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A Model-Based Approach for Identifying Signatures of Ancient Balancing Selection in Genetic Data


In the past, balancing selection was a topic of great theoretical interest that received much attention. However, there has been little focus toward developing methods to identify regions of the genome that are under balancing selection. In this article, we present the first set of likelihood-based methods that explicitly model the spatial distribution of polymorphism expected near a site under long-term balancing selection. Simulation results show that our methods outperform commonly-used summary statistics for identifying regions under balancing selection. Finally, we performed a scan for balancing selection in Africans and Europeans using our new methods and identified a gene called FANK1 as our top candidate outside the HLA region. We hypothesize that the maintenance of polymorphism at FANK1 is the result of segregation distortion.


Vyšlo v časopise: A Model-Based Approach for Identifying Signatures of Ancient Balancing Selection in Genetic Data. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004561
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004561

Souhrn

In the past, balancing selection was a topic of great theoretical interest that received much attention. However, there has been little focus toward developing methods to identify regions of the genome that are under balancing selection. In this article, we present the first set of likelihood-based methods that explicitly model the spatial distribution of polymorphism expected near a site under long-term balancing selection. Simulation results show that our methods outperform commonly-used summary statistics for identifying regions under balancing selection. Finally, we performed a scan for balancing selection in Africans and Europeans using our new methods and identified a gene called FANK1 as our top candidate outside the HLA region. We hypothesize that the maintenance of polymorphism at FANK1 is the result of segregation distortion.


Zdroje

1. FisherRA (1922) On the dominance ratio. Proc Roy Soc Edin 42: 321–341.

2. Andrés AM (2011) Balancing selection in the human genome. In: Encyclopedia of Life Sciences, Chichester: John Wiley and Sons.

3. WilsonDS, TurelliM (1986) Stable underdominance and the evolutionary invasion of empty niches. Am Nat 127: 835–850.

4. LeveneH (1953) Genetic equilibrium when more than one ecological niche is available. Am Nat 83: 331–333.

5. NagylakiT (1975) Polymorphisms in cyclically varying environments. Heredity 35: 67–74.

6. Charlesworth B, Charlesworth D (2010) Elements of evolutionary genetics. Greenwood Village, CO: Roberts and Company Publishers.

7. SégurelL, ThompsonEE, FlutreT, LovstadJ, VenkatA, et al. (2012) The ABO blood group is a trans-species polymorphism in primates. Proc Natl Acad Sci USA 109: 18493–18498.

8. KleinJ, SattaY, O'hUigínC (1993) The molecular descent of the major histocompatibility complex. Annu Rev Immunol 11: 269–95.

9. KleinJ, SatoA, NaglS, O'hUigínC (1998) Molecular trans-species polymorphism. Annu Rev Ecol Syst 29: 1–21.

10. KleinJ, SatoA, NikolaidisN (2007) MHC, TSP, and the origin of species: from immunogenetics to evlutionary genetics. Annu Rev Genet 41: 281–304.

11. HernandezRD, KelleyJL, ElyashivE, MeltonSC, AutonA, et al. (2011) Classic selective sweeps were rare in recent human evolution. Science 331: 920–924.

12. LohmuellerKE, AlbrechtsenA, LiY, YKS, KorneliussenT, et al. (2011) Natural selection affects multiple aspects of genetic variation at putatively neutral sites across the human genome. PLoS Genet 7: e1002326.

13. GrankaJM, HennBM, GignouxCR, KiddJM, BustamanteCD, et al. (2012) Limited evidence for classic selective sweeps in African populations. Genetics 92: 1049–64 doi:10.1534/genetics.112.144071

14. BubbKL, BoveeD, BuckleyD, HaugenE, KibukawaM, et al. (2006) Scan of human genome reveals no new loci under ancient balancing selection. Genetics 173: 2165–2177.

15. AndrésAM, HubiszMJ, IndapA, TorgersonDG, DegenhardtJD, et al. (2009) Targets of balancing selection in the human genome. Mol Biol Evol 26: 2755–2764.

16. HudsonRR, KreitmanM, AguadéM (1987) A test of neutral marker evolution based on nucleotide data. Genetics 116: 153–159.

17. TajimaF (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

18. InnanH (2006) Modified Hudson-Kreitman-Aguadé test and two-dimensional evaluation of neutrality tests. Genetics 173: 1725–1733.

19. LefflerEM, GaoZ, PfeiferS, SégurelL, AutonA, et al. (2013) Multiple instances of ancient balancing selection shared between humans and chimpanzees. Science 339: 1578–1582.

20. KaplanNL, DardenT, HudsonRR (1988) The coalescent proces in models with selection. Genetics 120: 819–829.

21. HudsonRR, KaplanNL (1988) The coalescent process in models with selection and recombination. Genetics 120: 831–840.

22. HudsonRR (2001) Two-locus sampling distributions and their application. Genetics 159: 1805–1817.

23. KimY, StephanW (2002) Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160: 765–777.

24. KimY, NielsenR (2004) Linkage disequilibrium as a signature of selective sweeps. Genetics 167: 1513–1524.

25. JensenJD, KimY, DuMontVB, AquadroCF, BustamanteCD (2005) Distinguishing between selective sweeps and demography using DNA polymorphism data. Genetics 170: 1401–1410.

26. NielsenR, WilliamsonS, KimY, HubiszMJ, ClarkAG, et al. (2005) Genomic scans for selective sweeps using SNP data. Genome Res 15: 1566–1575.

27. NielsenR, HubszMJ, HellmannI, TorgersonD, AndrésAM, et al. (2009) Darwinian and demographic forces affecting human protein coding genes. Genome Res 19: 838–849.

28. ChenH, PattersonN, ReichD (2010) Population differentiation as a test for selective sweeps. Genome Res 20: 393–402.

29. Thomas LH (1949) Elliptic problems in linear difference equations over a network. New York: Watson Sci. Comput. Lab. Rept., Columbia University.

30. TakahataN, NeiM (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility loci. Genetics 124: 967–978.

31. HedrickPW (2002) Pathogen resistance and geneic variation at MHC loci. Evolution 56: 1902–1908.

32. ZhengZ, ZhengH, YanW (2007) Fank1 is a testis-specific gene encoding a nuclear protein exclusively expressed during the transition from meiotic to the haploid phase of spermatogenesis. Gene Expr Patterns 7: 777–783.

33. WangH, SongW, HuT, ZhangN, MiaoS, et al. (2011) Fank1 interacts with Jab1 and regulates cell apoptosis via the AP-1 pathway. Cell Mol Life Sci 68: 2129–2139.

34. HwangKC, ParkSY, ParkSP, LimJH, CuiXS, et al. (2005) Specific maternal transcripts in bovie oocytes and cleavaged embryos: identification with novel DDRT-PCR methods. Mol Reprod Dev 71: 275–283.

35. ZuccottiM, MericoV, SacchiL, BelloneM (2008) Brink R T C nd Bellazzi, (2008) et al. Maternal Oct-4 is a potential key regulator of the developmental compentence of mouse oocytes. BMC Dev Biol 8: 97.

36. LiY, ZhuJ, TianG, LiN, LiQ, et al. (2010) The DNA methylome of human peripheral blood mononuclear cells. PLoS Biol 8: e1000533.

37. MeyerWK, ArbeithuberB, OberC, EbnerT, Tiemann-BoegeI, et al. (2012) Evaluating the evidence for transmission distortion in human pedigress. Genetics 191: 215–232.

38. AkeyJM, EberleMA, RiederMJ, CarlsonCS, ShriverMD, et al. (2004) Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol 2: e286.

39. EdenE, LipsonD, YogevS, YakhiniZ (2007) Discovering motifs in ranked lists of DNA sequences. PLoS Comput Biol 3: e39.

40. EdenE, NavonR, SteinfeldI, LipsonD, YakhiniZ (2009) GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48.

41. BartonNH, EtheridgeAM (2004) The effect of selection on genealogies. Genetics 166: 1115–1131.

42. BartonNH, EtheridgeAM, SturmAK (2004) Coalescence in a random background. Ann Appl Probab 14: 754–785.

43. GreenRE, KrauseJ, BriggsAW, MariciT, StenzelU, et al. (2010) A draft sequence of the Neandertal genome. Science 328: 710–722.

44. ReichD, GreenRE, KircherM, KrauseJ, PattersonN, et al. (2010) Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468: 1053–1060.

45. JensenJD, ThorntonKR, BustamanteCD, AquadroCF (2007) On the utility of linkage disequilibrium as a statistic for identifying targets of positive selection in nonequilibrium populations. Genetics 176: 2371–2379.

46. PavlidisP, JensenJD, StephanW (2010) Searching for footprints of positive selection in whole-genome SNP data from nonequilibrium populations. Genetics 185: 907–922.

47. PlagnolV, WallJD (2006) Possible ancestral structure in human populations. PLoS Genet 2: 972–979.

48. SlatkinM (2008) Linkage disequilibrium - understanding gthe evolutionary past and mapping the medical future. Nat Rev Genet 9: 477–485.

49. GrossmanSR, ShylakhterI, KarlssonEK, ByrneEH, MoralesS, et al. (2010) A composite of multiple signals distinguishes causal variants in regions of positive selection. Science 327: 883–886.

50. SabetiPC, ReichDE, HigginsJM, LevineHZP, RichterDJ, et al. (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419: 832–837.

51. VoightBF, KudravalliS, WenX, PritchardJK (2006) A map of recent positive selection in the human genome. PLoS Biol 4: e72.

52. Ferrer-AdmetllaA, LiangM, KorneliussenT, NielsenR (2014) On detecting incomplete soft or hard selective sweeps using haplotype structure. Mol Biol Evol 31: 1059–65 DOI: 10.1093/molbev/msu077

53. SchierupMH, HeinJ (2000) Consequences of recombination on traditional phylogenetic analysis. Genetics 156: 879–891.

54. ÚbedaF, HaigD (2004) Sex-specific meiotic drive and selection at an imprinted locus. Genetics 167: 2083–2095.

55. NielsenR, BustamanteCD, ClarkAG, GlanowskiS, StacktonTB, et al. (2005) A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 3: 976–985.

56. da FonsecaRR, KosiolC, VinařT, SiepelA, NielsenR (2010) Positive selection on apoptosis related genes. FEBS Lett 584: 469–476.

57. KosovaG, ScottNM, NiederbergerC, PrinsGS, OberC (2012) Genome-wide association study identifies candidate genes for male fertility traits in humans. Am J Hum Genet 90: 950–961.

58. SeidelHS, RockmanMV, KruglyakL (2008) Widespread gentic incompatibility in C. elegans maintained by balancing selection. Science 319: 589–594.

59. SellisD, CallahanBJ, PetrovDA, MesserPW (2012) Heterozygote advantage as a natural consequence of adaptation in diploids. Proc Natl Acad Sci USA 108: 20666–20671.

60. TakahataN, SattaY, KleinJ (1995) Divergence time and population size in the lineage leading to modern humans. Theor Popul Biol 48: 198–221.

61. KumarS, FilipskiA, SwamaV, WalkerA, HedgesSB (2005) Placing confidence limits on the molecular age of the human-chimpanzee divergence. Proc Natl Acad Sci USA 102: 18842–18847.

62. NachmanMW, CrowellSL (2000) Estimate of the mutation rate per nucleotide in humans. Genetics 156: 297–304.

63. Gillespie J (2004) Population genetics: a concise guide. Baltimore, MD: Johns Hopkins University Press, 2nd edition.

64. PickrellJK, CoopG, NovembreJ, KudravalliS, LiJZ, et al. (2009) Signals of recent positive selection in a worldwide sample of human populations. Genome Res 19: 826–837.

65. HudsonRR (2002) Generating samples under a Wright-Fisher neutral model. Bioinformatics 18: 337–338.

66. LohmuellerKE, BustamanteCD, ClarkAG (2009) Methods for human demographic inference using halptype patterns from genomewide single-nucleotide polymorphism data. Genetics 182: 217–231.

67. LohmuellerKE, BustamanteCD, ClarkAG (2011) Detectig directional selection in the presence of recent admixture in African-Americans. Genetics 187: 823–835.

68. MarthGT, CzabarkaE, MurvaiJ, SherryST (2004) The allele frequency spectrum in genome-wide human variation data reveals signals of differential demographic history in three large world populations. Genetics 166: 351–372.

69. DrmanacR, SparksAB, CallowMJ, HalpernAL, BurnsNL, et al. (2009) Human genome sequencing using unchained base reads on self-assembling DNA nanoarrays. Science 327: 78–81.

70. PembertonTJ, WangC, LiJZ, RosenbergNA (2010) Inference of unexpected genetic relatedness among individuals in HapMap Phase III. Am J Hum Genet 87: 457–464.

71. WiggintonJE, CutlerDJ, AbecasisGR (2005) A note on exact tests of Hardy-Weinberg equilibrium. Am J Hum Genet 76: 887–893.

72. HernandezRD, WilliamsonSH, BustamanteCD (2007) Context dependence, ancestral misidentification, and spurious signatures of natural selection. Mol Biol Evol 28: 1792–1800.

73. KongA, ThorleifssonG, GudbjartssonDF, MassonG, SigurdssonA, et al. (2010) Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467: 1099–1103.

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