Genome Patterns of Selection and Introgression of Haplotypes in Natural Populations of the House Mouse ()
General parameters of selection, such as the frequency and strength of positive selection in natural populations or the role of introgression, are still insufficiently understood. The house mouse (Mus musculus) is a particularly well-suited model system to approach such questions, since it has a defined history of splits into subspecies and populations and since extensive genome information is available. We have used high-density single-nucleotide polymorphism (SNP) typing arrays to assess genomic patterns of positive selection and introgression of alleles in two natural populations of each of the subspecies M. m. domesticus and M. m. musculus. Applying different statistical procedures, we find a large number of regions subject to apparent selective sweeps, indicating frequent positive selection on rare alleles or novel mutations. Genes in the regions include well-studied imprinted loci (e.g. Plagl1/Zac1), homologues of human genes involved in adaptations (e.g. alpha-amylase genes) or in genetic diseases (e.g. Huntingtin and Parkin). Haplotype matching between the two subspecies reveals a large number of haplotypes that show patterns of introgression from specific populations of the respective other subspecies, with at least 10% of the genome being affected by partial or full introgression. Using neutral simulations for comparison, we find that the size and the fraction of introgressed haplotypes are not compatible with a pure migration or incomplete lineage sorting model. Hence, it appears that introgressed haplotypes can rise in frequency due to positive selection and thus can contribute to the adaptive genomic landscape of natural populations. Our data support the notion that natural genomes are subject to complex adaptive processes, including the introgression of haplotypes from other differentiated populations or species at a larger scale than previously assumed for animals. This implies that some of the admixture found in inbred strains of mice may also have a natural origin.
Vyšlo v časopise:
Genome Patterns of Selection and Introgression of Haplotypes in Natural Populations of the House Mouse (). PLoS Genet 8(8): e32767. doi:10.1371/journal.pgen.1002891
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002891
Souhrn
General parameters of selection, such as the frequency and strength of positive selection in natural populations or the role of introgression, are still insufficiently understood. The house mouse (Mus musculus) is a particularly well-suited model system to approach such questions, since it has a defined history of splits into subspecies and populations and since extensive genome information is available. We have used high-density single-nucleotide polymorphism (SNP) typing arrays to assess genomic patterns of positive selection and introgression of alleles in two natural populations of each of the subspecies M. m. domesticus and M. m. musculus. Applying different statistical procedures, we find a large number of regions subject to apparent selective sweeps, indicating frequent positive selection on rare alleles or novel mutations. Genes in the regions include well-studied imprinted loci (e.g. Plagl1/Zac1), homologues of human genes involved in adaptations (e.g. alpha-amylase genes) or in genetic diseases (e.g. Huntingtin and Parkin). Haplotype matching between the two subspecies reveals a large number of haplotypes that show patterns of introgression from specific populations of the respective other subspecies, with at least 10% of the genome being affected by partial or full introgression. Using neutral simulations for comparison, we find that the size and the fraction of introgressed haplotypes are not compatible with a pure migration or incomplete lineage sorting model. Hence, it appears that introgressed haplotypes can rise in frequency due to positive selection and thus can contribute to the adaptive genomic landscape of natural populations. Our data support the notion that natural genomes are subject to complex adaptive processes, including the introgression of haplotypes from other differentiated populations or species at a larger scale than previously assumed for animals. This implies that some of the admixture found in inbred strains of mice may also have a natural origin.
Zdroje
1. AkeyJM (2009) Constructing genomic maps of positive selection in humans: Where do we go from here? Genome Research 19: 711–722.
2. OleksykTK, SmithMW, O'BrienSJ (2010) Genome-wide scans for footprints of natural selection. Philosophical Transactions of the Royal Society B-Biological Sciences 365: 185–205.
3. SabetiPC, SchaffnerSF, FryB, LohmuellerJ, VarillyP, et al. (2006) Positive natural selection in the human lineage. Science 312: 1614–1620.
4. TangK, ThorntonKR, StonekingM (2007) A new approach for using genome scans to detect recent positive selection in the human genome. PLos Biol 5: e171 doi:10.1371/journal.pbio.0050171.
5. ChenH, PattersonN, ReichD (2010) Population differentiation as a test for selective sweeps. Genome Research 20: 393–402.
6. 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.
7. BartonNH (2001) The role of hybridization in evolution. Molecular Ecology 10: 551–568.
8. BurkeJM, ArnoldML (2001) Genetics and the fitness of hybrids. Annual Review of Genetics 35: 31–52.
9. MalletJ (2007) Hybrid speciation. Nature 446: 279–283.
10. NolteAW, TautzD (2010) Understanding the onset of hybrid speciation. Trends in Genetics 26: 54–58.
11. KulathinalRJ, StevisonLS, NoorMAF (2009) The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing. PLoS Genet 5: e1000550 doi:10.1371/journal.pgen.1000550.
12. GreenRE, KrauseJ, BriggsAW, MaricicT, StenzelU, et al. (2010) A Draft Sequence of the Neandertal Genome. Science 328: 710–722.
13. SongY, EndepolsS, KlemannN, RichterD, MatuschkaFR, et al. (2011) Adaptive Introgression of Anticoagulant Rodent Poison Resistance by Hybridization between Old World Mice. Current Biology 21: 1296–1301.
14. SalazarC, BaxterSW, Pardo-DiazC, WuG, SurridgeA, et al. (2010) Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies. PLoS Genet 6: e1000930 doi:10.1371/journal.pgen.1000930.
15. IhleS, RavaoarimananaI, ThomasM, TautzD (2006) An analysis of signatures of selective sweeps in natural populations of the house mouse. Molecular Biology and Evolution 23: 790–797.
16. TeschkeM, MukabayireO, WieheT, TautzD (2008) Identification of Selective Sweeps in Closely Related Populations of the House Mouse Based on Microsatellite Scans. Genetics 180: 1537–1545.
17. StaubachF, TeschkeM, VoolstraCR, WolfJBW, TautzD (2010) A test of the neutral model of expression change in natural populations of house mouse subspcies. Evolution 64: 549–560.
18. GuenetJL, BonhommeF (2003) Wild mice: an ever-increasing contribution to a popular mammalian model. Trends in Genetics 19: 24–31.
19. GeraldesA, BassetP, GibsonB, SmithKL, HarrB, et al. (2008) Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Molecular Ecology 17: 5349–5363.
20. Rajabi-MahamH, OrthA, BonhommeF (2008) Phylogeography and postglacial expansion of Mus musculus domesticus inferred from mitochondrial DNA coalescent, from Iran to Europe. Molecular Ecology 17: 627–641.
21. Britton-DavidianJ, Fel-ClairF, LopezJ, AlibertP, BoursotP (2005) Postzygotic isolation between the two European subspecies of the house mouse: estimates from fertility patterns in wild and laboratory-bred hybrids. Biological Journal of the Linnean Society 84: 379–393.
22. GoodJM, HandelMA, NachmanMW (2008) Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice. Evolution 62: 50–65.
23. CucchiT, VigneJD, AuffrayJC (2005) First occurrence of the house mouse (Mus musculus domesticus Schwarz & Schwarz, 1943) in the Western Mediterranean: a zooarchaeological revision of subfossil occurrences. Biological Journal of the Linnean Society 84: 429–445.
24. CucchiT, BalasescuA, BemC, RaduV, VigneJD, et al. (2011) New insights into the invasive process of the eastern house mouse (Mus musculus musculus): Evidence from the burnt houses of Chalcolithic Romania. Holocene 21: 1195–1202.
25. YangH, DingYM, HutchinsLN, SzatkiewiczJ, BellTA, et al. (2009) A customized and versatile high-density genotyping array for the mouse. Nature Methods 6: 663–U655.
26. BainesJF, HarrB (2007) Reduced X-linked diversity in derived populations of house mice. Genetics 175: 1911–1921.
27. LaurieCC, NickersonDA, AndersonAD, WeirBS, LivingstonRJ, et al. (2007) Linkage disequilibrium in wild mice. PLoS Genet 3: e144 doi:10.1371/journal.pgen.0030144.
28. ShimuraH, HattoriN, KuboS, MizunoY, AsakawaS, et al. (2000) Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nature Genetics 25: 302–305.
29. HoweJR, BairJL, SayedMG, AndersonME, MitrosFA, et al. (2001) Germline mutations of the gene encoding bone morphogenetic protein receptor 1A in juvenile polyposis. Nature Genetics 28: 184–187.
30. PandaS, SatoTK, CastrucciAM, RollagMD, DeGripWJ, et al. (2002) Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298: 2213–2216.
31. PirasG, El KharroubiA, KozlovS, Escalante-AlcaldeD, HernandezL, et al. (2000) Zac1 (Lot1), a potential tumor suppressor gene, and the gene for epsilon-sarcoglycan are maternally imprinted genes: Identification by a subtractive screen of novel uniparental fibroblast lines. Molecular and Cellular Biology 20: 3308–3315.
32. KamiyaM, JudsonH, OkazakiY, KusakabeM, MuramatsuM, et al. (2000) The cell cycle control gene ZAC/PLAGL1 is imprinted - a strong candidate gene for transient neonatal diabetes. Human Molecular Genetics 9: 453–460.
33. WiderC, LincolnSJ, HeckmanMG, DiehlNN, StoneJT, et al. (2009) Phactr2 and Parkinson's disease. Neuroscience Letters 453: 9–11.
34. PerryGH, DominyNJ, ClawKG, LeeAS, FieglerH, et al. (2007) Diet and the evolution of human amylase gene copy number variation. Nature Genetics 39: 1256–1260.
35. MatsumotoY, KatayamaK, OkamotoT, YamadaK, TakashimaN, et al. (2011) Impaired Auditory-Vestibular Functions and Behavioral Abnormalities of Slitrk6-Deficient Mice. PLoS ONE 6: e16497 doi:10.1371/journal.pone.0016497.
36. DavydovEV, GoodeDL, SirotaM, CooperGM, SidowA, et al. (2010) Identifying a High Fraction of the Human Genome to be under Selective Constraint Using GERP plus. PLoS Comput Biol 6: e1001025 doi:10.1371/journal.pcbi.1001025.
37. PriceAL, TandonA, PattersonN, BarnesKC, RafaelsN, et al. (2009) Sensitive Detection of Chromosomal Segments of Distinct Ancestry in Admixed Populations. PLoS Genet 5: e1000519 doi:10.1371/journal.pgen.1000519.
38. MoritaT, KubotaH, MurataK, NozakiM, DelarbreC, et al. (1992) Evolution of the mouse t-haplotype - recent and worldwide introgression to Mus musculus. Proceedings of the National Academy of Sciences of the United States of America 89: 6851–6855.
39. HernandezRD, KelleyJL, ElyashivE, MeltonSC, AutonA, et al. (2011) Classic Selective Sweeps Were Rare in Recent Human Evolution. Science 331: 920–924.
40. SalcedoT, GeraldesA, NachmanMW (2007) Nucleotide variation in wild and inbred mice. Genetics 177: 2277–2291.
41. PrzeworskiM (2002) The signature of positive selection at randomly chosen loci. Genetics 160: 1179–1189.
42. Domazet-LosoT, TautzD (2008) An Ancient Evolutionary Origin of Genes Associated with Human Genetic Diseases. Molecular Biology and Evolution 25: 2699–2707.
43. PerlmanRL (2011) EVOLUTIONARY BIOLOGY a basic science for medicine in the 21st century. Perspectives in Biology and Medicine 54: 75–88.
44. BonhommeF, RivalsE, OrthA, GrantGR, JeffreysAJ, et al. (2007) Species-wide distribution of highly polymorphic minisatellite markers suggests past and present genetic exchanges among House Mouse subspecies. Genome Biology 8.
45. TeeterKC, PayseurBA, HarrisLW, BakewellMA, ThibodeauLM, et al. (2008) Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Research 18: 67–76.
46. WangLY, LuzynskiK, PoolJE, JanousekV, DufkovaP, et al. (2011) Measures of linkage disequilibrium among neighbouring SNPs indicate asymmetries across the house mouse hybrid zone. Molecular Ecology 20: 2985–3000.
47. StemshornKC, ReedFA, NolteAW, TautzD (2011) Rapid formation of distinct hybrid lineages after secondary contact of two fish species (Cottus sp.). Molecular Ecology 20: 1475–1491.
48. WhiteMA, AneC, DeweyCN, LargetBR, PayseurBA (2009) Fine-Scale Phylogenetic Discordance across the House Mouse Genome. PLoS Genet 5: e1000729 doi:10.1371/journal.pgen.1000729.
49. KeaneTM, GoodstadtL, DanecekP, WhiteMA, WongK, et al. (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477: 289–294.
50. PoolJE, NielsenR (2009) Inference of historical changes in migration rate from the lengths of migrant tracts. Genetics 181: 711–719.
51. HurstJL, PayneCE, NevisonCM, MarieAD, HumphriesRE, et al. (2001) Individual recognition in mice mediated by major urinary proteins. Nature 414: 631–634.
52. MudgeJM, ArmstrongSD, McLarenK, BeynonRJ, HurstJL, et al. (2008) Dynamic instability of the major urinary protein gene family revealed by genomic and phenotypic comparisons between C57 and 129 strain mice. Genome Biology 9.
53. ReichD, GreenRE, KircherM, KrauseJ, PattersonN, et al. (2010) Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468: 1053–1060.
54. ShifmanS, BellJT, CopleyRR, TaylorMS, WilliamsRW, et al. (2006) A high-resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS Biol 4: e395 doi:10.1371/journal.pbio.0040395.
55. ScheetP, StephensM (2006) A fast and flexible statistical model for large-scale population genotype data: Applications to inferring missing genotypes and haplotypic phase. American Journal of Human Genetics 78: 629–644.
56. HudsonRR (2002) Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18: 337–338.
57. WeirBS, CockerhamCC (1984) Estimationg F-statistics for the analysis of population structure. Evolution 38: 1358–1370.
58. VoightBF, KudaravalliS, WenXQ, PritchardJK (2006) A map of recent positive selection in the human genome. PLoS Biol 4: e72 doi:10.1371/journal.pbio.0040072.
59. KentWJ, SugnetCW, FureyTS, RoskinKM, PringleTH, et al. (2002) The human genome browser at UCSC. Genome Research 12: 996–1006.
60. KarolchikD, HinrichsAS, FureyTS, RoskinKM, SugnetCW, et al. (2004) The UCSC Table Browser data retrieval tool. Nucleic Acids Research 32: D493–D496.
61. BerrizGF, BeaverJE, CenikC, TasanM, RothFP (2009) Next generation software for functional trend analysis. Bioinformatics 25: 3043–3044.
62. BarrettJC, FryB, MallerJ, DalyMJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263–265.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 8
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