Evolutionary and population (epi)genetics of immunity to infection

Abstract

Immune response is one of the functions that have been more strongly targeted by natural selection during human evolution. The evolutionary genetic dissection of the immune system has greatly helped to distinguish genes and functions that are essential, redundant or advantageous for human survival. It is also becoming increasingly clear that admixture between early Eurasians with now-extinct hominins such as Neanderthals or Denisovans, or admixture between modern human populations, can be beneficial for human adaptation to pathogen pressures. In this review, we discuss how the integration of population genetics with functional genomics in diverse human populations can inform about the changes in immune functions related to major lifestyle transitions (e.g., from hunting and gathering to farming), the action of natural selection to the evolution of the immune system, and the history of past epidemics. We also highlight the need of expanding the characterization of the immune system to a larger array of human populations—particularly neglected human groups historically exposed to different pathogen pressures—to fully capture the relative contribution of genetic, epigenetic, and environmental factors to immune response variation in humans.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Abi-Rached L, Jobin MJ, Kulkarni S, McWhinnie A, Dalva K, Gragert L, Babrzadeh F, Gharizadeh B, Luo M, Plummer FA et al (2011) The shaping of modern human immune systems by multiregional admixture with archaic humans. Science 334:89–94

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Ackerman H, Usen S, Jallow M, Sisay-Joof F, Pinder M, Kwiatkowski DP (2005) A comparison of case-control and family-based association methods: the example of sickle-cell and malaria. Ann Hum Genet 69:559–565

    CAS  PubMed  Google Scholar 

  3. Aguirre-Gamboa R, Joosten I, Urbano PCM, van der Molen RG, van Rijssen E, van Cranenbroek B, Oosting M, Smeekens S, Jaeger M, Zorro M et al (2016) Differential effects of environmental and genetic factors on T and B cell immune traits. Cell Rep 17:2474–2487

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Allison AC (1954) Protection afforded by sickle-cell trait against subtertian malareal infection. Br Med J 1:290–294

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Anderson RM, May RM (1991) Infectious diseases of humans: dynamics and control. Oxford Science Publications

  6. Andres AM, Hubisz MJ, Indap A, Torgerson DG, Degenhardt JD, Boyko AR, Gutenkunst RN, White TJ, Green ED, Bustamante CD et al (2009) Targets of balancing selection in the human genome. Mol Biol Evol 26:2755–2764

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Bakker OB, Aguirre-Gamboa R, Sanna S, Oosting M, Smeekens SP, Jaeger M, Zorro M, Vosa U, Withoff S, Netea-Maier RT et al (2018) Integration of multi-omics data and deep phenotyping enables prediction of cytokine responses. Nat Immunol 19:776–786

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Barkhash AV, Perelygin AA, Babenko VN, Myasnikova NG, Pilipenko PI, Romaschenko AG, Voevoda MI, Brinton MA (2010) Variability in the 2'-5'-oligoadenylate synthetase gene cluster is associated with human predisposition to tick-borne encephalitis virus-induced disease. J Infect Dis 202:1813–1818

    CAS  PubMed  Google Scholar 

  9. Barreiro LB, Ben-Ali M, Quach H, Laval G, Patin E, Pickrell JK, Bouchier C, Tichit M, Neyrolles O, Gicquel B et al (2009) Evolutionary dynamics of human Toll-like receptors and their different contributions to host defense. PLoS Genet 5:e1000562

    PubMed  PubMed Central  Google Scholar 

  10. Barreiro LB, Quintana-Murci L (2010) From evolutionary genetics to human immunology: how selection shapes host defence genes. Nat Rev Genet 11:17–30

    CAS  Google Scholar 

  11. Berg JJ, Coop G (2014) A population genetic signal of polygenic adaptation. PLoS Genet 10:e1004412

    PubMed  PubMed Central  Google Scholar 

  12. Boisson-Dupuis S, Ramirez-Alejo N, Li Z, Patin E, Rao G, Kerner G, Lim CK, Krementsov DN, Hernandez N, Ma CS, et al (2018) Tuberculosis and impaired IL-23-dependent IFN-gamma immunity in humans homozygous for a common TYK2 missense variant. Sci Immunol 3

  13. Braidwood RJ (1960) The agricultural revolution. Sci Am 203:130–152

    Google Scholar 

  14. Brinkworth JF, Barreiro LB (2014) The contribution of natural selection to present-day susceptibility to chronic inflammatory and autoimmune disease. Curr Opin Immunol 31:66–78

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Brodin P, Duffy D, Quintana-Murci L (2019) A call for blood-in human immunology. Immunity 50:1335–1336

    CAS  Google Scholar 

  16. Busby GB, Christ R, Band G, Leffler EM, Le QS, Rockett K, Kwiatkowski D, Spencer C. 2017. Inferring adaptive gene-flow in recent African history. bioRxiv doi.org/10.1101/205252

  17. Casanova JL, Abel L (2013) The genetic theory of infectious diseases: a brief history and selected illustrations. Annu Rev Genom Hum Genet 14:215–243

    CAS  Google Scholar 

  18. Casanova JL, Abel L (2018) Human genetics of infectious diseases: Unique insights into immunological redundancy. Semin Immunol 36:1–12

    CAS  Google Scholar 

  19. Dannemann M, Andres AM, Kelso J (2016) Introgression of neandertal- and denisovan-like haplotypes contributes to adaptive variation in human toll-like receptors. Am J Hum Genet 98:22–33

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Dannemann M, Racimo F (2018) Something old, something borrowed: admixture and adaptation in human evolution. Curr Opin Genet Dev 53:1–8

    CAS  PubMed  Google Scholar 

  21. Daub JT, Hofer T, Cutivet E, Dupanloup I, Quintana-Murci L, Robinson-Rechavi M, Excoffier L (2013) Evidence for polygenic adaptation to pathogens in the human genome. Mol Biol Evol 30:1544–1558

    CAS  PubMed  Google Scholar 

  22. DeGiorgio M, Lohmueller KE, Nielsen R (2014) A model-based approach for identifying signatures of ancient balancing selection in genetic data. PLoS Genet 10:e1004561

    PubMed  PubMed Central  Google Scholar 

  23. Deschamps M, Laval G, Fagny M, Itan Y, Abel L, Casanova JL, Patin E, Quintana-Murci L (2016) Genomic signatures of selective pressures and introgression from archaic hominins at human innate immunity genes. Am J Hum Genet 98:5–21

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Diamond J (2002) Evolution, consequences and future of plant and animal domestication. Nature 418:700–707

    CAS  PubMed  Google Scholar 

  25. Diamond J, Bellwood P (2003) Farmers and their languages: the first expansions. Science 300:597–603

    CAS  PubMed  Google Scholar 

  26. El Awady MK, Anany MA, Esmat G, Zayed N, Tabll AA, Helmy A, El Zayady AR, Abdalla MS, Sharada HM, El Raziky M et al (2011) Single nucleotide polymorphism at exon 7 splice acceptor site of OAS1 gene determines response of hepatitis C virus patients to interferon therapy. J Gastroenterol Hepatol 26:843–850

    PubMed  PubMed Central  Google Scholar 

  27. Enard D, Petrov DA (2018) Evidence that RNA viruses drove adaptive introgression between neanderthals and modern humans. Cell 175(360–371):e313

    Google Scholar 

  28. Fagny M, Patin E, MacIsaac JL, Rotival M, Flutre T, Jones MJ, Siddle KJ, Quach H, Harmant C, McEwen LM et al (2015) The epigenomic landscape of African rainforest hunter-gatherers and farmers. Nat Commun 6:10047

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Fan S, Hansen ME, Lo Y, Tishkoff SA (2016) Going global by adapting local: A review of recent human adaptation. Science 354:54–59

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Field Y, Boyle EA, Telis N, Gao Z, Gaulton KJ, Golan D, Yengo L, Rocheleau G, Froguel P, McCarthy MI et al (2016) Detection of human adaptation during the past 2000 years. Science 354:760–764

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Fraser HB, Lam LL, Neumann SM, Kobor MS (2012) Population-specificity of human DNA methylation. Genome Biol 13:R8

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Fumagalli M, Sironi M (2014) Human genome variability, natural selection and infectious diseases. Curr Opin Immunol 30C:9–16

    Google Scholar 

  33. Furuse Y, Suzuki A, Oshitani H (2010) Origin of measles virus: divergence from rinderpest virus between the 11th and 12th centuries. Virol J 7:52

    PubMed  PubMed Central  Google Scholar 

  34. Gignoux CR, Henn BM, Mountain JL (2011) Rapid, global demographic expansions after the origins of agriculture. Proc Natl Acad Sci U S A 108:6044–6049

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Gittelman RM, Schraiber JG, Vernot B, Mikacenic C, Wurfel MM, Akey JM (2016) Archaic hominin admixture facilitated adaptation to out-of-africa environments. Curr Biol 26:3375–3382

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Gonzalez JP, Nakoune E, Slenczka W, Vidal P, Morvan JM (2000) Ebola and Marburg virus antibody prevalence in selected populations of the Central African Republic. Microbes Infect 2:39–44

    CAS  PubMed  Google Scholar 

  37. Gouy A, Daub JT, Excoffier L (2017) Detecting gene subnetworks under selection in biological pathways. Nucleic Acids Res 45:e149

    PubMed  PubMed Central  Google Scholar 

  38. Grossman SR, Andersen KG, Shlyakhter I, Tabrizi S, Winnicki S, Yen A, Park DJ, Griesemer D, Karlsson EK, Wong SH et al (2013) Identifying recent adaptations in large-scale genomic data. Cell 152:703–713

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Harris DR (1967) New light on plant domestication and origins of agriculture—review. Geogr Rev 57:90–107

    Google Scholar 

  40. Harrison GF, Sanz J, Boulais J, Mina MJ, Grenier JC, Leng Y, Dumaine A, Yotova V, Bergey CM, Nsobya SL et al (2019) Natural selection contributed to immunological differences between hunter-gatherers and agriculturalists. Nat Ecol Evol 3:1253–1264

    PubMed  PubMed Central  Google Scholar 

  41. Hellenthal G, Busby GB, Band G, Wilson JF, Capelli C, Falush D, Myers S (2014) A genetic atlas of human admixture history. Science 343:747–751

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Heyn H, Moran S, Hernando-Herraez I, Sayols S, Gomez A, Sandoval J, Monk D, Hata K, Marques-Bonet T, Wang L et al (2013) DNA methylation contributes to natural human variation. Genome Res 23:1363–1372

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Hodgson JA, Pickrell JK, Pearson LN, Quillen EE, Prista A, Rocha J, Soodyall H, Shriver MD, Perry GH (2014) Natural selection for the Duffy-null allele in the recently admixed people of Madagascar. Proc Biol Sci 281:20140930

    PubMed  PubMed Central  Google Scholar 

  44. Husquin LT, Rotival M, Fagny M, Quach H, Zidane N, McEwen LM, MacIsaac JL, Kobor MS, Aschard H, Patin E et al (2018) Exploring the genetic basis of human population differences in DNA methylation and their causal impact on immune gene regulation. Genome Biol 19:222

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Ichiyama K, Chen T, Wang X, Yan X, Kim BS, Tanaka S, Ndiaye-Lobry D, Deng Y, Zou Y, Zheng P et al (2015) The methylcytosine dioxygenase Tet2 promotes DNA demethylation and activation of cytokine gene expression in T cells. Immunity 42:613–626

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Johnson ED, Gonzalez JP, Georges A (1993) Filovirus activity among selected ethnic groups inhabiting the tropical forest of equatorial Africa. Trans R Soc Trop Med Hyg 87:536–538

    CAS  PubMed  Google Scholar 

  47. Karlsson EK, Kwiatkowski DP, Sabeti PC (2014) Natural selection and infectious disease in human populations. Nat Rev Genet 15:379–393

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Kaufmann E, Sanz J, Dunn JL, Khan N, Mendonca LE, Pacis A, Tzelepis F, Pernet E, Dumaine A, Grenier JC et al (2018) BCG educates hematopoietic stem cells to generate protective innate immunity against tuberculosis. Cell 172(176–190):e119

    Google Scholar 

  49. Key FM, Teixeira JC, de Filippo C, Andres AM (2014) Advantageous diversity maintained by balancing selection in humans. Curr Opin Genet Dev 29C:45–51

    Google Scholar 

  50. Klein J, Sato A, Nikolaidis N (2007) MHC, TSP, and the origin of species: from immunogenetics to evolutionary genetics. Annu Rev Genet 41:281–304

    CAS  PubMed  Google Scholar 

  51. Kwon YC, Kang JI, Hwang SB, Ahn BY (2013) The ribonuclease L-dependent antiviral roles of human 2',5'-oligoadenylate synthetase family members against hepatitis C virus. FEBS Lett 587:156–164

    CAS  PubMed  Google Scholar 

  52. Laso-Jadart R, Harmant C, Quach H, Zidane N, Tyler-Smith C, Mehdi Q, Ayub Q, Quintana-Murci L, Patin E (2017) The genetic legacy of the indian ocean slave trade: recent admixture and post-admixture selection in the Makranis of Pakistan. Am J Hum Genet 101:977–984

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Laval G, Peyregne S, Zidane N, Harmant C, Renaud F, Patin E, Prugnolle F, Quintana-Murci L (2019) Recent adaptive acquisition by rainforest hunter-gatherers of the late pleistocene sickle-cell mutation suggests past ecological differences in exposure to malaria in Africa. Am J Hum Genet 104(3):553–561

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Lawlor DA, Ward FE, Ennis PD, Jackson AP, Parham P (1988) HLA-A and B polymorphisms predate the divergence of humans and chimpanzees. Nature 335:268–271

    CAS  PubMed  Google Scholar 

  55. Leffler EM, Gao Z, Pfeifer S, Segurel L, Auton A, Venn O, Bowden R, Bontrop R, Wall JD, Sella G et al (2013) Multiple instances of ancient balancing selection shared between humans and chimpanzees. Science 339:1578–1582

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Li Y, Oosting M, Smeekens SP, Jaeger M, Aguirre-Gamboa R, Le KTT, Deelen P, Ricano-Ponce I, Schoffelen T, Jansen AFM et al (2016) A Functional Genomics Approach to Understand Variation in Cytokine Production in Humans. Cell 167(1099–1110):e1014

    Google Scholar 

  57. Lim JK, Lisco A, McDermott DH, Huynh L, Ward JM, Johnson B, Johnson H, Pape J, Foster GA, Krysztof D et al (2009) Genetic variation in OAS1 is a risk factor for initial infection with West Nile virus in man. PLoS Pathog 5:e1000321

    PubMed  PubMed Central  Google Scholar 

  58. Lindo J, Huerta-Sanchez E, Nakagome S, Rasmussen M, Petzelt B, Mitchell J, Cybulski JS, Willerslev E, DeGiorgio M, Malhi RS (2016) A time transect of exomes from a Native American population before and after European contact. Nat Commun 7:13175

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Lopez M, Choin J, Sikora M, Siddle K, Harmant C, Costa HA, Silvert M, Mouguiama-Daouda P, Hombert JM, Froment A et al (2019) Genomic Evidence for Local Adaptation of Hunter-Gatherers to the African Rainforest. Curr Biol 29(2926–2935):e2924

    Google Scholar 

  60. Manry J, Laval G, Patin E, Fornarino S, Itan Y, Fumagalli M, Sironi M, Tichit M, Bouchier C, Casanova JL et al (2011) Evolutionary genetic dissection of human interferons. J Exp Med 208:2747–2759

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Marcus JH, Novembre J (2017) Visualizing the geography of genetic variants. Bioinformatics 33:594–595

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Marr AK, MacIsaac JL, Jiang R, Airo AM, Kobor MS, McMaster WR (2014) Leishmania donovani infection causes distinct epigenetic DNA methylation changes in host macrophages. PLoS Pathog 10:e1004419

    PubMed  PubMed Central  Google Scholar 

  63. Martin BJE, Brind’Amour J, Jensen KN, Kuzmin A, Liu ZC, Lorincz M, Howe LJ. 2019. The majority of histone acetylation is a consequence of transcription. bioRxiv.

  64. Mathieson I, Lazaridis I, Rohland N, Mallick S, Patterson N, Roodenberg SA, Harney E, Stewardson K, Fernandes D, Novak M et al (2015) Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528:499–503

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, Palombo EA, Iturriza-Gómara M, Maes P, Patton JT (2008) Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 82:3204–3219

    CAS  PubMed  PubMed Central  Google Scholar 

  66. McNeill WH (1989) Plagues and peoples. Anchor Books, New York

    Google Scholar 

  67. Mendez FL, Watkins JC, Hammer MF (2012) A haplotype at STAT2 Introgressed from neanderthals and serves as a candidate of positive selection in Papua New Guinea. Am J Hum Genet 91:265–274

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Mendez FL, Watkins JC, Hammer MF (2013) Neandertal origin of genetic variation at the cluster of OAS immunity genes. Mol Biol Evol 30:798–801

    CAS  PubMed  Google Scholar 

  69. Mitroulis I, Ruppova K, Wang B, Chen LS, Grzybek M, Grinenko T, Eugster A, Troullinaki M, Palladini A, Kourtzelis I et al (2018) Modulation of myelopoiesis progenitors is an integral component of trained immunity. Cell 172(147–161):e112

    Google Scholar 

  70. Nedelec Y, Sanz J, Baharian G, Szpiech ZA, Pacis A, Dumaine A, Grenier JC, Freiman A, Sams AJ, Hebert S et al (2016) Genetic ancestry and natural selection drive population differences in immune responses to pathogens. Cell 167(657–669):e621

    Google Scholar 

  71. Netea MG, Joosten LA, Latz E, Mills KH, Natoli G, Stunnenberg HG, O'Neill LA, Xavier RJ (2016) Trained immunity: A program of innate immune memory in health and disease. Science 352:aaf1098

    PubMed  PubMed Central  Google Scholar 

  72. Netea MG, van der Meer JW (2017) Trained immunity: an ancient way of remembering. Cell Host Microbe 21:297–300

    CAS  PubMed  Google Scholar 

  73. Olalde I, Allentoft ME, Sanchez-Quinto F, Santpere G, Chiang CW, DeGiorgio M, Prado-Martinez J, Rodriguez JA, Rasmussen S, Quilez J et al (2014) Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507:225–228

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Otto TD, Gilabert A, Crellen T, Böhme U, Arnathau C, Sanders M, Oyola SO, Okouga AP, Boundenga L, Willaume E (2018) Genomes of all known members of a Plasmodium subgenus reveal paths to virulent human malaria. Nature microbiology 3:687

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Owers KA, Sjodin P, Schlebusch CM, Skoglund P, Soodyall H, Jakobsson M (2017) Adaptation to infectious disease exposure in indigenous Southern African populations. Proc Biol Sci. https://doi.org/10.1098/rspb.2017.0226

    Article  PubMed  PubMed Central  Google Scholar 

  76. Pacis A, Mailhot-Leonard F, Tailleux L, Randolph HE, Yotova V, Dumaine A, Grenier JC, Barreiro LB (2019) Gene activation precedes DNA demethylation in response to infection in human dendritic cells. Proc Natl Acad Sci USA 116:6938–6943

    CAS  PubMed  Google Scholar 

  77. Pacis A, Tailleux L, Morin AM, Lambourne J, MacIsaac JL, Yotova V, Dumaine A, Danckaert A, Luca F, Grenier JC et al (2015) Bacterial infection remodels the DNA methylation landscape of human dendritic cells. Genome Res 25:1801–1811

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Patin E, Lopez M, Grollemund R, Verdu P, Harmant C, Quach H, Laval G, Perry GH, Barreiro LB, Froment A et al (2017) Dispersals and genetic adaptation of Bantu-speaking populations in Africa and North America. Science 356:543–546

    CAS  PubMed  Google Scholar 

  79. Patin E, Quintana-Murci L (2018) The demographic and adaptive history of central African hunter-gatherers and farmers. Curr Opin Genet Dev 53:90–97

    CAS  PubMed  Google Scholar 

  80. Petr M, Paabo S, Kelso J, Vernot B (2019) Limits of long-term selection against Neandertal introgression. Proc Natl Acad Sci USA 116(5):1639–1644

    CAS  PubMed  Google Scholar 

  81. Piasecka B, Duffy D, Urrutia A, Quach H, Patin E, Posseme C, Bergstedt J, Charbit B, Rouilly V, MacPherson CR et al (2018) Distinctive roles of age, sex, and genetics in shaping transcriptional variation of human immune responses to microbial challenges. Proc Natl Acad Sci USA 115:E488–E497

    CAS  PubMed  Google Scholar 

  82. Pierron D, Heiske M, Razafindrazaka H, Pereda-Loth V, Sanchez J, Alva O, Arachiche A, Boland A, Olaso R, Deleuze JF et al (2018) Strong selection during the last millennium for African ancestry in the admixed population of Madagascar. Nat Commun 9:932

    PubMed  PubMed Central  Google Scholar 

  83. Pritchard JK, Pickrell JK, Coop G (2010) The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr Biol 20:R208–215

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Quach H, Rotival M, Pothlichet J, Loh YE, Dannemann M, Zidane N, Laval G, Patin E, Harmant C, Lopez M et al (2016) Genetic adaptation and neandertal admixture shaped the immune system of human populations. Cell 167(643–656):e617

    Google Scholar 

  85. Quintana-Murci L (2019) Human immunology through the lens of evolutionary genetics. Cell 177:184–199

    CAS  Google Scholar 

  86. Quintana-Murci L, Alcais A, Abel L, Casanova JL (2007) Immunology in natura: clinical, epidemiological and evolutionary genetics of infectious diseases. Nat Immunol 8:1165–1171

    CAS  Google Scholar 

  87. Quintana-Murci L, Clark AG (2013) Population genetic tools for dissecting innate immunity in humans. Nat Rev Immunol 13:280–293

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Racimo F, Berg JJ, Pickrell JK (2018) Detecting polygenic adaptation in admixture graphs. Genetics 208:1565–1584

    PubMed  PubMed Central  Google Scholar 

  89. Racimo F, Marnetto D, Huerta-Sanchez E (2017) Signatures of archaic adaptive introgression in present-day human populations. Mol Biol Evol 34:296–317

    CAS  PubMed  Google Scholar 

  90. Rishishwar L, Conley AB, Wigington CH, Wang L, Valderrama-Aguirre A, Jordan IK (2015) Ancestry, admixture and fitness in Colombian genomes. Sci Rep 5:12376

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Sams AJ, Dumaine A, Nedelec Y, Yotova V, Alfieri C, Tanner JE, Messer PW, Barreiro LB (2016) Adaptively introgressed Neandertal haplotype at the OAS locus functionally impacts innate immune responses in humans. Genome Biol 17:246

    PubMed  PubMed Central  Google Scholar 

  92. Sankararaman S, Mallick S, Dannemann M, Prufer K, Kelso J, Paabo S, Patterson N, Reich D (2014) The genomic landscape of Neanderthal ancestry in present-day humans. Nature 507:354–357

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Sankararaman S, Mallick S, Patterson N, Reich D (2016) The combined landscape of Denisovan and Neanderthal Ancestry in present-day humans. Curr Biol 26:1241–1247

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Sanz J, Randolph HE, Barreiro LB (2018) Genetic and evolutionary determinants of human population variation in immune responses. Curr Opin Genet Dev 53:28–35

    CAS  PubMed  Google Scholar 

  95. Schirmer M, Smeekens SP, Vlamakis H, Jaeger M, Oosting M, Franzosa EA, Horst RT, Jansen T, Jacobs L, Bonder MJ et al (2016) Linking the human gut microbiome to inflammatory cytokine production capacity. Cell 167:1897

    CAS  PubMed  Google Scholar 

  96. Segurel L, Thompson EE, Flutre T, Lovstad J, Venkat A, Margulis SW, Moyse J, Ross S, Gamble K, Sella G et al (2012) The ABO blood group is a trans-species polymorphism in primates. Proc Natl Acad Sci USA 109:18493–18498

    CAS  PubMed  Google Scholar 

  97. Siewert KM, Voight BF (2017) Detecting long-term balancing selection using allele frequency correlation. Mol Biol Evol 34:2996–3005

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Sinclair SH, Yegnasubramanian S, Dumler JS (2015) Global DNA methylation changes and differential gene expression in Anaplasma phagocytophilum-infected human neutrophils. Clin Epigenetics 7:77

    PubMed  PubMed Central  Google Scholar 

  99. Skoglund P, Mathieson I (2018) Ancient genomics of modern humans: the first decade. Annu Rev Genom Hum Genet 19:381–404

    CAS  Google Scholar 

  100. Sundararaman SA, Plenderleith LJ, Liu W, Loy DE, Learn GH, Li Y, Shaw KS, Ayouba A, Peeters M, Speede S (2016) Genomes of cryptic chimpanzee Plasmodium species reveal key evolutionary events leading to human malaria. Nat Commun 7:11078

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Suzuki Y, Nei M (2002) Origin and evolution of influenza virus hemagglutinin genes. Mol Biol Evol 19:501–509

    PubMed  Google Scholar 

  102. Tang H, Choudhry S, Mei R, Morgan M, Rodriguez-Cintron W, Burchard EG, Risch NJ (2007) Recent genetic selection in the ancestral admixture of Puerto Ricans. Am J Hum Genet 81:626–633

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Teixeira JC, de Filippo C, Weihmann A, Meneu JR, Racimo F, Dannemann M, Nickel B, Fischer A, Halbwax M, Andre C et al (2015) Long-term balancing selection in LAD1 maintains a missense trans-species polymorphism in humans, chimpanzees, and bonobos. Mol Biol Evol 32:1186–1196

    CAS  PubMed  Google Scholar 

  104. Thornton R (1997) Aboriginal North American Population and Rates of Decline, ca. a.d. 1500–1901. Curr Anthropol 38:310–315

    Google Scholar 

  105. Turchin MC, Chiang CW, Palmer CD, Sankararaman S, Reich D, Hirschhorn JN (2012) Evidence of widespread selection on standing variation in Europe at height-associated SNPs. Nat Genet 44:1015–1019

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Vasseur E, Boniotto M, Patin E, Laval G, Quach H, Manry J, Crouau-Roy B, Quintana-Murci L (2012) The evolutionary landscape of cytosolic microbial sensors in humans. Am J Hum Genet 91:27–37

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Vigne JD (2011) The origins of animal domestication and husbandry: a major change in the history of humanity and the biosphere. C R Biol 334:171–181

    PubMed  Google Scholar 

  108. Wiencke JK, Butler R, Hsuang G, Eliot M, Kim S, Sepulveda MA, Siegel D, Houseman EA, Kelsey KT (2016) The DNA methylation profile of activated human natural killer cells. Epigenetics 11:363–380

    PubMed  PubMed Central  Google Scholar 

  109. Wolfe ND, Dunavan CP, Diamond J (2007) Origins of major human infectious diseases. Nature 447:279–283

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Zeder MA (2008) Domestication and early agriculture in the Mediterranean Basin: Origins, diffusion, and impact. Proc Natl Acad Sci USA 105:11597–11604

    CAS  PubMed  Google Scholar 

  111. Zhang X, Ulm A, Somineni HK, Oh S, Weirauch MT, Zhang HX, Chen X, Lehn MA, Janssen EM, Ji H (2014) DNA methylation dynamics during ex vivo differentiation and maturation of human dendritic cells. Epigenet Chromatin 7:21

    Google Scholar 

  112. Zhou Q, Zhao L, Guan Y (2016) Strong selection at MHC in Mexicans since admixture. PLoS Genet 12:e1005847

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work has been supported by grants NIH R01-GM115656 and R01-GM134376 to L.B.B, and by the Institut Pasteur, the French Government’s Investissement d’Avenir program, Laboratoires d’Excellence “Integrative Biology of Emerging Infectious Diseases” (ANR-10- LABX-62-IBEID) and “Milieu Intérieur” (ANR-10-LABX-69-01), and the Fondation pour la Recherche Médicale (Equipe FRM DEQ20180339214) to L.Q.-M. We thank Maitane Gutierrez and Maxime Rotival for assistance with Fig. 1 and Fig. 2, respectively.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Luis B. Barreiro.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Barreiro, L.B., Quintana-Murci, L. Evolutionary and population (epi)genetics of immunity to infection. Hum Genet 139, 723–732 (2020). https://doi.org/10.1007/s00439-020-02167-x

Download citation