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. 1991 Dec;129(4):1147–1158. doi: 10.1093/genetics/129.4.1147

Molecular Population Genetics of the Distal Portion of the X Chromosome in Drosophila: Evidence for Genetic Hitchhiking of the Yellow-Achaete Region

D J Begun 1, C F Aquadro 1
PMCID: PMC1204778  PMID: 1664405

Abstract

We have estimated DNA sequence variation and differentiation within and between Drosophila melanogaster and its sibling species, Drosophila simulans, using six-cutter restriction site variation at yellow-achaete (y-ac), phosphogluconate dehydrogenase (Pgd), and period (per). These three gene regions are of varying distance from the telomere of the X chromosome and range from very low to moderate rates of recombination in D. melanogaster. According to Tajima's test of neutrality, the Pgd region has been influenced by balancing selection in D. melanogaster. This is consistent with previous data suggesting the allozyme polymorphism at this locus is visible to selection. The Hudson, Kreitman, Aguade test of neutrality reveals a significant departure from neutrality for the y-ac region compared to the per or rosy regions in D. simulans. There is also a significant departure for the y-ac region compared to the Adh 5' flanking region in D. melanogaster. In both species the departure appears to be due to reduced variation at y-ac compared to that expected from divergence between D. simulans and D. melanogaster. We conclude that recent hitchhiking associated with the selective fixation of one or more advantageous mutants in the y-ac region is the best explanation for reduced variation at y-ac.

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Selected References

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  1. Aquadro C. F., Desse S. F., Bland M. M., Langley C. H., Laurie-Ahlberg C. C. Molecular population genetics of the alcohol dehydrogenase gene region of Drosophila melanogaster. Genetics. 1986 Dec;114(4):1165–1190. doi: 10.1093/genetics/114.4.1165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aquadro C. F., Lado K. M., Noon W. A. The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. Genetics. 1988 Aug;119(4):875–888. doi: 10.1093/genetics/119.4.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beech R. N., Brown A. J. Insertion-deletion variation at the yellow-achaete-scute region in two natural populations of Drosophila melanogaster. Genet Res. 1989 Feb;53(1):7–15. doi: 10.1017/s0016672300027804. [DOI] [PubMed] [Google Scholar]
  4. Bender W., Spierer P., Hogness D. S. Chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex in Drosophila melanogaster. J Mol Biol. 1983 Jul 25;168(1):17–33. doi: 10.1016/s0022-2836(83)80320-9. [DOI] [PubMed] [Google Scholar]
  5. Birky C. W., Jr, Walsh J. B. Effects of linkage on rates of molecular evolution. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6414–6418. doi: 10.1073/pnas.85.17.6414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Campuzano S., Carramolino L., Cabrera C. V., Ruíz-Gómez M., Villares R., Boronat A., Modolell J. Molecular genetics of the achaete-scute gene complex of D. melanogaster. Cell. 1985 Feb;40(2):327–338. doi: 10.1016/0092-8674(85)90147-3. [DOI] [PubMed] [Google Scholar]
  7. Cavener D. R., Clegg M. T. Evidence for biochemical and physiological differences between enzyme genotypes in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4444–4447. doi: 10.1073/pnas.78.7.4444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Choudhary M., Singh R. S. A Comprehensive Study of Genic Variation in Natural Populations of Drosophila melanogaster. III. Variations in Genetic Structure and Their Causes between Drosophila melanogaster and Its Sibling Species Drosophila simulans. Genetics. 1987 Dec;117(4):697–710. doi: 10.1093/genetics/117.4.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. David J. R., Capy P. Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 1988 Apr;4(4):106–111. doi: 10.1016/0168-9525(88)90098-4. [DOI] [PubMed] [Google Scholar]
  10. Eanes W. F., Labate J., Ajioka J. W. Restriction-map variation with the yellow-achaete-scute region in five populations of Drosophila melanogaster. Mol Biol Evol. 1989 Sep;6(5):492–502. doi: 10.1093/oxfordjournals.molbev.a040565. [DOI] [PubMed] [Google Scholar]
  11. Golding G. B., Aquadro C. F., Langley C. H. Sequence evolution within populations under multiple types of mutation. Proc Natl Acad Sci U S A. 1986 Jan;83(2):427–431. doi: 10.1073/pnas.83.2.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gutierrez A. G., Christensen A. C., Manning J. E., Lucchesi J. C. Cloning and dosage compensation of the 6-phosphogluconate dehydrogenase gene (Pgd+) of Drosophila melanogaster. Dev Genet. 1989;10(3):155–161. doi: 10.1002/dvg.1020100305. [DOI] [PubMed] [Google Scholar]
  13. Hillis D. M., Moritz C., Porter C. A., Baker R. J. Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science. 1991 Jan 18;251(4991):308–310. doi: 10.1126/science.1987647. [DOI] [PubMed] [Google Scholar]
  14. Hudson R. R. Estimating genetic variability with restriction endonucleases. Genetics. 1982 Apr;100(4):711–719. doi: 10.1093/genetics/100.4.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. 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]
  18. Langley C. H., Montgomery E., Hudson R., Kaplan N., Charlesworth B. On the role of unequal exchange in the containment of transposable element copy number. Genet Res. 1988 Dec;52(3):223–235. doi: 10.1017/s0016672300027695. [DOI] [PubMed] [Google Scholar]
  19. Lewontin R C. The Interaction of Selection and Linkage. I. General Considerations; Heterotic Models. Genetics. 1964 Jan;49(1):49–67. doi: 10.1093/genetics/49.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Macpherson J. N., Weir B. S., Leigh Brown A. J. Extensive linkage disequilibrium in the achaete-scute complex of Drosophila melanogaster. Genetics. 1990 Sep;126(1):121–129. doi: 10.1093/genetics/126.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Maruyama T., Fuerst P. A. Population bottlenecks and nonequilibrium models in population genetics. I. Allele numbers when populations evolve from zero variability. Genetics. 1984 Nov;108(3):745–763. doi: 10.1093/genetics/108.3.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Montgomery E., Charlesworth B., Langley C. H. A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet Res. 1987 Feb;49(1):31–41. doi: 10.1017/s0016672300026707. [DOI] [PubMed] [Google Scholar]
  23. Nei M., Jin L. Variances of the average numbers of nucleotide substitutions within and between populations. Mol Biol Evol. 1989 May;6(3):290–300. doi: 10.1093/oxfordjournals.molbev.a040547. [DOI] [PubMed] [Google Scholar]
  24. Nei M., Li W. H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5269–5273. doi: 10.1073/pnas.76.10.5269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  26. Stephan W., Langley C. H. Molecular genetic variation in the centromeric region of the X chromosome in three Drosophila ananassae populations. I. Contrasts between the vermilion and forked loci. Genetics. 1989 Jan;121(1):89–99. doi: 10.1093/genetics/121.1.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Tajima F. The effect of change in population size on DNA polymorphism. Genetics. 1989 Nov;123(3):597–601. doi: 10.1093/genetics/123.3.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Westneat D. F., Noon W. A., Reeve H. K., Aquadro C. F. Improved hybridization conditions for DNA 'fingerprints' probed with M13. Nucleic Acids Res. 1988 May 11;16(9):4161–4161. doi: 10.1093/nar/16.9.4161. [DOI] [PMC free article] [PubMed] [Google Scholar]

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