Abstract
We present the results of a restriction site survey of variation at five loci in Drosophila athabasca, complimenting a previous study of the period locus. There is considerably greater differentiation between the three semispecies of D. athabasca at the period locus and two other X-linked genes (no-on-transient-A and E74A) than at three autosomal genes (Xdh, Adh and RC98). Using a modification of the HKA test, which uses fixed differences between the semispecies and a test based on differences in Fst among loci, we show that the greater differentiation of the X-linked loci compared with the autosomal loci is inconsistent with a neutral model of molecular evolution. We explore several evolutionary scenarios by computer simulation, including differential migration of X and autosomal genes, very low levels of migration among the semispecies, selective sweeps, and background selection, and conclude that X-linked selective sweeps in at least two of the semispecies are the best explanation for the data. This evidence that natural selection acted on the X-chromosome suggests that another X-linked trait, mating song differences among the semispecies, may have been the target of selection.
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- 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 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]
- Chia W., Karp R., McGill S., Ashburner M. Molecular analysis of the Adh region of the genome of Drosophila melanogaster. J Mol Biol. 1985 Dec 20;186(4):689–706. doi: 10.1016/0022-2836(85)90389-4. [DOI] [PubMed] [Google Scholar]
- Coté B., Bender W., Curtis D., Chovnick A. Molecular mapping of the rosy locus in Drosophila melanogaster. Genetics. 1986 Apr;112(4):769–783. doi: 10.1093/genetics/112.4.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ewing A. W. The genetic basis of sound production in Drosophila pseudoobscura and D. persimilis. Anim Behav. 1969 Aug;17(3):555–560. doi: 10.1016/0003-3472(69)90164-x. [DOI] [PubMed] [Google Scholar]
- Ford M. J., Yoon C. K., Aquadro C. F. Molecular evolution of the period gene in Drosophila athabasca. Mol Biol Evol. 1994 Mar;11(2):169–182. doi: 10.1093/oxfordjournals.molbev.a040101. [DOI] [PubMed] [Google Scholar]
- Hey J., Kliman R. M. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol Biol Evol. 1993 Jul;10(4):804–822. doi: 10.1093/oxfordjournals.molbev.a040044. [DOI] [PubMed] [Google Scholar]
- Hey J. The structure of genealogies and the distribution of fixed differences between DNA sequence samples from natural populations. Genetics. 1991 Aug;128(4):831–840. doi: 10.1093/genetics/128.4.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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., Kreitman M., Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. doi: 10.1093/genetics/116.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones C. W., Dalton M. W., Townley L. H. Interspecific comparisons of the structure and regulation of the Drosophila ecdysone-inducible gene E74. Genetics. 1991 Mar;127(3):535–543. doi: 10.1093/genetics/127.3.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones K. R., Rubin G. M. Molecular analysis of no-on-transient A, a gene required for normal vision in Drosophila. Neuron. 1990 May;4(5):711–723. doi: 10.1016/0896-6273(90)90197-n. [DOI] [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]
- Karl S. A., Avise J. C. Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. Science. 1992 Apr 3;256(5053):100–102. doi: 10.1126/science.1348870. [DOI] [PubMed] [Google Scholar]
- Kliman R. M., Hey J. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics. 1993 Feb;133(2):375–387. doi: 10.1093/genetics/133.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kulkarni S. J., Steinlauf A. F., Hall J. C. The dissonance mutant of courtship song in Drosophila melanogaster: isolation, behavior and cytogenetics. Genetics. 1988 Feb;118(2):267–285. doi: 10.1093/genetics/118.2.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lande R., Kirkpatrick M. Ecological speciation by sexual selection. J Theor Biol. 1988 Jul 8;133(1):85–98. doi: 10.1016/s0022-5193(88)80026-2. [DOI] [PubMed] [Google Scholar]
- Lewontin R. C., Krakauer J. Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics. 1973 May;74(1):175–195. doi: 10.1093/genetics/74.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marfany G., Gonzàlez-Duarte R. The Drosophila subobscura Adh genomic region contains valuable evolutionary markers. Mol Biol Evol. 1992 Mar;9(2):261–277. doi: 10.1093/oxfordjournals.molbev.a040718. [DOI] [PubMed] [Google Scholar]
- Miller D. D., Voelker R. A. Salivary gland chromosome variation in the Drosophila affinis subgroup. IV. The short arm of the X chromosome in "western" and "eastern" Drosophila athabasca. J Hered. 1969 Nov-Dec;60(6):307–311. doi: 10.1093/oxfordjournals.jhered.a108001. [DOI] [PubMed] [Google Scholar]
- Miller D. D., Voelker R. A. Salivary gland chromosome variation in the Drosophila affinis subgroup. V. The B and E chromosomes of "western" and "eastern" Drosophila athabasca. J Hered. 1972 Jan-Feb;63(1):2–10. [PubMed] [Google Scholar]
- Nei M., Maruyama T. Letters to the editors: Lewontin-Krakauer test for neutral genes. Genetics. 1975 Jun;80(2):395–395. doi: 10.1093/genetics/80.2.395. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noor M. A. Speciation driven by natural selection in Drosophila. Nature. 1995 Jun 22;375(6533):674–675. doi: 10.1038/375674a0. [DOI] [PubMed] [Google Scholar]
- Pogson G. H., Mesa K. A., Boutilier R. G. 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. doi: 10.1093/genetics/139.1.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riley M. A. Nucleotide sequence of the Xdh region in Drosophila pseudoobscura and an analysis of the evolution of synonymous codons. Mol Biol Evol. 1989 Jan;6(1):33–52. doi: 10.1093/oxfordjournals.molbev.a040529. [DOI] [PubMed] [Google Scholar]
- Robertson A. Letters to the editors: Remarks on the Lewontin-Krakauer test. Genetics. 1975 Jun;80(2):396–396. doi: 10.1093/genetics/80.2.396. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Russo C. A., Takezaki N., Nei M. Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol. 1995 May;12(3):391–404. doi: 10.1093/oxfordjournals.molbev.a040214. [DOI] [PubMed] [Google Scholar]
- Wiehe T. H., Stephan W. Analysis of a genetic hitchhiking model, and its application to DNA polymorphism data from Drosophila melanogaster. Mol Biol Evol. 1993 Jul;10(4):842–854. doi: 10.1093/oxfordjournals.molbev.a040046. [DOI] [PubMed] [Google Scholar]
- Yoon C. K., Aquadro C. F. Mitochondrial DNA variation among the Drosophila athabasca semispecies and Drosophila affinis. J Hered. 1994 Nov-Dec;85(6):421–426. doi: 10.1093/oxfordjournals.jhered.a111495. [DOI] [PubMed] [Google Scholar]