Introgression of Neandertal- and Denisovan-like Haplotypes Contributes to Adaptive Variation in Human Toll-like Receptors

American Journal of Human Genetics

Volumn 98, Issue 1, 2016, Pages 22-33

  Dannemann, Michael ^a,b   Andrés, Aida M ^a   Kelso, Janet ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR;

ALLELE; ALLERGIC DISEASE; ARTICLE; CHROMOSOME 4; CONTROLLED STUDY; DENISOVAN LIKE HAPLOTYPE; GENE EXPRESSION; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GEOGRAPHIC DISTRIBUTION; HAPLOTYPE; HELICOBACTER PYLORI; HUMAN; HUMAN TISSUE; INNATE IMMUNITY; INTROGRESSION; MUTATION RATE; NEANDERTAL LIKE HAPLOTYPE; POPULATION DIFFERENTIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROPREVALENCE; SINGLE NUCLEOTIDE POLYMORPHISM; ADAPTATION; ANIMAL; CELL LINE; GENETICS; HOMO NEANDERTHALENSIS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL LINE; HAPLOTYPES; HUMANS; NEANDERTHALS; POLYMORPHISM, SINGLE NUCLEOTIDE; TOLL-LIKE RECEPTORS;

EID: 84954244556     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2015.11.015     Document Type: Article

References (59)

1. R.E. Green, J. Krause, A.W. Briggs, T. Maricic, U. Stenzel, M. Kircher, N. Patterson, H. Li, W. Zhai, M.H. Fritz, and et al. A draft sequence of the Neandertal genome Science 328 2010 710 722
2. M. Meyer, M. Kircher, M.T. Gansauge, H. Li, F. Racimo, S. Mallick, J.G. Schraiber, F. Jay, K. Prüfer, C. de Filippo, and et al. A high-coverage genome sequence from an archaic Denisovan individual Science 338 2012 222 226
3. K. Prüfer, F. Racimo, N. Patterson, F. Jay, S. Sankararaman, S. Sawyer, A. Heinze, G. Renaud, P.H. Sudmant, C. de Filippo, and et al. The complete genome sequence of a Neanderthal from the Altai Mountains Nature 505 2014 43 49
4. D. Reich, R.E. Green, M. Kircher, J. Krause, N. Patterson, E.Y. Durand, B. Viola, A.W. Briggs, U. Stenzel, P.L. Johnson, and et al. Genetic history of an archaic hominin group from Denisova Cave in Siberia Nature 468 2010 1053 1060
5. S. Sankararaman, S. Mallick, M. Dannemann, K. Prüfer, J. Kelso, S. Pääbo, N. Patterson, and D. Reich The genomic landscape of Neanderthal ancestry in present-day humans Nature 507 2014 354 357
6. B. Vernot, and J.M. Akey Resurrecting surviving Neandertal lineages from modern human genomes Science 343 2014 1017 1021
7. L. Ségurel, and L. Quintana-Murci Preserving immune diversity through ancient inheritance and admixture Curr. Opin. Immunol. 30 2014 79 84
8. E. Huerta-Sánchez, X. Jin, Asan, Z. Bianba, B.M. Peter, N. Vinckenbosch, Y. Liang, X. Yi, M. He, M. Somel, and et al. Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA Nature 512 2014 194 197
9. L. Abi-Rached, M.J. Jobin, S. Kulkarni, A. McWhinnie, K. Dalva, L. Gragert, F. Babrzadeh, B. Gharizadeh, M. Luo, F.A. Plummer, and et al. The shaping of modern human immune systems by multiregional admixture with archaic humans Science 334 2011 89 94
10. A.L. Williams, S.B. Jacobs, H. Moreno-Macías, A. Huerta-Chagoya, C. Churchhouse, C. Márquez-Luna, H. García-Ortíz, M.J. Gómez-Vázquez, N.P. Burtt, C.A. Aguilar-Salinas, et al. SIGMA Type 2 Diabetes Consortium Sequence variants in SLC16A11 are a common risk factor for type 2 diabetes in Mexico Nature 506 2014 97 101
11. F.L. Mendez, J.C. Watkins, and M.F. Hammer A haplotype at STAT2 introgressed from neanderthals and serves as a candidate of positive selection in Papua New Guinea Am. J. Hum. Genet. 91 2012 265 274
12. F.L. Mendez, J.C. Watkins, and M.F. Hammer Neandertal origin of genetic variation at the cluster of OAS immunity genes Mol. Biol. Evol. 30 2013 798 801
13. S. Akira, S. Uematsu, and O. Takeuchi Pathogen recognition and innate immunity Cell 124 2006 783 801
14. L. Quintana-Murci, and A.G. Clark Population genetic tools for dissecting innate immunity in humans Nat. Rev. Immunol. 13 2013 280 293
15. L.B. Barreiro, M. Ben-Ali, H. Quach, G. Laval, E. Patin, J.K. Pickrell, C. Bouchier, M. Tichit, O. Neyrolles, B. Gicquel, and et al. Evolutionary dynamics of human Toll-like receptors and their different contributions to host defense PLoS Genet. 5 2009 e1000562
16. H. Laayouni, M. Oosting, P. Luisi, M. Ioana, S. Alonso, I. Ricaño-Ponce, G. Trynka, A. Zhernakova, T.S. Plantinga, S.C. Cheng, and et al. Convergent evolution in European and Rroma populations reveals pressure exerted by plague on Toll-like receptors Proc. Natl. Acad. Sci. USA 111 2014 2668 2673
17. F. Racimo, S. Sankararaman, R. Nielsen, and E. Huerta-Sánchez Evidence for archaic adaptive introgression in humans Nat. Rev. Genet. 16 2015 359 371
18. V. Plagnol, and J.D. Wall Possible ancestral structure in human populations PLoS Genet. 2 2006 e105
19. J. Mayerle, C.M. den Hoed, C. Schurmann, L. Stolk, G. Homuth, M.J. Peters, L.G. Capelle, K. Zimmermann, F. Rivadeneira, S. Gruska, and et al. Identification of genetic loci associated with Helicobacter pylori serologic status JAMA 309 2013 1912 1920
20. D.A. Hinds, G. McMahon, A.K. Kiefer, C.B. Do, N. Eriksson, D.M. Evans, B. St Pourcain, S.M. Ring, J.L. Mountain, U. Francke, and et al. A genome-wide association meta-analysis of self-reported allergy identifies shared and allergy-specific susceptibility loci Nat. Genet. 45 2013 907 911
21. G.R. Abecasis, A. Auton, L.D. Brooks, M.A. DePristo, R.M. Durbin, R.E. Handsaker, H.M. Kang, G.T. Marth, G.A. McVean 1000 Genomes Project Consortium An integrated map of genetic variation from 1,092 human genomes Nature 491 2012 56 65
22. A. Auton, L.D. Brooks, R.M. Durbin, E.P. Garrison, H.M. Kang, J.O. Korbel, J.L. Marchini, S. McCarthy, G.A. McVean, G.R. Abecasis 1000 Genomes Project Consortium A global reference for human genetic variation Nature 526 2015 68 74
23. E. Paradis pegas: an R package for population genetics with an integrated-modular approach Bioinformatics 26 2010 419 420
24. E. Paradis, J. Claude, and K. Strimmer APE: analyses of phylogenetics and evolution in R language Bioinformatics 20 2004 289 290
25. A.S. Hinrichs, D. Karolchik, R. Baertsch, G.P. Barber, G. Bejerano, H. Clawson, M. Diekhans, T.S. Furey, R.A. Harte, F. Hsu, and et al. The UCSC Genome Browser Database: update 2006 Nucleic Acids Res. 34 2006 D590 D598
26. K.W. Broman, J.C. Murray, V.C. Sheffield, R.L. White, and J.L. Weber Comprehensive human genetic maps: individual and sex-specific variation in recombination Am. J. Hum. Genet. 63 1998 861 869
27. C. Dib, S. Fauré, C. Fizames, D. Samson, N. Drouot, A. Vignal, P. Millasseau, S. Marc, J. Hazan, E. Seboun, and et al. A comprehensive genetic map of the human genome based on 5,264 microsatellites Nature 380 1996 152 154
28. A. Kong, D.F. Gudbjartsson, J. Sainz, G.M. Jonsdottir, S.A. Gudjonsson, B. Richardsson, S. Sigurdardottir, J. Barnard, B. Hallbeck, G. Masson, and et al. A high-resolution recombination map of the human genome Nat. Genet. 31 2002 241 247
29. D.M. Altshuler, R.A. Gibbs, L. Peltonen, D.M. Altshuler, R.A. Gibbs, L. Peltonen, E. Dermitzakis, S.F. Schaffner, F. Yu, L. Peltonen, et al. International HapMap 3 Consortium Integrating common and rare genetic variation in diverse human populations Nature 467 2010 52 58
30. A.G. Hinch, A. Tandon, N. Patterson, Y. Song, N. Rohland, C.D. Palmer, G.K. Chen, K. Wang, S.G. Buxbaum, E.L. Akylbekova, and et al. The landscape of recombination in African Americans Nature 476 2011 170 175
31. P. Danecek, A. Auton, G. Abecasis, C.A. Albers, E. Banks, M.A. DePristo, R.E. Handsaker, G. Lunter, G.T. Marth, S.T. Sherry, et al. 1000 Genomes Project Analysis Group The variant call format and VCFtools Bioinformatics 27 2011 2156 2158
32. GTEx Consortium The Genotype-Tissue Expression (GTEx) project Nat. Genet. 45 2013 580 585
33. M.I. Love, W. Huber, and S. Anders Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Genome Biol. 15 2014 550
34. T. Lappalainen, M. Sammeth, M.R. Friedländer, P.A. 't Hoen, J. Monlong, M.A. Rivas, M. Gonzàlez-Porta, N. Kurbatova, T. Griebel, P.G. Ferreira, et al. Geuvadis Consortium Transcriptome and genome sequencing uncovers functional variation in humans Nature 501 2013 506 511
35. S. Anders, and W. Huber Differential expression analysis for sequence count data Genome Biol. 11 2010 R106
36. E.P. Consortium ENCODE Project Consortium An integrated encyclopedia of DNA elements in the human genome Nature 489 2012 57 74
37. K. Prüfer, B. Muetzel, H.H. Do, G. Weiss, P. Khaitovich, E. Rahm, S. Pääbo, M. Lachmann, and W. Enard FUNC: a package for detecting significant associations between gene sets and ontological annotations BMC Bioinformatics 8 2007 41
38. M. Ashburner, C.A. Ball, J.A. Blake, D. Botstein, H. Butler, J.M. Cherry, A.P. Davis, K. Dolinski, S.S. Dwight, J.T. Eppig, et al. The Gene Ontology Consortium Gene ontology: tool for the unification of biology Nat. Genet. 25 2000 25 29
39. M.J. Li, P. Wang, X. Liu, E.L. Lim, Z. Wang, M. Yeager, M.P. Wong, P.C. Sham, S.J. Chanock, and J. Wang GWASdb: a database for human genetic variants identified by genome-wide association studies Nucleic Acids Res. 40 2012 D1047 D1054
40. J. Rogers, and R.A. Gibbs Comparative primate genomics: emerging patterns of genome content and dynamics Nat. Rev. Genet. 15 2014 347 359
41. A. Yu, C. Zhao, Y. Fan, W. Jang, A.J. Mungall, P. Deloukas, A. Olsen, N.A. Doggett, N. Ghebranious, K.W. Broman, and J.L. Weber Comparison of human genetic and sequence-based physical maps Nature 409 2001 951 953
42. B.M. Henn, L.R. Botigué, S. Gravel, W. Wang, A. Brisbin, J.K. Byrnes, K. Fadhlaoui-Zid, P.A. Zalloua, A. Moreno-Estrada, J. Bertranpetit, and et al. Genomic ancestry of North Africans supports back-to-Africa migrations PLoS Genet. 8 2012 e1002397
43. F. Sánchez-Quinto, L.R. Botigué, S. Civit, C. Arenas, M.C. Avila-Arcos, C.D. Bustamante, D. Comas, and C. Lalueza-Fox North African populations carry the signature of admixture with Neandertals PLoS ONE 7 2012 e47765
44. B.Y. Kim, and K.E. Lohmueller Selection and reduced population size cannot explain higher amounts of Neandertal ancestry in East Asian than in European human populations Am. J. Hum. Genet. 96 2015 454 461
45. B. Vernot, and J.M. Akey Complex history of admixture between modern humans and Neandertals Am. J. Hum. Genet. 96 2015 448 453
46. P. Qin, and M. Stoneking Denisovan ancestry in East Eurasian and Native American populations Mol. Biol. Evol. 32 2015 2665 2674
47. I. Lazaridis, N. Patterson, A. Mittnik, G. Renaud, S. Mallick, K. Kirsanow, P.H. Sudmant, J.G. Schraiber, S. Castellano, M. Lipson, and et al. Ancient human genomes suggest three ancestral populations for present-day Europeans Nature 513 2014 409 413
48. Q. Fu, H. Li, P. Moorjani, F. Jay, S.M. Slepchenko, A.A. Bondarev, P.L. Johnson, A. Aximu-Petri, K. Prüfer, C. de Filippo, and et al. Genome sequence of a 45,000-year-old modern human from western Siberia Nature 514 2014 445 449
49. F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism Genetics 123 1989 585 595
50. J.C. Fay, and C.I. Wu Hitchhiking under positive Darwinian selection Genetics 155 2000 1405 1413
51. B.S. Weir, and C.C. Cockerham Estimating F-statistics for the analysis of population structure Evolution 38 1984 1358 1370
52. P.C. Sabeti, D.E. Reich, J.M. Higgins, H.Z. Levine, D.J. Richter, S.F. Schaffner, S.B. Gabriel, J.V. Platko, N.J. Patterson, G.J. McDonald, and et al. Detecting recent positive selection in the human genome from haplotype structure Nature 419 2002 832 837
53. S. Wright Genetical structure of populations Nature 166 1950 247 249
54. D. Enard, F. Depaulis, and H. Roest Crollius Human and non-human primate genomes share hotspots of positive selection PLoS Genet. 6 2010 e1000840
55. H. Quach, D. Wilson, G. Laval, E. Patin, J. Manry, J. Guibert, L.B. Barreiro, E. Nerrienet, E. Verschoor, A. Gessain, and et al. Different selective pressures shape the evolution of Toll-like receptors in human and African great ape populations Hum. Mol. Genet. 22 2013 4829 4840
56. S. Sankararaman, N. Patterson, H. Li, S. Pääbo, and D. Reich The date of interbreeding between Neandertals and modern humans PLoS Genet. 8 2012 e1002947
57. Q. Fu, A. Mittnik, P.L. Johnson, K. Bos, M. Lari, R. Bollongino, C. Sun, L. Giemsch, R. Schmitz, J. Burger, and et al. A revised timescale for human evolution based on ancient mitochondrial genomes Curr. Biol. 23 2013 553 559
58. P.W. Hedrick Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation Mol. Ecol. 22 2013 4606 4618
59. F.M. Key, J.C. Teixeira, C. de Filippo, and A.M. Andrés Advantageous diversity maintained by balancing selection in humans Curr. Opin. Genet. Dev. 29 2014 45 51