Abstract
DNA sequence surveys of Drosophila melanogaster populations show a strong positive correlation between the recombination rate experienced by a locus and its level of nucleotide polymorphism. In particular, surveys of the fourth chromosome gene ci(D) show greatly reduced levels of nucleotide variation; this observation was originally interpreted in terms of selective sweeps occurring on the nonrecombining fourth chromosome. Subsequent theoretical work has, however, uncovered several other selective processes that can reduce variation. In this study, we revisit the Drosophila fourth chromosome, investigating variation in 5-6 kb of the gene ankyrin in D. melanogaster and D. simulans. Silent nucleotide site diversity is approximately 5 x 10(-4) for both species, consistent with the previous observations of low variation at ci(D). Given the observed frequency spectra at ankyrin, coalescent simulations indicate that reduced diversity in the region is unlikely to be due to a selective sweep alone. We find evidence for recombinational exchange at this locus, and both species appear to be fixed for an insertion of the transposable element HB in an intron of ankyrin.
Full Text
The Full Text of this article is available as a PDF (310.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
- 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]
- Aguadé M., Meyers W., Long A. D., Langley C. H. Single-strand conformation polymorphism analysis coupled with stratified DNA sequencing reveals reduced sequence variation in the su(s) and su(wa) regions of the Drosophila melanogaster X chromosome. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4658–4662. doi: 10.1073/pnas.91.11.4658. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Akashi H. Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster. Genetics. 1996 Nov;144(3):1297–1307. doi: 10.1093/genetics/144.3.1297. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Andolfatto P. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 2001 Mar;18(3):279–290. doi: 10.1093/oxfordjournals.molbev.a003804. [DOI] [PubMed] [Google Scholar]
- Andolfatto P., Przeworski M. Regions of lower crossing over harbor more rare variants in African populations of Drosophila melanogaster. Genetics. 2001 Jun;158(2):657–665. doi: 10.1093/genetics/158.2.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bandelt H. J., Forster P., Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999 Jan;16(1):37–48. doi: 10.1093/oxfordjournals.molbev.a026036. [DOI] [PubMed] [Google Scholar]
- Begun D. J., Aquadro C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. doi: 10.1038/356519a0. [DOI] [PubMed] [Google Scholar]
- Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999 Jan 15;27(2):573–580. doi: 10.1093/nar/27.2.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berry A. J., Ajioka J. W., Kreitman M. Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics. 1991 Dec;129(4):1111–1117. doi: 10.1093/genetics/129.4.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Biémont C., Cizeron G. Distribution of transposable elements in Drosophila species. Genetica. 1999;105(1):43–62. doi: 10.1023/a:1003718520490. [DOI] [PubMed] [Google Scholar]
- Braverman J. M., Hudson R. R., Kaplan N. L., Langley C. H., Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. doi: 10.1093/genetics/140.2.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brierley H. L., Potter S. S. Distinct characteristics of loop sequences of two Drosophila foldback transposable elements. Nucleic Acids Res. 1985 Jan 25;13(2):485–500. doi: 10.1093/nar/13.2.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Charlesworth B. Background selection and patterns of genetic diversity in Drosophila melanogaster. Genet Res. 1996 Oct;68(2):131–149. doi: 10.1017/s0016672300034029. [DOI] [PubMed] [Google Scholar]
- Charlesworth B., Lapid A., Canada D. The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genet Res. 1992 Oct;60(2):103–114. doi: 10.1017/s0016672300030792. [DOI] [PubMed] [Google Scholar]
- Charlesworth B., Lapid A., Canada D. The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements. Genet Res. 1992 Oct;60(2):115–130. doi: 10.1017/s0016672300030809. [DOI] [PubMed] [Google Scholar]
- 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]
- Charlesworth B., Sniegowski P., Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature. 1994 Sep 15;371(6494):215–220. doi: 10.1038/371215a0. [DOI] [PubMed] [Google Scholar]
- Charlesworth D., Charlesworth B., Morgan M. T. The pattern of neutral molecular variation under the background selection model. Genetics. 1995 Dec;141(4):1619–1632. doi: 10.1093/genetics/141.4.1619. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Comeron J. M., Kreitman M., Aguadé M. Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics. 1999 Jan;151(1):239–249. doi: 10.1093/genetics/151.1.239. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fay J. C., Wu C. I. Hitchhiking under positive Darwinian selection. Genetics. 2000 Jul;155(3):1405–1413. doi: 10.1093/genetics/155.3.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frisse L., Hudson R. R., Bartoszewicz A., Wall J. D., Donfack J., Di Rienzo A. Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. Am J Hum Genet. 2001 Aug 29;69(4):831–843. doi: 10.1086/323612. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fu Y. X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997 Oct;147(2):915–925. doi: 10.1093/genetics/147.2.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gillespie J. H. Junk ain't what junk does: neutral alleles in a selected context. Gene. 1997 Dec 31;205(1-2):291–299. doi: 10.1016/s0378-1119(97)00470-8. [DOI] [PubMed] [Google Scholar]
- Hackstein J. H., Hochstenbach R. The elusive fertility genes of Drosophila: the ultimate haven for selfish genetic elements. Trends Genet. 1995 May;11(5):195–200. doi: 10.1016/S0168-9525(00)89043-5. [DOI] [PubMed] [Google Scholar]
- Harris L. J., Baillie D. L., Rose A. M. Sequence identity between an inverted repeat family of transposable elements in Drosophila and Caenorhabditis. Nucleic Acids Res. 1988 Jul 11;16(13):5991–5998. doi: 10.1093/nar/16.13.5991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hawley R. S., McKim K. S., Arbel T. Meiotic segregation in Drosophila melanogaster females: molecules, mechanisms, and myths. Annu Rev Genet. 1993;27:281–317. doi: 10.1146/annurev.ge.27.120193.001433. [DOI] [PubMed] [Google Scholar]
- Henikoff S. Detection of Caenorhabditis transposon homologs in diverse organisms. New Biol. 1992 Apr;4(4):382–388. [PubMed] [Google Scholar]
- Hey J., Wakeley J. A coalescent estimator of the population recombination rate. Genetics. 1997 Mar;145(3):833–846. doi: 10.1093/genetics/145.3.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hilliker A. J., Harauz G., Reaume A. G., Gray M., Clark S. H., Chovnick A. Meiotic gene conversion tract length distribution within the rosy locus of Drosophila melanogaster. Genetics. 1994 Aug;137(4):1019–1026. doi: 10.1093/genetics/137.4.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hudson R. R., Kaplan N. L. Deleterious background selection with recombination. Genetics. 1995 Dec;141(4):1605–1617. doi: 10.1093/genetics/141.4.1605. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hudson R. R., Kaplan N. L. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 1985 Sep;111(1):147–164. doi: 10.1093/genetics/111.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Langley C. H., Lazzaro B. P., Phillips W., Heikkinen E., Braverman J. M. Linkage disequilibria and the site frequency spectra in the su(s) and su(w(a)) regions of the Drosophila melanogaster X chromosome. Genetics. 2000 Dec;156(4):1837–1852. doi: 10.1093/genetics/156.4.1837. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maside X., Assimacopoulos S., Charlesworth B. Rates of movement of transposable elements on the second chromosome of Drosophila melanogaster. Genet Res. 2000 Jun;75(3):275–284. doi: 10.1017/s0016672399004474. [DOI] [PubMed] [Google Scholar]
- McVean G. A., Charlesworth B. The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics. 2000 Jun;155(2):929–944. doi: 10.1093/genetics/155.2.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McVean G. A., Vieira J. Inferring parameters of mutation, selection and demography from patterns of synonymous site evolution in Drosophila. Genetics. 2001 Jan;157(1):245–257. doi: 10.1093/genetics/157.1.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Nachman M. W., Crowell S. L. Estimate of the mutation rate per nucleotide in humans. Genetics. 2000 Sep;156(1):297–304. doi: 10.1093/genetics/156.1.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Perlitz M., Stephan W. The mean and variance of the number of segregating sites since the last hitchhiking event. J Math Biol. 1997 Nov;36(1):1–23. doi: 10.1007/s002850050087. [DOI] [PubMed] [Google Scholar]
- Pritchard J. K., Schaeffer S. W. Polymorphism and divergence at a Drosophila pseudogene locus. Genetics. 1997 Sep;147(1):199–208. doi: 10.1093/genetics/147.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Przeworski M., Wall J. D., Andolfatto P. Recombination and the frequency spectrum in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 2001 Mar;18(3):291–298. doi: 10.1093/oxfordjournals.molbev.a003805. [DOI] [PubMed] [Google Scholar]
- Reugels A. M., Kurek R., Lammermann U., Bünemann H. Mega-introns in the dynein gene DhDhc7(Y) on the heterochromatic Y chromosome give rise to the giant threads loops in primary spermatocytes of Drosophila hydei. Genetics. 2000 Feb;154(2):759–769. doi: 10.1093/genetics/154.2.759. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rozas J., Rozas R. DnaSP version 2.0: a novel software package for extensive molecular population genetics analysis. Comput Appl Biosci. 1997 Jun;13(3):307–311. [PubMed] [Google Scholar]
- 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]
- Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
- Stephan W. An improved method for estimating the rate of fixation of favorable mutations based on DNA polymorphism data. Mol Biol Evol. 1995 Sep;12(5):959–962. doi: 10.1093/oxfordjournals.molbev.a040274. [DOI] [PubMed] [Google Scholar]
- Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics. 1983 Oct;105(2):437–460. doi: 10.1093/genetics/105.2.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takahata N., Ishii K., Matsuda H. Effect of temporal fluctuation of selection coefficient on gene frequency in a population. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4541–4545. doi: 10.1073/pnas.72.11.4541. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wall J. D. A comparison of estimators of the population recombination rate. Mol Biol Evol. 2000 Jan;17(1):156–163. doi: 10.1093/oxfordjournals.molbev.a026228. [DOI] [PubMed] [Google Scholar]
- Watterson G. A. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. doi: 10.1016/0040-5809(75)90020-9. [DOI] [PubMed] [Google Scholar]
- Weiss G., von Haeseler A. Inference of population history using a likelihood approach. Genetics. 1998 Jul;149(3):1539–1546. doi: 10.1093/genetics/149.3.1539. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zickler D., Kleckner N. Meiotic chromosomes: integrating structure and function. Annu Rev Genet. 1999;33:603–754. doi: 10.1146/annurev.genet.33.1.603. [DOI] [PubMed] [Google Scholar]