Masculinization of the X Chromosome in the Pea Aphid

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Evolutionary theory predicts that sexually antagonistic mutations accumulate differentially on the X chromosome and autosomes in species with an XY sex-determination system, with effects (masculinization or feminization of the X) depending on the dominance of mutations. Organisms with alternative modes of inheritance of sex chromosomes offer interesting opportunities for studying sexual conflicts and their resolution, because expectations for the preferred genomic location of sexually antagonistic alleles may differ from standard systems. Aphids display an XX/X0 system and combine an unusual inheritance of the X chromosome with the alternation of sexual and asexual reproduction. In this study, we first investigated theoretically the accumulation of sexually antagonistic mutations on the aphid X chromosome. Our results show that i) the X is always more favourable to the spread of male-beneficial alleles than autosomes, and should thus be enriched in sexually antagonistic alleles beneficial for males, ii) sexually antagonistic mutations beneficial for asexual females accumulate preferentially on autosomes, iii) in contrast to predictions for standard systems, these qualitative results are not affected by the dominance of mutations. Under the assumption that sex-biased gene expression evolves to solve conflicts raised by the spread of sexually antagonistic alleles, one expects that male-biased genes should be enriched on the X while asexual female-biased genes should be enriched on autosomes. Using gene expression data (RNA-Seq) in males, sexual females and asexual females of the pea aphid, we confirm these theoretical predictions. Although other mechanisms than the resolution of sexual antagonism may lead to sex-biased gene expression, we argue that they could hardly explain the observed difference between X and autosomes. On top of reporting a strong masculinization of the aphid X chromosome, our study highlights the relevance of organisms displaying an alternative mode of sex chromosome inheritance to understanding the forces shaping chromosome evolution.

Vyšlo v časopise: Masculinization of the X Chromosome in the Pea Aphid. PLoS Genet 9(8): e32767. doi:10.1371/journal.pgen.1003690
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003690

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Zdroje

1. CoxRM, CalsbeekR (2009) Sexually antagonistic selection, sexual dimorphism, and the resolution of intralocus sexual conflict. Am Nat 173: 176–187.

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

3. FryJD (2010) The genomic location of sexually antagonistic variation: some cautionary comments. Evolution 64: 1510–1516.

4. MullonC, PomiankowskiA, ReuterM (2012) The effects of selection and genetic drift on the genomic distribution of sexually antagonistic alleles. Evolution 66: 3743–3753.

5. PattenMM, HaigD (2009) Maintenance or loss of genetic variation under sexual and parental antagonism at a sex-linked locus. Evolution 63: 2888–2895.

6. JordanCY, CharlesworthD (2012) The potential for sexually antagonistic polymorphism in different genomic regions. Evolution 66: 505–516.

7. LahnBT, PageDC (1997) Functional coherence of the human Y chromosome. Science 278: 675–680.

8. SkaletskyH, Kuroda-KawaguchiT, MinxPJ, CordumHS, HillierL, et al. (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423: 825–837.

9. CarvalhoAB, DoboBA, VibranovskiMD, ClarkAG (2001) Identification of five new genes on the Y chromosome of Drosophila melanogaster. Proc Natl Acad Sci U S A 98: 13225–13230.

10. MoghadamHK, PointerMA, WrightAE, BerlinS, MankJE (2012) W chromosome expression responds to female-specific selection. Proc Natl Acad Sci U S A 109: 8207–8211.

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

12. DeanR, PerryJC, PizzariT, MankJE, WigbyS (2012) Experimental evolution of a novel sexually antagonistic allele. PLoS Genet 8: e1002917.

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

14. VicosoB, KaiserVB, BachtrogD (2013) Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution. Proc Natl Acad Sci U S A 110: 6453–6458.

15. OttoSP, PannellJR, PeichelCL, AshmanTL, CharlesworthD, et al. (2011) About PAR: The distinct evolutionary dynamics of the pseudoautosomal region. Trends Genet 27: 358–367.

16. KhilPP, SmirnovaNA, RomanienkoPJ, Camerini-OteroRD (2004) The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet 36: 642–646.

17. WangPJ, McCarreyJR, YangF, PageDC (2001) An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27: 422–426.

18. LercherMJ, UrrutiaAO, HurstLD (2003) Evidence that the human X chromosome is enriched for male-specific but not female-specific genes. Mol Biol Evol 20: 1113–1116.

19. BellottDW, SkaletskyH, PyntikovaT, MardisER, GravesT, et al. (2010) Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466: 612–617.

20. ZhangYE, VibranovskiMD, LandbackP, MaraisGAB, LongM (2010) Chromosomal redistribution of male-biased genes in mammalian evolution with two bursts of gene gain on the X chromosome. PLoS Biol 8: e1000494.

21. ReinkeV, GilIS, WardS, KazmerK (2004) Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131: 311–323.

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

23. ParisiM, NuttallR, NaimanD, BouffardG, MalleyJ, et al. (2003) Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299: 697–700.

24. SturgillD, ZhangY, ParisiM, OliverB (2007) Demasculinization of X chromosomes in the Drosophila genus. Nature 450: 238–242.

25. ZhangYE, VibranovskiMD, KrinskyBH, LongM (2010) Age-dependent chromosomal distribution of male-biased genes in Drosophila. Genome Res 20: 1526–1533.

26. BakerDA, NolanT, FischerB, PinderA, CrisantiA, et al. (2011) A comprehensive gene expression atlas of sex- and tissue-specificity in the malaria vector, Anopheles gambiae. Bmc Genomics 12: 296.

27. MagnussonK, LycettGJ, MendesAM, LyndA, PapathanosPA, et al. (2012) Demasculinization of the Anopheles gambiae X chromosome. Bmc Evol Biol 12: 69.

28. HahnMW, LanzaroGC (2005) Female-biased gene expression in the malaria mosquito Anopheles gambiae. Curr Biol 15: R192–R193.

29. PrinceEG, KirklandD, DemuthJP (2010) Hyperexpression of the X chromosome in both sexes results in extensive female bias of X-linked genes in the flour beetle. Genome Biol Evol 2: 336–346.

30. ArunkumarKP, MitaK, NagarajuJ (2009) The silkworm Z chromosome is enriched in testis-specific genes. Genetics 182: 493–501.

31. StorchovaR, DivinaP (2006) Nonrandom representation of sex-biased genes on chicken Z chromosome. J Mol Evol 63: 676–681.

32. KaiserVB, EllegrenH (2006) Nonrandom distribution of genes with sex-biased expression in the chicken genome. Evolution 60: 1945–1951.

33. MankJE, EllegrenH (2009) Sex-linkage of sexually antagonistic genes is predicted by female, but not male, effects in birds. Evolution 63: 1464–1472.

34. EllegrenH (2011) Emergence of male-biased genes on the chicken Z-chromosome: Sex-chromosome contrasts between male and female heterogametic systems. Genome Res 21: 2082–2086.

35. MorkovskyL, StorchovaR, PlachyJ, IvanekR, DivinaP, et al. (2010) The chicken Z chromosome is enriched for genes with preferential expression in ovarian somatic cells. J Mol Evol 70: 129–136.

36. HenseW, BainesJF, ParschJ (2007) X chromosome inactivation during Drosophila spermatogenesis. PLoS Biol 5: e273.

37. SchoenmakersS, WassenaarE, HoogerbruggeJW, LavenJSE, GrootegoedJA, et al. (2009) Female meiotic sex chromosome inactivation in chicken. PLoS Genet 5: e1000466.

38. VibranovskiMD, LopesHF, KarrTL, LongM (2009) Stage-specific expression profiling of Drosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testis-expressed genes. PLoS Genet 5: e1000731.

39. EllegrenH, ParschJ (2007) The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8: 689–698.

40. MeiklejohnCD, LandeenEL, CookJM, KinganSB, PresgravesDC (2011) Sex chromosome-specific regulation in the Drosophila male germline but little evidence for chromosomal dosage compensation or meiotic inactivation. PLoS Biol 9: e1001126.

41. MeiklejohnCD, PresgravesDC (2012) Little evidence for demasculinization of the Drosophila X chromosome among genes expressed in the male germline. Genome Biol Evol 4: 895–904.

42. BakerBS, GormanM, MarinI (1994) Dosage compensation in Drosophila. Annu Rev Genet 28: 491–521.

43. BachtrogD, TodaNRT, LocktonS (2010) Dosage compensation and demasculinization of X chromosomes in Drosophila. Curr Biol 20: 1476–1481.

44. VicosoB, CharlesworthB (2009) The deficit of male-biased genes on the D. melanogaster X chromosome is expression-dependent: a consequence of dosage compensation? J Mol Evol 68: 576–583.

45. MankJE, EllegrenH (2009) All dosage compensation is local: Gene-by-gene regulation of sex-biased expression on the chicken Z chromosome. Heredity 102: 312–320.

46. EllegrenH, Hultin-RosenbergL, BrunstromB, DenckerL, KultimaK, et al. (2007) Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. Bmc Biology 5: 40.

47. RiceWR (1987) The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex-chromosomes. Evolution 41: 911–914.

48. CharlesworthD, CharlesworthB, MaraisG (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95: 118–128.

49. BergeroR, CharlesworthD (2009) The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol 24: 94–102.

50. BachtrogD, KirkpatrickM, MankJE, McDanielSF, PiresJC, et al. (2011) Are all sex chromosomes created equal? Trends Genet 27: 350–357.

51. JaquiéryJ, StoeckelS, RispeC, MieuzetL, LegeaiF, et al. (2012) Accelerated evolution of sex chromosomes in aphids, an X0 system. Mol Biol Evol 29: 837–847.

52. WilsonACC, SunnucksP, HalesDF (1997) Random loss of X chromosome at male determination in an aphid, Sitobion near fragariae, detected using an X-linked polymorphic microsatellite marker. Genet Res 69: 233–236.

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

54. MannaF, MartinG, LenormandT (2011) Fitness landscapes: an alternative theory for the dominance of mutation. Genetics 189: 923–937.

55. AgrawalAF, WhitlockMC (2011) Inferences about the distribution of dominance drawn from yeast gene knockout data. Genetics 187: 553–566.

56. HalkettF, PlantegenestM, BonhommeJ, SimonJC (2008) Gene flow between sexual and facultatively asexual lineages of an aphid species and the maintenance of reproductive mode variation. Mol Ecol 17: 2998–3007.

57. BrissonJA, NuzhdinSV (2008) Rarity of males in pea aphids results in mutational decay. Science 319: 58–58.

58. RhenT (2000) Sex-limited mutations and the evolution of sexual dimorphism. Evolution 54: 37–43.

59. CoyneJA, KayEH, Pruett-JonesS (2008) The genetic basis of sexual dimorphism in birds. Evolution 62: 214–219.

60. LoehlinDW, OliveiraD, EdwardsR, GiebelJD, ClarkME, et al. (2010) Non-coding changes cause sex-specific wing size differences between closely related species of Nasonia. PLoS Genet 6: e1000821.

61. ConnallonT, ClarkAG (2011) The resolution of sexual antagonism by gene duplication. Genetics 187: 919–937.

62. GallachM, BetranE (2011) Gene duplication might resolve intralocus sexual conflict. Trends Ecol Evol 26: 558–559.

63. DayT, BondurianskyR (2004) Intralocus sexual conflict can drive the evolution of genomic imprinting. Genetics 167: 1537–1546.

64. MankJE, EllegrenH (2009) Are sex-biased genes more dispensable? Biol Lett 5: 409–412.

65. OleksiakMF, ChurchillGA, CrawfordDL (2002) Variation in gene expression within and among natural populations. Nat Genet 32: 261–266.

66. HarrisonPW, WrightAE, MankJE (2012) The evolution of gene expression and the transcriptome-phenotype relationship. Semin Cell Dev Biol 23: 222–229.

67. MankJE, Hultin-RosenbergL, ZwahlenM, EllegrenH (2008) Pleiotropic constraint hampers the resolution of sexual antagonism in vertebrate gene expression. Am Nat 171: 35–43.

68. HaranoT, OkadaK, NakayamaS, MiyatakeT, HoskenDJ (2010) Intralocus sexual conflict unresolved by sex-limited trait expression. Curr Biol 20: 2036–2039.

69. BeanCJ, SchanerCE, KellyWG (2004) Meiotic pairing and imprinted X chromatin assembly in Caenorhabditis elegans. Nat Genet 36: 100–105.

70. HamiltonWD (1967) Extraordinary sex-ratios. Science 156: 477–488.

71. DengXX, HiattJB, NguyenDK, ErcanS, SturgillD, et al. (2011) Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nat Genet 43: 1179–1185.

72. KharchenkoPV, XiRB, ParkPJ (2011) Evidence for dosage compensation between the X chromosome and autosomes in mammals. Nat Genet 43: 1167–1169.

73. MankJE, HoskenDJ, WedellN (2011) Some inconvenient thruths about sex chromosome dosage compensation and the potential role of sexual conflict. Evolution 65: 2133–2144.

74. JulienP, BrawandD, SoumillonM, NecsuleaA, LiechtiA, et al. (2012) Mechanisms and evolutionary patterns of mammalian and avian dosage compensation. PLoS Biol 10: e1001328.

75. MuyleA, ZempN, DeschampsC, MoussetS, WidmerA, et al. (2012) Rapid de novo evolution of X chromosome dosage compensation in Silene latifolia, a plant with young sex chromosomes. PLoS Biol 10: e1001308.

76. ShakesDC, NevaBJ, HuynhH, ChaudhuriJ, Pires-daSilvaA (2011) Asymmetric spermatocyte division as a mechanism for controlling sex ratios. Nat Commun 2: 157.

77. NemetschkeL, EberhardtAG, HertzbergH, StreitA (2010) Genetics, chromatin diminution, and sex chromosome evolution in the parasitic nematode genus Strongyloides. Curr Biol 20: 1687–1696.

78. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.

79. Le TrionnaireG, FrancisF, Jaubert-PossamaiS, BonhommeJ, De PauwE, et al. (2009) Transcriptomic and proteomic analyses of seasonal photoperiodism in the pea aphid. Bmc Genomics 10: 456.

80. LegeaiF, ShigenobuS, GauthierJP, ColbourneJ, RispeC, et al. (2010) AphidBase: a centralized bioinformatic resource for annotation of the pea aphid genome. Ins Mol Biol 19: 5–12.

81. WuTD, NacuS (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26: 873–881.

82. IAGC (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biology 8: e1000313.

83. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.

84. MandrioliM, BorsattiF (2007) Analysis of heterochromatic epigenetic markers in the holocentric chromosomes of the aphid Acyrthosiphon pisum. Chromosome Res 15: 1015–1022.