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Meiotic Drive Impacts Expression and Evolution of X-Linked Genes in Stalk-Eyed Flies


Sex chromosome meiotic drive causes changes in the sex-ratios of natural populations, and may even lead to extinction if the driving element reaches high frequency. However, very little is known about the genes that cause sex-ratio drive, and no causal gene has been identified in a species that consistently exhibits distorted sex ratios in natural populations. Several species of stalk-eyed flies in southeast Asia – genus Teleopsis – express X chromosome drive, but the genes underlying drive have been difficult to locate due to reduced recombination between drive and standard X chromosomes presumably caused by the presence of a large inversion. Here, we use high throughput RNA sequencing to identify over 500 transcripts that are differentially expressed in the testes due to the effects of a driving X chromosome (XSR) in T. dalmanni. Most of these are X-linked, evolve more rapidly than control genes, and exhibit elevated expression in the gonads. Finally, XSR has become genetically differentiated from standard X chromosomes – using the RNA sequence data, we found nearly 1000 sites in X-linked transcripts and only a handful in autosomal transcripts where there was a fixed nucleotide difference. We conclude that XSR has led to widespread sequence and expression divergence on the X chromosome in T. dalmanni.


Vyšlo v časopise: Meiotic Drive Impacts Expression and Evolution of X-Linked Genes in Stalk-Eyed Flies. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004362
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004362

Souhrn

Sex chromosome meiotic drive causes changes in the sex-ratios of natural populations, and may even lead to extinction if the driving element reaches high frequency. However, very little is known about the genes that cause sex-ratio drive, and no causal gene has been identified in a species that consistently exhibits distorted sex ratios in natural populations. Several species of stalk-eyed flies in southeast Asia – genus Teleopsis – express X chromosome drive, but the genes underlying drive have been difficult to locate due to reduced recombination between drive and standard X chromosomes presumably caused by the presence of a large inversion. Here, we use high throughput RNA sequencing to identify over 500 transcripts that are differentially expressed in the testes due to the effects of a driving X chromosome (XSR) in T. dalmanni. Most of these are X-linked, evolve more rapidly than control genes, and exhibit elevated expression in the gonads. Finally, XSR has become genetically differentiated from standard X chromosomes – using the RNA sequence data, we found nearly 1000 sites in X-linked transcripts and only a handful in autosomal transcripts where there was a fixed nucleotide difference. We conclude that XSR has led to widespread sequence and expression divergence on the X chromosome in T. dalmanni.


Zdroje

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

2. Fisher R (1930) The genetical theory of natural selection. Oxford University Press.

3. JaenikeJ (1999) Suppression of sex-ratio meiotic drive and the maintenance of Y-chromosome polymorphism in Drosophila. Evolution 53: 1326.

4. JaenikeJ (1996) Sex-ratio meiotic drive in the Drosophila quinaria group. The American Naturalist 148: 237 doi: 10.1086/285923

5. PriceTAR, BretmanAJ, AventTD, SnookRR, HurstGDD, et al. (2008) Sex ratio distorter reduces sperm competitive ability in an insect. Evolution 62: 1644–1652 doi:10.1111/j.1558-5646.2008.00386.x

6. CurtsingerJW, FeldmanMW (1980) Experimental and theoretical analysis of the ‘Sex-ratio’ polymorphism in Drosophila pseudoobscura. Genetics 94: 445–466.

7. HiraizumiY, SandlerL, CrowJF (1960) Meiotic drive in natural populations of Drosophila melanogaster. III. Populational implications of the segregation-distorter locus. Evolution 14: 433 doi: 10.2307/2405993

8. MercotH, AtlanA, JacquesM, Montchamp-MoreauC (1995) Sex-ratio distortion in Drosophila simulans: co-occurence of a meiotic drive and a suppressor of drive. Journal of Evolutionary Biology 8: 283–300 doi:10.1046/j.1420-9101.1995.8030283.x

9. ReedFA, ReevesRG, AquadroCF (2005) Evidence of susceptibility and resistance to cryptic X-linked meiotic drive in natural populations of Drosophila melanogaster. Evolution 59: 1280–1291.

10. TaoY, MaslyJP, AraripeL, KeY, HartlDL (2007) A sex-ratio meiotic drive system in Drosophila simulans. I: an autosomal suppressor. PLoS Biology 5: e292 doi: 10.1371/journal.pbio.0050292

11. TaoY, AraripeL, et al. (2007) A sex-ratio meiotic drive system in Drosophila simulans. II: an X-linked distorter. PLoS Biology 5: e293 doi: 10.1371/journal.pbio.0050293

12. OrrHA, IrvingS (2005) Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura. Genetics 169: 671–682 doi:10.1534/genetics.104.033274

13. CarvalhoA, KlaczkoL (1993) Autosomal suppressors of sex-ratio in Drosophila mediopunctata. Heredity 71: 546–551 doi:doi:10.1038/hdy.1993.174

14. JaenikeJ (2001) Sex chromosome meiotic drive. Annual Review of Ecology and Systematics 32: 25–49.

15. PalopoliMF, WuCI (1996) Rapid evolution of a coadapted gene complex: evidence from the Segregation Distorter (SD) system of meiotic drive in Drosophila melanogaster. Genetics 143: 1675–1688.

16. ChevinL-M, HospitalF (2006) The hitchhiking effect of an autosomal meiotic drive gene. Genetics 173: 1829–1832 doi: 10.1534/genetics.105.052977

17. DeromeN, MetayerK, Montchamp-MoreauC, VeuilleM (2004) Signature of selective sweep associated with evolution of sex-ratio drive in Drosophila simulans. Genetics 166: 1357–1366.

18. MeiklejohnCD, TaoY (2010) Genetic conflict and sex chromosome evolution. Trends in Ecology & Evolution 25: 215–223 doi:10.1016/j.tree.2009.10.005

19. HaigD, GrafenA (1991) Genetic scrambling as a defence against meiotic drive. Journal of Theoretical Biology 153: 531–558.

20. HurstL, PomiankowskiA (1991) Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomenon. Genetics 128: 841–858.

21. FrankSA (1991) Divergence of meiotic drive-suppression systems as an explanation for sex-biased hybrid sterility and inviability. Evolution 45: 262–267.

22. McDermottSR, NoorMAF (2010) The role of meiotic drive in hybrid male sterility. Philosophical Transactions of the Royal Society, B, Biological Sciences 365: 1265–1272 doi: 10.1098/rstb.2009.0264

23. PhadnisN, OrrHA (2009) A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323: 376–379.

24. McdermottSR, NoorMAF (2012) Mapping of within-species segregation distortion in Drosophila persimilis and hybrid sterility between D. persimilis and D. pseudoobscura. Journal of Evolutionary Biology 25: 2023–2032 doi:10.1111/j.1420-9101.2012.02581.x

25. DyerKA, CharlesworthB, JaenikeJ (2007) Chromosome-wide linkage disequilibrium as a consequence of meiotic drive. Proceedings of the National Academy of Sciences 104: 1587–1592.

26. JohnsPM, WolfenbargerLL, WilkinsonGS (2005) Genetic linkage between a sexually selected trait and X chromosome meiotic drive. Proceedings of the Royal Society of London B 272: 2097–2103.

27. FouvryL, OgereauD, BergerA, GavoryF, Montchamp-MoreauC (2011) Sequence analysis of the segmental duplication responsible for Paris sex-ratio drive in Drosophila simulans. G3: Genes, Genomes, Genetics 1: 401–410 doi: 10.1534/g3.111.000315

28. WilkinsonGS, JohnsPM, KelleherES, MuscedereML, LorsongA (2006) Fitness effects of X chromosome drive in the stalk-eyed fly, Cyrtodiopsis dalmanni. Journal of Evolutionary Biology 19: 1851–1860 doi:10.1111/j.1420-9101.2006.01169.x

29. PresgravesDC, SeveranceE, WilkinsonGS (1997) Sex chromosome meiotic drive in stalk-eyed flies. Genetics 147: 1169–1180.

30. BakerRH, WilkinsonGS (2010) Comparative genomic hybridization (CGH) reveals a Neo-X chromosome and biased gene movement in stalk-eyed flies (genus Teleopsis). PLoS Genetics 6: e1001121 doi: 10.1371/journal.pgen.1001121

31. WilkinsonGS, PresgravesDC, CrymesL (1998) Male eye span in stalk-eyed flies indicates genetic quality by meiotic drive suppresion. Nature 391: 276–278.

32. FryCL, WilkinsonGS (2004) Sperm survival in female stalk-eyed flies depends on seminal fluid and meiotic drive. Evolution 58: 1622 doi: 10.1554/03-748

33. JohnsPM, WilkinsonGS (2007) X chromosome influences sperm length in the stalk-eyed fly Cyrtodiopsis dalmanni. Heredity 99: 56–61 doi:10.1038/sj.hdy.6800963

34. LandeR, WilkinsonGS (1999) Models of sex-ratio meiotic drive and sexual selection in stalk-eyed flies. Genetical Research 74: 245–253.

35. CottonA, FoldvariM, CottonS, PomiankowskiA (2014) Male eyespan size is associated with meiotic drive in wild stalk-eyed flies (Teleopsis dalmanni). Heredity 112: 363–369 doi:10.1038/hdy.2013.131

36. WrightTF, JohnsPM, WaltersJR, LernerAP, SwallowJG, et al. (2004) Microsatellite variation among divergent populations of stalk-eyed flies, genus Cyrtodiopsis. Genetical Research 84: 27–40 doi:10.1017/S0016672304006986

37. ChristiansonSJ, BrandCL, WilkinsonGS (2011) Reduced polymorphism associated with X chromosome meiotic drive in the stalk-eyed fly Teleopsis dalmanni. PLoS ONE 6: e27254 doi: 10.1371/journal.pone.0027254

38. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760 doi:10.1093/bioinformatics/btp324

39. LiB, DeweyCN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323 doi:10.1186/1471-2105-12-323

40. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biology 11: R106 doi:10.1186/gb-2010-11-10-r106

41. MercerTR, DingerME, MattickJS (2009) Long non-coding RNAs: insights into functions. Nature Reviews Genetics 10: 155–159 doi:10.1038/nrg2521

42. DjebaliS, DavisCA, MerkelA, DobinA, LassmannT, et al. (2012) Landscape of transcription in human cells. Nature 489: 101–108 doi:10.1038/nature11233

43. HaasBJ, PapanicolaouA, YassourM, GrabherrM, BloodPD, et al. (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols 8: 1494–1512 doi:10.1038/nprot.2013.084

44. ReinerA, YekutieliD, BenjaminiY (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19: 368–375 doi:10.1093/bioinformatics/btf877

45. WilkinsonGS, SanchezMI (2001) Sperm development, age and sex chromosome meiotic drive in the stalk-eyed fly, Cyrtodiopsis whitei. Heredity 87: 17–24 doi:10.1046/j.1365-2540.2001.00898.x

46. EdwardsAWF (1961) The population genetics of “sex-ratio” in Drosophila pseudoobscura. Heredity 16: 291–304 doi:10.1038/hdy.1961.35

47. BetranE, ThorntonK, LongM (2002) Retroposed new genes out of the X in Drosophila. Genome Research 12: 1854–1859.

48. VibranovskiMD, ZhangY, LongMY (2009) General gene movement off the X chromosome in the Drosophila genus. Genome Research 19: 897–903.

49. ZhangYE, VibranovskiMD, KrinskyBH, LongM (2010) Age-dependent chromosomal distribution of male-biased genes in Drosophila. Genome Research 20: 1526–1533 doi:10.1101/gr.107334.110

50. CocquetJ, EllisPJ, MahadevaiahSK, AffaraNA, VaimanD, et al. (2012) A genetic basis for a postmeiotic X versus Y chromosome intragenomic conflict in the mouse. PLoS Genetics 8: e1002900 doi: 10.1371/journal.pgen.1002900

51. WiegmannBM, TrautweinMD, WinklerIS, BarrNB, KimJ-W, et al. (2011) Episodic radiations in the fly tree of life. Proceedings of the National Academy of Sciences 108: 5690–5695 doi:10.1073/pnas.1012675108

52. SwallowJG, WallaceLE, ChristiansonSJ, JohnsPM, WilkinsonGS (2005) Genetic divergence does not predict change in ornament expression among populations of stalk-eyed flies. Molecular Ecology 14: 3787–3800 doi:10.1111/j.1365-294X.2005.02691.x

53. HaertyW, JagadeeshanS, KulathinalRJ, WongA, Ravi RamK, et al. (2007) Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177: 1321–1335 doi:10.1534/genetics.107.078865

54. MullerHJ (1964) The relation of recombination to mutational advance. Mutation Research 106: 2–9.

55. CharlesworthB, CharlesworthD (2000) The degeneration of Y chromosomes. Philosophical Transactions of the Royal Society London, B, Biological Sciences 355: 1563–1572 doi: 10.1098/rstb.2000.0717

56. WuC-I (1983) The fate of autosomal modifiers of the sex-ratio trait in Drosophila and other sex-linked meiotic drive systems. Theoretical Population Biology 24: 107–120.

57. HuangDW, ShermanBT, LempickiRA (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 4: 44–57 doi:10.1038/nprot.2008.211

58. McKeeBD (1984) Sex chromosome meiotic drive in Drosophila melanogaster males. Genetics 106: 403–422.

59. KomitopoulouK, GansM, MargaritisL, KafatosF, MassonM (1983) Isolation and characterization of sex-linked female-sterile mutants in Drosophila melanogaster. Genetics 105: 897–920.

60. FischerBE, WasbroughE, MeadowsLA, RandletO, DorusS, et al. (2012) Conserved properties of Drosophila and human spermatozoal mRNA repertoires. Proceedings of the Royal Society B: Biological Sciences 279: 2636–2644 doi:10.1098/rspb.2012.0153

61. CattaneoF, PasiniME, IntraJ, MatsumotoM, BrianiF, et al. (2006) Identification and expression analysis of Drosophila melanogaster genes encoding beta-hexosaminidases of the sperm plasma membrane. Glycobiology 16: 786–800 doi:10.1093/glycob/cwl007

62. LiMA, AllsJD, AvanciniRM, KooK, GodtD (2003) The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nature Cell Biology 5: 994–1000 doi: 10.1038/ncb1058

63. BakerRH, MorganJ, WangX, BooreJL, WilkinsonGS (2009) Genomic analysis of a sexually-selected character: EST sequencing and microarray analysis of eye-antennal imaginal discs in the stalk-eyed fly Teleopsis dalmanni (Diopsidae). BMC Genomics 10: 361 doi:10.1186/1471-2164-10-361

64. WilkinsonGS, PresgravesDC, CrymesL (1998) Male eye span in stalk-eyed flies indicates genetic quality by meiotic drive suppression. Nature 391: 276–279 doi:10.1038/34640

65. MarroneAK, KucherenkoMM, RishkoVM, ShcherbataHR (2011) New dystrophin/dystroglycan interactors control neuron behavior in Drosophila eye. BMC Neuroscience 12: 93 doi: 10.1186/1471-2202-12-93

66. Fischer-VizeJA, MosleyKL (1994) Marbles mutants: uncoupling cell determination and nuclear migration in the developing Drosophila eye. Development 120: 2609–2618.

67. YadlapalliS, YamashitaYM (2013) Chromosome-specific nonrandom sister chromatid segregation during stem-cell division. Nature 498: 251–254 doi:10.1038/nature12106

68. GershensonS (1928) A new sex-ratio abnormality in Drosophila obscura. Genetics 13: 488–507.

69. SturtevantA, DobzhanskyT (1936) Geographical distribution and cytology of “sex ratio” in Drosophila pseudoobscura and related species. Genetics 21: 473–490.

70. NovitskiE (1947) Genetic analysis of an anomalous sex ratio condition in Drosophila afinis. Genetics 32: 526–534.

71. WallaceB (1948) Studies on “sex ratio” in Drosophila pseudoobscura. Evolution 2: 189–217.

72. SandlerL, NovitskiE (1957) Meiotic drive as an evolutionary force. The American Naturalist 91: 105 doi: 10.1086/281969

73. StalkerHD (1961) The genetic systems modifying meiotic drive in Drosophila paramelanica. Genetics 46: 177–202.

74. ThomsonG, FeldmanMW (1975) Population genetics of modifiers of meiotic drive. IV. On the evolution of sex-ratio distortion. Theoretical Population Biology 8: 202–211.

75. RandersonJP, JigginsFM, HurstLD (2000) Male killing can select for male mate choice: a novel solution to the paradox of the lek. Proceedings of the Royal Society of London B 267: 867–874.

76. HaigD, BergstromCT (1995) Multiple mating, sperm competition and meiotic drive. Journal of Evolutionary Biology 8: 265–282.

77. Lindsley DL, Zimm GG (1992) The Genome of Drosophila melanogaster. Academic Press, San diego.

78. KinganSB, GarriganD, HartlDL (2010) Recurrent selection on the Winters sex-ratio genes in Drosophila. Genetics 184: 253–265 doi:10.1534/genetics.109.109587

79. BastideH, CazemajorM, OgereauD, DeromeN, HospitalF, et al. (2011) Rapid rise and fall of selfish sex-ratio X chromosomes in Drosophila simulans: spatiotemporal analysis of phenotypic and molecular data. Molecular Biology and Evolution 28: 2461–2470 doi:doi: 10.1093/molbev/msr074

80. HartlDL (1975) Modifier theory and meiotic drive. Theoretical Population Biology 7: 168–174.

81. WilkinsonGS, SwallowJG, ChristensenSJ, MaddenK (2003) Phylogeography of sex ratio and multiple mating in stalk-eyed flies from southeast Asia. Genetica 117: 37–46.

82. WalshPS, MetzgerDA, HiguchiR (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 506–513.

83. GrabherrMG, HaasBJ, YassourM, LevinJZ, ThompsonDA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29: 644–652 doi:10.1038/nbt.1883

84. MinocheAE, DohmJC, HimmelbauerH (2011) Evaluation of genomic high-throughput sequencing data generated on Illumina HiSeq and Genome Analyzer systems. Genome Biology 12: R112 doi:10.1186/gb-2011-12-11-r112

85. RobinsonMD, McCarthyDJ, SmythGK (2009) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140 doi:10.1093/bioinformatics/btp616

86. LivakKJ, SchmittgenTD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408 doi:10.1006/meth.2001.1262

87. Slater G (2000). Algorithms for the Analysis of Expressed Sequence Tags. PhD Thesis. Cambridge, UK: University of Cambridge.

88. SieversF, WilmA, DineenD, GibsonTJ, KarplusK, et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology 7: 539 Available: http://www.nature.com/doifinder/10.1038/msb.2011.75. Accessed 27 May 2013.

89. Korber B, Rodrigo AG, Learn GH (2000) HIV signature and sequence variation analysis. In: Computational Analysis of HIV Molecular Sequences, Chapter 4. Kluwer Academic Publishers.: Dordrecht, Netherlands pp. 55–72. http://www.hiv.lanl.gov.

90. HuangDW, ShermanBT, LempickiRA (2008) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research 37: 1–13 doi:10.1093/nar/gkn923

91. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079 doi:10.1093/bioinformatics/btp352

92. ExcoffierL, DupanloupI, Huerta-SánchezE, SousaVC, FollM (2013) Robust demographic inference from genomic and SNP data. PLoS Genetics 9: e1003905 doi: 10.1371/journal.pgen.1003905

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