Natural Selection and the Frequency Distributions of ``silent'' DNA Polymorphism in Drosophila (original) (raw)

Abstract

In Escherichia coli, Saccharomyces cerevisiae, and Drosophila melanogaster, codon bias may be maintained by a balance among mutation pressure, genetic drift, and natural selection favoring translationally superior codons. Under such an evolutionary model, silent mutations fall into two fitness categories: preferred mutations that increase codon bias and unpreferred changes in the opposite direction. This prediction can be tested by comparing the frequency spectra of synonymous changes segregating within populations; natural selection will elevate the frequencies of advantageous mutations relative to that of deleterious changes. The frequency distributions of preferred and unpreferred mutations differ in the predicted direction among 99 alleles of two D. pseudoobscura genes and five alleles of eight D. simulans genes. This result confirms the existence of fitness classes of silent mutations. Maximum likelihood estimates suggest that selection intensity at silent sites is, on average, very weak in both D. pseudoobscura and D. simulans (|N(e)s| & 1). Inference of evolutionary processes from within-species sequence variation is often hindered by the assumption of a stationary frequency distribution. This assumption can be avoided when identifying the action of selection and tested when estimating selection intensity.

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Selected References

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  1. Aguade M., Miyashita N., Langley C. H. Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics. 1989 Jul;122(3):607–615. doi: 10.1093/genetics/122.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Andersson S. G., Kurland C. G. Codon preferences in free-living microorganisms. Microbiol Rev. 1990 Jun;54(2):198–210. doi: 10.1128/mr.54.2.198-210.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ayala F. J., Hartl D. L. Molecular drift of the bride of sevenless (boss) gene in Drosophila. Mol Biol Evol. 1993 Sep;10(5):1030–1040. doi: 10.1093/oxfordjournals.molbev.a040052. [DOI] [PubMed] [Google Scholar]
  4. Beckman J. S., Weber J. L. Survey of human and rat microsatellites. Genomics. 1992 Apr;12(4):627–631. doi: 10.1016/0888-7543(92)90285-z. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Begun D. J., Aquadro C. F. African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature. 1993 Oct 7;365(6446):548–550. doi: 10.1038/365548a0. [DOI] [PubMed] [Google Scholar]
  7. Begun D. J., Aquadro C. F. Molecular population genetics of the distal portion of the X chromosome in Drosophila: evidence for genetic hitchhiking of the yellow-achaete region. Genetics. 1991 Dec;129(4):1147–1158. doi: 10.1093/genetics/129.4.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Begun D. J., Aquadro C. F. Molecular variation at the vermilion locus in geographically diverse populations of Drosophila melanogaster and D. simulans. Genetics. 1995 Jul;140(3):1019–1032. doi: 10.1093/genetics/140.3.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Begun D. J., Aquadro C. F. Molecular variation at the vermilion locus in geographically diverse populations of Drosophila melanogaster and D. simulans. Genetics. 1995 Jul;140(3):1019–1032. doi: 10.1093/genetics/140.3.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bennetzen J. L., Hall B. D. Codon selection in yeast. J Biol Chem. 1982 Mar 25;257(6):3026–3031. [PubMed] [Google Scholar]
  11. 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. doi: 10.1093/genetics/134.3.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Bowcock A. M., Ruiz-Linares A., Tomfohrde J., Minch E., Kidd J. R., Cavalli-Sforza L. L. High resolution of human evolutionary trees with polymorphic microsatellites. Nature. 1994 Mar 31;368(6470):455–457. doi: 10.1038/368455a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Carulli J. P., Krane D. E., Hartl D. L., Ochman H. Compositional heterogeneity and patterns of molecular evolution in the Drosophila genome. Genetics. 1993 Jul;134(3):837–845. doi: 10.1093/genetics/134.3.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Charlesworth B., Morgan M. T., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. doi: 10.1093/genetics/134.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Crombie T., Boyle J. P., Coggins J. R., Brown A. J. The folding of the bifunctional TRP3 protein in yeast is influenced by a translational pause which lies in a region of structural divergence with Escherichia coli indoleglycerol-phosphate synthase. Eur J Biochem. 1994 Dec 1;226(2):657–664. doi: 10.1111/j.1432-1033.1994.tb20093.x. [DOI] [PubMed] [Google Scholar]
  18. Crombie T., Swaffield J. C., Brown A. J. Protein folding within the cell is influenced by controlled rates of polypeptide elongation. J Mol Biol. 1992 Nov 5;228(1):7–12. doi: 10.1016/0022-2836(92)90486-4. [DOI] [PubMed] [Google Scholar]
  19. Curran J. F. Analysis of effects of tRNA:message stability on frameshift frequency at the Escherichia coli RF2 programmed frameshift site. Nucleic Acids Res. 1993 Apr 25;21(8):1837–1843. doi: 10.1093/nar/21.8.1837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Curran J. F., Yarus M. Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. J Mol Biol. 1989 Sep 5;209(1):65–77. doi: 10.1016/0022-2836(89)90170-8. [DOI] [PubMed] [Google Scholar]
  21. Curran J. F., Yarus M. Use of tRNA suppressors to probe regulation of Escherichia coli release factor 2. J Mol Biol. 1988 Sep 5;203(1):75–83. doi: 10.1016/0022-2836(88)90092-7. [DOI] [PubMed] [Google Scholar]
  22. Damerval C., Maurice A., Josse J. M., de Vienne D. Quantitative trait loci underlying gene product variation: a novel perspective for analyzing regulation of genome expression. Genetics. 1994 May;137(1):289–301. doi: 10.1093/genetics/137.1.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. David P., Delay B., Berthou P., Jarne P. Alternative models for allozyme-associated heterosis in the marine bivalve Spisula ovalis. Genetics. 1995 Apr;139(4):1719–1726. doi: 10.1093/genetics/139.4.1719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Dib C., Fauré S., Fizames C., Samson D., Drouot N., Vignal A., Millasseau P., Marc S., Hazan J., Seboun E. A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature. 1996 Mar 14;380(6570):152–154. doi: 10.1038/380152a0. [DOI] [PubMed] [Google Scholar]
  26. Dietrich W. F., Miller J., Steen R., Merchant M. A., Damron-Boles D., Husain Z., Dredge R., Daly M. J., Ingalls K. A., O'Connor T. J. A comprehensive genetic map of the mouse genome. Nature. 1996 Mar 14;380(6570):149–152. doi: 10.1038/380149a0. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. England P. R., Briscoe D. A., Frankham R. Microsatellite polymorphisms in a wild population of Drosophila melanogaster. Genet Res. 1996 Jun;67(3):285–290. doi: 10.1017/s0016672300033760. [DOI] [PubMed] [Google Scholar]
  29. Estoup A., Garnery L., Solignac M., Cornuet J. M. Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics. 1995 Jun;140(2):679–695. doi: 10.1093/genetics/140.2.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ewens W. J. Population genetics theory in relation to the neutralist-selectionist controversy. Adv Hum Genet. 1977;8:67–134. doi: 10.1007/978-1-4615-8267-0_2. [DOI] [PubMed] [Google Scholar]
  31. Ewens W. J. The sampling theory of selectively neutral alleles. Theor Popul Biol. 1972 Mar;3(1):87–112. doi: 10.1016/0040-5809(72)90035-4. [DOI] [PubMed] [Google Scholar]
  32. Eyre-Walker A., Bulmer M. Reduced synonymous substitution rate at the start of enterobacterial genes. Nucleic Acids Res. 1993 Sep 25;21(19):4599–4603. doi: 10.1093/nar/21.19.4599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Eyre-Walker A., Bulmer M. Synonymous substitution rates in enterobacteria. Genetics. 1995 Aug;140(4):1407–1412. doi: 10.1093/genetics/140.4.1407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Fu Y. X. Estimating effective population size or mutation rate using the frequencies of mutations of various classes in a sample of DNA sequences. Genetics. 1994 Dec;138(4):1375–1386. doi: 10.1093/genetics/138.4.1375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Fu Y. X., Li W. H. Maximum likelihood estimation of population parameters. Genetics. 1993 Aug;134(4):1261–1270. doi: 10.1093/genetics/134.4.1261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Garton D. W., Koehn R. K., Scott T. M. Multiple-locus heterozygosity and the physiological energetics of growth in the coot clam, Mulinia lateralis, from a natural population. Genetics. 1984 Oct;108(2):445–455. doi: 10.1093/genetics/108.2.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Gillespie J. H., Turelli M. Genotype-environment interactions and the maintenance of polygenic variation. Genetics. 1989 Jan;121(1):129–138. doi: 10.1093/genetics/121.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Grosjean H., Fiers W. Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene. 1982 Jun;18(3):199–209. doi: 10.1016/0378-1119(82)90157-3. [DOI] [PubMed] [Google Scholar]
  39. Hale L. R., Singh R. S. Mitochondrial DNA variation and genetic structure in populations of Drosophila melanogaster. Mol Biol Evol. 1987 Nov;4(6):622–637. doi: 10.1093/oxfordjournals.molbev.a040466. [DOI] [PubMed] [Google Scholar]
  40. Hartl D. L., Moriyama E. N., Sawyer S. A. Selection intensity for codon bias. Genetics. 1994 Sep;138(1):227–234. doi: 10.1093/genetics/138.1.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Hudson R. R. Estimating the recombination parameter of a finite population model without selection. Genet Res. 1987 Dec;50(3):245–250. doi: 10.1017/s0016672300023776. [DOI] [PubMed] [Google Scholar]
  42. Hudson R. R., Slatkin M., Maddison W. P. Estimation of levels of gene flow from DNA sequence data. Genetics. 1992 Oct;132(2):583–589. doi: 10.1093/genetics/132.2.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Ikemura T. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. J Mol Biol. 1981 Sep 25;151(3):389–409. doi: 10.1016/0022-2836(81)90003-6. [DOI] [PubMed] [Google Scholar]
  44. Ikemura T. Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs. J Mol Biol. 1982 Jul 15;158(4):573–597. doi: 10.1016/0022-2836(82)90250-9. [DOI] [PubMed] [Google Scholar]
  45. Jorde P. E., Ryman N. Demographic genetics of brown trout (Salmo trutta) and estimation of effective population size from temporal change of allele frequencies. Genetics. 1996 Jul;143(3):1369–1381. doi: 10.1093/genetics/143.3.1369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. KAHANA S. E., LOWRY O. H., SCHULZ D. W., PASSONNEAU J. V., CRAWFORD E. J. The kinetics of phosphoglucoisomerase. J Biol Chem. 1960 Aug;235:2178–2184. [PubMed] [Google Scholar]
  47. Kacser H., Burns J. A. The molecular basis of dominance. Genetics. 1981 Mar-Apr;97(3-4):639–666. doi: 10.1093/genetics/97.3-4.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Karl S. A., Avise J. C. PCR-based assays of mendelian polymorphisms from anonymous single-copy nuclear DNA: techniques and applications for population genetics. Mol Biol Evol. 1993 Mar;10(2):342–361. doi: 10.1093/oxfordjournals.molbev.a040002. [DOI] [PubMed] [Google Scholar]
  49. Keith T. P., Brooks L. D., Lewontin R. C., Martinez-Cruzado J. C., Rigby D. L. Nearly identical allelic distributions of xanthine dehydrogenase in two populations of Drosophila pseudoobscura. Mol Biol Evol. 1985 May;2(3):206–216. doi: 10.1093/oxfordjournals.molbev.a040348. [DOI] [PubMed] [Google Scholar]
  50. Kimura M., Ohta T. Protein polymorphism as a phase of molecular evolution. Nature. 1971 Feb 12;229(5285):467–469. doi: 10.1038/229467a0. [DOI] [PubMed] [Google Scholar]
  51. 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]
  52. Kliman R. M., Hey J. The effects of mutation and natural selection on codon bias in the genes of Drosophila. Genetics. 1994 Aug;137(4):1049–1056. doi: 10.1093/genetics/137.4.1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Koehn R. K., Diehl W. J., Scott T. M. The differential contribution by individual enzymes of glycolysis and protein catabolism to the relationship between heterozygosity and growth rate in the coot clam, Mulinia lateralis. Genetics. 1988 Jan;118(1):121–130. doi: 10.1093/genetics/118.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. 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]
  55. 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]
  56. Kreitman M. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature. 1983 Aug 4;304(5925):412–417. doi: 10.1038/304412a0. [DOI] [PubMed] [Google Scholar]
  57. Latter B. D. Enzyme polymorphisms: gene frequency distributions with mutation and selection for optimal activity. Genetics. 1975 Feb;79(2):325–331. doi: 10.1093/genetics/79.2.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Lewontin R. C., Hubby J. L. A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics. 1966 Aug;54(2):595–609. doi: 10.1093/genetics/54.2.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Lewontin R. C. Twenty-five years ago in Genetics: electrophoresis in the development of evolutionary genetics: milestone or millstone? Genetics. 1991 Aug;128(4):657–662. doi: 10.1093/genetics/128.4.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Lynch M. The consequences of fluctuating selection for isozyme polymorphisms in Daphnia. Genetics. 1987 Apr;115(4):657–669. doi: 10.1093/genetics/115.4.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Martin C. H., Mayeda C. A., Meyerowitz E. M. Evolution and expression of the Sgs-3 glue gene of Drosophila. J Mol Biol. 1988 May 20;201(2):273–287. doi: 10.1016/0022-2836(88)90138-6. [DOI] [PubMed] [Google Scholar]
  62. McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
  63. Michalakis Y., Veuille M. Length variation of CAG/CAA trinucleotide repeats in natural populations of Drosophila melanogaster and its relation to the recombination rate. Genetics. 1996 Aug;143(4):1713–1725. doi: 10.1093/genetics/143.4.1713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Miller S. A., Dykes D. D., Polesky H. F. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988 Feb 11;16(3):1215–1215. doi: 10.1093/nar/16.3.1215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Moriyama E. N., Hartl D. L. Codon usage bias and base composition of nuclear genes in Drosophila. Genetics. 1993 Jul;134(3):847–858. doi: 10.1093/genetics/134.3.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Moriyama E. N., Powell J. R. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 1996 Jan;13(1):261–277. doi: 10.1093/oxfordjournals.molbev.a025563. [DOI] [PubMed] [Google Scholar]
  67. Muki T., Watanabe T. K., Yamaguchi O. The genetic structure of natural populations of Drosophila melanogaster. XII. Linkage disequilibrium in a large local population. Genetics. 1974 Aug;77(4):771–793. doi: 10.1093/genetics/77.4.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Nei M., Roychoudhury A. K. Sampling variances of heterozygosity and genetic distance. Genetics. 1974 Feb;76(2):379–390. doi: 10.1093/genetics/76.2.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. 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]
  70. Ota T. Statistical analyses of Drosophila and human protein polymorphisms. Proc Natl Acad Sci U S A. 1975 Aug;72(8):3194–3196. doi: 10.1073/pnas.72.8.3194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Palumbi S. R., Baker C. S. Contrasting population structure from nuclear intron sequences and mtDNA of humpback whales. Mol Biol Evol. 1994 May;11(3):426–435. doi: 10.1093/oxfordjournals.molbev.a040115. [DOI] [PubMed] [Google Scholar]
  72. Pardue M. L., Lowenhaupt K., Rich A., Nordheim A. (dC-dA)n.(dG-dT)n sequences have evolutionarily conserved chromosomal locations in Drosophila with implications for roles in chromosome structure and function. EMBO J. 1987 Jun;6(6):1781–1789. doi: 10.1002/j.1460-2075.1987.tb02431.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Pogson G. H. Expression of overdominance for specific activity at the phosphoglucomutase-2 locus in the Pacific oyster, Crassostrea gigas. Genetics. 1991 May;128(1):133–141. doi: 10.1093/genetics/128.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Pogson G. H., Zouros E. Allozyme and RFLP heterozygosities as correlates of growth rate in the scallop Placopecten magellanicus: a test of the associative overdominance hypothesis. Genetics. 1994 May;137(1):221–231. doi: 10.1093/genetics/137.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Pogson G. H., Zouros E. Allozyme and RFLP heterozygosities as correlates of growth rate in the scallop Placopecten magellanicus: a test of the associative overdominance hypothesis. Genetics. 1994 May;137(1):221–231. doi: 10.1093/genetics/137.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Purvis I. J., Bettany A. J., Santiago T. C., Coggins J. R., Duncan K., Eason R., Brown A. J. The efficiency of folding of some proteins is increased by controlled rates of translation in vivo. A hypothesis. J Mol Biol. 1987 Jan 20;193(2):413–417. doi: 10.1016/0022-2836(87)90230-0. [DOI] [PubMed] [Google Scholar]
  77. Rassmann K., Schlötterer C., Tautz D. Isolation of simple-sequence loci for use in polymerase chain reaction-based DNA fingerprinting. Electrophoresis. 1991 Feb-Mar;12(2-3):113–118. doi: 10.1002/elps.1150120205. [DOI] [PubMed] [Google Scholar]
  78. Reynolds J., Weir B. S., Cockerham C. C. Estimation of the coancestry coefficient: basis for a short-term genetic distance. Genetics. 1983 Nov;105(3):767–779. doi: 10.1093/genetics/105.3.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Sawyer S. A., Dykhuizen D. E., Hartl D. L. Confidence interval for the number of selectively neutral amino acid polymorphisms. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6225–6228. doi: 10.1073/pnas.84.17.6225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Sawyer S. A., Hartl D. L. Population genetics of polymorphism and divergence. Genetics. 1992 Dec;132(4):1161–1176. doi: 10.1093/genetics/132.4.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Schaeffer S. W., Miller E. L. Estimates of gene flow in Drosophila pseudoobscura determined from nucleotide sequence analysis of the alcohol dehydrogenase region. Genetics. 1992 Oct;132(2):471–480. doi: 10.1093/genetics/132.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Schaeffer S. W., Miller E. L. Estimates of linkage disequilibrium and the recombination parameter determined from segregating nucleotide sites in the alcohol dehydrogenase region of Drosophila pseudoobscura. Genetics. 1993 Oct;135(2):541–552. doi: 10.1093/genetics/135.2.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Schaeffer S. W., Miller E. L. Nucleotide sequence analysis of Adh genes estimates the time of geographic isolation of the Bogota population of Drosophila pseudoobscura. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6097–6101. doi: 10.1073/pnas.88.14.6097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Schatz G., Dobberstein B. Common principles of protein translocation across membranes. Science. 1996 Mar 15;271(5255):1519–1526. doi: 10.1126/science.271.5255.1519. [DOI] [PubMed] [Google Scholar]
  85. Schlötterer C., Pemberton J. The use of microsatellites for genetic analysis of natural populations. EXS. 1994;69:203–214. doi: 10.1007/978-3-0348-7527-1_11. [DOI] [PubMed] [Google Scholar]
  86. Schlötterer C., Tautz D. Slippage synthesis of simple sequence DNA. Nucleic Acids Res. 1992 Jan 25;20(2):211–215. doi: 10.1093/nar/20.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Schug M. D., Mackay T. F., Aquadro C. F. Low mutation rates of microsatellite loci in Drosophila melanogaster. Nat Genet. 1997 Jan;15(1):99–102. doi: 10.1038/ng0197-99. [DOI] [PubMed] [Google Scholar]
  88. Sharp P. M., Li W. H. An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol. 1986;24(1-2):28–38. doi: 10.1007/BF02099948. [DOI] [PubMed] [Google Scholar]
  89. Sharp P. M., Li W. H. On the rate of DNA sequence evolution in Drosophila. J Mol Evol. 1989 May;28(5):398–402. doi: 10.1007/BF02603075. [DOI] [PubMed] [Google Scholar]
  90. Sharp P. M., Li W. H. The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol Biol Evol. 1987 May;4(3):222–230. doi: 10.1093/oxfordjournals.molbev.a040443. [DOI] [PubMed] [Google Scholar]
  91. Shields D. C., Sharp P. M., Higgins D. G., Wright F. "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol. 1988 Nov;5(6):704–716. doi: 10.1093/oxfordjournals.molbev.a040525. [DOI] [PubMed] [Google Scholar]
  92. 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]
  93. Simonsen K. L., Churchill G. A., Aquadro C. F. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics. 1995 Sep;141(1):413–429. doi: 10.1093/genetics/141.1.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Singh R. S., Rhomberg L. R. A Comprehensive Study of Genic Variation in Natural Populations of Drosophila melanogaster. I. Estimates of Gene Flow from Rare Alleles. Genetics. 1987 Feb;115(2):313–322. doi: 10.1093/genetics/115.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  96. Smith J. M., Smith N. H. Site-specific codon bias in bacteria. Genetics. 1996 Mar;142(3):1037–1043. doi: 10.1093/genetics/142.3.1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Sueoka N. Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2653–2657. doi: 10.1073/pnas.85.8.2653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Tautz D., Schlötterer Simple sequences. Curr Opin Genet Dev. 1994 Dec;4(6):832–837. doi: 10.1016/0959-437x(94)90067-1. [DOI] [PubMed] [Google Scholar]
  99. Taylor M. F., Shen Y., Kreitman M. E. A population genetic test of selection at the molecular level. Science. 1995 Dec 1;270(5241):1497–1499. doi: 10.1126/science.270.5241.1497. [DOI] [PubMed] [Google Scholar]
  100. Valdes A. M., Slatkin M., Freimer N. B. Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics. 1993 Mar;133(3):737–749. doi: 10.1093/genetics/133.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Varenne S., Buc J., Lloubes R., Lazdunski C. Translation is a non-uniform process. Effect of tRNA availability on the rate of elongation of nascent polypeptide chains. J Mol Biol. 1984 Dec 15;180(3):549–576. doi: 10.1016/0022-2836(84)90027-5. [DOI] [PubMed] [Google Scholar]
  102. Viard F., Bremond P., Labbo R., Justy F., Delay B., Jarne P. Microsatellites and the genetics of highly selfing populations in the freshwater snail Bulinus truncatus. Genetics. 1996 Apr;142(4):1237–1247. doi: 10.1093/genetics/142.4.1237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Watt W. B. Adaptation at Specific Loci. II. Demographic and Biochemical Elements in the Maintenance of the Colias Pgi Polymorphism. Genetics. 1983 Apr;103(4):691–724. doi: 10.1093/genetics/103.4.691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Watt W. B. Adaptation at specific loci. I. Natural selection on phosphoglucose isomerase of Colias butterflies: Biochemical and population aspects. Genetics. 1977 Sep;87(1):177–194. doi: 10.1093/genetics/87.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. Watt W. B., Cassin R. C., Swan M. S. Adaptation at Specific Loci. III. Field Behavior and Survivorship Differences among Colias Pgi Genotypes Are Predictable from IN VITRO Biochemistry. Genetics. 1983 Apr;103(4):725–739. doi: 10.1093/genetics/103.4.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Watterson G. A. Heterosis or neutrality? Genetics. 1977 Apr;85(4):789–814. doi: 10.1093/genetics/85.4.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Weber J. L. Informativeness of human (dC-dA)n.(dG-dT)n polymorphisms. Genomics. 1990 Aug;7(4):524–530. doi: 10.1016/0888-7543(90)90195-z. [DOI] [PubMed] [Google Scholar]
  108. Weber J. L., May P. E. Abundant class of human DNA polymorphisms which can be typed using the polymerase chain reaction. Am J Hum Genet. 1989 Mar;44(3):388–396. [PMC free article] [PubMed] [Google Scholar]
  109. Wright S. The Distribution of Gene Frequencies Under Irreversible Mutation. Proc Natl Acad Sci U S A. 1938 Jul;24(7):253–259. doi: 10.1073/pnas.24.7.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  110. Zhivotovsky L. A., Feldman M. W. Microsatellite variability and genetic distances. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11549–11552. doi: 10.1073/pnas.92.25.11549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. Zouros E., Freeman K. R., Ball A. O., Pogson G. H. Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature. 1992 Oct 1;359(6394):412–414. doi: 10.1038/359412a0. [DOI] [PubMed] [Google Scholar]