Abstract
Sex chromosomes are generally morphologically and functionally distinct, but the evolutionary forces that cause this differentiation are poorly understood. Drosophila americana americana was used in this study to examine one aspect of sex chromosome evolution, the degeneration of nonrecombining Y chromosomes. The primary X chromosome of D. a. americana is fused with a chromosomal element that was ancestrally an autosome, causing this homologous chromosomal pair to segregate with the sex chromosomes. Sequence variation at the Alcohol Dehydrogenase (Adh) gene was used to determine the pattern of nucleotide variation on the neo-sex chromosomes in natural populations. Sequences of Adh were obtained for neo-X and neo-Y chromosomes of D. a. americana, and for Adh of D. a. texana, in which it is autosomal. No significant sequence differentiation is present between the neo-X and neo-Y chromosomes of D. a. americana or the autosomes of D. a. texana. There is a significantly lower level of sequence diversity on the neo-Y chromosome relative to the neo-X in D. a. americana. This reduction in variability on the neo-Y does not appear to have resulted from a selective sweep. Coalescent simulations of the evolutionary transition of an autosome into a Y chromosome indicate there may be a low level of recombination between the neo-X and neo-Y alleles of Adh and that the effective population size of this chromosome may have been reduced below the expected value of 25% of the autosomal effective size, possibly because of the effects of background selection or sexual selection.
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- Barton N. H. The effects of linkage and density-dependent regulation on gene flow. Heredity (Edinb) 1986 Dec;57(Pt 3):415–426. doi: 10.1038/hdy.1986.142. [DOI] [PubMed] [Google Scholar]
- Barton N., Bengtsson B. O. The barrier to genetic exchange between hybridising populations. Heredity (Edinb) 1986 Dec;57(Pt 3):357–376. doi: 10.1038/hdy.1986.135. [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]
- Caballero A. On the effective size of populations with separate sexes, with particular reference to sex-linked genes. Genetics. 1995 Feb;139(2):1007–1011. doi: 10.1093/genetics/139.2.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Charlesworth B., Charlesworth D., Hnilicka J., Yu A., Guttman D. S. Lack of degeneration of loci on the neo-Y chromosome of Drosophila americana americana. Genetics. 1997 Apr;145(4):989–1002. doi: 10.1093/genetics/145.4.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Charlesworth B., Charlesworth D. Rapid fixation of deleterious alleles can be caused by Muller's ratchet. Genet Res. 1997 Aug;70(1):63–73. doi: 10.1017/s0016672397002899. [DOI] [PubMed] [Google Scholar]
- Charlesworth B. Model for evolution of Y chromosomes and dosage compensation. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5618–5622. doi: 10.1073/pnas.75.11.5618. [DOI] [PMC free article] [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., Nordborg M., Charlesworth D. The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet Res. 1997 Oct;70(2):155–174. doi: 10.1017/s0016672397002954. [DOI] [PubMed] [Google Scholar]
- Charlesworth B. The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet Res. 1994 Jun;63(3):213–227. doi: 10.1017/s0016672300032365. [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]
- Fridolfsson A. K., Cheng H., Copeland N. G., Jenkins N. A., Liu H. C., Raudsepp T., Woodage T., Chowdhary B., Halverson J., Ellegren H. Evolution of the avian sex chromosomes from an ancestral pair of autosomes. Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8147–8152. doi: 10.1073/pnas.95.14.8147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fu Y. X., Li W. H. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. doi: 10.1093/genetics/133.3.693. [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., Hauschteck-Jungen E., Beukeboom L. W. Is the Y chromosome of Drosophila an evolved supernumerary chromosome? Bioessays. 1996 Apr;18(4):317–323. doi: 10.1002/bies.950180410. [DOI] [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]
- Hilton H., Hey J. DNA sequence variation at the period locus reveals the history of species and speciation events in the Drosophila virilis group. Genetics. 1996 Nov;144(3):1015–1025. doi: 10.1093/genetics/144.3.1015. [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]
- Marín I., Franke A., Bashaw G. J., Baker B. S. The dosage compensation system of Drosophila is co-opted by newly evolved X chromosomes. Nature. 1996 Sep 12;383(6596):160–163. doi: 10.1038/383160a0. [DOI] [PubMed] [Google Scholar]
- Muller H J. Genetic Variability, Twin Hybrids and Constant Hybrids, in a Case of Balanced Lethal Factors. Genetics. 1918 Sep;3(5):422–499. doi: 10.1093/genetics/3.5.422. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nagylaki T. The inbreeding effective population number in dioecious populations. Genetics. 1995 Jan;139(1):473–485. doi: 10.1093/genetics/139.1.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nordborg M. Structured coalescent processes on different time scales. Genetics. 1997 Aug;146(4):1501–1514. doi: 10.1093/genetics/146.4.1501. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nurminsky D. I., Moriyama E. N., Lozovskaya E. R., Hartl D. L. Molecular phylogeny and genome evolution in the Drosophila virilis species group: duplications of the alcohol dehydrogenase gene. Mol Biol Evol. 1996 Jan;13(1):132–149. doi: 10.1093/oxfordjournals.molbev.a025551. [DOI] [PubMed] [Google Scholar]
- Orr H. A., Kim Y. An adaptive hypothesis for the evolution of the Y chromosome. Genetics. 1998 Dec;150(4):1693–1698. doi: 10.1093/genetics/150.4.1693. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rice W. R. Degeneration of a nonrecombining chromosome. Science. 1994 Jan 14;263(5144):230–232. doi: 10.1126/science.8284674. [DOI] [PubMed] [Google Scholar]
- Rice W. R. Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics. 1987 May;116(1):161–167. doi: 10.1093/genetics/116.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rice W. R. Male fitness increases when females are eliminated from gene pool: implications for the Y chromosome. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6217–6221. doi: 10.1073/pnas.95.11.6217. [DOI] [PMC free article] [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]
- Steinemann M., Steinemann S. Enigma of Y chromosome degeneration: neo-Y and neo-X chromosomes of Drosophila miranda a model for sex chromosome evolution. Genetica. 1998;102-103(1-6):409–420. [PubMed] [Google Scholar]
- Takahata N., Nei M. Gene genealogy and variance of interpopulational nucleotide differences. Genetics. 1985 Jun;110(2):325–344. doi: 10.1093/genetics/110.2.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tominaga H., Narise S. Sequence evolution of the Gpdh gene in the Drosophila virilis species group. Genetica. 1995;96(3):293–302. doi: 10.1007/BF01439583. [DOI] [PubMed] [Google Scholar]
- Wakeley J. Segregating sites in Wright's island model. Theor Popul Biol. 1998 Apr;53(2):166–174. doi: 10.1006/tpbi.1997.1355. [DOI] [PubMed] [Google Scholar]
- Wakeley J. The variance of pairwise nucleotide differences in two populations with migration. Theor Popul Biol. 1996 Feb;49(1):39–57. doi: 10.1006/tpbi.1996.0002. [DOI] [PubMed] [Google Scholar]
