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Introgression from Domestic Goat Generated Variation at the Major Histocompatibility Complex of Alpine Ibex


The major histocompatibility complex (MHC), a crucial component of the defense against pathogens, contains the most polymorphic functional genes in vertebrate genomes. The extraordinary genetic variation is generally considered to be ancient. We investigated whether a previously neglected mechanism, introgression from related species, provides an additional source of MHC variation. We show that introgression from domestic goat dramatically increased genetic variation at the MHC of Alpine ibex, a species that had nearly gone extinct during the 18th century, but has been restored to large numbers since. We show that Alpine ibex share one of only two alleles at a generally highly polymorphic MHC locus with domestic goats and that the chromosomal region containing the goat-type allele has a signature of recent introgression. Our finding contradicts the long-standing view that ancient trans-species polymorphism is the sole source of the extraordinary genetic variability at the MHC. Instead, we show that in Alpine ibex introgression generated genetic diversity at a MHC locus. Our study supports the view that loci favoring genetic polymorphism may be susceptible to adaptive introgression from related species and will encourage future research to identify unexpected signatures of introgression.


Vyšlo v časopise: Introgression from Domestic Goat Generated Variation at the Major Histocompatibility Complex of Alpine Ibex. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004438
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004438

Souhrn

The major histocompatibility complex (MHC), a crucial component of the defense against pathogens, contains the most polymorphic functional genes in vertebrate genomes. The extraordinary genetic variation is generally considered to be ancient. We investigated whether a previously neglected mechanism, introgression from related species, provides an additional source of MHC variation. We show that introgression from domestic goat dramatically increased genetic variation at the MHC of Alpine ibex, a species that had nearly gone extinct during the 18th century, but has been restored to large numbers since. We show that Alpine ibex share one of only two alleles at a generally highly polymorphic MHC locus with domestic goats and that the chromosomal region containing the goat-type allele has a signature of recent introgression. Our finding contradicts the long-standing view that ancient trans-species polymorphism is the sole source of the extraordinary genetic variability at the MHC. Instead, we show that in Alpine ibex introgression generated genetic diversity at a MHC locus. Our study supports the view that loci favoring genetic polymorphism may be susceptible to adaptive introgression from related species and will encourage future research to identify unexpected signatures of introgression.


Zdroje

1. SattaY, LiYJ, TakahataN (1998) The neutral theory and natural selection in the HLA region. Front Biosci 3: d459–d467.

2. BeckS, GeraghtyD, InokoH, RowenL, AguadoB, et al. (1999) Complete sequence and gene map of a human major histocompatibility complex. Nature 401: 921–923.

3. GaudieriS, DawkinsR, HabaraK, KulskiJ, GojoboriT (2000) SNP profile within the human major histocompatibility complex reveals an extreme and interrupted level of nucleotide diversity. Genome Res 10: 1579–1586.

4. KleinJ, FigueroaF (1986) Evolution of the major histocompatibility complex. Crit Rev Immunol 6: 295–386.

5. GregersenJW, KrancKR, KeX, SvendsenP, MadsenLS, et al. (2006) Functional epistasis on a common MHC haplotype associated with multiple sclerosis. Nature 443: 574–577 doi:10.1038/nature05133

6. de BakkerPIW, McVeanG, SabetiPC, MirettiMM, GreenT, et al. (2006) A high-resolution HLA and SNP haplotype map for disease association studies in the extended human MHC. Nat Genet 38: 1166–1172 doi:10.1038/ng1885

7. KlochA, BabikW, BajerA, SińskiE, RadwanJ (2010) Effects of an MHC-DRB genotype and allele number on the load of gut parasites in the bank vole Myodes glareolus. Mol Ecol 19 Suppl 1255–265 doi:10.1111/j.1365-294X.2009.04476.x

8. OliverMK, TelferS, PiertneySB (2009) Major histocompatibility complex (MHC) heterozygote superiority to natural multi-parasite infections in the water vole (Arvicola terrestris). Proc Biol Sci 276: 1119–1128 doi:10.1046/j.1440-1711.1998.00772.x

9. WesterdahlH, AsgharM, HasselquistD, BenschS (2012) Quantitative disease resistance: to better understand parasite-mediated selection on major histocompatibility complex. Proc Biol Sci 279: 577–584 doi:10.1098/rspb.2011.0917

10. SpurginL, RichardsonDS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc Biol Sci 277: 979–988 doi:10.1098/rspb.2009.2084

11. PiertneySB, OliverMK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96: 7–21 doi:10.1038/sj.hdy.6800724

12. Van OosterhoutC (2009) A new theory of MHC evolution: beyond selection on the immune genes. Proc Biol Sci 276: 657–665 doi:10.1098/rspb.2008.1299

13. TakahataN, SattaY, KleinJ (1992) Polymorphism and balancing selection at major histocompatibility complex loci. Genetics 130: 925–938.

14. SchierupMH, VekemansX, CharlesworthD (2000) The effect of subdivision on variation at multi-allelic loci under balancing selection. Genet Res 76: 51–62.

15. FigueroaF, GüntherE, KleinJ (1988) MHC polymorphism pre-dating speciation. Nature 335: 265–267 doi:10.1038/335265a0

16. HedrickPW (2013) Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol Ecol 22: 4606–4618 doi:10.1111/mec.12415

17. CastricV, BechsgaardJ, SchierupMH, VekemansX (2008) Repeated adaptive introgression at a gene under multiallelic balancing selection. PLoS Genet 4: e1000168 doi:10.1371/journal.pgen.1000168

18. FeulnerPGD, GrattenJ, KijasJW, VisscherPM, PembertonJM, et al. (2013) Introgression and the fate of domesticated genes in a wild mammal population. Mol Ecol 22: 4210–4221 doi:10.1111/mec.12378

19. WegnerKM, EizaguirreC (2012) New(t)s and views from hybridizing MHC genes: introgression rather than trans-species polymorphism may shape allelic repertoires. Mol Ecol 21: 779–781 doi:10.1111/j.1365-294X.2011.05401.x

20. Abi-RachedL, JobinMJ, KulkarniS, McWhinnieA, DalvaK, et al. (2011) The shaping of modern human immune systems by multiregional admixture with archaic humans. Science 334: 89–94 doi:10.1126/science.1209202

21. VilaC, SeddonJ, EllegrenH (2005) Genes of domestic mammals augmented by backcrossing with wild ancestors. Trends Genet 21: 214–218 doi:10.1016/j.tig.2005.02.004

22. Nadachowska-BrzyskaK, ZielińskiP, RadwanJ, BabikW (2012) Interspecific hybridization increases MHC class II diversity in two sister species of newts. Mol Ecol 21: 887–906 doi:10.1111/j.1365-294X.2011.05347.x

23. NaderiS, RezaeiH-R, PompanonF, BlumMGB, NegriniR, et al. (2008) The goat domestication process inferred from large-scale mitochondrial DNA analysis of wild and domestic individuals. Proc Natl Acad Sci U S A 105: 17659–17664 doi:10.1073/pnas.0804782105

24. MaudetC, MillerC, BassanoB, Breitenmoser-WurstenC, GauthierD, et al. (2002) Microsatellite DNA and recent statistical methods in wildlife conservation management: applications in Alpine ibex (Capra ibex ibex). Mol Ecol 11: 421–436.

25. BiebachI, KellerLF (2009) A strong genetic footprint of the re-introduction history of Alpine ibex (Capra ibex ibex). Mol Ecol 18: 5046–5058 doi:10.1111/j.1365-294X.2009.04420.x

26. BiebachI, KellerLF (2010) Inbreeding in reintroduced populations: the effects of early reintroduction history and contemporary processes. Conserv Genet 11: 527–538 doi:10.1007/s10592-009-0019-6

27. SchaschlH, WandelerP, SuchentrunkF, Obexer-RuffG, GoodmanSJ (2006) Selection and recombination drive the evolution of MHC class II DRB diversity in ungulates. Heredity 97: 427–437 doi:10.1038/sj.hdy.6800892

28. AlasaadS, BiebachI, GrossenC, SoriguerRC, PérezJM, et al. (2012) Microsatellite-based genotyping of MHC class II DRB1 gene in Iberian and Alpine ibex. Eur J Wildl Res 58: 743–748 doi:10.1007/s10344-011-0592-0

29. TakadaT, KikkawaY, YonekawaH, AmanoT (1998) Analysis of goat MHC class II DRA and DRB genes: identification of the expressed gene and new DRB alleles. Immunogenetics 48: 408–412 doi:10.1007/s002510050452

30. SchaschlH, SuchentrunkF, HammerS, GoodmanSJ (2005) Recombination and the origin of sequence diversity in the DRB MHC class II locus in chamois (Rupicapra spp.). Immunogenetics 57: 108–115 doi:10.1007/s00251-005-0784-4

31. MonaS, CrestanelloB, Bankhead-DronnetS, PecchioliE, IngrossoS, et al. (2008) Disentangling the effects of recombination, selection, and demography on the genetic variation at a major histocompatibility complex class II gene in the alpine chamois. Mol Ecol 17: 4053–4067 doi:10.1111/j.1365-294X.2008.03892.x

32. SchwaigerF, BuitkampJ, WeyersE, EpplenJ (1993) Typing of Artiodactyl MHC-DRB genes with the help of intronic simple repeated DNA-sequences. Mol Ecol 2: 55–59.

33. Klein J (1986) Natural history of the major histocompatibility complex. John Wiley & Sons. 1 pp.

34. RopiquetA, HassaninA (2006) Hybrid origin of the Pliocene ancestor of wild goats. Mol Phylogenet Evol 41: 395–404 doi:10.1016/j.ympev.2006.05.033

35. Hernández FernándezM, VrbaES (2005) A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biol Rev 80: 269–302.

36. GiacomettiM, RogantiR, de TannD, Stahlberger-SaitbekovaN, Obexer-RuffG (2004) Alpine ibex Capra ibex ibex x domestic goat C. aegagrus domestica hybrids in a restricted area of southern Switzerland. Wildlife Biol 10: 137–143.

37. Klein J, Sato A, Nagl S, O'hUigín C (1998) Molecular trans-species polymorphism. Annu Rev Ecol Syst: 1–21.

38. BernatchezL, LandryC (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evolution Biol 16: 363–377.

39. PritchardJ, StephensM, DonnellyP (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

40. DongY, XieM, JiangY, XiaoN, DuX, et al. (2012) Sequencing and automated whole-genome optical mapping of the genome of a domestic goat (Capra hircus). Nat Biotechnol 31: 135–141 doi:10.1038/nbt.2478

41. BruenT, PhilippeH, BryantD (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172: 2665–2681.

42. Tosser-KloppG, BardouP, BouchezO, CabauC, CrooijmansR, et al. (2014) Design and characterization of a 52K SNP chip for goats. PLoS ONE 9: e86227 doi:10.1371/journal.pone.0086227

43. HusonDH, BryantD (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254–267 doi:10.1093/molbev/msj030

44. SlatkinM (2008) Linkage disequilibrium — understanding the evolutionary past and mapping the medical future. Nat Rev Genet 9: 477–485 doi:10.1038/nrg2361

45. CutterAD, PayseurBA (2013) Genomic signatures of selection at linked sites: unifying the disparity among species. Nat Rev Genet 14: 262–274 doi:10.1038/nrg3425

46. SabetiP, ReichD, HigginsJ, LevineH, RichterD, et al. (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419: 832–837.

47. VoightB, KudaravalliS, WenX, PritchardJ (2006) A map of recent positive selection in the human genome. Plos Biol 4: 446–458 doi:10.1371/journal.pbio.0040072

48. AllendorfF, LearyR, SpruellP, WenburgJ (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16: 613–622.

49. DerrJN, HedrickPW, HalbertND, PloughL, DobsonLK, et al. (2012) Phenotypic effects of cattle mitochondrial DNA in American bison. Conserv Biol 26: 1130–1136 doi:10.1111/j.1523-1739.2012.01905.x

50. AndersonTM, vonHoldtBM, CandilleSI, MusianiM, GrecoC, et al. (2009) Molecular and evolutionary history of melanism in North American gray wolves. Science 323: 1339–1343 doi:10.1126/science.1165448

51. EtterPD, BasshamS, HohenlohePA, JohnsonEA, CreskoWA (2011) SNP discovery and genotyping for evolutionary genetics using RAD sequencing. Methods Mol Biol 772: 157–178 doi:_10.1007/978-1-61779-228-1_9

52. LangmeadB, SalzbergSL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359 doi:10.1038/nmeth.1923

53. DePristoMA, BanksE, PoplinR, GarimellaKV, MaguireJR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491–498 doi:10.1038/ng.806

54. McKennaA, HannaM, BanksE, SivachenkoA, CibulskisK, et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297–1303 doi:10.1101/gr.107524.110

55. LischerHEL, ExcoffierL (2012) PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics 28: 298–299 doi:10.1093/bioinformatics/btr642

56. PurcellS, NealeB, Todd-BrownK, ThomasL, FerreiraMAR, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559–575 doi:10.1086/519795

57. ScheetP, StephensM (2006) A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78: 629–644 doi:10.1086/502802

58. HillWG, WeirBS (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol 33: 54–78.

59. GautierM, NavesM (2011) Footprints of selection in the ancestral admixture of a New World Creole cattle breed. Mol Ecol 20: 3128–3143 doi:10.1111/j.1365-294X.2011.05163.x

60. KatohK, StandleyDM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780 doi:10.1093/molbev/mst010

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Genetika Reprodukčná medicína

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PLOS Genetics


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