#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

An Excess of Gene Expression Divergence on the X Chromosome in Embryos: Implications for the Faster-X Hypothesis


The X chromosome is present as a single copy in the heterogametic sex, and this hemizygosity is expected to drive unusual patterns of evolution on the X relative to the autosomes. For example, the hemizgosity of the X may lead to a lower chromosomal effective population size compared to the autosomes, suggesting that the X might be more strongly affected by genetic drift. However, the X may also experience stronger positive selection than the autosomes, because recessive beneficial mutations will be more visible to selection on the X where they will spend less time being masked by the dominant, less beneficial allele—a proposal known as the faster-X hypothesis. Thus, empirical studies demonstrating increased genetic divergence on the X chromosome could be indicative of either adaptive or non-adaptive evolution. We measured gene expression in Drosophila species and in D. melanogaster inbred strains for both embryos and adults. In the embryos we found that expression divergence is on average more than 20% higher for genes on the X chromosome relative to the autosomes; but in contrast, in the inbred strains, gene expression variation is significantly lower on the X chromosome. Furthermore, expression divergence of genes on Muller's D element is significantly greater along the branch leading to the obscura sub-group, in which this element segregates as a neo-X chromosome. In the adults, divergence is greatest on the X chromosome for males, but not for females, yet in both sexes inbred strains harbour the lowest level of gene expression variation on the X chromosome. We consider different explanations for our results and conclude that they are most consistent within the framework of the faster-X hypothesis.


Vyšlo v časopise: An Excess of Gene Expression Divergence on the X Chromosome in Embryos: Implications for the Faster-X Hypothesis. PLoS Genet 8(12): e32767. doi:10.1371/journal.pgen.1003200
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003200

Souhrn

The X chromosome is present as a single copy in the heterogametic sex, and this hemizygosity is expected to drive unusual patterns of evolution on the X relative to the autosomes. For example, the hemizgosity of the X may lead to a lower chromosomal effective population size compared to the autosomes, suggesting that the X might be more strongly affected by genetic drift. However, the X may also experience stronger positive selection than the autosomes, because recessive beneficial mutations will be more visible to selection on the X where they will spend less time being masked by the dominant, less beneficial allele—a proposal known as the faster-X hypothesis. Thus, empirical studies demonstrating increased genetic divergence on the X chromosome could be indicative of either adaptive or non-adaptive evolution. We measured gene expression in Drosophila species and in D. melanogaster inbred strains for both embryos and adults. In the embryos we found that expression divergence is on average more than 20% higher for genes on the X chromosome relative to the autosomes; but in contrast, in the inbred strains, gene expression variation is significantly lower on the X chromosome. Furthermore, expression divergence of genes on Muller's D element is significantly greater along the branch leading to the obscura sub-group, in which this element segregates as a neo-X chromosome. In the adults, divergence is greatest on the X chromosome for males, but not for females, yet in both sexes inbred strains harbour the lowest level of gene expression variation on the X chromosome. We consider different explanations for our results and conclude that they are most consistent within the framework of the faster-X hypothesis.


Zdroje

1. HaldaneJBS (1924) A mathematical theory of natural and artificial selection. part i. Trans Camb Phil Soc 23: 19–41.

2. MullerHJ (1940) The New Systematics, Oxford University Press, chapter Bearings of the Drosophila work on systematics. 185–268.

3. AveryPJ (1984) The population genetics of haplo-diploids and x-linked genes. Genet Res 44: 321–341.

4. HartlDL (1971) Some aspects of natural selection in arrhenotokous populations. Am Zool 11: 309–325.

5. CharlesworthB, CoyneJ, BartonNH (1987) The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130: 113–146.

6. RiceWR (1984) Sex chromosomes and the evolution of sexual dimorphism. Evolution 38: 735–742.

7. VicosoB, CharlesworthB (2006) Evolution on the x chromosome: unusual patterns and processes. Nat Rev Genet 7: 645–653.

8. HaldaneJBS (1921) Sex-ratio and unisexual sterility in hybrid animals. J Genet 12: 101–109.

9. GurbichTA, BachtrogD (2008) Gene content evolution on the x chromosome. Curr Opin Genet Dev 18: 493–498.

10. SkuseDH (2005) X-linked genes and mental functioning. Hum Mol Genet 14 Spec No 1: R27–R32.

11. InnocentiP, MorrowEH (2010) The sexually antagonistic genes of drosophila melanogaster. PLoS Biol 8: e1000335 doi:10.1371/journal.pbio.1000335.

12. ZechnerU, WildaM, Kehrer-SawatzkiH, VogelW, FundeleR, et al. (2001) A high density of x-linked genes for general cognitive ability: a run-away process shaping human evolution? Trends Genet 17: 697–701.

13. DobzhanskyT (1936) Studies on hybrid sterility. ii. localization of sterility factors in drosophila pseudoobscura hybrids. Genetics 21: 113–135.

14. TempletonAR (1977) Analysis of head shape differences between two interfertile species of hawaiian drosophila. Evolution 31: 630–641.

15. CoyneJA, CharlesworthB (1986) Location of an x-linked factor causing sterility in male hybrids of drosophila simulans and d. mauritiana. Heredity (Edinb) 57: 243–246.

16. LuJ, WuCI (2005) Weak selection revealed by the whole-genome comparison of the x chromosome and autosomes of human and chimpanzee. Proc Natl Acad Sci U S A 102: 4063–4067.

17. ConsortiumCSA (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437: 69–87.

18. HvilsomC, QianY, BataillonT, LiY, MailundT, et al. (2012) Extensive x-linked adaptive evolution in central chimpanzees. Proc Natl Acad Sci U S A 109: 2054–2059.

19. BetancourtAJ, PresgravesDC, SwansonWJ (2002) A test for faster x evolution in drosophila. Mol Biol Evol 19: 1816–1819.

20. ThorntonK, BachtrogD, AndolfattoP (2006) X chromosomes and autosomes evolve at similar rates in drosophila: no evidence for faster-x protein evolution. Genome Res 16: 498–504.

21. ConnallonT (2007) Adaptive protein evolution of x-linked and autosomal genes in drosophila: implications for faster-x hypotheses. Mol Biol Evol 24: 2566–2572.

22. ThorntonK, LongM (2002) Rapid divergence of gene duplicates on the drosophila melanogaster x chromosome. Mol Biol Evol 19: 918–925.

23. CountermanBA, Ortz-BarrientosD, NoorMAF (2004) Using comparative genomic data to test for fast-x evolution. Evolution 58: 656–660.

24. ThorntonK, LongM (2005) Excess of amino acid substitutions relative to polymorphism between x-linked duplications in drosophila melanogaster. Mol Biol Evol 22: 273–284.

25. HuTT, EisenMB, ThorntonKR, AndolfattoP (2012) A second generation assembly of the drosophila simulans genome provides new insights into patterns of lineage-specific divergence. Genome Res

26. BachtrogD, JensenJD, ZhangZ (2009) Accelerated adaptive evolution on a newly formed x chromosome. PLoS Biol 7: e1000082 doi:10.1371/journal.pbio.1000082.

27. JaquieryJ, StoeckelS, RispeC, MieuzetL, LegeaiF, et al. (2012) Accelerated evolution of sex chromosomes in aphids, an x0 system. Mol Biol Evol 29: 837–847.

28. MankJE, AxelssonE, EllegrenH (2007) Fast-x on the z: rapid evolution of sex-linked genes in birds. Genome Res 17: 618–624.

29. AndolfattoP (2005) Adaptive evolution of non-coding dna in drosophila. Nature 437: 1149–1152.

30. KalinkaAT, VargaKM, GerrardDT, PreibischS, CorcoranDL, et al. (2010) Gene expression divergence recapitulates the developmental hourglass model. Nature 468: 811–814.

31. ZhangY, SturgillD, ParisiM, KumarS, OliverB (2007) Constraint and turnover in sex-biased gene expression in the genus drosophila. Nature 450: 233–237.

32. AyrolesJF, CarboneMA, StoneEA, JordanKW, LymanRF, et al. (2009) Systems genetics of complex traits in drosophila melanogaster. Nat Genet 41: 299–307.

33. MackayTFC, RichardsS, StoneEA, BarbadillaA, AyrolesJF, et al. (2012) The drosophila melanogaster genetic reference panel. Nature 482: 173–178.

34. VicosoB, CharlesworthB (2009) Effective population size and the faster-x effect: an extended model. Evolution 63: 2413–2426.

35. RifkinSA, HouleD, KimJ, WhiteKP (2005) A mutation accumulation assay reveals a broad capacity for rapid evolution of gene expression. Nature 438: 220–223.

36. HouleD, MorikawaB, LynchM (1996) Comparing mutational variabilities. Genetics 143: 1467–1483.

37. MikhaylovaLM, NurminskyDI (2011) Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the drosophila x chromosome. BMC Biol 9: 29.

38. TomancakP, BermanBP, BeatonA, WeiszmannR, KwanE, et al. (2007) Global analysis of patterns of gene expression during drosophila embryogenesis. Genome Biol 8: R145.

39. FrankeA, DernburgA, BashawGJ, BakerBS (1996) Evidence that msl-mediated dosage compensation in drosophila begins at blastoderm. Development 122: 2751–2760.

40. LottSE, VillaltaJE, SchrothGP, LuoS, TonkinLA, et al. (2011) Noncanonical compensation of zygotic x transcription in early drosophila melanogaster development revealed through single-embryo rna-seq. PLoS Biol 9: e1000590 doi:10.1371/journal.pbio.1000590.

41. HuangW, RichardsS, CarboneMA, ZhuD, AnholtRRH, et al. (2012) Epistasis dominates the genetic architecture of drosophila quantitative traits. Proc Natl Acad Sci U S A 109: 15553–15559.

42. ConnallonT, ClarkAG (2010) Sex linkage, sex-specific selection, and the role of recombination in the evolution of sexually dimorphic gene expression. Evolution 64: 3417–3442.

43. LlopartA (2012) The rapid evolution of x-linked male-biased gene expression and the large-x effect in drosophila yakuba, d. santomea and their hybrids. Mol Biol Evol 29: 3873–3886.

44. BrawandD, SoumillonM, NecsuleaA, JulienP, CsrdiG, et al. (2011) The evolution of gene expression levels in mammalian organs. Nature 478: 343–348.

45. GoodJM, GigerT, DeanMD, NachmanMW (2010) Widespread over-expression of the x chromosome in sterile fhybrid mice. PLoS Genet 6: e1001148 doi:10.1371/journal.pgen.1001148.

46. MeiselRP, MaloneJH, ClarkAG (2012) Faster-x evolution of gene expression in drosophila. PLoS Genet 8: e1003013 doi:10.1371/journal.pgen.1003013.

47. SinghND, MacphersonJM, JensenJD, PetrovDA (2007) Similar levels of x-linked and autosomal nucleotide variation in african and non-african populations of drosophila melanogaster. BMC Evol Biol 7: 202.

48. SinghND, DavisJC, PetrovDA (2005) X-linked genes evolve higher codon bias in drosophila and caenorhabditis. Genetics 171: 145–155.

49. SinghND, LarracuenteAM, ClarkAG (2008) Contrasting the efficacy of selection on the x and autosomes in drosophila. Mol Biol Evol 25: 454–467.

50. VicosoB, HaddrillPR, CharlesworthB (2008) A multispecies approach for comparing sequence evolution of x-linked and autosomal sites in drosophila. Genet Res (Camb) 90: 421–431.

51. TakahashiKH, TanakaK, ItohM, Takano-ShimizuT (2009) Reduced x-linked rare polymorphism in males in comparison to females of drosophila melanogaster. J Hered 100: 97–105.

52. CamposJL, CharlesworthB, HaddrillPR (2012) Molecular evolution in nonrecombining regions of the drosophila melanogaster genome. Genome Biol Evol 4: 278–288.

53. AndolfattoP, WongKM, BachtrogD (2011) Effective population size and the efficacy of selection on the x chromosomes of two closely related drosophila species. Genome Biol Evol 3: 114–128.

54. WittkoppPJ, HaerumBK, ClarkAG (2004) Evolutionary changes in cis and trans gene regulation. Nature 430: 85–88.

55. LemosB, AraripeLO, FontanillasP, HartlDL (2008) Dominance and the evolutionary accumulation of cis- and trans-effects on gene expression. Proc Natl Acad Sci U S A 105: 14471–14476.

56. WittkoppPJ, HaerumBK, ClarkAG (2008) Regulatory changes underlying expression differences within and between drosophila species. Nat Genet 40: 346–350.

57. WangHY, FuY, McPeekMS, LuX, NuzhdinS, et al. (2008) Complex genetic interactions underlying expression differences between drosophila races: analysis of chromosome substitutions. Proc Natl Acad Sci U S A 105: 6362–6367.

58. WittkoppPJ, HaerumBK, ClarkAG (2008) Independent effects of cis- and trans-regulatory variation on gene expression in drosophila melanogaster. Genetics 178: 1831–1835.

59. McManusCJ, CoolonJD, DuffMO, Eipper-MainsJ, GraveleyBR, et al. (2010) Regulatory divergence in drosophila revealed by mrna-seq. Genome Res 20: 816–825.

60. GrazeRM, McIntyreLM, MainBJ, WayneML, NuzhdinSV (2009) Regulatory divergence in drosophila melanogaster and d. simulans, a genomewide analysis of allele-specific expression. Genetics 183: 547–61, 1SI-21SI.

61. LuX, ShapiroJA, TingCT, LiY, LiC, et al. (2010) Genome-wide misexpression of x-linked versus autosomal genes associated with hybrid male sterility. Genome Res 20: 1097–1102.

62. SternDL (2000) Evolutionary developmental biology and the problem of variation. Evolution 54: 1079–1091.

63. Prud'hommeB, GompelN, CarrollSB (2007) Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A 104 Suppl 1: 8605–8612.

64. WrayGA (2007) The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8: 206–216.

65. RebeizM, PoolJE, KassnerVA, AquadroCF, CarrollSB (2009) Stepwise modification of a modular enhancer underlies adaptation in a drosophila population. Science 326: 1663–1667.

66. PeterIS, DavidsonEH (2011) Evolution of gene regulatory networks controlling body plan development. Cell 144: 970–985.

67. BurkeMK, DunhamJP, ShahrestaniP, ThorntonKR, RoseMR, et al. (2010) Genome-wide analysis of a long-term evolution experiment with drosophila. Nature 467: 587–590.

68. OrrHA, BetancourtAJ (2001) Haldane's sieve and adaptation from the standing genetic variation. Genetics 157: 875–884.

69. SellisD, CallahanBJ, PetrovDA, MesserPW (2011) Heterozygote advantage as a natural consequence of adaptation in diploids. Proc Natl Acad Sci U S A 108: 20666–20671.

70. WaddingtonCH (1942) Canalization of development and the inheritance of acquired characters. Nature 150: 563–565.

71. FisherRA (1928) The possible modification of the response of the wild type to recurrent mutations. Am Nat 62: 115–126.

72. BourguetD (1999) The evolution of dominance. Heredity 83: 1–4.

73. ProulxSR, PhillipsPC (2005) The opportunity for canalization and the evolution of genetic networks. Am Nat 165: 147–162.

74. BilliardS, CastricV (2011) Evidence for fisher's dominance theory: how many ‘special cases’? Trends Genet 27: 441–445.

75. WagnerA (2008) Robustness and evolvability: a paradox resolved. Proc Biol Sci 275: 91–100.

76. MaselJ, TrotterMV (2010) Robustness and evolvability. Trends Genet 26: 406–414.

77. DraghiJA, ParsonsTL, WagnerGP, PlotkinJB (2010) Mutational robustness can facilitate adaptation. Nature 463: 353–355.

78. KerrMK, MartinM, ChurchillGA (2000) Analysis of variance for gene expression microarray data. J Comput Biol 7: 819–837.

79. SmythGK (2005) Bioinformatics and Computational Biology Solutions using R and Bioconductor, Springer, chapter Limma: linear models for microarray data. 397–420.

80. FelsensteinJ (1989) Phylip - phylogeny inference package (version 3.2). Cladistics 5: 164–166.

81. MarkowTA, O'GradyPM (2007) Drosophila biology in the genomic age. Genetics 177: 1269–1276.

82. R Development Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. ISBN 3-900051-07-0.

83. RanzJM, Castillo-DavisCI, MeiklejohnCD, HartlDL (2003) Sex-dependent gene expression and evolution of the drosophila transcriptome. Science 300: 1742–1745.

84. MeiklejohnCD, ParschJ, RanzJM, HartlDL (2003) Rapid evolution of male-biased gene expression in drosophila. Proc Natl Acad Sci U S A 100: 9894–9899.

85. ZeileisA, MeyerD, HornikK (2007) Residual-based shadings for visualizing (conditional) independence. J Comp Graph Stat 16: 507–525.

86. AlexaA, RahnenfhrerJ, LengauerT (2006) Improved scoring of functional groups from gene expression data by decorrelating go graph structure. Bioinformatics 22: 1600–1607.

87. GrossmannS, BauerS, RobinsonPN, VingronM (2007) Improved detection of overrepresentation of gene-ontology annotations with parent child analysis. Bioinformatics 23: 3024–3031.

88. Pollard KS, Gilbert HN, Ge Y, S T, Dudoit S (2003) multtest: Resampling-based multiple hypothesis testing. Technical report, R package version 2.8.0.

89. RobertsonA (1966) A mathematical model of the culling process in dairy cattle. Anim Prod 8: 95–108.

90. PriceGR (1970) Selection and covariance. Nature 227: 520–521.

91. YuleGU (1903) Notes on the theory of association of attributes in statistics. Biometrika 2: 121–134.

92. SimpsonEH (1951) The interpretation of interaction in contingency tables. J Roy Statist Soc B 13: 238–241.

93. BlythCR (1972) On simpson's paradox and the sure-thing principle. J of the American Statistical Association 67: 364–366.

94. WagnerCH (1982) Simpson's paradox in real life. The American Statistician 36: 46–48.

95. WilcoxAJ (2001) On the importance–and the unimportance–of birthweight. Int J Epidemiol 30: 1233–1241.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 12
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#