–1032.
De Luca M., Roshina N. V., Geiger-Thornsberry G. L., Lyman R. F., Pasyukova E. G. and Mackay T. F. C. 2003 Dopa decarboxylase (Ddc) affects variation in Drosophila longevity. Nature Genet. 34, 429–433.
Depaulis F., Brazier L. and Veuille M. 1999 Selective sweep at the Drosophila melanogaster Suppressor of Hairless locus and its association with the In(2L)t inversion polymorphism. Genetics 152, 1017–1024.
Eveleth D. D., Gietz R. D., Spencer C. A., Nargang F. E., Hodgetts R. B. and Marsh J. L. 1986 Sequence and structure of the dopa decarboxylase gene of Drosophila: evidence for novel RNA splicing variants. EMBO J. 5, 2663–2672.
Fay J. C. and Wu C-I. 2000 Hitchhiking under positive Darwinian selection. Genetics 155, 1405–1413.
Fu Y-X. and Li W-H. 1993 Statistical tests of neutrality of mutations. Genetics 133, 693–709.
Hey J. and Wakeley J. 1997 A coalescent estimator of the population recombination rate. Genetics 145, 833–846.
Hudson R. R. 1987 Estimating the recombination parameter of a finite population model without selection. Genet. Res. 50, 245–250.
Hudson R. R. and Kaplan N. L. 1985 Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111, 147–164.
Hudson R. R., Kreitman M. and Aguadé M. 1987 A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153–159.
Hudson R. R., Boos D. D. and Kaplan N. L. 1992 A statistical test for detecting geographic subdivision. Mol. Biol. Evol. 9, 138–151.
Hudson R. R., Bailey K., Skarecky D., Kwiatowski J. and Ayala F. J. 1994 Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics 136, 1329–1340.
Hudson R. R., Sáez A. G. and Ayala F. J. 1997 DNA variation at the Sod locus of Drosophila melanogaster: an unfolding story of natural selection. Proc. Natl. Acad. Sci. USA 94, 7725–7729.
Kim Y. and Stephan W. 2000 Joint effects of genetic hitchhiking and background selection on neutral variation. Genetics 155, 1415–1427.
Kliman R. M. and Hey J. 1993 Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol. Biol. Evol. 10, 1239–1258.
Kreitman M. and Hudson R. R. 1991 Inferring the evolutionary histories of the Adh and Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. Genetics 127, 565–582.
Lazzaro B. P. and Clark A. G. 2003 Molecular population genetics of inducible antibacterial peptide genes in Drosophila melanogaster. Mol. Biol. Evol. 20, 914–923.
Lewontin R. C. 1995 The detection of linkage disequilibrium in molecular sequence data. Genetics 140, 377–388.
McDonald J. H. 1996 Detecting non-neutral heterogeneity across a region of DNA sequence in the ratio of polymorphism to divergence. Mol. Biol. Evol. 13, 253–260.
McDonald J. H. 1998 Improved tests for heterogeneity across a region of DNA sequence in the ratio of polymorphism to divergence. Mol. Biol. Evol. 15, 377–384.
McDonald J. H. and Kreitman M. 1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652–654.
Nurminsky D., Aguiar D. D., Bustamante C. D. and Hartl D. L. 2001 Chromosomal effects of rapid gene evolution in Drosophila melanogaster. Science 291, 128–130.
Parsch J., Meiklejohn C. A. and Hartl D. L. 2001 Patterns of DNA sequence variation suggest the recent action of positive selection in the janus-ocnus region of Drosophila simulans. Genetics 159, 647–657.
Przeworski M. 2002 The signature of positive selection at randomly chosen loci. Genetics 160, 1179–1189.
Przeworski M., Wall J. D. and Andolfatto P. 2001 Recombination and the frequency spectrum in Drosophila melanogaster and Drosophila simulans. Mol. Biol. Evol. 18, 291–298.
Rozas J. and Rozas R. 1999 DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174–175.
Sáez A. G., Tatarenkov A., Barrio E., Becerra N. H. and Ayala F. J. 2003 Patterns of DNA sequence polymorphism at Sod vicinities in Drosophila melanogaster: unraveling the footprint of a recent selective sweep. Proc. Natl. Acad. Sci. USA 100, 1793–1798.
Tajima F. 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
Tsaur S-C., Ting C.-T. and Wu C-I. 1998 Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism. Mol. Biol. Evol. 15, 1040–1046.
Watterson G. A. 1975 On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 10, 256–276.
Williams D. A. 1976 Improved likelihood ratio tests for complete contingency tables. Biometrika 63, 33–37.
Wright T. R. F. 1996 Phenotypic analysis of the dopa decarboxylase gene cluster mutants in Drosophila melanogaster. J. Hered. 87, 175–190.
Zurovcova M. and Ayala F. J. 2002 Polymorphism patterns in two tightly linked developmental genes, Idgf1 and Idgf3, of Drosophila melanogaster. Genetics 162, 177–188.
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Tatarenkov, A., Ayala, F.J. Nucleotide variation at the dopa decarboxylase (Ddc) gene in natural populations of Drosophila melanogaster . J Genet 86, 125–137 (2007). https://doi.org/10.1007/s12041-007-0017-8
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DOI: https://doi.org/10.1007/s12041-007-0017-8