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Chapter 7 : Evolutionary History and Population Genetics of Human Malaria Parasites

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Abstract:

The central theme of this chapter is the molecular evolution of species of the genus —the experimental methods, conclusions, and confounding elements peculiar to . While one section of the chapter is a brief summary of studies on the evolutionary history of and related organisms, another is a summary of the molecular population genetics of contemporary world populations of the two most virulent human malaria parasites. In addition to humans, parasites infect a range of vertebrate hosts, including birds, lizards, rodents, and nonhuman primates. Malaria has also been found in African rodents, and many of the species have been adapted to laboratory mice and rats and used as models for human malarias. ovale and cause the rarest and least virulent forms of malaria. Population studies of and , however, have already yielded unexpected results, paradoxical conclusions, and questions calling for additional research. Genome-level research has made it possible to explore malaria evolution in greater depth and rigor to help complete the picture. These changes have come through malaria parasite genome projects (for , , , and ) and their associated databases, access to automated DNA sequencers in most modern laboratories, an increasingly sophisticated understanding of the unusual molecular biology and evolution of the parasites, and improvements in methods of statistical inference from DNA sequence differences within and among populations.

Citation: Zilversmit M, Hartl D. 2005. Evolutionary History and Population Genetics of Human Malaria Parasites, p 95-109. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch7
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FIGURE 1

Summary phylogenetic tree showing the relationship between malaria parasites of mammals. Note that primate species are monophyletic, with the exception of the - pairing, which is outside both rodent and primate clades. Rodent and primate parasites form monophyletic groups. Branch lengths are not proportional; only nodes with statistical support of ≥85% are shown ( ).

Citation: Zilversmit M, Hartl D. 2005. Evolutionary History and Population Genetics of Human Malaria Parasites, p 95-109. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch7
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Image of FIGURE 2
FIGURE 2

Unrooted tree showing the relationship of infrakingdom Alveolata () to other infrakingdoms (including parasites and genomic models) within the domain Eukarya ( ).The dotted line indicates the possible sister relationship of Plantae to some protist groups ( ). Branch lengths are not proportional; only nodes showing statistical support of ≥85% are included.

Citation: Zilversmit M, Hartl D. 2005. Evolutionary History and Population Genetics of Human Malaria Parasites, p 95-109. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch7
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Image of FIGURE 3
FIGURE 3

Placement of the order Haemosporidia with the phylum Apicomplexa and relation of Apicomplexa within Alveolata. The infrakingdom Discicristata is the sister group to Alveolata and includes several well-studied parasites. Branch lengths are not proportional; only nodes showing statistical support of ≥85% are included ( ).

Citation: Zilversmit M, Hartl D. 2005. Evolutionary History and Population Genetics of Human Malaria Parasites, p 95-109. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch7
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Image of FIGURE 4
FIGURE 4

An unrooted neighbor-joining tree showing the relationships between nine populations. Only nodes with a bootstrap value of >75% are shown. Note that the African isolates (Zimbabwe, Congo, Uganda) from an area of high transmission show a large overall difference from the other isolates, but the relationship of the individual isolates cannot be distinguished with any statistical certainty. However, in South America, the Colombian and Bolivian-Brazilian isolates show a greater distance from each other than even overall distances from isolates from elsewhere in the world. (Figure adapted from .)

Citation: Zilversmit M, Hartl D. 2005. Evolutionary History and Population Genetics of Human Malaria Parasites, p 95-109. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch7
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References

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1. Anderson, T. J. C.,, B. Haubold,, J.T. Williams,, J. G. Estrada-Franco,, L. Richardson,, R. Mollinedo,, M. Bockarie,, J. Mokili,, S. Mharakurwa,, N. French,, J. Whitworth,, I. D. Velez,, A. H. Brockman,, F. Nosten,, M. U. Ferreira,, and K. P. Day. 2000. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol. Biol. Evol. 17: 1467 1482.
2. Baldauf, S. L.,, A. J. Roger,, I. Wenk-Siefert,, and W. F. Doolittle. 2000. A kingdom-level phylogeny of eukaryotes on combined protein data. Science 290: 972 977.
3. Barry, A. E.,, A. Leliwa,, M. Choi,, K. M. Nielsen,, D. L. Hartl,, and K. P. Day. 2003. DNA sequence artifacts and the estimation of time to the most recent common ancestor (TMRCA) of Plasmodium falciparum. Mol. Biochem. Parasitol . 130: 143 147.
4. Bastien, O.,, S. Lespinats,, S. Roy,, K. Metayer,, B. Fertil,, J. J. Codani,, and E. Marechal. 2004. Analysis of the compositional biases in Plasmodium falciparum genome and proteome using Arabidopsis thaliana as a reference. Gene 336: 163 173.
5. Cavalier-Smith, T., 1991. Cell diversification in heterotrophic flagellates, p. 113 131. In D. J. Patterson, and J. Larsen (ed.), The Biology of Freeliving Heterotrophic Flagellates. Oxford University Press, New York, N.Y.
6. Cavalier-Smith, T. 2004. Only six kingdoms of life. Proc. R. Soc. Lond. B Biol. Sci. 271: 1251 1262.
7. Cavalier-Smith, T.,, and E. E.-Y. Chao. 2003. Phylogeny of choanozoa, apusozoa, and other protozoa and early eukaryote megaevolution. J. Mol. Evol. 56: 540 563.
8. Coatney, G. R.,, W. E. Collins,, M. Warren,, and P. G. Contacos. 1971. The Primate Malarias. U.S. Department of Health, Education and Welfare, Bethesda, Md.
9. Conway, D. J. 1997. Natural selection on polymorphic malaria antigens and the search for a vaccine. Parasitol. Today 13: 26 29.
10. Conway, D. J.,, C. Roper,, A. M. Oduola,, D. E. Arnot,, P. G. Kremsner,, M. P. Grobusch,, C. F. Curtis,, and B. M. Greenwood. 1999. High recombination rate in natural populations of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 96: 4506 4511.
11. Conway, D. J.,, C. Fanello,, J. M. Lloyd,, B. M. Al- Joubori,, A. H. Baloch,, S. D. Somanath,, C. Roper,, A. M. Oduola,, B. Mulder,, M. M. Povoa,, B. Singh,, and A. W. Thomas. 2000. Origin of Plasmodium falciparum malaria is traced by mitochondrial DNA. Mol. Biochem. Parasitol. 111: 163 171.
12. Corredor, V.,, and V. Enea. 1993. Plasmodial ribosomal RNA as phylogenetic probe: a cautionary note. Mol. Biol. Evol. 10: 924 926.
13. Coulson, R. M.,, N. Hall,, and C. A. Ouzounis. 2004. Comparative genomics of transcriptional control in the human malaria parasite Plasmodium falciparum. Genome Res. 14: 1548 1554.
14. Drakeley C. J.,, M. T. Duraisingh,, M. Povoa,, D. J. Conway,, G. A. Targett,, and D. A. Baker. 1996. Geographical distribution of a variant epitope of Pfs48/45, a Plasmodium falciparum transmissionblocking vaccine candidate. Mol. Biochem. Parasitol. 81: 253 257.
15. Escalante, A. A.,, and F. J. Ayala. 1994. Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc. Natl. Acad. Sci. USA 91: 11373 11377.
16. Escalante, A. A.,, and F. J. Ayala. 1995. Evolutionary origin of Plasmodium and other apicomplexa based on rRNA genes. Proc. Natl. Acad. Sci. USA 92: 5793 5799.
17. Escalante, A. A.,, E. Barrio,, and F. J. Ayala. 1995. Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein. Mol. Biol. Evol. 12: 616 626.
18. Escalante, A. A.,, D. E. Freeland,, W. E. Collins,, and A. A. Lal. 1998. The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc. Natl. Acad. Sci. USA 95: 8124 8129.
19. Escalante, A. A.,, I. F. Goldman,, P. De Rijk,, R. De Wachter,, W. E. Collins,, S. H. Qari,, and A. A. Lal. 1997. Phylogenetic study of the genus Plasmodium based on the secondary structure-based alignment of the small subunit ribosomal RNA. Mol. Biochem. Parasitol. 90: 317 321.
20. Feng, X.,, J. M. Carlton,, D. A. Joy,, J. Mu,, T. Furuya,, B. Suh,, Y. Wang,, J. W. Barnwell,, and X.-Z. Su. 2003. Single nucleotide polymorphisms and genome diversity in Plasmodium vivax. Proc. Natl. Acad. Sci. USA 100: 8502 8507.
21. Figtree, M.,, C. J. Pasay,, R. Slade,, Q. Cheng,, N. Cloonan,, J. Walker,, and A. Saul. 2000. Plasmodium vivax synonymous substitution frequencies, evolution and population structure deduced from diversity in AMA 1 and MSP 1 genes. Mol. Biochem. Parasitol. 108: 53 66.
22. Gardner, M. J.,, N. Hall,, E. Fung,, O. White,, M. Berriman,, R. W. Hyman,, J. M. Carlton,, A. Pain,, K. E. Nelson,, S. Bowman,, I. T. Paulsen,, K. James,, J. A. Eisen,, K. Rutherford,, S. L. Salzberg,, A. Craig,, S. Kyes,, M. S. Chan,, V. Nene,, S. J. Shallom,, B. Suh,, J. Peterson,, S. Angiuoli,, M. Pertea,, J. Allen,, J. Selengut,, D. Haft,, M. W. Mather,, A. B. Vaidya,, D. M. Martin,, A. H. Fairlamb,, M. J. Fraunholz,, D. S. Roos,, S. A. Ralph,, G. I. McFadden,, L. M. Cummings,, G. M. Subramanian,, C. Mungall,, J. C. Venter,, D. J. Carucci,, S. L. Hoffman,, C. Newbold,, R. W. Davis,, C. M. Fraser,, and B. Barrell. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498 511.
23. Gutierrez, A.,, J. Vicini,, M. E. Patarroyo,, L. A. Murillo,, and M. A. Patarroyo. 2000. Plasmodium vivax: polymorphism in the merozoite surface protein 1 gene from wild Colombian isolates. Exp. Parasitol. 95: 215 219.
24. Hartl, D. L.,, and A. G. Clark. 1997. Principles of Population Genetics, 3rd ed. Sinauer Associates, Sunderland, Mass.
25. Hedges, S. B. 2002. The origin and evolution of model organisms. Nat. Rev. Genet. 3: 838 849.
26. Hughes, A. L.,, and F. Verra. 2001. Very large longterm effective population size in the virulent human malaria parasite Plasmodium falciparum. Proc. R. Soc. Lond. B Biol. Sci. 268: 1855 1860.
27. Ingman, M.,, H. Kaessmann,, S. Pääbo,, and U. Glyllensten. 2000. Mitochondrial genome variation and the origin of modern humans. Nature 408: 708 713.
28. Iwamoto, S.,, J. Li,, N. Sugimoto,, H. Okuda,, and E. Kajii. 1996. Characterization of the Duffy gene promoter: evidence for tissue-specific abolishment of expression in Fy(a-b-) of black individuals. Biochem. Biophys. Res. Commun. 222: 852 859.
29. Joy, D. A.,, X. Feng,, J. Mu,, T. Furuya,, K. Chotivanich,, A. U. Krettli,, M. Ho,, A. Wang,, N. J. White,, E. Suh,, P. Beerli,, and X. Su. 2003. Early origin and recent expansion of Plasmodium falciparum. Science 300: 318 321.
30. Kedzierski, L.,, A. A. Escalante,, R. Isea,, C. G. Black,, J. W. Barnwell,, and R. L. Coppel. 2002. Phylogenetic analysis of the genus Plasmodium based on the gene encoding adenylosuccinate lyase. Infect. Genet. Evol. 1: 297 301.
31. Kimura, M. 1968. Evolutionary rate at the molecular level. Nature 217: 624 626.
32. Kissinger, J. C.,, W. E. Collins,, J. Li,, and T. F. Mc-Cutchan. 1998. Plasmodium inui is not closely related to other quartan Plasmodium species. J. Parasitol. 84: 278 282.
33. Kumar, S.,, and B. S. Hedges. 1998. A molecular timescale for vertebrate evolution. Nature 392: 917 920.
34. Kurvadina, O. N.,, B. S. Leander,, V. V. Aleshin,, A. P. Myl'Nikov,, P. J. Keeling,, and T. G. Simdyanov. 2002. The phylogeny of colopodellids (Alveolata) using small subunit rRNA gene sequences suggests they are the free-living sister group to apicomplexans. J. Eukaryot. Microbiol. 49: 498 504.
35. Leander, B. S.,, O. N. Kuvardina,, V. V. Aleshin,, A. P. Mylnikov,, and P. J. Keeling. 2003. Molecular phylogeny and surface morphology of Colpodella edax (Alveolata): insights into the phagotrophic ancestry of apicomplexans. J. Eukaryot. Microbiol. 50: 334 340.
36. Leclerc, M. C.,, P. Durand,, C. Gauthier,, S. Patot,, N. Billotte,, M. Menegon,, C. Severini,, F. J. Ayala,, and F. Renaud. 2004. Meager genetic variability of the human malaria agent Plasmodium vivax. Proc. Natl.Acad. Sci. USA 101: 14455 14460.
37. Li, J.,, W. E. Collins,, R. A. Wirtz,, D. Rathore,, A. Lal,, and T. F. McCutchan. 2001. Geographic subdivision of the range of the malaria parasite Plasmodium vivax. Emerg. Infect. Dis. 7: 35 42.
38. Livingstone, F. B. 1958. Anthropological implications of sickle cell gene distribution in West Africa. Am. Anthropol. 60: 533 562.
39. McCutchan, T. F.,, J. B. Dame,, L. H. Miller,, and J. Barnwell. 1984. Evolutionary relatedness of Plasmodium species as determined by the structure of DNA. Science 225: 808 811.
40. McCutchan, T. F.,, J. C. Kissinger,, M. G. Touray,, J. M. Rogers,, J. Li,, M. Sullivan,, E. M. Braga,, A. U. Krettli,, and L. H. Miller. 1996. Comparison of circumsporozoite proteins from avian and mammalian malarias: biological and phylogenetic implications. Proc. Natl. Acad. Sci. USA 93: 11889 11894.
41. Miller, L. H.,, S. J. Mason,, D. F. Clyde,, and M. H. McGinnis. 1976. The resistance factor to Plasmodium vivax in blacks: the Duffy blood group genotype, FyFy. New Engl. J. Med. 295: 302 304.
42. Mu, J.,, J. Duan,, K. D. Makova,, D. A. Joy,, C. Q. Huynh,, O. H. Branch,, W. H. Li,, and X. Z. Su. 2002. Chromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum. Nature 418: 323 326.
43. Nielsen, K. M.,, J. Kasper,, M. Choi,, T. Bedford,, K. Kristiansen,, D. F. Wirth,, S. K. Volkman,, E. R. Lozovsky,, and D. L. Hartl. 2003. Gene conversion as a source of nucleotide diversity in Plasmodium falciparum. Mol. Biol. Evol. 20: 726 734.
44. Pace, N. R. 1997. A molecular view of microbial diversity and the biosphere. Science 276: 734 740.
45. Paul, R. E. L.,, F. Ariey,, and V. Robert. 2003. The evolutionary ecology of Plasmodium. Ecol. Lett. 6: 866 880.
46. Perkins, S. L.,, and J. J. Schall. 2002. A molecular phylogeny of malaria parasites recovered from cytochrome b gene sequences. J. Parasitol. 88: 972 978.
47. Philippe, H. 2000. Long branch attraction and protist phylogeny. Protist 151: 307 316.
48. Qari, S. H.,, Y. P. Shi,, N. J. Pieniazek,, W. E. Collins,, and A. A. Lal. 1996. Phylogenetic relationship among the malaria parasites based on small subunit rRNA gene sequences: monophyletic nature of the human malaria parasite, Plasmodium falciparum. Mol. Phylogenet. Evol. 6: 157 165.
49. Rasti, N.,, M. Wahlgren,, and Q. Chen. 2004. Molecular aspects of malaria pathogenesis. FEMS Immunol. Med. Microbiol. 41: 9 26.
50. Remsen, J.,, and P. O'Grady. 2002. Phylogeny of Drosophilinae (Diptera: Drosophilidae), with comments on combined analysis and character support. Mol. Phylogenet. Evol. 24: 249 264.
51. Rich, S. M.,, and F. J. Ayala. 2000. Population structure and recent evolution of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 97: 6994 70001.
52. Rich, S. M.,, R. R. Hudson,, and F. J. Ayala. 1997. Plasmodium falciparum antigenic diversity: evidence of clonal population structure. Proc. Natl. Acad. Sci. USA 94: 13040 13045.
53. Rich, S. M.,, M. C. Licht,, R. R. Hudson,, and F. J. Ayala. 1998. Malaria's Eve: evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 95: 4425 4430.
54. Rokas, A.,, B. L. Williams,, N. King,, and S. B. Carroll. 2003. Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425: 798 804.
55. Russell, P. F.,, L. S. West,, R. D. Manwell,, and G. M. MacDonald. 1963. Practical Malariology, 2nd ed. Oxford University Press, London, United Kingdom.
56. Saunders, M. A.,, M. F. Hammer,, and M. W. Nachman. 2002. Nucleotide variability at G6pd and the signature of malarial selection in humans. Genetics 162: 1849 1861.
57. Schug, M. D.,, C. M. Hutter,, M. A. Noor,, and C. F. Aquadro. 1998. Mutation and evolution of microsatellites in Drosophila melanogaster. Genetica 102–103: 359 356.
58. Siddall, M. E.,, and J. R. Barta. 1992. Phylogeny of Plasmodium species: estimation and inference. J. Parasitol . 78: 567 568.
59. Su, X.-Z.,, and J. C. Wootton. 2004. Genetic mapping in the human malaria parasite Plasmodium falciparum. Mol. Microbiol. 53: 1573 1582.
60. Templeton, A. 2002. Out of Africa again and again. Nature 416: 45 51.
61. Tishkoff, S. A.,, R. Varkonyi,, N. Cahinhinan,, S. Abbes,, G. Argyropoulos,, G. Destro-Bisol,, A. Drousiotou,, B. Dangerfield,, G. Lefranc,, J. Loiselet,, A. Piro,, M. Stoneking,, A. Tagarelli,, G. Tagarelli,, H. Elias,. E. H. Touma,, S. M. Williams,, and A. G. Clark. 2001. Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science 293: 455 482.
62. Vaidya, A. B.,, M. S. Lashgari,, L. G. Pologe,, and J. Morrisey. 1993. Structural features of Plasmodium cytochrome-b that may underlie susceptibility to 8- aminoquinolines and hydroxynaphthoquinones. Mol. Biochem. Parasitol. 58: 33 42.
63. Vargas-Serrato, E.,, V. Corredor,, and M. R. Galinski. 2003. Phylogenetic analysis of CSP and MSP- 9 gene sequences demonstrates the close relationship of Plasmodium coatneyi to Plasmodium knowlesi. Infect. Genet. Evol. 3: 67 73.
64. Volkman, S. K.,, A. E. Barry,, E. J. Lyons,, K. M. Nielsen,, S. M. Thomas,, M. Choi,, S. S. Thakore,, K. P. Day,, D. F. Wirth,, and D. L. Hartl. 2001. Recent origin of Plasmodium falciparum from a single progenitor. Science 293: 482 484.
65. Waters, A. P.,, D. G. Higgins,, and T. F. McCutchan. 1991. Plasmodium falciparum appears to have arisen as a result of a lateral transfer between avian and human hosts. Proc. Natl. Acad. Sci. USA 88: 3140 3144.
66. Waters, A. P.,, D. G. Higgins,, and T. F. McCutchan. 1993. Evolutionary relatedness of some primate models of Plasmodium. Mol. Biol. Evol. 10: 914 923.
67. White, N. J., 2003. Malaria, p. 1205 1296. In G. C. Cook, and A. Zumla (ed.), Manson's Tropical Diseases, 21st ed. W. B. Saunders, Philadelphia, Pa.
68. Woese, C. R.,, O. Kandler,, and M. L. Wheelis. 1990. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. USA 87: 4576 4579.
69. Zilversmit, M.,, P. M. O'Grady,, and R. DeSalle,. 2002. Shallow genomics, phylogenetics, and evolution in the family Drosophilidae, p. 512 523. In R. Altman,, A. K. Dunker,, L. Hunter,, K.Lauderdale,, and T. Klein, (ed.) Pacific Symposium on Biocomputing. World Scientific Publishing Co. Pte. Ltd., Riveredge, N. J.
70. Zimmerman, P. A.,, I. Woolley,, G. L. Masinde,, S. M. Miller,, D. T. McNamara,, F. Hazlett,, C. S. Mgone,, M. P. Alpers,, B. Genton,, B. A. Boatini,, and J. W. Kazura. 1999. Emergence of FY*A null in a Plasmodium vivax-endemic region of Papua New Guinea. Proc. Natl.Acad. Sci. USA 96: 13973 13977.

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