Out of Africa: origins and evolution of the human malaria parasites Plasmodium falciparum and Plasmodium vivax

International Journal for Parasitology

Volumn 47, Issue 2-3, 2017, Pages 87-97

  Loy, Dorothy E ^a,b   Liu, Weimin ^a   Li, Yingying ^a   Learn, Gerald H ^a   Plenderleith, Lindsey J ^c   Sundararaman, Sesh A ^a,b   Sharp, Paul M ^c   Hahn, Beatrice H ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

African apes; Evolution; Laverania; Malaria; Plasmodium falciparum; Plasmodium vivax; Zoonotic transmission

Indexed keywords

DISEASE TRANSMISSION; EVOLUTION; MALARIA; PATHOGEN; PRIMATE; PROTOZOAN;

AFRICA; ANIMAL EXPERIMENT; ASIA; BIOLOGY; CHIMPANZEE; GENOMICS; GORILLA; HUMAN VERSUS ANIMAL COMPARISON; MACACA; MUTATION; NONHUMAN; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PREVENTION; PUBLIC HEALTH; SPECIES; ANIMAL; GENETICS; HUMAN; MALARIA FALCIPARUM; MOLECULAR EVOLUTION; PARASITOLOGY; PLASMODIUM VIVAX MALARIA; ZOONOSIS;

ASIA;

PAN; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX;

AFRICA; ANIMALS; EVOLUTION, MOLECULAR; HUMANS; MALARIA, FALCIPARUM; MALARIA, VIVAX; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; ZOONOSES;

EID: 85002170805     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2016.05.008     Document Type: Review

References (73)

1. Amambua-Ngwa, A., Tetteh, K.K., Manske, M., Gomez-Escobar, N., Stewart, L.B., Deerhake, M.E., Cheeseman, I.H., Newbold, C.I., Holder, A.A., Knuepfer, E., Janha, O., Jallow, M., Campino, S., Macinnis, B., Kwiatkowski, D.P., Conway, D.J., Population genomic scan for candidate signatures of balancing selection to guide antigen characterization in malaria parasites. PLoS Genet., 8, 2012, e1002992.
2. Ayouba, A., Mouacha, F., Learn, G.H., Mpoudi-Ngole, E., Rayner, J.C., Sharp, P.M., Hahn, B.H., Delaporte, E., Peeters, M., Ubiquitous Hepatocystis infections, but no evidence of Plasmodium falciparum-like malaria parasites in wild greater spot-nosed monkeys (Cercopithecus nictitans). Int. J. Parasitol. 42 (2012), 709–713.
3. Bhatt, S., Weiss, D.J., Cameron, E., Bisanzio, D., Mappin, B., Dalrymple, U., Battle, K.E., Moyes, C.L., Henry, A., Eckhoff, P.A., Wenger, E.A., Briet, O., Penny, M.A., Smith, T.A., Bennett, A., Yukich, J., Eisele, T.P., Griffin, J.T., Fergus, C.A., Lynch, M., Lindgren, F., Cohen, J.M., Murray, C.L., Smith, D.L., Hay, S.I., Cibulskis, R.E., Gething, P.W., The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526 (2015), 207–211.
4. Blacklock, B., Adler, S., A parasite resembling Plasmodium falciparum in a chimpanzee. Ann. Trop. Med. Parasitol. XVI (1922), 99–106.
5. Bopp, S.E.R., Manary, M.J., Bright, A.T., Johnston, G.L., Dharia, N.V., Luna, F.L., McCormack, S., Plouffe, D., McNamara, C.W., Walker, J.R., Fidock, D.A., Denchi, E.L., Winzeler, E.A., Mitotic evolution of Plasmodium falciparum shows a stable core genome but recombination in antigen families. PLoS Genet., 9, 2013, e1003293.
6. Boundenga, L., Ollomo, B., Rougeron, V., Mouele, L.Y., Mve-Ondo, B., Delicat-Loembet, L.M., Moukodoum, N.D., Okouga, A.P., Arnathau, C., Elguero, E., Durand, P., Liegeois, F., Boue, V., Motsch, P., Le Flohic, G., Ndoungouet, A., Paupy, C., Ba, C.T., Renaud, F., Prugnolle, F., Diversity of malaria parasites in great apes in Gabon. Malar. J., 14, 2015, 111.
7. Bray, R.S., Studies on malaria in chimpanzees VI. Laverania falciparum. Am. J. Trop. Med. Hyg. 7 (1958), 20–24.
8. Brumpt, E., Les parasites du paludisme des chimpanzes. CR Soc. Biol. 130 (1939), 837–840.
9. Caldecott, J.O., Miles, L., World Atlas of Great Apes and their Conservation. 2005, University of California Press, Berkley, California, USA.
10. Carter, R., Speculations on the origins of Plasmodium vivax malaria. Trends Parasitol. 19 (2003), 214–219.
11. Carter, R., Mendis, K.N., Evolutionary and historical aspects of the burden of malaria. Clin. Microbiol. Rev. 15 (2002), 564–594.
12. Coatney G.R., Collins W.E., Warren, M., Contacos P.G., 1971. The Primate Malarias. US Government Printing Office, Washington, DC. http://phsource.us/PH/PARA/Book/primate_24.pdf.
13. Contacos, P.G., Coatney, G.R., Orihel, T.C., Collins, W.E., Chin, W., Jeter, M.H., Transmission of Plasmodium schwetzi from the chimpanzee to man by mosquito bite. Am. J. Trop. Med. Hyg. 19 (1970), 190–195.
14. Conway, D.J., Fanello, C., Lloyd, J.M., Al-Joubori, B.M., Baloch, A.H., Somanath, S.D., Roper, C., Oduola, A.M., Mulder, B., Povoa, M.M., Singh, B., Thomas, A.W., Origin of Plasmodium falciparum malaria is traced by mitochondrial DNA. Mol. Biochem. Parasitol. 111 (2000), 163–171.
15. Culleton, R., Carter, R., African Plasmodium vivax: distribution and origins. Int. J. Parasitol. 42 (2012), 1091–1097.
16. De Nys, H.M., Calvignac-Spencer, S., Boesch, C., Dorny, P., Wittig, R.M., Mundry, R., Leendertz, F.H., Malaria parasite detection increases during pregnancy in wild chimpanzees. Malar. J., 13, 2014, 413.
17. De Nys, H.M., Calvignac-Spencer, S., Thiesen, U., Boesch, C., Wittig, R.M., Mundry, R., Leendertz, F.H., Age-related effects on malaria parasite infection in wild chimpanzees. Biol. Lett., 9, 2013, 20121160.
18. Delicat-Loembet, L., Rougeron, V., Ollomo, B., Arnathau, C., Roche, B., Elguero, E., Moukodoum, N.D., Okougha, A.P., Mve Ondo, B., Boundenga, L., Houze, S., Galan, M., Nkoghe, D., Leroy, E.M., Durand, P., Paupy, C., Renaud, F., Prugnolle, F., No evidence for ape Plasmodium infections in humans in Gabon. PLoS One, 10, 2015, e0126933.
19. Duval, L., Fourment, M., Nerrienet, E., Rousset, D., Sadeuh, S.A., Goodman, S.M., Andriaholinirina, N.V., Randrianarivelojosia, M., Paul, R.E., Robert, V., Ayala, F.J., Ariey, F., African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. Proc. Natl. Acad. Sci. U.S.A. 107 (2010), 10561–10566.
20. Escalante, A.A., Ayala, F.J., Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc. Natl. Acad. Sci. U.S.A. 91 (1994), 11373–11377.
21. Escalante, A.A., Cornejo, O.E., Freeland, D.E., Poe, A.C., Durrego, E., Collins, W.E., Lal, A.A., A monkey's tale: The origin of Plasmodium vivax as a human malaria parasite. Proc. Natl. Acad. Sci. U.S.A. 102 (2005), 1980–1985.
22. Hedrick, P.W., Population genetics of malaria resistance in humans. Heredity (Edinb) 107 (2011), 283–304.
23. Herbert, A., Boundenga, L., Meyer, A., Moukodoum, D.N., Okouga, A.P., Arnathau, C., Durand, P., Magnus, J., Ngoubangoye, B., Willaume, E., Ba, C.T., Rougeron, V., Renaud, F., Ollomo, B., Prugnolle, F., Malaria-like symptoms associated with a natural Plasmodium reichenowi infection in a chimpanzee. Malar. J., 14, 2015, 220.
24. Howes, R.E., Patil, A.P., Piel, F.B., Nyangiri, O.A., Kabaria, C.W., Gething, P.W., Zimmerman, P.A., Barnadas, C., Beall, C.M., Gebremedhin, A., Menard, D., Williams, T.N., Weatherall, D.J., Hay, S.I., The global distribution of the Duffy blood group. Nat. Commun., 2, 2011, 266.
25. Hughes, A.L., Verra, F., Very large long-term effective population size in the virulent human malaria parasite Plasmodium falciparum. Proc. Biol. Sci. 268 (2001), 1855–1860.
26. Ioerger, T.R., Clark, A.G., Kao, T.H., Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc. Natl. Acad. Sci. U.S.A. 87 (1990), 9732–9735.
27. Jongwutiwes, S., Putaporntip, C., Iwasaki, T., Ferreira, M.U., Kanbara, H., Hughes, A.L., Mitochondrial genome sequences support ancient population expansion in Plasmodium vivax. Mol. Biol. Evol. 22 (2005), 1733–1739.
28. Kaiser, M., Lowa, A., Ulrich, M., Ellerbrok, H., Goffe, A.S., Blasse, A., Zommers, Z., Couacy-Hymann, E., Babweteera, F., Zuberbuhler, K., Metzger, S., Geidel, S., Boesch, C., Gillespie, T.R., Leendertz, F.H., Wild chimpanzees infected with 5 Plasmodium species. Emerg. Infect. Dis. 16 (2010), 1956–1959.
29. Krief, S., Escalante, A.A., Pacheco, M.A., Mugisha, L., Andre, C., Halbwax, M., Fischer, A., Krief, J.M., Kasenene, J.M., Crandfield, M., Cornejo, O.E., Chavatte, J.M., Lin, C., Letourneur, F., Gruner, A.C., McCutchan, T.F., Renia, L., Snounou, G., On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from bonobos. PLoS Pathog., 6, 2010, e1000765.
30. Liu, W., Li, Y., Learn, G.H., Rudicell, R.S., Robertson, J.D., Keele, B.F., Ndjango, J.B., Sanz, C.M., Morgan, D.B., Locatelli, S., Gonder, M.K., Kranzusch, P.J., Walsh, P.D., Delaporte, E., Mpoudi-Ngole, E., Georgiev, A.V., Muller, M.N., Shaw, G.M., Peeters, M., Sharp, P.M., Rayner, J.C., Hahn, B.H., Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467 (2010), 420–425.
31. Liu, W., Li, Y., Peeters, M., Rayner, J.C., Sharp, P.M., Shaw, G.M., Hahn, B.H., Single genome amplification and direct amplicon sequencing of Plasmodium spp. DNA from ape fecal specimens. Protocol Exchange, 2010, 10.1038/nprot.2010.156.
32. Liu, W., Li, Y., Shaw, K.S., Learn, G.H., Plenderleith, L.J., Malenke, J.A., Sundararaman, S.A., Ramirez, M.A., Crystal, P.A., Smith, A.G., Bibollet-Ruche, F., Ayouba, A., Locatelli, S., Esteban, A., Mouacha, F., Guichet, E., Butel, C., Ahuka-Mundeke, S., Inogwabini, B.I., Ndjango, J.B., Speede, S., Sanz, C.M., Morgan, D.B., Gonder, M.K., Kranzusch, P.J., Walsh, P.D., Georgiev, A.V., Muller, M.N., Piel, A.K., Stewart, F.A., Wilson, M.L., Pusey, A.E., Cui, L., Wang, Z., Farnert, A., Sutherland, C.J., Nolder, D., Hart, J.A., Hart, T.B., Bertolani, P., Gillis, A., LeBreton, M., Tafon, B., Kiyang, J., Djoko, C.F., Schneider, B.S., Wolfe, N.D., Mpoudi-Ngole, E., Delaporte, E., Carter, R., Culleton, R.L., Shaw, G.M., Rayner, J.C., Peeters, M., Hahn, B.H., Sharp, P.M., African origin of the malaria parasite Plasmodium vivax. Nat. Commun., 5, 2014, 3346.
33. Liu, W., Sundararaman, S.A., Loy, D.E., Learn, G.H., Li, Y., Plenderleith, L.J., Ndjango, J.-B.N., Speede, S., Atencia, R., Cox, D., Shaw, G.M., Ayouba, A., Peeters, M., Rayner, J.C., Hahn, B.H., Sharp, P.M., Multigenomic delineation of Plasmodium species of Laverania subgenus infecting wild-living chimpanzees and gorillas. Genome Biol. Evol. 8 (2016), 1929–1939.
34. Livingstone, F.B., Anthropological implications of sickle cell gene distribution in West Africa. Am. Anthropol. 60 (1958), 533–562.
35. Livingstone, F.B., The Duffy blood groups, vivax malaria, and malaria selection in human populations: a review. Hum. Biol. 56 (1984), 413–425.
36. Lynch, M., Evolution of the mutation rate. Trends Genet. 26 (2010), 345–352.
37. Makanga, B., Yangari, P., Rahola, N., Rougeron, V., Elguero, E., Boundenga, L., Moukodoum, N.D., Okouga, A.P., Arnathau, C., Durand, P., Willaume, E., Ayala, D., Fontenille, D., Ayala, F.J., Renaud, F., Ollomo, B., Prugnolle, F., Paupy, C., Ape malaria transmission and potential for ape-to-human transfers in Africa. Proc. Natl. Acad. Sci. U.S.A., 2016, 201603008.
38. Mellars, P., Going east: new genetic and archaeological perspectives on the modern human colonization of Eurasia. Science 313 (2006), 796–800.
39. Miller, L.H., Mason, S.J., Clyde, D.F., McGinniss, M.H., The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N. Engl. J. Med. 295 (1976), 302–304.
40. Molina-Cruz, A., Barillas-Mury, C., Mosquito vectors of ape malarias: another piece of the puzzle. Proc. Natl. Acad. Sci. U.S.A. 113 (2016), 5153–5154.
41. Mu, J., Joy, D.A., Duan, J., Huang, Y., Carlton, J., Walker, J., Barnwell, J., Beerli, P., Charleston, M.A., Pybus, O.G., Su, X.Z., Host switch leads to emergence of Plasmodium vivax malaria in humans. Mol. Biol. Evol. 22 (2005), 1686–1693.
42. Nair, S., Williams, J.T., Brockman, A., Paiphun, L., Mayxay, M., Newton, P.N., Guthmann, J.P., Smithuis, F.M., Hien, T.T., White, N.J., Nosten, F., Anderson, T.J., A selective sweep driven by pyrimethamine treatment in Southeast Asian malaria parasites. Mol. Biol. Evol. 20 (2003), 1526–1536.
43. Neafsey, D.E., Galinsky, K., Jiang, R.H., Young, L., Sykes, S.M., Saif, S., Gujja, S., Goldberg, J.M., Young, S., Zeng, Q., Chapman, S.B., Dash, A.P., Anvikar, A.R., Sutton, P.L., Birren, B.W., Escalante, A.A., Barnwell, J.W., Carlton, J.M., The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum. Nat. Genet. 44 (2012), 1046–1050.
44. Ochola, L.I., Tetteh, K.K., Stewart, L.B., Riitho, V., Marsh, K., Conway, D.J., Allele frequency-based and polymorphism-versus-divergence indices of balancing selection in a new filtered set of polymorphic genes in Plasmodium falciparum. Mol. Biol. Evol. 27 (2010), 2344–2351.
45. Ollomo, B., Durand, P., Prugnolle, F., Douzery, E., Arnathau, C., Nkoghe, D., Leroy, E., Renaud, F., A new malaria agent in African hominids. PLoS Pathog., 5, 2009, e1000446.
46. Otto, T.D., Rayner, J.C., Bohme, U., Pain, A., Spottiswoode, N., Sanders, M., Quail, M., Ollomo, B., Renaud, F., Thomas, A.W., Prugnolle, F., Conway, D.J., Newbold, C., Berriman, M., Genome sequencing of chimpanzee malaria parasites reveals possible pathways of adaptation to human hosts. Nat. Commun., 5, 2014, 4754.
47. Pacheco, M.A., Battistuzzi, F.U., Junge, R.E., Cornejo, O.E., Williams, C.V., Landau, I., Rabetafika, L., Snounou, G., Jones-Engel, L., Escalante, A.A., Timing the origin of human malarias: the lemur puzzle. BMC Evol. Biol., 11, 2011, 299.
48. Pacheco, M.A., Cranfield, M., Cameron, K., Escalante, A.A., Malarial parasite diversity in chimpanzees: the value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens. Malar. J., 12, 2013, 238.
49. Paget-McNicol, S., Saul, A., Mutation rates in the dihydrofolate reductase gene of Plasmodium falciparum. Parasitology 122 (2001), 497–505.
50. Paupy, C., Makanga, B., Ollomo, B., Rahola, N., Durand, P., Magnus, J., Willaume, E., Renaud, F., Fontenille, D., Prugnolle, F., Anopheles moucheti and Anopheles vinckei are candidate vectors of ape Plasmodium parasites, including Plasmodium praefalciparum in Gabon. PLoS One, 8, 2013, e57294.
51. Polley, S.D., Tetteh, K.K., Lloyd, J.M., Akpogheneta, O.J., Greenwood, B.M., Bojang, K.A., Conway, D.J., Plasmodium falciparum merozoite surface protein 3 is a target of allele-specific immunity and alleles are maintained by natural selection. J. Infect. Dis. 195 (2007), 279–287.
52. Prugnolle, F., Durand, P., Neel, C., Ollomo, B., Ayala, F.J., Arnathau, C., Etienne, L., Mpoudi-Ngole, E., Nkoghe, D., Leroy, E., Delaporte, E., Peeters, M., Renaud, F., African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 107 (2010), 1458–1463.
53. Prugnolle, F., Ollomo, B., Durand, P., Yalcindag, E., Arathau, C., Elguero, E., Berry, A., Pourrut, X., Gonzalez, J.P., Nkoghe, D., Akiana, J., Verrier, D., Leroy, E., Ayala, F.J., Renaud, F., African monkeys are infected by Plasmodium falciparum nonhuman primate-specific strains. Proc. Natl. Acad. Sci. U.S.A. 108 (2011), 11948–11953.
54. Prugnolle, F., Rougeron, V., Becquart, P., Berry, A., Makanga, B., Rahola, N., Arnathau, C., Ngoubangoye, B., Menard, S., Willaume, E., Ayala, F.J., Fontenille, D., Ollomo, B., Durand, P., Paupy, C., Renaud, F., Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 8123–8128.
55. Ramachandran, S., Deshpande, O., Roseman, C.C., Rosenberg, N.A., Feldman, M.W., Cavalli-Sforza, L.L., Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc. Natl. Acad. Sci. U.S.A. 102 (2005), 15942–15947.
56. Reichenow, E., Über das Vorkommen der Malariaparasiten des Menschen bei den Afrikanischen Menschenaffen. Centralbl. f. Bakt. I. Abt. Orig. 85 (1920), 207–216.
57. Rich, S.M., Leendertz, F.H., Xu, G., LeBreton, M., Djoko, C.F., Aminake, M.N., Takang, E.E., Diffo, J.L.D., Pike, B.L., Rosenthal, B.M., Formenty, P., Boesch, C., Ayala, F.J., Wolfe, F.D., The origin of malignant malaria. Proc. Natl. Acad. Sci. U.S.A. 106 (2009), 14902–14907.
58. Rich, S.M., Licht, M.C., Hudson, R.R., Ayala, F.J., Malaria's Eve: evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 95 (1998), 4425–4430.
59. Roy, S.W., The Plasmodium gaboni genome illuminates allelic dimorphism of immunologically important surface antigens in P. falciparum. Infect. Genet. Evol. 36 (2015), 441–449.
60. Roy, S.W., Ferreira, M.U., A new model for the origins of allelic dimorphism in Plasmodium falciparum. Parasitol. Int. 64 (2015), 229–237.
61. Roy, S.W., Ferreira, M.U., Hartl, D.L., Evolution of allelic dimorphism in malarial surface antigens. Heredity (Edinb) 100 (2008), 103–110.
62. Sharp, P.M., Liu, W., Learn, G.H., Rayner, J.C., Peeters, M., Hahn, B.H., Source of the human malaria parasite Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 108 (2011), E744–E745.
63. Sluiter, C.P., Swellengrebel, N.H., Ihle, J.E., De dierlijke parasieten van den mensch en van onze huisdieren. third ed., 1922, Scheltema and Holkema's Boekhandel, Amsterdam, Netherlands.
64. Sundararaman, S.A., Liu, W., Keele, B.F., Learn, G.H., Bittinger, K., Mouacha, F., Ahuka-Mundeke, S., Manske, M., Sherrill-Mix, S., Li, Y., Malenke, J.A., Delaporte, E., Laurent, C., Mpoudi Ngole, E., Kwiatkowski, D.P., Shaw, G.M., Rayner, J.C., Peeters, M., Sharp, P.M., Bushman, F.D., Hahn, B.H., Plasmodium falciparum-like parasites infecting wild apes in southern Cameroon do not represent a recurrent source of human malaria. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 7020–7025.
65. Sundararaman, S.A., Plenderleith, L.J., Liu, W., Loy, D.E., Learn, G.H., Li, Y., Shaw, K.S., Ayouba, A., Peeters, M., Speede, S., Shaw, G.M., Bushman, F.D., Brisson, D., Rayner, J.C., Sharp, P.M., Hahn, B.H., Genomes of cryptic chimpanzee Plasmodium species reveal key evolutionary events leading to human malaria. Nat. Commun., 7, 2016, 11078.
66. Tachibana, S., Sullivan, S.A., Kawai, S., Nakamura, S., Kim, H.R., Goto, N., Arisue, N., Palacpac, N.M., Honma, H., Yagi, M., Tougan, T., Katakai, Y., Kaneko, O., Mita, T., Kita, K., Yasutomi, Y., Sutton, P.L., Shakhbatyan, R., Horii, T., Yasunaga, T., Barnwell, J.W., Escalante, A.A., Carlton, J.M., Tanabe, K., Plasmodium cynomolgi genome sequences provide insight into Plasmodium vivax and the monkey malaria clade. Nat. Genet. 44 (2012), 1051–1055.
67. Tanabe, K., Mackay, M., Goman, M., Scaife, J.G., Allelic dimorphism in a surface antigen gene of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 195 (1987), 273–287.
68. Tanabe, K., Mita, T., Jombart, T., Eriksson, A., Horibe, S., Palacpac, N., Ranford-Cartwright, L., Sawai, H., Sakihama, N., Ohmae, H., Nakamura, M., Ferreira, M.U., Escalante, A.A., Prugnolle, F., Bjorkman, A., Farnert, A., Kaneko, A., Horii, T., Manica, A., Kishino, H., Balloux, F., Plasmodium falciparum accompanied the human expansion out of Africa. Curr. Biol. 20 (2010), 1283–1289.
69. Taylor, S.M., Parobek, C.M., Fairhurst, R.M., Haemoglobinopathies and the clinical epidemiology of malaria: a systematic review and meta-analysis. Lancet Infect. Dis. 12 (2012), 457–468.
70. Tetteh, K.K., Osier, F.H., Salanti, A., Kamuyu, G., Drought, L., Failly, M., Martin, C., Marsh, K., Conway, D.J., Analysis of antibodies to newly described Plasmodium falciparum merozoite antigens supports MSPDBL2 as a predicted target of naturally acquired immunity. Infect. Immun. 81 (2013), 3835–3842.
71. Valkiunas, G., Ashford, R.W., Bensch, S., Killick-Kendrick, R., Perkins, S., A cautionary note concerning Plasmodium in apes. Trends Parasitol. 27 (2011), 231–232.
72. Volkman, S.K., Sabeti, P.C., DeCaprio, D., Neafsey, D.E., Schaffner, S.F., Milner, D.A. Jr., Daily, J.P., Sarr, O., Ndiaye, D., Ndir, O., Mboup, S., Duraisingh, M.T., Lukens, A., Derr, A., Stange-Thomann, N., Waggoner, S., Onofrio, R., Ziaugra, L., Mauceli, E., Gnerre, S., Jaffe, D.B., Zainoun, J., Wiegand, R.C., Birren, B.W., Hartl, D.L., Galagan, J.E., Lander, E.S., Wirth, D.F., A genome-wide map of diversity in Plasmodium falciparum. Nat. Genet. 39 (2007), 113–119.
73. World Health Organization, World Health Organization World Malaria Report 2015. 2015, WHO Press, Geneva, Switzerland.