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Genetics. May 2004; 167(1): 377–385.
PMCID: PMC1470867

Reduced variation on the chicken Z chromosome.


Understanding the population genetic factors that shape genome variability is pivotal to the design and interpretation of studies using large-scale polymorphism data. We analyzed patterns of polymorphism and divergence at Z-linked and autosomal loci in the domestic chicken (Gallus gallus) to study the influence of mutation, effective population size, selection, and demography on levels of genetic diversity. A total of 14 autosomal introns (8316 bp) and 13 Z-linked introns (6856 bp) were sequenced in 50 chicken chromosomes from 10 highly divergent breeds. Genetic variation was significantly lower at Z-linked than at autosomal loci, with one segregating site every 39 bp at autosomal loci (theta(W) = 5.8 +/- 0.8 x 10(-3)) and one every 156 bp on the Z chromosome (theta(W) = 1.4 +/- 0.4 x 10(-3)). This difference may in part be due to a low male effective population size arising from skewed reproductive success among males, evident both in the wild ancestor-the red jungle fowl-and in poultry breeding. However, this effect cannot entirely explain the observed three- to fourfold reduction in Z chromosome diversity. Selection, in particular selective sweeps, may therefore have had an impact on reducing variation on the Z chromosome, a hypothesis supported by the observation of heterogeneity in diversity levels among loci on the Z chromosome and the lower recombination rate on Z than on autosomes. Selection on sex-linked genes may be particularly important in organisms with female heterogamety since the heritability of sex-linked sexually antagonistic alleles advantageous to males is improved when fathers pass a Z chromosome to their sons.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bartosch-Härlid Anna, Berlin Sofia, Smith Nick G C, Møller Anders P, Ellegren Hans. Life history and the male mutation bias. Evolution. 2003 Oct;57(10):2398–2406. [PubMed]
  • Begun DJ, Whitley P. Reduced X-linked nucleotide polymorphism in Drosophila simulans. Proc Natl Acad Sci U S A. 2000 May 23;97(11):5960–5965. [PMC free article] [PubMed]
  • Betrán Esther, Thornton Kevin, Long Manyuan. Retroposed new genes out of the X in Drosophila. Genome Res. 2002 Dec;12(12):1854–1859. [PMC free article] [PubMed]
  • Bitgood JJ. Linkage relationships of the Z-linked silver, slow feathering, and pop-eye loci. Poult Sci. 1999 Aug;78(8):1100–1101. [PubMed]
  • Braverman JM, Hudson RR, Kaplan NL, Langley CH, Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. [PMC free article] [PubMed]
  • Burnside J, Liou SS, Zhong C, Cogburn LA. Abnormal growth hormone receptor gene expression in the sex-linked dwarf chicken. Gen Comp Endocrinol. 1992 Oct;88(1):20–28. [PubMed]
  • Carmichael AN, Fridolfsson AK, Halverson J, Ellegren H. Male-biased mutation rates revealed from Z and W chromosome-linked ATP synthase alpha-subunit (ATP5A1) sequences in birds. J Mol Evol. 2000 May;50(5):443–447. [PubMed]
  • Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. [PMC free article] [PubMed]
  • Charlesworth D, Charlesworth B, Morgan MT. The pattern of neutral molecular variation under the background selection model. Genetics. 1995 Dec;141(4):1619–1632. [PMC free article] [PubMed]
  • Cho RJ, Mindrinos M, Richards DR, Sapolsky RJ, Anderson M, Drenkard E, Dewdney J, Reuber TL, Stammers M, Federspiel N, et al. Genome-wide mapping with biallelic markers in Arabidopsis thaliana. Nat Genet. 1999 Oct;23(2):203–207. [PubMed]
  • Civetta A, Singh RS. High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species. J Mol Evol. 1995 Dec;41(6):1085–1095. [PubMed]
  • Coyne JA. Genetics and speciation. Nature. 1992 Feb 6;355(6360):511–515. [PubMed]
  • Dimcheff Derek E, Drovetski Sergei V, Mindell David P. Phylogeny of Tetraoninae and other galliform birds using mitochondrial 12S and ND2 genes. Mol Phylogenet Evol. 2002 Aug;24(2):203–215. [PubMed]
  • Ebersberger Ingo, Metzler Dirk, Schwarz Carsten, Päbo Svante. Genomewide comparison of DNA sequences between humans and chimpanzees. Am J Hum Genet. 2002 Jun;70(6):1490–1497. [PMC free article] [PubMed]
  • Ellegren H, Fridolfsson AK. Male-driven evolution of DNA sequences in birds. Nat Genet. 1997 Oct;17(2):182–184. [PubMed]
  • Ellegren Hans, Smith Nick G C, Webster Matthew T. Mutation rate variation in the mammalian genome. Curr Opin Genet Dev. 2003 Dec;13(6):562–568. [PubMed]
  • Fay JC, Wu CI. A human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation. Mol Biol Evol. 1999 Jul;16(7):1003–1005. [PubMed]
  • Fridolfsson AK, Cheng H, Copeland NG, Jenkins NA, Liu HC, 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. [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]
  • Fumihito A, Miyake T, Sumi S, Takada M, Ohno S, Kondo N. One subspecies of the red junglefowl (Gallus gallus gallus) suffices as the matriarchic ancestor of all domestic breeds. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12505–12509. [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]
  • Groenen MA, Cheng HH, Bumstead N, Benkel BF, Briles WE, Burke T, Burt DW, Crittenden LB, Dodgson J, Hillel J, et al. A consensus linkage map of the chicken genome. Genome Res. 2000 Jan;10(1):137–147. [PMC free article] [PubMed]
  • Parsanejad R, Zadworny D, Kuhnlein U. Genetic variability of the cytosolic phosphoenolpyruvate carboxykinase gene in white leghorn chickens. Poult Sci. 2002 Nov;81(11):1668–1670. [PubMed]
  • Hammer Michael F, Blackmer Felisa, Garrigan Dan, Nachman Michael W, Wilder Jason A. Human population structure and its effects on sampling Y chromosome sequence variation. Genetics. 2003 Aug;164(4):1495–1509. [PMC free article] [PubMed]
  • Patil N, Berno AJ, Hinds DA, Barrett WA, Doshi JM, Hacker CR, Kautzer CR, Lee DH, Marjoribanks C, McDonough DP, et al. Blocks of limited haplotype diversity revealed by high-resolution scanning of human chromosome 21. Science. 2001 Nov 23;294(5547):1719–1723. [PubMed]
  • Hardison Ross C, Roskin Krishna M, Yang Shan, Diekhans Mark, Kent W James, Weber Ryan, Elnitski Laura, Li Jia, O'Connor Michael, Kolbe Diana, et al. Covariation in frequencies of substitution, deletion, transposition, and recombination during eutherian evolution. Genome Res. 2003 Jan;13(1):13–26. [PMC free article] [PubMed]
  • Pizzari T, Birkhead TR. The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism. Biol Rev Camb Philos Soc. 2002 May;77(2):183–209. [PubMed]
  • Hillel Jossi, Groenen Martien A M, Tixier-Boichard Michèle, Korol Abraham B, David Lior, Kirzhner Valery M, Burke Terry, Barre-Dirie Asili, Crooijmans Richard P M A, Elo Kari, et al. Biodiversity of 52 chicken populations assessed by microsatellite typing of DNA pools. Genet Sel Evol. 2003 Sep-Oct;35(5):533–557. [PMC free article] [PubMed]
  • Presgraves Daven C, Balagopalan Lakshmi, Abmayr Susan M, Orr H Allen. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature. 2003 Jun 12;423(6941):715–719. [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]
  • Ptak Susan E, Przeworski Molly. Evidence for population growth in humans is confounded by fine-scale population structure. Trends Genet. 2002 Nov;18(11):559–563. [PubMed]
  • Hurst LD, Ellegren H. Sex biases in the mutation rate. Trends Genet. 1998 Nov;14(11):446–452. [PubMed]
  • Ranz José M, Castillo-Davis Cristian I, Meiklejohn Colin D, Hartl Daniel L. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science. 2003 Jun 13;300(5626):1742–1745. [PubMed]
  • Waterston Robert H, Lindblad-Toh Kerstin, Birney Ewan, Rogers Jane, Abril Josep F, Agarwal Pankaj, Agarwala Richa, Ainscough Rachel, Alexandersson Marina, et al. Initial sequencing and comparative analysis of the mouse genome. Nature. 2002 Dec 5;420(6915):520–562. [PubMed]
  • Sachidanandam R, Weissman D, Schmidt SC, Kakol JM, Stein LD, Marth G, Sherry S, Mullikin JC, Mortimore BJ, Willey DL, et al. A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms. Nature. 2001 Feb 15;409(6822):928–933. [PubMed]
  • Iyengar Vikram K, Reeve H Kern, Eisner Thomas. Paternal inheritance of a female moth's mating preference. Nature. 2002 Oct 24;419(6909):830–832. [PubMed]
  • Kahn NW, Quinn TW. Male-driven evolution among Eoaves? A test of the replicative division hypothesis in a heterogametic female (ZW) system. J Mol Evol. 1999 Dec;49(6):750–759. [PubMed]
  • Kaplan NL, Hudson RR, Langley CH. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. [PMC free article] [PubMed]
  • Reinke V, Smith HE, Nance J, Wang J, Van Doren C, Begley R, Jones SJ, Davis EB, Scherer S, Ward S, et al. A global profile of germline gene expression in C. elegans. Mol Cell. 2000 Sep;6(3):605–616. [PubMed]
  • Koch R, van Luenen HG, van der Horst M, Thijssen KL, Plasterk RH. Single nucleotide polymorphisms in wild isolates of Caenorhabditis elegans. Genome Res. 2000 Nov;10(11):1690–1696. [PMC free article] [PubMed]
  • Rosenberg NA, Burke T, Elo K, Feldman MW, Freidlin PJ, Groenen MA, Hillel J, Mäki-Tanila A, Tixier-Boichard M, Vignal A, et al. Empirical evaluation of genetic clustering methods using multilocus genotypes from 20 chicken breeds. Genetics. 2001 Oct;159(2):699–713. [PMC free article] [PubMed]
  • Lercher MJ, Williams EJ, Hurst LD. Local similarity in evolutionary rates extends over whole chromosomes in human-rodent and mouse-rat comparisons: implications for understanding the mechanistic basis of the male mutation bias. Mol Biol Evol. 2001 Nov;18(11):2032–2039. [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]
  • Lercher Martin J, Urrutia Araxi O, Hurst Laurence D. Evidence that the human X chromosome is enriched for male-specific but not female-specific genes. Mol Biol Evol. 2003 Jul;20(7):1113–1116. [PubMed]
  • Saetre Glenn-Peter, Borge Thomas, Lindroos Katarina, Haavie Jon, Sheldon Ben C, Primmer Craig, Syvänen Ann-Christine. Sex chromosome evolution and speciation in Ficedula flycatchers. Proc Biol Sci. 2003 Jan 7;270(1510):53–59. [PMC free article] [PubMed]
  • Levin I, Crittenden LB, Dodgson JB. Genetic map of the chicken Z chromosome using random amplified polymorphic DNA (RAPD) markers. Genomics. 1993 Apr;16(1):224–230. [PubMed]
  • Saifi GM, Chandra HS. An apparent excess of sex- and reproduction-related genes on the human X chromosome. Proc Biol Sci. 1999 Jan 22;266(1415):203–209. [PMC free article] [PubMed]
  • Li Wen Hsiung, Yi Soojin, Makova Kateryna. Male-driven evolution. Curr Opin Genet Dev. 2002 Dec;12(6):650–656. [PubMed]
  • Schmid M, Nanda I, Guttenbach M, Steinlein C, Hoehn M, Schartl M, Haaf T, Weigend S, Fries R, Buerstedde JM, et al. First report on chicken genes and chromosomes 2000. Cytogenet Cell Genet. 2000;90(3-4):169–218. [PubMed]
  • Smith JM, Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed]
  • Simonsen KL, Churchill GA, Aquadro CF. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics. 1995 Sep;141(1):413–429. [PMC free article] [PubMed]
  • Meiklejohn Colin D, Parsch John, Ranz José M, Hartl Daniel L. Rapid evolution of male-biased gene expression in Drosophila. Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):9894–9899. [PMC free article] [PubMed]
  • Miyata T, Hayashida H, Kuma K, Mitsuyasu K, Yasunaga T. Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harb Symp Quant Biol. 1987;52:863–867. [PubMed]
  • Smith EJ, Shi L, Smith G. Expressed sequence tags for the chicken genome from a normalized 10-day-old white leghorn whole-embryo cDNA library. 3. DNA sequence analysis of genetic variation in commercial chicken populations. Genome. 2002 Apr;45(2):261–267. [PubMed]
  • Mullikin JC, Hunt SE, Cole CG, Mortimore BJ, Rice CM, Burton J, Matthews LH, Pavitt R, Plumb RW, Sims SK, et al. An SNP map of human chromosome 22. Nature. 2000 Sep 28;407(6803):516–520. [PubMed]
  • Nanda I, Haaf T, Schartl M, Schmid M, Burt DW. Comparative mapping of Z-orthologous genes in vertebrates: implications for the evolution of avian sex chromosomes. Cytogenet Genome Res. 2002;99(1-4):178–184. [PubMed]
  • Smith Nick G C, Webster Matthew T, Ellegren Hans. Deterministic mutation rate variation in the human genome. Genome Res. 2002 Sep;12(9):1350–1356. [PMC free article] [PubMed]
  • Orr HA, Coyne JA. The genetics of postzygotic isolation in the Drosophila virilis group. Genetics. 1989 Mar;121(3):527–537. [PMC free article] [PubMed]
  • Swanson Willie J, Vacquier Victor D. The rapid evolution of reproductive proteins. Nat Rev Genet. 2002 Feb;3(2):137–144. [PubMed]
  • Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7375–7379. [PMC free article] [PubMed]
  • Wade Claire M, Kulbokas Edward J, 3rd, Kirby Andrew W, Zody Michael C, Mullikin James C, Lander Eric S, Lindblad-Toh Kerstin, Daly Mark J. The mosaic structure of variation in the laboratory mouse genome. Nature. 2002 Dec 5;420(6915):574–578. [PubMed]
  • Wang PJ, McCarrey JR, Yang F, Page DC. An abundance of X-linked genes expressed in spermatogonia. Nat Genet. 2001 Apr;27(4):422–426. [PubMed]
  • Tajima F. The effect of change in population size on DNA polymorphism. Genetics. 1989 Nov;123(3):597–601. [PMC free article] [PubMed]
  • Zhu YL, Song QJ, Hyten DL, Van Tassell CP, Matukumalli LK, Grimm DR, Hyatt SM, Fickus EW, Young ND, Cregan PB. Single-nucleotide polymorphisms in soybean. Genetics. 2003 Mar;163(3):1123–1134. [PMC free article] [PubMed]
  • Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9161–9166. [PMC free article] [PubMed]
  • Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. [PMC free article] [PubMed]

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