• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Nov 2003; 165(3): 1317–1328.
PMCID: PMC1462813

Sequence differentiation associated with an inversion on the neo-X chromosome of Drosophila americana.

Abstract

Sex chromosomes originate from pairs of autosomes that acquire controlling genes in the sex-determining cascade. Universal mechanisms apparently influence the evolution of sex chromosomes, because this chromosomal pair is characteristically heteromorphic in a broad range of organisms. To examine the pattern of initial differentiation between sex chromosomes, sequence analyses were performed on a pair of newly formed sex chromosomes in Drosophila americana. This species has neo-sex chromosomes as a result of a centromeric fusion between the X chromosome and an autosome. Sequences were analyzed from the Alcohol dehydrogenase (Adh), big brain (bib), and timeless (tim) gene regions, which represent separate positions along this pair of neo-sex chromosomes. In the northwestern range of the species, the bib and Adh regions exhibit significant sequence differentiation for neo-X chromosomes relative to neo-Y chromosomes from the same geographic region and other chromosomal populations of D. americana. Furthermore, a nucleotide site defining a common haplotype in bib is shown to be associated with a paracentric inversion [In(4)ab] on the neo-X chromosome, and this inversion suppresses recombination between neo-X and neo-Y chromosomes. These observations are consistent with the inversion acting as a recombination modifier that suppresses exchange between these neo-sex chromosomes, as predicted by models of sex chromosome evolution.

Full Text

The Full Text of this article is available as a PDF (154K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Depaulis F, Veuille M. Neutrality tests based on the distribution of haplotypes under an infinite-site model. Mol Biol Evol. 1998 Dec;15(12):1788–1790. [PubMed]
  • Depaulis F, Mousset S, Veuille M. Haplotype tests using coalescent simulations conditional on the number of segregating sites. Mol Biol Evol. 2001 Jun;18(6):1136–1138. [PubMed]
  • Dobzhansky T, Epling C. The Suppression of Crossing Over in Inversion Heterozygotes of Drosophila Pseudoobscura. Proc Natl Acad Sci U S A. 1948 Apr;34(4):137–141. [PMC free article] [PubMed]
  • Fay JC, Wu CI. Hitchhiking under positive Darwinian selection. Genetics. 2000 Jul;155(3):1405–1413. [PMC free article] [PubMed]
  • Fu YX, Li WH. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. [PMC free article] [PubMed]
  • Gibson Jonathan R, Chippindale Adam K, Rice William R. The X chromosome is a hot spot for sexually antagonistic fitness variation. Proc Biol Sci. 2002 Mar 7;269(1490):499–505. [PMC free article] [PubMed]
  • Gordo I, Charlesworth B. The speed of Muller's ratchet with background selection, and the degeneration of Y chromosomes. Genet Res. 2001 Oct;78(2):149–161. [PubMed]
  • Marshall Graves JA, Shetty S. Sex from W to Z: evolution of vertebrate sex chromosomes and sex determining genes. J Exp Zool. 2001 Sep 15;290(5):449–462. [PubMed]
  • Hey J, Wakeley J. A coalescent estimator of the population recombination rate. Genetics. 1997 Mar;145(3):833–846. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Hudson RR, Kreitman M, Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. [PMC free article] [PubMed]
  • Atanassov I, Delichère C, Filatov DA, Charlesworth D, Negrutiu I, Monéger F. Analysis and evolution of two functional Y-linked loci in a plant sex chromosome system. Mol Biol Evol. 2001 Dec;18(12):2162–2168. [PubMed]
  • Hudson RR, Boos DD, Kaplan NL. A statistical test for detecting geographic subdivision. Mol Biol Evol. 1992 Jan;9(1):138–151. [PubMed]
  • Bachtrog Doris. Adaptation shapes patterns of genome evolution on sexual and asexual chromosomes in Drosophila. Nat Genet. 2003 Jun;34(2):215–219. [PubMed]
  • Bachtrog Doris, Charlesworth Brian. Reduced adaptation of a non-recombining neo-Y chromosome. Nature. 2002 Mar 21;416(6878):323–326. [PubMed]
  • Kim Y, Stephan W. Joint effects of genetic hitchhiking and background selection on neutral variation. Genetics. 2000 Jul;155(3):1415–1427. [PMC free article] [PubMed]
  • Lahn BT, Page DC. Four evolutionary strata on the human X chromosome. Science. 1999 Oct 29;286(5441):964–967. [PubMed]
  • Burris PA, Zhang Y, Rusconi JC, Corbin V. The pore-forming and cytoplasmic domains of the neurogenic gene product, BIG BRAIN, are conserved between Drosophila virilis and Drosophila melanogaster. Gene. 1998 Jan 5;206(1):69–76. [PubMed]
  • McAllister Bryant F. Chromosomal and allelic variation in Drosophila americana: selective maintenance of a chromosomal cline. Genome. 2002 Feb;45(1):13–21. [PubMed]
  • Charlesworth B. The evolution of chromosomal sex determination and dosage compensation. Curr Biol. 1996 Feb 1;6(2):149–162. [PubMed]
  • McAllister BF, Charlesworth B. Reduced sequence variability on the Neo-Y chromosome of Drosophila americana americana. Genetics. 1999 Sep;153(1):221–233. [PMC free article] [PubMed]
  • McAllister BF, McVean GA. Neutral evolution of the sex-determining gene transformer in Drosophila. Genetics. 2000 Apr;154(4):1711–1720. [PMC free article] [PubMed]
  • Charlesworth B, Charlesworth D. The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci. 2000 Nov 29;355(1403):1563–1572. [PMC free article] [PubMed]
  • Moore Richard C, Kozyreva Olga, Lebel-Hardenack Sabine, Siroky Jiri, Hobza Roman, Vyskot Boris, Grant Sarah R. Genetic and functional analysis of DD44, a sex-linked gene from the dioecious plant Silene latifolia, provides clues to early events in sex chromosome evolution. Genetics. 2003 Jan;163(1):321–334. [PMC free article] [PubMed]
  • Charlesworth Deborah. Plant sex determination and sex chromosomes. Heredity (Edinb) 2002 Feb;88(2):94–101. [PubMed]
  • Myers MP, Rothenfluh A, Chang M, Young MW. Comparison of chromosomal DNA composing timeless in Drosophila melanogaster and D. virilis suggests a new conserved structure for the TIMELESS protein. Nucleic Acids Res. 1997 Dec 1;25(23):4710–4714. [PMC free article] [PubMed]
  • Coyne JA, Aulard S, Berry A. Lack of underdominance in a naturally occurring pericentric inversion in Drosophila melanogaster and its implications for chromosome evolution. Genetics. 1991 Nov;129(3):791–802. [PMC free article] [PubMed]
  • Navarro A, Betrán E, Zapata C, Ruiz A. Dynamics of gametic disequilibria between loci linked to chromosome inversions: the recombination-redistributing effect of inversions. Genet Res. 1996 Feb;67(1):67–76. [PubMed]
  • Schlötterer C. Microsatellite analysis indicates genetic differentiation of the neo-sex chromosomes in Drosophila americana americana. Heredity (Edinb) 2000 Dec;85(Pt 6):610–616. [PubMed]
  • Navarro A, Barbadilla A, Ruiz A. Effect of inversion polymorphism on the neutral nucleotide variability of linked chromosomal regions in Drosophila. Genetics. 2000 Jun;155(2):685–698. [PMC free article] [PubMed]
  • Nurminsky DI, Moriyama EN, Lozovskaya ER, Hartl DL. 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. [PubMed]
  • Orr HA, Kim Y. An adaptive hypothesis for the evolution of the Y chromosome. Genetics. 1998 Dec;150(4):1693–1698. [PMC free article] [PubMed]
  • Ousley A, Zafarullah K, Chen Y, Emerson M, Hickman L, Sehgal A. Conserved regions of the timeless (tim) clock gene in Drosophila analyzed through phylogenetic and functional studies. Genetics. 1998 Feb;148(2):815–825. [PMC free article] [PubMed]
  • Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics. 1983 Oct;105(2):437–460. [PMC free article] [PubMed]
  • Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. [PMC free article] [PubMed]
  • Piálek J, Barton NH. The spread of an advantageous allele across a barrier: the effects of random drift and selection against heterozygotes. Genetics. 1997 Feb;145(2):493–504. [PMC free article] [PubMed]
  • Vieira J, McAllister BF, Charlesworth B. Evidence for selection at the fused1 locus of Drosophila americana. Genetics. 2001 May;158(1):279–290. [PMC free article] [PubMed]
  • Rice WR. Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics. 1987 May;116(1):161–167. [PMC free article] [PubMed]
  • Rice WR. Sexually antagonistic genes: experimental evidence. Science. 1992 Jun 5;256(5062):1436–1439. [PubMed]
  • Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. [PubMed]
  • Rice Geoffrey W. Annotated bibliography for the history of medicine & health in New Zealand. Med Hist. 1996 Apr;40(2):256–257. [PMC free article]
  • Whiting JH, Jr, Pliley MD, Farmer JL, Jeffery DE. In situ hybridization analysis of chromosomal homologies in Drosophila melanogaster and Drosophila virilis. Genetics. 1989 May;122(1):99–109. [PMC free article] [PubMed]
  • Rozas J, Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...