Malaria was a weak selective force in ancient Europeans

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Gelabert, Pere ^a   Olalde, Iñigo ^a   De DIos, Toni ^a   Civit, Sergi ^b   Lalueza Fox, Carles ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; CAUCASIAN; DISEASE RESISTANCE; EUROPE; GENETIC SELECTION; GENETICS; HISTORY; HUMAN; MALARIA; PHYSIOLOGY; PLASMODIUM; SINGLE NUCLEOTIDE POLYMORPHISM;

ALLELES; DISEASE RESISTANCE; EUROPE; EUROPEAN CONTINENTAL ANCESTRY GROUP; HISTORY, ANCIENT; HUMANS; MALARIA; PLASMODIUM; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC;

EID: 85018735524     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-01534-5     Document Type: Article

References (57)

1. Kwiatkowski, D. P. How Malaria Has Affected the Human Genome and What Human Genetics Can Teach Us about Malaria. Am. J. Hum. Genet. 77, 171-192, doi:10.1086/432519 (2005).
2. Carter, R. Speculations on the origins of Plasmodium vivax malaria. Trends Parasitol. 19, 214-219, doi:10.1016/S1471-4922(03)00070-9 (2003).
3. Rich, S. M., Licht, M. C., Hudson, R. R., Ayala, F. J. Malaria's Eve: Evidence of a rcent population bottleneck throughout the world populations of Plasmodium falciparum. Proc. NAtl. Acad. Sci 95, 4425-4430, doi:10.1073/pnas.95.8.4425 (1998).
4. Tishkoff, S. A., et al. Haplotype diversity and linkage disequilibrium at human G6PD: Recent origin of alleles that confer malarial resistance. Science 293, 455-462, doi:10.1126/science.1061573 (2001).
5. Ohashi, J., et al. Extended linkage disequilibrium surrounding the hemoglobin E variant due to malarial selection. Am. J. Hum. Genet. 74, 1198-1208, doi:10.1086/421330 (2004).
6. Gelabert, P., et al. Mitochondrial DNA from the eradicated European Plasmodium vivax and P. falciparum from 70-year-old slides from the Ebro Delta in Spain. Proc. Natl. Acad. Sci USA. 113, 11495-11500, doi:10.1073/pnas.1611017113 (2016).
7. Liu, W., et al. African origin of the malaria parasite Plasmodium vivax. Nat. Commun. 5, 3346, doi:10.1038/ncomms4346 (2014).
8. Olalde, I., Lalueza-Fox, C. Modern humans' paleogenomics and the new evidences on the European prehistory. Sci. Technol. Archaeol. Res. 1, 1-9, doi:10.1179/2054892315Y.0000000002 (2015).
9. Mathieson, I., et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499-503, doi:10.1038/nature16152 (2015).
10. Haak, W., et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207-211, doi:10.1038/nature14317 (2015).
11. Allentoft, M. E., et al. Population genomics of Bronze Age Eurasia. Nature 522, 167-172, doi:10.1038/nature14507 (2015).
12. Timmann, C., et al. Genome-wide association study indicates two novel resistance loci for severe malaria. Nature 489, 443-446, doi:10.1038/nature11334 (2012).
13. Jallow, M., et al. Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat. Genet. 41, 657-665, doi:10.1038/ng.388 (2009).
14. Browning, B. L., Browning, S. R. Genotype imputation with millions of reference samples. Am. J. Hum. Genet. 98, 116-126, doi:10.1016/j.ajhg.2015.11.020 (2016).
15. Schraiber, J. G., Evans, S. N., Slatkin, M. Bayesian Inference of Natural Selection from Allele Frequency Time Series. Genetics 203, 493-511, doi:10.1534/genetics.116.187278 (2016).
16. Rich, S. M., et al. The origin of malignant malaria. Proc. Natl. Acad. Sci. USA 106, 14902-14907, doi:10.1073/pnas.0907740106 (2009).
17. Nagao, E., Seydel, K. B., Dvorak, J. A. Detergent-resistant erythrocyte membrane rafts are modified by a Plasmodium falciparum infection. Exp Parasitol 102, 57-59, doi:10.1016/S0014-4894(02)00143-1 (2002).
18. Miller, L. H., Mason, S. J., Clyde, D. F., McGinniss, M. H. The Resistance Factor to Plasmodium vivax in Blacks. N. Engl. J. Med. 295, 302-304, doi:10.1056/NEJM197608052950602 (1976).
19. Luzzatto, L., Usanga, F. A., Reddy, S. Glucose-6-phosphate dehydrogenase deficient red cells: Resistance to infection by malarial parasites. Science 164, 839-842, doi:10.1126/science.164.3881.839 (1969).
20. Garcia-Garcera, M., et al. Fragmentation of contaminant and endogenous DNA in ancient samples determined by shotgun sequencing; prospects for human palaeogenomics. PLoS One 6, e24161, doi:10.1371/journal.pone.0024161 (2011).
21. Olalde, I., et al. A Common Genetic Origin for Early Farmers from Mediterranean Cardial and Central European LBK Cultures. Mol. Biol. Evol. 32, 3132-3142, doi:10.1093/molbev/msv181 (2015).
22. Klnç, G. M., et al. The Demographic Development of the First Farmers in Anatolia. Curr. Biol. 26, 1-8, doi:10.1016/j.cub.2016.07.057 (2016).
23. Hofmanová, Z., et al. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl. Acad. Sci. USA 113, 6886-6891, doi:10.1073/pnas.1523951113 (2016).
24. Khor, C. C., et al. A Mal functional variant is associated with protection against invasive pneumococcal disease, bacteremia, malaria and tuberculosis. Nat. Genet. 39, 523-528, doi:10.1038/ng1976 (2007).
25. Willcocks, L. C., et al. A defunctioning polymorphism in FCGR2B is associated with protection against malaria but susceptibility to systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 107, 7881-7885, doi:10.1073/pnas.0915133107 (2010).
26. Clatworthy, M. R., et al. Systemic lupus erythematosus-associated defects in the inhibitory receptor FcgammaRIIb reduce susceptibility to malaria. Proc. Natl. Acad. Sci. USA 104, 7169-7174, doi:10.1073/pnas.0608889104 (2007).
27. Gazarini, M. L., Thomas, A. P., Pozzan, T., Garcia, C. R. S. Calcium signaling in a low calcium environment: How the intracellular malaria parasite solves the problem. J. Cell Biol. 161, 103-110, doi:10.1083/jcb.200212130 (2003).
28. Rockett, K. A., et al. Reappraisal of known malaria resistance loci in a large multicenter study. Nat. Genet. 46, 1197-1204, doi:10.1038/ng.3107 (2014).
29. Pybus, M., et al. 1000 Genomes Selection Browser 1.0: A genome browser dedicated to signatures of natural selection in modern humans. Nucleic Acids Res. 42, D903-D909, doi:10.1093/nar/gkt1188 (2014).
30. Lazaridis, I., et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409-413, doi:10.1038/nature13673 (2014).
31. Llamas, B., et al. Ancient mitochondrial DNA provides high-resolution time scale of the peopling of the Americas. Sci. Adv. 2, e1501385-e1501385, doi:10.1126/sciadv.1501385 (2016).
32. Olalde, I., et al. Derived immune and ancestral pigmentation alleles in a 7, 000-year-old Mesolithic European. Nature 507, 225-228, doi:10.1038/nature12960 (2014).
33. Skoglund, P., et al. Genomic diversity and admixture differs for Stone-Age Scandinavian foragers and farmers. Science 344, 747-750, doi:10.1126/science.1253448 (2014).
34. Gamba, C., et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat. Commun. 5, 5257, doi:10.1038/ncomms6257 (2014).
35. Seguin-Orlando, A., et al. Paleogenomics. Genomic structure in Europeans dating back at least 36, 200 years. Science 346, 1113-1118, doi:10.1126/science.aaa0114 (2014).
36. Jones, E. R., et al. Upper Palaeolithic genomes reveal deep roots of modern Eurasians. Nat. Commun. 6, 8912, doi:10.1038/ncomms9912 (2015).
37. Cassidy, L. M., et al. Neolithic and Bronze Age migration to Ireland and establishment of the insular Atlantic genome. Proc. Natl. Acad. Sci. USA 113, 368-373, doi:10.1073/pnas.1518445113 (2016).
38. Martiniano, R., et al. Genomic signals of migration and continuity in Britain before the Anglo-Saxons. Nat. Commun. 7, 10326, doi:10.1038/ncomms10326 (2016).
39. Schiffels, S., et al. Iron Age and Anglo-Saxon genomes from East England reveal British migration history. Nat. Commun. 7, 10408, doi:10.1038/ncomms10408 (2016).
40. Fu, Q., et al. Genome sequence of a 45, 000-year-old modern human from western Siberia. Nature 514, 445-449, doi:10.1038/nature13810 (2014).
41. Fu, Q., et al. An early modern human from Romania with a recent Neanderthal ancestor. Nature 524, 216-219, doi:10.1038/nature14558 (2015).
42. Fu, Q., et al. The genetic history of Ice Age Europe. Nature 534, 200-205, doi:10.1038/nature17993 (2016).
43. Hirono, A., Beutler, E. Alternative splicing of human glucose-6-phosphate dehydrogenase messenger RNA in different tissues. J. Clin. Invest. 83, 343-346, doi:10.1172/JCI113881 (1989).
44. Gouagna, L. C., et al. Genetic variation in human HBB is associated with Plasmodium falciparum transmission. Nat. Genet. 42, 328-331, doi:10.1038/ng.554 (2010).
45. Agarwal, A., et al. Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Blood 96, 2358-2363 (2000).
46. Zimmerman, P. A., et al. Emergence of FY∗A(null) in a Plasmodium vivax-endemic region of Papua New Guinea. Proc. Natl. Acad. Sci. USA 96, 13973-13977, doi:10.1073/pnas.96.24.13973 (1999).
47. Tournamille, C., Colin, Y., Cartron, J. P., Le Van Kim, C. Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat. Genet. 10, 224-228, doi:10.1038/ng0695-224 (1995).
48. Yamamoto, F., Clausen, H., White, T., Marken, J., Hakomori, S. Molecular genetic basis of the histo-blood group ABO system. Nature 345, 229-233, doi:10.1038/345229a0 (1990).
49. Blumenfeld, O. O., Patnaik, S. K. Allelic genes of blood group antigens: A source of human mutations and cSNPs documented in the Blood Group Antigen Gene Mutation Database. Hum. Mutat. 23, 8-16, doi:10.1002/humu.10296 (2004).
50. Boren, T., Falk, P., Roth, K. A., Larson, G., Normark, S. Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262, 1892-1895, doi:10.1126/science.8018146 (1993).
51. Swerdlow, D. L., et al. Severe life-threatening cholera associated with blood group O in Peru: Implications for the Latin American epidemic. J. Infect. Dis. 170, 468-472, doi:10.1093/infdis/170.2.468 (1994).
52. Gupta, H., et al. Categorical complexities of Plasmodium falciparum malaria in individuals is associated with genetic variations in ADORA2A and GRK5 genes. Infect. Genet. Evol. 34, 188-199, doi:10.1016/j.meegid.2015.06.010 (2015).
53. Sudmant, P. H., et al. An integrated map of structural variation in 2, 504 human genomes. Nature 526, 75-81, doi:10.1038/nature15394 (2015).
54. Gilbert, M. T. P., et al. Distribution patterns of postmortem damage in human mitochondrial DNA. Am. J. Hum. Genet. 72, 32-47, doi:10.1086/345378 (2003).
55. Weir, B. S., Hill, W. G. Estimating F-statistics. Annu. Rev. Genet. 36, 721-750, doi:10.1146/annurev.genet.36.050802.093940 (2002).
56. Goudet, J., Roussett, F. Testing Differentiation in Diploid Populations. Genetics 144, 1933-1940 (1996).
57. Zhao, X., Smith, D. L., Tatem, A. J. Exploring the spatiotemporal drivers of malaria elimination in Europe. Malar. J. 15, 122, doi:10.1186/s12936-016-1175-z (2016).