Classic Selective Sweeps Revealed by Massive Sequencing in Cattle

English version České info

Human driven selection during domestication and subsequent breed formation has likely left detectable signatures within the genome of modern cattle. The elucidation of these signatures of selection is of interest from the perspective of evolutionary biology, and for identifying domestication-related genes that ultimately may help to further genetically improve this economically important animal. To this end, we employed a panel of more than 15 million autosomal SNPs identified from re-sequencing of 43 Fleckvieh animals. We mainly applied two somewhat complementary statistics, the integrated Haplotype Homozygosity Score (iHS) reflecting primarily ongoing selection, and the Composite of Likelihood Ratio (CLR) having the most power to detect completed selection after fixation of the advantageous allele. We find 106 candidate selection regions, many of which are harboring genes related to phenotypes relevant in domestication, such as coat coloring pattern, neurobehavioral functioning and sensory perception including KIT, MITF, MC1R, NRG4, Erbb4, TMEM132D and TAS2R16, among others. To further investigate the relationship between genes with signatures of selection and genes identified in QTL mapping studies, we use a sample of 3062 animals to perform four genome-wide association analyses using appearance traits, body size and somatic cell count. We show that regions associated with coat coloring significantly (P<0.0001) overlap with the candidate selection regions, suggesting that the selection signals we identify are associated with traits known to be affected by selection during domestication. Results also provide further evidence regarding the complexity of the genetics underlying coat coloring in cattle. This study illustrates the potential of population genetic approaches for identifying genomic regions affecting domestication-related phenotypes and further helps to identify specific regions targeted by selection during speciation, domestication and breed formation of cattle. We also show that Linkage Disequilibrium (LD) decays in cattle at a much faster rate than previously thought.

Vyšlo v časopise: Classic Selective Sweeps Revealed by Massive Sequencing in Cattle. PLoS Genet 10(2): e32767. doi:10.1371/journal.pgen.1004148
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004148

Souhrn

Zdroje

1. Bradley DG, Cunningham EP (1999) Genetic aspects of domestication. In: Fries R, Ruvinsky A, Eds. The Genetics of Cattle. pp 15–31.

2. BollonginoR, BurgerJ, PowellA, MashkourM, VigneJ-D, et al. (2012) Modern Taurine Cattle Descended from Small Number of Near-Eastern Founders. Mol Biol Evol 29: 2101–2104 doi:10.1093/molbev/mss092

3. LoftusRT, MacHughDE, BradleyDG, SharpPM, CunninghamP (1994) Evidence for two independent domestications of cattle. Proc Natl Acad Sci U S A 91: 2757–2761.

4. TroyCS, MacHughDE, BaileyJF, MageeDA, LoftusRT, et al. (2001) Genetic evidence for Near-Eastern origins of European cattle. Nature 410: 1088–1091 doi:10.1038/35074088

5. FAO (2007) The state of the world's animal genetics resources for food and agriculture. ftp://ftp.fao.org/docrep/fao/010/a1250e/a1250e02.pdf

6. Zeder MA.”Pathways to Animal Domestication (Melinda A. Zeder, 2012),” in BoneCommons, Item #11838, http://alexandriaarchive.org/bonecommons/items/show/1838 (accessed April 5, 2013).

7. The Bovine HapMap Consortium (2009) GibbsRA, TaylorJF, Van TassellCP, BarendseW, et al. (2009) Genome-Wide Survey of SNP Variation Uncovers the Genetic Structure of Cattle Breeds. Science 324: 528–532 doi:10.1126/science.1167936

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

9. FayJC, WuC-I (2000) Hitchhiking Under Positive Darwinian Selection. Genetics 155: 1405–1413.

10. SabetiPC, ReichDE, HigginsJM, LevineHZP, RichterDJ, et al. (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419: 832–837 doi:10.1038/nature01140

11. NielsenR, WilliamsonS, KimY, HubiszMJ, ClarkAG, et al. (2005) Genomic scans for selective sweeps using SNP data. Genome Res 15: 1566–1575 doi:10.1101/gr.4252305

12. VoightBF, KudaravalliS, WenX, PritchardJK (2006) A Map of Recent Positive Selection in the Human Genome. PLoS Biology 4: e72 doi:10.1371/journal.pbio.0040072

13. RubinC-J, ZodyMC, ErikssonJ, MeadowsJRS, SherwoodE, et al. (2010) Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464: 587–591 doi:10.1038/nature08832

14. NielsenR (2000) Estimation of Population Parameters and Recombination Rates From Single Nucleotide Polymorphisms. Genetics 154: 931–942.

15. KuhnerMK, BeerliP, YamatoJ, FelsensteinJ (2000) Usefulness of Single Nucleotide Polymorphism Data for Estimating Population Parameters. Genetics 156: 439–447.

16. WakeleyJ, NielsenR, Liu-CorderoSN, ArdlieK (2001) The Discovery of Single-Nucleotide Polymorphisms–and Inferences about Human Demographic History. Am J Hum Genet 69: 1332–1347 doi:10.1086/324521

17. LynnDJ, FreemanAR, MurrayC, BradleyDG (2005) A Genomics Approach to the Detection of Positive Selection in Cattle:. Genetics 170: 1189–1196 doi:10.1534/genetics.104.039040

18. MacEachernS, HayesB, McEwanJ, GoddardM (2009) An examination of positive selection and changing effective population size in Angus and Holstein cattle populations (Bos taurus) using a high density SNP genotyping platform and the contribution of ancient polymorphism to genomic diversity in Domestic cattle. BMC Genomics 10: 181 doi:10.1186/1471-2164-10-181

19. FloriL, FritzS, JaffrézicF, BoussahaM, GutI, et al. (2009) The Genome Response to Artificial Selection: A Case Study in Dairy Cattle. PLoS ONE 4: e6595 doi:10.1371/journal.pone.0006595

20. StellaA, Ajmone-MarsanP, LazzariB, BoettcherP (2010) Identification of Selection Signatures in Cattle Breeds Selected for Dairy Production. Genetics 185: 1451–1461 doi:10.1534/genetics.110.116111

21. QanbariS, PimentelECG, TetensJ, ThallerG, LichtnerP, et al. (2010b) A genome-wide scan for signatures of recent selection in Holstein cattle. Anim Genet 41: 377–389 doi:10.1111/j.1365-2052.2009.02016.x

22. QanbariS, GianolaD, HayesB, SchenkelF, MillerS, et al. (2011) Application of site and haplotype-frequency based approaches for detecting selection signatures in cattle. BMC Genomics 12: 318 doi:10.1186/1471-2164-12-318

23. JansenS, AignerB, PauschH, WysockiM, EckS, et al. (2013) Assessment of the genomic variation in a cattle population by re-sequencing of key animals at low to medium coverage. BMC Genomics 14: 446 doi:10.1186/1471-2164-14-446

24. SargolzaeiM, SchenkelFS, JansenGB, SchaefferLR (2008) Extent of linkage disequilibrium in Holstein cattle in North America. J Dairy Sci 91: 2106–2117 doi:10.3168/jds.2007-0553

25. QanbariS, PimentelECG, TetensJ, ThallerG, LichtnerP, et al. (2010a) The pattern of linkage disequilibrium in German Holstein cattle. Anim Genet 41: 346–356 doi:10.1111/j.1365-2052.2009.02011.x

26. BoykoAR, WilliamsonSH, IndapAR, DegenhardtJD, HernandezRD, et al. (2008) Assessing the Evolutionary Impact of Amino Acid Mutations in the Human Genome. PLoS Genet 4: e1000083 doi:10.1371/journal.pgen.1000083

27. LiY, VinckenboschN, TianG, Huerta-SanchezE, JiangT, et al. (2010) Resequencing of 200 human exomes identifies an excess of low-frequency non-synonymous coding variants. Nat Genet 42: 969–972 doi:10.1038/ng.680

28. PritchardJK, PrzeworskiM (2001) Linkage Disequilibrium in Humans: Models and Data. Am J Hum Genet 69: 1–14.

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

30. HayesBJ, PryceJ, ChamberlainAJ, BowmanPJ, GoddardME (2010) Genetic Architecture of Complex Traits and Accuracy of Genomic Prediction: Coat Colour, Milk-Fat Percentage, and Type in Holstein Cattle as Contrasting Model Traits. PLoS Genet 6: e1001139 doi:10.1371/journal.pgen.1001139

31. HaaseB, BrooksSA, TozakiT, BurgerD, PoncetP-A, et al. (2009) Seven novel KIT mutations in horses with white coat colour phenotypes. Animal Genetics 40: 623–629 doi:10.1111/j.1365-2052.2009.01893.x

32. RubinC-J, MegensH-J, BarrioAM, MaqboolK, SayyabS, et al. (2012) Strong signatures of selection in the domestic pig genome. PNAS 109: 19529–19536 doi:10.1073/pnas.1217149109

33. BaxterLL, HouL, LoftusSK, PavanWJ (2004) Spotlight on Spotted Mice: A Review of White Spotting Mouse Mutants and Associated Human Pigmentation Disorders. Pigment Cell Research 17: 215–224 doi:10.1111/j.1600-0749.2004.00147.x

34. HouL, PanthierJJ, ArnheiterH (2000) Signaling and transcriptional regulation in the neural crest-derived melanocyte lineage: interactions between KIT and MITF. Development 127: 5379–5389.

35. KlunglandH, VageDI, Gomez-RayaL, AdalsteinssonS, LienS (1995) The role of melanocyte-stimulating hormone (MSH) receptor in bovine coat color determination. Mammalian Genome 6: 636–639 doi:10.1007/BF00352371

36. ChoiJ, YoungJAT, CallawayEM (2010) Selective viral vector transduction of ErbB4 expressing cortical interneurons in vivo with a viral receptor–ligand bridge protein. PNAS 107: 16703–16708 doi:10.1073/pnas.1006233107

37. PickrellJK, CoopG, NovembreJ, KudaravalliS, LiJZ, et al. (2009) Signals of recent positive selection in a worldwide sample of human populations. Genome Res 19: 826–837 doi:10.1101/gr.087577.108

38. StefanssonH, PeturssonH, SigurdssonE, SteinthorsdottirV, BjornsdottirS, et al. (2002) Neuregulin 1 and Susceptibility to Schizophrenia. The American Journal of Human Genetics 71: 877–892 doi:10.1086/342734

39. MeiL, XiongW-C (2008) Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 9: 437–452 doi:10.1038/nrn2392

40. PetukhovaL, DuvicM, HordinskyM, NorrisD, PriceV, et al. (2010) Genome-wide association study in alopecia areata implicates both innate and adaptive immunity. Nature 466: 113–117 doi:10.1038/nature09114

41. ErhardtA, AkulaN, SchumacherJ, CzamaraD, KarbalaiN, et al. (2012) Replication and meta-analysis of TMEM132D gene variants in panic disorder. Transl Psychiatry 2: e156 doi:10.1038/tp.2012.85

42. NyegaardM, DemontisD, FoldagerL, HedemandA, FlintTJ, et al. (2010) CACNA1C (rs1006737) is associated with schizophrenia. Mol Psychiatry 15: 119–121 doi:10.1038/mp.2009.69

43. BrownSM, ClapcoteSJ, MillarJK, TorranceHS, AndersonSM, et al. (2011) Synaptic modulators Nrxn1 and Nrxn3 are disregulated in a Disc1 mouse model of schizophrenia. Mol Psychiatry 16: 585–587 doi:10.1038/mp.2010.134

44. YuL, ArbezN, NuciforaLG, SellGL, DelisiLE, et al. (2013) A mutation in NPAS3 segregates with mental illness in a small family. Mol Psychiatry doi:10.1038/mp.2012.192

45. MinelliA, ScassellatiC, BonviciniC, PerezJ, GennarelliM (2009) An association of GRIK3 Ser310Ala functional polymorphism with personality traits. Neuropsychobiology 59: 28–33 doi:10.1159/000202827

46. BarakT, KwanKY, LouviA, DemirbilekV, SaygıS, et al. (2011) Recessive LAMC3 mutations cause malformations of occipital cortical development. Nat Genet 43: 590–594 doi:10.1038/ng.836

47. AcheBW, YoungJM (2005) Olfaction: Diverse Species, Conserved Principles. Neuron 48: 417–430 doi:10.1016/j.neuron.2005.10.022

48. Moreno-EstradaA, CasalsF, Ramírez-SorianoA, OlivaB, CalafellF, et al. (2008) Signatures of Selection in the Human Olfactory Receptor OR5I1 Gene. Mol Biol Evol 25: 144–154 doi:10.1093/molbev/msm240

49. ChenR, IrwinDM, ZhangY-P (2012) Differences in Selection Drive Olfactory Receptor Genes in Different Directions in Dogs and Wolf. Mol Biol Evol 29: 3475–3484 doi:10.1093/molbev/mss153

50. GroenenMAM, ArchibaldAL, UenishiH, TuggleCK, TakeuchiY, et al. (2012) Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491: 393–398 doi:10.1038/nature11622

51. ElsikCG, TellamRL, WorleyKC (2009) The Genome Sequence of Taurine Cattle: A Window to Ruminant Biology and Evolution. Science 324: 522–528 doi:10.1126/science.1169588

52. DongD, JonesG, ZhangS (2009) Dynamic evolution of bitter taste receptor genes in vertebrates. BMC Evolutionary Biology 9: 12 doi:10.1186/1471-2148-9-12

53. LucaF, PerryGH, Di RienzoA (2010) Evolutionary Adaptations to Dietary Changes. Annual Review of Nutrition 30: 291–314 doi:10.1146/annurev-nutr-080508-141048

54. KosiolC, VinařT, da FonsecaRR, HubiszMJ, BustamanteCD, et al. (2008) Patterns of Positive Selection in Six Mammalian Genomes. PLoS Genet 4: e1000144 doi:10.1371/journal.pgen.1000144

55. AthanasiadisG, EstebanE, Gayà -VidalM, DugoujonJ-M, MoschonasN, et al. (2010) Different Evolutionary Histories of the Coagulation Factor VII Gene in Human Populations?: Evolutionary Patterns of the F7 Gene. Annals of Human Genetics 74: 34–45 doi:10.1111/j.1469-1809.2009.00557.x

56. UtsunomiyaYT, Pérez O'BrienAM, SonstegardTS, Van TassellCP, do CarmoAS, et al. (2013) Detecting Loci under Recent Positive Selection in Dairy and Beef Cattle by Combining Different Genome-Wide Scan Methods. PLoS ONE 8: e64280 doi:10.1371/journal.pone.0064280

57. Saldana-CaboverdeA, KosL (2010) Roles of endothelin signaling in melanocyte development and melanoma. Pigment Cell & Melanoma Research 23: 160–170 doi:10.1111/j.1755-148X.2010.00678.x

58. AberdamE, AubergerP, OrtonneJ-P, BallottiR (2000) Neprilysin, a Novel Target for Ultraviolet B Regulation of Melanogenesis Via Melanocortins. Journal of Investigative Dermatology 115: 381–387 doi:10.1046/j.1523-1747.2000.00075.x

59. YangJ, LeeSH, GoddardME, VisscherPM (2011) GCTA: A Tool for Genome-wide Complex Trait Analysis. The American Journal of Human Genetics 88: 76–82 doi:10.1016/j.ajhg.2010.11.011

60. PauschH, WangX, JungS, KrogmeierD, EdelC, et al. (2012) Identification of QTL for UV-Protective Eye Area Pigmentation in Cattle by Progeny Phenotyping and Genome-Wide Association Analysis. PLoS ONE 7: e36346 doi:10.1371/journal.pone.0036346

61. KijasJM, MollerM, PlastowG, AnderssonL (2001) A frameshift mutation in MC1R and a high frequency of somatic reversions cause black spotting in pigs. Genetics 158: 779–785.

62. AkeyJM, ZhangG, ZhangK, JinL, ShriverMD (2002) Interrogating a high-density SNP map for signatures of natural selection. Genome Res 12: 1805–1814 doi:10.1101/gr.631202

63. NuijensJH, Berkel PHCvan, SchanbacherFL (1996) Structure and biological actions of lactoferrin. J Mammary Gland Biol Neoplasia 1: 285–295 doi:10.1007/BF02018081

64. JensenK, GüntherJ, TalbotR, PetzlW, ZerbeH, et al. (2013) Escherichia coli- and Staphylococcus aureus-induced mastitis differentially modulate transcriptional responses in neighbouring uninfected bovine mammary gland quarters. BMC Genomics 14: 36 doi:10.1186/1471-2164-14-36

65. HartgersFC, VissersJL, LoomanMW, van ZoelenC, HuffineC, et al. (2000) DC-STAMP, a novel multimembrane-spanning molecule preferentially expressed by dendritic cells. Eur J Immunol 30: 3585–3590 doi:#;#;;10.1002/1521-4141(200012)30:12<3585::AID-IMMU3585>3.0.CO;2-Y

66. SawataniY, MiyamotoT, NagaiS, MaruyaM, ImaiJ, et al. (2008) The role of DC-STAMP in maintenance of immune tolerance through regulation of dendritic cell function. Int Immunol 20: 1259–1268 doi:10.1093/intimm/dxn082

67. SaneckaA, AnsemsM, ProsserAC, DanielskiK, WarnerK, et al. (2011) DC-STAMP knock-down deregulates cytokine production and T-cell stimulatory capacity of LPS-matured dendritic cells. BMC Immunol 12: 57 doi:10.1186/1471-2172-12-57

68. KarimL, TakedaH, LinL, DruetT, AriasJAC, et al. (2011) Variants modulating the expression of a chromosome domain encompassing PLAG1 influence bovine stature. Nat Genet 43: 405–413 doi:10.1038/ng.814

69. PauschH, FlisikowskiK, JungS, EmmerlingR, EdelC, et al. (2011) Genome-wide association study identifies two major loci affecting calving ease and growth-related traits in cattle. Genetics 187: 289–297 doi: 10.1534/genetics.110.124057

70. BrowningBL, BrowningSR (2009) A Unified Approach to Genotype Imputation and Haplotype-Phase Inference for Large Data Sets of Trios and Unrelated Individuals. The American Journal of Human Genetics 84: 210–223 doi:10.1016/j.ajhg.2009.01.005

71. HowieB, FuchsbergerC, StephensM, MarchiniJ, AbecasisGR (2012) Fast and accurate genotype imputation in genome-wide association studies through pre-phasing. Nat Genet 44: 955–959 doi:10.1038/ng.2354

72. PauschH, AignerB, EmmerlingR, EdelC, GötzK-U, et al. (2013) Imputation of high-density genotypes in the Fleckvieh cattle population. Genetics Selection Evolution 45: 3 doi:10.1186/1297-9686-45-3

73. GautierM, VitalisR (2012) rehh: an R package to detect footprints of selection in genome-wide SNP data from haplotype structure. Bioinformatics 28: 1176–1177 doi:10.1093/bioinformatics/bts115

74. SmithJM, HaighJ (1974) The hitch-hiking effect of a favourable gene. Genetics Research 23: 23–35 doi:10.1017/S0016672300014634

75. KangHM, SulJH, ServiceSK, ZaitlenNA, KongS, et al. (2010) Variance component model to account for sample structure in genome-wide association studies. Nat Genet 42: 348–354 doi:10.1038/ng.548

76. HayesBJ, BowmanPJ, ChamberlainAC, VerbylaK, GoddardME (2009) Accuracy of genomic breeding values in multi-breed dairy cattle populations. Genetics Selection Evolution 41: 51 doi:10.1186/1297-9686-41-51

77. HiraokaS, FuruichiT, NishimuraG, ShibataS, YanagishitaM, et al. (2007) Nucleotide-sugar transporter SLC35D1 is critical to chondroitin sulfate synthesis in cartilage and skeletal development in mouse and human. Nat Med 13: 1363–1367 doi:10.1038/nm1655

78. ZhuH, ShahS, Shyh-ChangN, ShinodaG, EinhornWS, et al. (2010) Lin28a transgenic mice manifest size and puberty phenotypes identified in human genetic association studies. Nat Genet 42: 626–630 doi:10.1038/ng.593