Natural selection for the Duffy-null allele in the recently admixed people of Madagascar

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1789, 2014, Pages

  Hodgson, Jason A ^a,b   Pickrell, Joseph K ^c,d   Pearson, Laurel N ^a   Quillen, Ellen E ^a,e   Prista, António ^f   Rocha, Jorge ^g,h   Soodyall, Himla ⁱ   Shriver, Mark D ^a   Perry, George H ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c NEW YORK GENOME CENTER   (United States)

^d Och Spine at New York Presbyterian Hospitals   (United States)

^e SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^f Universidade Pedagógica Campus de Lhanguene   (Mozambique)

^g CENTRO DE INVESTIGAÇÃO EM BIODIVERSIDADE E RECURSOS GENÉTICOS   (Portugal)

^h UNIVERSITY OF PORTO   (Portugal)

ⁱ NATIONAL HEALTH LABORATORY SERVICE   (South Africa)

Author keywords

Adaptive evolution; Duffy blood group; Malagasy population genetics; Migration; Vivax malaria

Indexed keywords

BLOOD GROUP DUFFY SYSTEM; CELL SURFACE RECEPTOR; DARC PROTEIN, HUMAN;

ALLELE; ANCESTRY; DATA ACQUISITION; DEMOGRAPHY; GENETIC VARIATION; GENOME; MALARIA; NATURAL SELECTION; SIMULATION;

AFRICA SOUTH OF THE SAHARA; ASIAN CONTINENTAL ANCESTRY GROUP; BIOLOGICAL MODEL; BLACK PERSON; BLOOD GROUP DUFFY SYSTEM; COMPUTER SIMULATION; GENE FREQUENCY; GENETIC DRIFT; GENETIC SELECTION; GENETICS; HUMAN; MADAGASCAR; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM;

AFRICA SOUTH OF THE SAHARA; AFRICAN CONTINENTAL ANCESTRY GROUP; ASIAN CONTINENTAL ANCESTRY GROUP; COMPUTER SIMULATION; DUFFY BLOOD-GROUP SYSTEM; GENE FREQUENCY; GENETIC DRIFT; GENETICS; GENETICS, POPULATION; HUMANS; MADAGASCAR; MODELS, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, CELL SURFACE; SELECTION, GENETIC;

MADAGASCAR;

EID: 84903715719     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.0930     Document Type: Article

References (51)

1. Sabeti PC et al. 2007 Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913-918. (doi:10.1038/ nature06250)
2. Pickrell JK et al. 2009 Signals of recent positive selection in a worldwide sample of human populations. Genome Res. 19, 826-837. (doi:10. 1101/gr.087577.108)
3. Jeong C, Alkorta-Aranburu G, Basnyat B, Neupane M, Witonsky DB, Pritchard JK, Beall CM, Di Rienzo A. 2014 Admixture facilitates genetic adaptations to high altitude in Tibet. Nat. Commun. 5, 3281. (doi:10.1038/ncomms4281)
4. Vernot B, Akey JM. 2014 Resurrecting surviving Neandertal lineages from modern human genomes. Science 343, 1017-1021. (doi:10.1126/science. 1245938)
5. Tournamille C, Colin Y, Cartron JP, Le Van Kim C. 1995 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)
6. Howes RE et al. 2011 The global distribution of the Duffy blood group. Nat. Commun. 2, 266. (doi:10. 1038/ncomms1265)
7. Miller LH, Mason SJ, Clyde DF, McGinniss MH. 1976 The resistance factor to Plasmodium vivax in blacks: the Duffy-blood-group genotype, FyFy. N. Engl. J. Med. 295, 302-304. (doi:10.1056/ NEJM197608052950602)
8. Cavasini CE et al. 2007 Plasmodium vivax infection among Duffy antigen-negative individuals from the Brazilian Amazon region: an exception? Trans. R. Soc. Trop. Med. Hyg. 101, 1042-1044. (doi:10. 1016/j.trstmh.2007.04.011)
9. Menard D et al. 2010 Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc. Natl Acad. Sci. USA 107, 5967-5971. (doi:10.1073/pnas.0912496107)
10. Zimmerman PA et al. 1999 Emergence of FY*A(null) in a Plasmodium vivax-endemic region of Papua New Guinea. Proc. Natl Acad. Sci. USA 96, 13 973-13 977. (doi:10.1073/pnas.96.24.13973)
11. Durbin RM et al. 2010 A map of human genome variation from population-scale sequencing. Nature 467, 1061-1073. (doi:10.1038/nature09534)
12. Guerra CA et al. 2010 The international limits and population at risk of Plasmodium vivax transmission in 2009. PLoS Negl. Trop. Dis. 4, e774. (doi:10.1371/ journal.pntd.0000774)
13. Livingstone FB. 1984 The Duffy blood groups, vivax malaria, and malaria selection in human populations: a review. Hum. Biol. 56, 413-425.
14. Hamblin MT, Thompson EE, Di Rienzo A. 2002 Complex signatures of natural selection at the Duffy blood group locus. Am. J. Hum. Genet. 70, 369-383. (doi:10.1086/338628)
15. Hamblin MT, Di Rienzo A. 2000 Detection of the signature of natural selection in humans: evidence from the Duffy blood group locus. Am. J. Hum. Genet. 66, 1669-1679. (doi:10.1086/302879)
16. Escalante AA, Cornejo OE, Freeland DE, Poe AC, Durrego E, Collins WE, Lal AA. 2005 A monkey's tale: the origin of Plasmodium vivax as a human malaria parasite. Proc. Natl Acad. Sci. USA 102, 1980-1985. (doi:10.1073/pnas.0409652102)
17. Perez VR, Godfrey LR, Nowak-Kemp M, Burney DA, Ratsimbazafy J, Vasey N. 2005 Evidence of early butchery of giant lemurs in Madagascar. J. Hum. Evol. 49, 722-742. (doi:10.1016/j.jhevol.2005. 08.004)
18. Dewar RE, Richard AF. 2012 Madagascar: a history of arrivals, what happened, and will happen next*. Annu. Rev. Anthropol. 41, 495-517. (doi:10.1146/ annurev-anthro-092611-145758)
19. Dewar RE, Radimilahy C, Wright HT, Jacobs Z, Kelly GO, Berna F. 2013 Stone tools and foraging in northern Madagascar challenge Holocene extinction models. Proc. Natl Acad. Sci. USA 110, 12 583-12 588. (doi:10.1073/pnas.1306100110)
20. Cox MP, Nelson MG, Tumonggor MK, Ricaut FX, Sudoyo H. 2012 A small cohort of Island southeast Asian women founded Madagascar. Proc. R. Soc. B 279, 2761-2768. (doi:10.1098/rspb. 2012.0012)
21. Tofanelli S, Bertoncini S, Castri L, Luiselli D, Calafell F, Donati G, Paoli G. 2009 On the origins and admixture of Malagasy: new evidence from high-resolution analyses of paternal and maternal lineages. Mol. Biol. Evol. 26, 2109-2124. (doi:10.1093/molbev/msp120)
22. Hurles ME, Sykes BC, Jobling MA, Forster P. 2005 The dual origin of the Malagasy in Island southeast Asia and East Africa: evidence from maternal and paternal lineages. Am. J. Hum. Genet. 76, 894-901. (doi:10.1086/430051)
23. Tofanelli S, Bertoncini S. 2010 Origin and evolutionary history of the Malagasy. In Encyclopedia of Life Sciences. Chichester, UK: John Wiley & Sons Ltd.
24. Pierron D et al. 2014 Genome-wide evidence of Austronesian-Bantu admixture and cultural reversion in a hunter-gatherer group of Madagascar. Proc. Natl Acad. Sci. USA 111, 936-941. (doi:10. 1073/pnas.1321860111)
25. Dewar RE, Wright HT. 1993 The culture history of Madagascar. J. World Prehistory 7, 417-466. (doi:10.1007/BF00997802)
26. Beaujard P. 2011 The first migrants to Madagascar and their introduction of plants: linguistic and ethnological evidence. Azania Archaeol. Res. Afr. 46, 169-189. (doi:10.1080/0067270X.2011.580142)
27. Blench R. 2007 New palaeozoogeographical evidence for the settlement of Madagascar. Azania Archaeol. Res. Afr. 42, 69-82. (doi:10.1080/ 00672700709480451)
28. Pearson MP, Godden K. 2010 Pastoralists, warriors and colonists: the archaeology of southern Madagascar. Oxford, UK: Archaeopress.
29. Central Intelligence Agency 2014 Madagascar. In The world factbook. See http://www.cia.gov/library/ publications/the-world-factbook/.
30. Alexander DH, Novembre J, Lange K. 2009 Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664. (doi:10. 1101/gr.094052.109)
31. Pagani L et al. 2012 Ethiopian genetic diversity reveals linguistic stratification and complex influences on the Ethiopian gene pool. Am. J. Hum. Genet. 91, 83-96. (doi:10.1016/j.ajhg.2012.05.015)
32. Pickrell JK, Patterson N, Loh PR, Lipson M, Berger B, Stoneking M, Pakendorf B, Reich D. 2014 Ancient west Eurasian ancestry in southern and eastern Africa. Proc. Natl Acad. Sci. USA 111, 2632-2637. (doi:10.1073/pnas.1313787111)
33. Hodgson JA, Mulligan CJ, Al-Meeri A, Raaum RL. 2014 Early back-to-Africa migration into the Horn of Africa. PLoS Genet. 10, e1004393. (doi:10.1371/ journal.pgen.1004393)
34. Hartl DL, Clark AG. 2007 Principles of population genetics, 4th edn. Sunderland, MA: Sinauer.
35. Carter R. 2003 Speculations on the origins of Plasmodium vivax malaria. Trends Parasitol. 19, 214-219. (doi:10.1016/S1471-4922(03)00070-9)
36. Prugnolle F et al. 2013 Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. Proc. Natl Acad. Sci. USA 110, 8123-8128. (doi:10.1073/pnas.1306004110)
37. Liu W et al. 2014 African origin of the malaria parasite Plasmodium vivax. Nat. Commun. 5, 3346. (doi:10.1038/ncomms4346)
38. Mellars P. 2006 A new radiocarbon revolution and the dispersal of modern humans in Eurasia. Nature 439, 931-935. (doi:10.1038/nature04521)
39. Seixas S, Ferrand N, Rocha J. 2002 Microsatellite variation and evolution of the human Duffy blood group polymorphism. Mol. Biol. Evol. 19, 1802-1806. (doi:10.1093/oxfordjournals.molbev.a004003)
40. Green RE et al. 2010 A draft sequence of the Neandertal genome. Science 328, 710-722. (doi:10.1126/science.1188021)
41. Reich D et al. 2010 Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468, 1053-1060. (doi:10.1038/nature09710)
42. Bryc K et al. 2010 Genome-wide patterns of population structure and admixture in West Africans and African Americans. Proc. Natl Acad. Sci. USA 107, 786-791. (doi:10.1073/pnas.0909559107)
43. Jin W, Xu S, Wang H, Yu Y, Shen Y, Wu B, Jin L. 2012 Genome-wide detection of natural selection in African Americans pre-and post-admixture. Genome Res. 22, 519-527. (doi:10.1101/gr.124784. 111)
44. 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. (doi:10.1086/520769)
45. Brisbin A et al. 2012 PCAdmix: principal components-based assignment of ancestry along each chromosome in individuals with admixed ancestry from two or more populations. Hum. Biol. 84, 343-364. (doi:10.3378/027.084.0401)
46. Basu A, Tang H, Zhu X, Gu CC, Hanis C, Boerwinkle E, Risch N. 2008 Genome-wide distribution of ancestry in Mexican Americans. Hum. Genet. 124, 207-214. (doi:10.1007/s00439-008-0541-5)
47. Schlebusch CM et al. 2012 Genomic variation in seven Khoe-San groups reveals adaptation and complex African history. Science 338, 374-379. (doi:10.1126/science.1227721)
48. Hedrick PW. 1999 Balancing selection and MHC. Genetica 104, 207-214. (doi:10.1023/ A:1026494212540)
49. Simonson TS et al. 2010 Genetic evidence for highaltitude adaptation in Tibet. Science 329, 72-75. (doi:10.1126/science.1189406)
50. Beall CM et al. 2010 Natural selection on EPAS1 (HIF2alpha) associated with low hemoglobin concentration in Tibetan highlanders. Proc. Natl Acad. Sci. USA 107, 11 459-11 464. (doi:10.1073/ pnas.1002443107)
51. Yi X et al. 2010 Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329, 75-78. (doi:10.1126/science.1190371)