Natural selection and infectious disease in human populations

The ancient biological 'arms race' between microbial pathogens and humans has shaped genetic variation in modern populations, and this has important implications for the growing field of medical genomics. As humans migrated throughout the world, populations encountered distinct pathogens, and natural selection increased the prevalence of alleles that are advantageous in the new ecosystems in both host and pathogens. This ancient history now influences human infectious disease susceptibility and microbiome homeostasis, and contributes to common diseases that show geographical disparities, such as autoimmune and metabolic disorders. Using new high-throughput technologies, analytical methods and expanding public data resources, the investigation of natural selection is leading to new insights into the function and dysfunction of human biology.

[1]  M. Bamshad,et al.  Signatures of natural selection in the human genome , 2003, Nature Reviews Genetics.

[2]  G. Jackson,et al.  Evidence for a heritable predisposition to death due to influenza. , 2008, The Journal of infectious diseases.

[3]  K. Barnes,et al.  Disease in Human Evolution: The Reemergence of Infectious Disease in the Third Epidemiological Transition , 2014 .

[4]  D. Vlahov,et al.  MYH9 is a major-effect risk gene for focal segmental glomerulosclerosis , 2008, Nature Genetics.

[5]  B. Charlesworth,et al.  The effect of deleterious mutations on neutral molecular variation. , 1993, Genetics.

[6]  S. Shchelkunov,et al.  Molecular evolution of poxviruses , 2008, Russian Journal of Genetics.

[7]  Paul Kellam,et al.  IFITM3 restricts the morbidity and mortality associated with influenza , 2012, Nature.

[8]  Pardis C Sabeti,et al.  Sequence-based association and selection scans identify drug resistance loci in the Plasmodium falciparum malaria parasite , 2012, Proceedings of the National Academy of Sciences.

[9]  Christopher R. Gignoux,et al.  Limited Evidence for Classic Selective Sweeps in African Populations , 2012, Genetics.

[10]  J. Akey,et al.  Genome-wide scans for loci under selection in humans , 2005, Human Genomics.

[11]  Or Zuk,et al.  A Composite of Multiple Signals Distinguishes Causal Variants in Regions of Positive Selection , 2010, Science.

[12]  H. Qu,et al.  Knowledge gaining by human genetic studies on tuberculosis susceptibility , 2011, Journal of Human Genetics.

[13]  Larry Wasserman,et al.  Using linkage genome scans to improve power of association in genome scans. , 2006, American journal of human genetics.

[14]  Yu Li,et al.  Genome Sequence Diversity and Clues to the Evolution of Variola (Smallpox) Virus , 2006, Science.

[15]  M. Netea,et al.  Genomewide association study of leprosy. , 2010, The New England journal of medicine.

[16]  L. Greco,et al.  The first large population based twin study of coeliac disease , 2002, Gut.

[17]  R. Nielsen,et al.  Ascertainment biases in SNP chips affect measures of population divergence. , 2010, Molecular biology and evolution.

[18]  J. Doull,et al.  Mortality of persons with leprosy prior to sulfone therapy, Cordova and Talisay, Cebu, Philippines. , 1954, International journal of Leprosy.

[19]  Steven Wolinsky,et al.  Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960 , 2008, Nature.

[20]  J. Akey,et al.  Selection and adaptation in the human genome. , 2013, Annual review of genomics and human genetics.

[21]  Yu Li,et al.  On the origin of smallpox: Correlating variola phylogenics with historical smallpox records , 2007, Proceedings of the National Academy of Sciences.

[22]  Matti Pirinen,et al.  Imputation-Based Meta-Analysis of Severe Malaria in Three African Populations , 2013, PLoS genetics.

[23]  E. Shapiro,et al.  Single-cell sequencing-based technologies will revolutionize whole-organism science , 2013, Nature Reviews Genetics.

[24]  Joseph K. Pickrell,et al.  Evolutionary Dynamics of Human Toll-Like Receptors and Their Different Contributions to Host Defense , 2009, PLoS genetics.

[25]  D. Absher,et al.  Population genomics of parallel phenotypic evolution in stickleback across stream–lake ecological transitions , 2012, Proceedings of the Royal Society B: Biological Sciences.

[26]  Albert J. Vilella,et al.  A high-resolution map of human evolutionary constraint using 29 mammals , 2011, Nature.

[27]  J. Taubenberger,et al.  Influenza Revisited , 2006, Emerging infectious diseases.

[28]  David J. Adams,et al.  The IFITM Proteins Mediate Cellular Resistance to Influenza A H1N1 Virus, West Nile Virus, and Dengue Virus , 2009, Cell.

[29]  H. Qu,et al.  What did we learn from the genome-wide association study for tuberculosis susceptibility? , 2011, Journal of Medical Genetics.

[30]  Pardis C Sabeti,et al.  Positive Natural Selection in the Human Lineage , 2006, Science.

[31]  Susan W. Margulis,et al.  The ABO blood group is a trans-species polymorphism in primates , 2012, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Manik Kuchroo,et al.  Common risk alleles for inflammatory diseases are targets of recent positive selection. , 2013, American journal of human genetics.

[33]  E. Lander,et al.  Genetic Screens in Human Cells Using the CRISPR-Cas9 System , 2013, Science.

[34]  Laurent Excoffier,et al.  Evidence for polygenic adaptation to pathogens in the human genome. , 2013, Molecular biology and evolution.

[35]  D. Ge,et al.  HLA-C cell surface expression and control of HIV / AIDS correlate with a variant upstream of HLA-C , 2009 .

[36]  J. Bach,et al.  The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update , 2010, Clinical and experimental immunology.

[37]  A. Hill.  Evolution, revolution and heresy in the genetics of infectious disease susceptibility , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[38]  A. Koike,et al.  Genome-Wide Association Study Confirming Association of HLA-DP with Protection against Chronic Hepatitis B and Viral Clearance in Japanese and Korean , 2012, PloS one.

[39]  D. Kwiatkowski,et al.  Methodological challenges of genome-wide association analysis in Africa , 2010, Nature Reviews Genetics.

[40]  K. Honda,et al.  The microbiome in infectious disease and inflammation. , 2012, Annual review of immunology.

[41]  V. Pankratz,et al.  Genome-wide association study of antibody response to smallpox vaccine. , 2012, Vaccine.

[42]  L. Miller,et al.  The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. , 1976, The New England journal of medicine.

[43]  Colm O'Dushlaine,et al.  INRICH: interval-based enrichment analysis for genome-wide association studies , 2012, Bioinform..

[44]  L. Quintana-Murci,et al.  Natural selection has driven population differentiation in modern humans , 2008, Nature Genetics.

[45]  Reem Abu Mallouh,et al.  The G428A Nonsense Mutation in FUT2 Provides Strong but Not Absolute Protection against Symptomatic GII.4 Norovirus Infection , 2009, PloS one.

[46]  Stefan Niemann,et al.  High Functional Diversity in Mycobacterium tuberculosis Driven by Genetic Drift and Human Demography , 2008, PLoS biology.

[47]  Sharon R Grossman,et al.  Integrating common and rare genetic variation in diverse human populations , 2010, Nature.

[48]  Carlos D Bustamante,et al.  Localizing Recent Adaptive Evolution in the Human Genome , 2007, PLoS genetics.

[49]  Soumya Raychaudhuri,et al.  Interrogating the major histocompatibility complex with high-throughput genomics. , 2012, Human molecular genetics.

[50]  David C. Wilson,et al.  Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease , 2012, Nature.

[51]  Ryan D. Hernandez,et al.  Natural selection on protein-coding genes in the human genome , 2005, Nature.

[52]  Shao-Cong Sun,et al.  Regulation of T cell development by the deubiquitinating enzyme CYLD , 2006, Nature Immunology.

[53]  T. Graeber,et al.  NOD2 triggers an interleukin-32–dependent human dendritic cell program in leprosy , 2012, Nature Medicine.

[54]  C. Stein,et al.  Genetic Epidemiology of Tuberculosis Susceptibility: Impact of Study Design , 2011, PLoS pathogens.

[55]  J. Rougemont,et al.  Comparative genomic and phylogeographic analysis of Mycobacterium leprae , 2009, Nature Genetics.

[56]  W. D. Laat,et al.  A Decade of 3c Technologies: Insights into Nuclear Organization References , 2022 .

[57]  Sandeep Kumar,et al.  Disability adjusted working life years (DAWLYs) of leprosy affected persons in India , 2013, The Indian journal of medical research.

[58]  R. Tapping,et al.  Cutting Edge: A Common Polymorphism Impairs Cell Surface Trafficking and Functional Responses of TLR1 but Protects against Leprosy1 , 2007, The Journal of Immunology.

[59]  R M May,et al.  Coevolution of hosts and parasites , 1982, Parasitology.

[60]  David Moher,et al.  The prevalence of celiac disease in average-risk and at-risk Western European populations: a systematic review. , 2005, Gastroenterology.

[61]  S. Olofsson,et al.  Glycoconjugate glycans as viral receptors , 2005, Annals of medicine.

[62]  A. Hall.  Noroviruses: the perfect human pathogens? , 2012, Journal of Infectious Diseases.

[63]  A. Paguio,et al.  ABO blood groups and cholera. , 1977, Annals of human biology.

[64]  H. Hakonarson,et al.  Analysing biological pathways in genome-wide association studies , 2010, Nature Reviews Genetics.

[65]  Sergei L. Kosakovsky Pond,et al.  Purifying Selection Can Obscure the Ancient Age of Viral Lineages , 2011, Molecular biology and evolution.

[66]  Niall Johnson,et al.  Updating the Accounts: Global Mortality of the 1918-1920 "Spanish" Influenza Pandemic , 2002, Bulletin of the history of medicine.

[67]  K. Shianna,et al.  Common human genetic variants and HIV-1 susceptibility: a genome-wide survey in a homogeneous African population , 2011, AIDS.

[68]  R. Nielsen,et al.  Signatures of Environmental Genetic Adaptation Pinpoint Pathogens as the Main Selective Pressure through Human Evolution , 2011, PLoS genetics.

[69]  M. Feldman,et al.  Genome wide association study SNPs in the human genome diversity project samples: does selection affect unlinked SNPs with shared trait associations? , 2010, Genome Biology.

[70]  Michael Levin,et al.  Genetic susceptibility to infectious diseases. , 2003, The Pediatric Infectious Disease Journal.

[71]  D. Serre,et al.  Whole Genome Sequencing of Field Isolates Reveals a Common Duplication of the Duffy Binding Protein Gene in Malagasy Plasmodium vivax Strains , 2013, PLoS neglected tropical diseases.

[72]  Yusuke Nakamura,et al.  Genome-wide association studies of tuberculosis in Asians identify distinct at-risk locus for young tuberculosis , 2012, Journal of Human Genetics.

[73]  Trish Berglund,et al.  Changing patterns of infectious disease , 1986 .

[74]  Mark Daly,et al.  What have we learned from six years of GWAS in autoimmune diseases, and what is next? , 2012, Current opinion in immunology.

[75]  Wei-Ting Hwang,et al.  Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. , 2014, The New England journal of medicine.

[76]  Atul J. Butte,et al.  Autoimmune Disease Classification by Inverse Association with SNP Alleles , 2009, PLoS genetics.

[77]  M. Emerman,et al.  Paleovirology—Modern Consequences of Ancient Viruses , 2010, PLoS biology.

[78]  S. Pääbo,et al.  A neutral explanation for the correlation of diversity with recombination rates in humans. , 2003, American journal of human genetics.

[79]  Le Cong,et al.  Multiplex Genome Engineering Using CRISPR/Cas Systems , 2013, Science.

[80]  P. Ashwood,et al.  The role of immune dysfunction in the pathophysiology of autism , 2012, Brain, Behavior, and Immunity.

[81]  Organização Mundial de Saúde,et al.  World malaria report 2011 , 2011 .

[82]  L. Quintana-Murci,et al.  From evolutionary genetics to human immunology: how selection shapes host defence genes , 2010, Nature Reviews Genetics.

[83]  Joshua M Akey,et al.  Where do we go from here? Constructing genomic maps of positive selection in humans: , 2009 .

[84]  Ron Pinhasi,et al.  Tracing the Origin and Spread of Agriculture in Europe , 2005, PLoS biology.

[85]  Taane G. Clark,et al.  A global network for investigating the genomic epidemiology of malaria , 2008, Nature.

[86]  J J Goedert,et al.  Genetic Restriction of HIV-1 Infection and Progression to AIDS by a Deletion Allele of the CKR5 Structural Gene , 1996, Science.

[87]  Laurent Abel,et al.  Leprosy as a genetic model for susceptibility to common infectious diseases , 2008, Human Genetics.

[88]  D. Malhotra,et al.  Leprosy and the Adaptation of Human Toll-Like Receptor 1 , 2010, PLoS pathogens.

[89]  D. Kwiatkowski.  How malaria has affected the human genome and what human genetics can teach us about malaria. , 2005, American journal of human genetics.

[90]  H. Ostrer,et al.  Dating the Origin of the CCR 5D 32 AIDS-Resistance Allele by the Coalescence of Haplotypes , 2007 .

[91]  A. Hill,et al.  Genetic susceptibility to infectious disease. , 2003, Trends in microbiology.

[92]  W. Settheetham-Ishida,et al.  Sero- and molecular typing of Duffy blood group in Southeast Asians and Oceanians. , 2000, Human biology.

[93]  F. Vannberg,et al.  Human genetic susceptibility to intracellular pathogens , 2011, Immunological reviews.

[94]  P. Roques,et al.  Island Biogeography Reveals the Deep History of SIV , 2010, Science.

[95]  P. Horby,et al.  The Role of Host Genetics in Susceptibility to Influenza: A Systematic Review , 2012, PloS one.

[96]  A. Morris,et al.  Genome-wide association analyses identifies a susceptibility locus for tuberculosis on chromosome 18q11.2 , 2010, Nature Genetics.

[97]  J. Bertranpetit,et al.  A natural history of FUT2 polymorphism in humans. , 2009, Molecular biology and evolution.

[98]  R. Nielsen.  Molecular signatures of natural selection. , 2005, Annual review of genetics.

[99]  C. Tournamille,et al.  Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy–negative individuals , 1995, Nature Genetics.

[100]  Paul M. V. Martin,et al.  2,500-year Evolution of the Term Epidemic , 2006, Emerging infectious diseases.

[101]  N. Bresolin,et al.  Crohn's disease loci are common targets of protozoa-driven selection. , 2013, Molecular biology and evolution.

[102]  D. Reich,et al.  MYH9 is associated with nondiabetic end-stage renal disease in African Americans , 2008, Nature Genetics.

[103]  Jeremiah D. Degenhardt,et al.  Targets of balancing selection in the human genome. , 2009, Molecular biology and evolution.

[104]  M. McCarthy,et al.  Genome-wide association studies for complex traits: consensus, uncertainty and challenges , 2008, Nature Reviews Genetics.

[105]  J. Goedert,et al.  Genome-Wide Association Study of Spontaneous Resolution of Hepatitis C Virus Infection: Data From Multiple Cohorts , 2013, Annals of Internal Medicine.

[106]  Liangdan Sun,et al.  Identification of two new loci at IL23R and RAB32 that influence susceptibility to leprosy , 2011, Nature Genetics.

[107]  Neville E. Sanjana,et al.  Genome-Scale CRISPR-Cas9 Knockout Screening in Human Cells , 2014, Science.

[108]  Matteo Fumagalli,et al.  Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions , 2009, The Journal of experimental medicine.

[109]  J. Ioannidis,et al.  Replication of past candidate loci for common diseases and phenotypes in 100 genome-wide association studies , 2010, European Journal of Human Genetics.

[110]  M. Newport,et al.  Common variants at 11p13 are associated with susceptibility to tuberculosis , 2012, Nature Genetics.

[111]  Eun Pyo Hong,et al.  Sample Size and Statistical Power Calculation in Genetic Association Studies , 2012, Genomics & informatics.

[112]  Eric S. Lander,et al.  Identifying Recent Adaptations in Large-Scale Genomic Data , 2013, Cell.

[113]  F. Collins,et al.  Potential etiologic and functional implications of genome-wide association loci for human diseases and traits , 2009, Proceedings of the National Academy of Sciences.

[114]  Jean-Pierre Bocquet-Appel,et al.  When the World’s Population Took Off: The Springboard of the Neolithic Demographic Transition , 2011, Science.

[115]  N. Foss,et al.  Endocrine dysfunction in leprosy , 2008, European Journal of Clinical Microbiology & Infectious Diseases.

[116]  M. Lathrop,et al.  Genome-wide association study of HPV seropositivity. , 2011, Human molecular genetics.

[117]  M. Worobey,et al.  Point, counterpoint: The evolution of pathogenic viruses and their human hosts , 2007 .

[118]  Falk Hildebrand,et al.  Origin, Spread and Demography of the Mycobacterium tuberculosis Complex , 2008, PLoS pathogens.

[119]  Peter Donnelly,et al.  Multiple Instances of Ancient Balancing Selection Shared Between Humans and Chimpanzees , 2013, Science.

[120]  C. Day,et al.  Cellular and Infection Microbiology Review Article Glycoconjugates Play a Key Role in Campylobacter Jejuni Infection: Interactions between Host and Pathogen , 2022 .

[121]  Adam Powell,et al.  The Origins of Lactase Persistence in Europe , 2009, PLoS Comput. Biol..

[122]  Jonathan K. Pritchard,et al.  Adaptations to Climate-Mediated Selective Pressures in Humans , 2011, PLoS genetics.

[123]  Barbara E. Stranger,et al.  Gene Expression Levels Are a Target of Recent Natural Selection in the Human Genome , 2008, Molecular biology and evolution.

[124]  Richard A Koup,et al.  Homozygous Defect in HIV-1 Coreceptor Accounts for Resistance of Some Multiply-Exposed Individuals to HIV-1 Infection , 1996, Cell.

[125]  D. Ménard,et al.  Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people , 2010, Proceedings of the National Academy of Sciences.

[126]  David Haussler,et al.  ENCODE Data in the UCSC Genome Browser: year 5 update , 2012, Nucleic Acids Res..

[127]  A C Heath,et al.  Multi-locus genome-wide association analysis supports the role of glutamatergic synaptic transmission in the etiology of major depressive disorder , 2012, Translational psychiatry.

[128]  Xiaofeng Zhu,et al.  Genome-wide comparison of African-ancestry populations from CARe and other cohorts reveals signals of natural selection. , 2011, American journal of human genetics.

[129]  Ryan D. Hernandez,et al.  Classic Selective Sweeps Were Rare in Recent Human Evolution , 2011, Science.

[130]  Peter Donnelly,et al.  Genome-wide and fine-resolution association analysis of malaria in West Africa , 2009, Nature Genetics.

[131]  W. Brakel.  Measuring leprosy stigma--a preliminary review of the leprosy literature. , 2003 .

[132]  Joseph K. Pickrell,et al.  Signals of recent positive selection in a worldwide sample of human populations. , 2009, Genome research.

[133]  M. Möller,et al.  Current findings, challenges and novel approaches in human genetic susceptibility to tuberculosis. , 2010, Tuberculosis.

[134]  D. Hartl,et al.  The origin of malaria: mixed messages from genetic diversity , 2004, Nature Reviews Microbiology.

[135]  C. Spencer,et al.  Screening for recently selected alleles by analysis of human haplotype similarity. , 2006, American journal of human genetics.

[136]  M. Oosting,et al.  Evolutionary and functional analysis of celiac risk loci reveals SH2B3 as a protective factor against bacterial infection. , 2010, American journal of human genetics.

[137]  Pardis C Sabeti,et al.  Natural Selection in a Bangladeshi Population from the Cholera-Endemic Ganges River Delta , 2013, Science Translational Medicine.

[138]  M. Levin,et al.  Genetic susceptibility to infectious diseases. , 2003, The Pediatric Infectious Disease Journal.

[139]  B. Crespo-Facorro,et al.  Inflammatory and immune response genes have significantly altered expression in schizophrenia , 2013, Molecular Psychiatry.

[140]  M. A. Malek,et al.  Impact of Rapid Urbanization on the Rates of Infection by Vibrio cholerae O1 and Enterotoxigenic Escherichia coli in Dhaka, Bangladesh , 2011, PLoS neglected tropical diseases.

[141]  Digambar Behera,et al.  Global tuberculosis control 2010 , 2012 .

[142]  René Bernards,et al.  Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-κB , 2003, Nature.

[143]  Pardis C Sabeti,et al.  Genome-wide detection and characterization of positive selection in human populations , 2007, Nature.

[144]  C. Winkler,et al.  Association of Trypanolytic ApoL1 Variants with Kidney Disease in African Americans , 2010, Science.

[145]  J. Boldsen.  Leprosy in Medieval Denmark--osteological and epidemiological analyses. , 2009, Anthropologischer Anzeiger; Bericht uber die biologisch-anthropologische Literatur.

[146]  R. Wilson,et al.  The Next-Generation Sequencing Revolution and Its Impact on Genomics , 2013, Cell.

[147]  F. Balloux,et al.  Pathogen-Driven Selection and Worldwide HLA Class I Diversity , 2005, Current Biology.

[148]  D. Kwiatkowski,et al.  Classical sickle beta-globin haplotypes exhibit a high degree of long-range haplotype similarity in African and Afro-Caribbean populations , 2007, BMC Genetics.

[149]  J. Pritchard,et al.  A Map of Recent Positive Selection in the Human Genome , 2006, PLoS biology.

[150]  David Heckerman,et al.  Influence of HLA-C Expression Level on HIV Control , 2013, Science.

[151]  R. Glass,et al.  Seroepidemiological studies of El Tor cholera in Bangladesh: association of serum antibody levels with protection. , 1985, The Journal of infectious diseases.

[152]  ENCODEConsortium,et al.  An Integrated Encyclopedia of DNA Elements in the Human Genome , 2012, Nature.

[153]  W. Mosley,et al.  Report of the 1966-67 cholera vaccine field trial in rural East Pakistan. 2. Results of the serological surveys in the study population--the relationship of case rate to antibody titre and an estimate of the inapparent infection rate with Vibrio cholerae. , 1969, Bulletin of the World Health Organization.

[154]  Manish M Patel,et al.  Systematic Literature Review of Role of Noroviruses in Sporadic Gastroenteritis , 2008, Emerging infectious diseases.

[155]  W. Potts,et al.  Major Histocompatibility Complex Heterozygote Superiority during Coinfection , 2003, Infection and Immunity.

[156]  Philippe Froguel,et al.  Genomewide association study of an AIDS-nonprogression cohort emphasizes the role played by HLA genes (ANRS Genomewide Association Study 02). , 2009, The Journal of infectious diseases.

[157]  Joseph K. Pickrell,et al.  The Role of Geography in Human Adaptation , 2009, PLoS genetics.

[158]  M. Clerici,et al.  The hygiene hypothesis: an evolutionary perspective. , 2010, Microbes and infection.

[159]  A. Dunning,et al.  Beyond GWASs: illuminating the dark road from association to function. , 2013, American journal of human genetics.

[160]  Elisabeth M. Bik,et al.  Distinct Distal Gut Microbiome Diversity and Composition in Healthy Children from Bangladesh and the United States , 2013, PloS one.

[161]  A. Yuksel,et al.  Androgenic status in patients with lepromatous leprosy. , 1994, British journal of urology.

[162]  Jack T Stapleton,et al.  The Major Genetic Determinants of HIV-1 Control Affect HLA Class I Peptide Presentation , 2010, Science.

[163]  Jason E. Kreutz,et al.  The potential impact of droplet microfluidics in biology. , 2013, Analytical chemistry.

[164]  Joseph K. Pickrell,et al.  The Genetics of Human Adaptation: Hard Sweeps, Soft Sweeps, and Polygenic Adaptation , 2010, Current Biology.

[165]  R. Wayne,et al.  High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[166]  David Reich,et al.  The Case for Selection at CCR5-Δ32 , 2005, PLoS biology.

[167]  Andre Franke,et al.  Genome-wide association study indicates two novel resistance loci for severe malaria , 2012, Nature.

[168]  Stefan Niemann,et al.  Variable host-pathogen compatibility in Mycobacterium tuberculosis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[169]  Kelley Lee.  The Global Dimensions of Cholera , 2001 .

[170]  Gregory A. Poland,et al.  Genome-wide analysis of polymorphisms associated with cytokine responses in smallpox vaccine recipients , 2012, Human Genetics.

[171]  David Reich,et al.  Combining evidence of natural selection with association analysis increases power to detect malaria-resistance variants. , 2007, American journal of human genetics.

[172]  S. Tax.  Horizons Of Anthropology , 1964 .

[173]  Bachti Alisjahbana,et al.  A genome wide association study of pulmonary tuberculosis susceptibility in Indonesians , 2012, BMC Medical Genetics.

[174]  D. Smith,et al.  Leprosy and fertility. , 1978, Human biology.

[175]  L. Svensson,et al.  Norovirus Gastroenteritis Outbreak with a Secretor-independent Susceptibility Pattern, Sweden , 2010, Emerging infectious diseases.

[176]  Sharon R Grossman,et al.  Detecting natural selection in genomic data. , 2013, Annual review of genetics.

[177]  D. Swallow,et al.  The lactase persistence/non-persistence polymorphism is controlled by a cis-acting element. , 1995, Human molecular genetics.

[178]  M. Pericak-Vance,et al.  Genetic epidemiology of the susceptibility to leprosy. , 1987, The Journal of clinical investigation.

[179]  Xi Jiang,et al.  Human susceptibility and resistance to Norwalk virus infection , 2003, Nature Medicine.

[180]  R. Pratesi,et al.  Why is coeliac disease endemic in the people of the Sahara? , 1999, The Lancet.

[181]  M. Shriver,et al.  Interrogating a high-density SNP map for signatures of natural selection. , 2002, Genome research.

[182]  K. Shianna,et al.  Host determinants of HIV-1 control in African Americans. , 2010, The Journal of infectious diseases.

[183]  Y. Kamatani,et al.  A genome-wide association study identifies variants in the HLA-DP locus associated with chronic hepatitis B in Asians , 2009, Nature Genetics.

[184]  Zhaohui S. Qin,et al.  A second generation human haplotype map of over 3.1 million SNPs , 2007, Nature.

[185]  Y. Kamatani,et al.  A genome-wide association study of chronic hepatitis B identified novel risk locus in a Japanese population. , 2011, Human molecular genetics.

[186]  M. Pirinen,et al.  Common variants in the HLA-DRB1-HLA-DQA1 Class II region are associated with susceptibility to visceral leishmaniasis , 2013, Nature Genetics.

[187]  A. Hill,et al.  Human genetic susceptibility to infectious disease , 2012, Nature Reviews Genetics.

[188]  Elizabeth T. Cirulli,et al.  Common Genetic Variation and the Control of HIV-1 in Humans , 2009, PLoS genetics.

[189]  R. Charles,et al.  Cholera's western front , 2010, The Lancet.

[190]  J. Klein,et al.  The molecular descent of the major histocompatibility complex. , 1993, Annual review of immunology.

[191]  S. Tishkoff,et al.  Effects of natural selection and gene conversion on the evolution of human glycophorins coding for MNS blood polymorphisms in malaria-endemic African populations. , 2011, American journal of human genetics.

[192]  P. Donnelly,et al.  Designing Genome-Wide Association Studies: Sample Size, Power, Imputation, and the Choice of Genotyping Chip , 2009, PLoS genetics.

[193]  Firdausi Qadri,et al.  Susceptibility to Vibrio cholerae Infection in a Cohort of Household Contacts of Patients with Cholera in Bangladesh , 2008, PLoS neglected tropical diseases.

[194]  Sue VandeWoude,et al.  Going Wild: Lessons from Naturally Occurring T-Lymphotropic Lentiviruses , 2006, Clinical Microbiology Reviews.

[195]  Data production leads,et al.  An integrated encyclopedia of DNA elements in the human genome , 2012 .