The action of falciparum malaria on the human and chimpanzee genomes compared: Absence of evidence for a genomic signature of malaria at HBB and G6PD in three subspecies of chimpanzee

Infection, Genetics and Evolution

Volumn 9, Issue 6, 2009, Pages 1248-1252

  MacFie, T S ^a   Nerrienet, E ^b   Bontrop, R E ^c   Mundy, N I ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CENTRE PASTEUR DU CAMEROUN   (Cameroon)

^c BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

Author keywords

globin; Balancing selection; Chimpanzee; G6PD; Malaria

Indexed keywords

BETA GLOBIN; GENOMIC DNA; GLUCOSE 6 PHOSPHATE DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHIMPANZEE; CONTROLLED STUDY; DISEASE RESISTANCE; GENE LOCUS; GENETIC ASSOCIATION; GENETIC VARIABILITY; HOST PARASITE INTERACTION; MALARIA FALCIPARUM; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTECTION; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES COMPARISON;

ANIMALS; BETA-GLOBINS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME; GLUCOSEPHOSPHATE DEHYDROGENASE; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNITY, INNATE; MALARIA, FALCIPARUM; PAN TROGLODYTES; PLASMODIUM FALCIPARUM; SELECTION, GENETIC; SPECIES SPECIFICITY; VIRULENCE;

PAN; PLASMODIUM FALCIPARUM; PRIMATES;

EID: 70449553947     PISSN: 15671348     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meegid.2009.06.025     Document Type: Article

References (40)

1. Adler S. Malaria in chimpanzees in Sierra Leone. Ann. Trop. Med. Parasitol. 17 (1923) 13-19
2. Allison A.C. Population genetics of abnormal haemoglobins and glucose-6-phosphate dehydrogenase deficiency. In: Jonxis J.H.P.e.a. (Ed). Abnormal Haemoglobins in Africa (1965), Blackwell Scientific, Oxford, England
3. Bandelt H.-J., Forster P., and Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16 (1999) 37-48
4. Blacklock B., and Adler S. A parasite resembling Plasmodium falciparum in a chimpanzee. Ann. Trop. Med. Parasitol. 16 (1922) 99-106
5. Chen F.C., and Li W.H. Genomic divergence between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am. J. Hum. Genet. 68 (2001) 444-456
6. s Senegal mutation. Am. J. Hum. Genet. 70 (2002) 207-223
7. de Groot N.G., Otting N., Doxiadis G.G.M., Balla-Jhagjhoorsingh S.S., Heeney J.L., van Rood J.J., Gagneux P., and Bontrop R.E. Evidence for an ancient selective sweep in the MHC class I gene repertoire of chimpanzees. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 11748-11753
8. Deinard A., and Kidd K. Identifying conservation units within captive chimpanzee populations. Am. J. Phys. Anthropol. 111 (2000) 25-44
9. Duval L., Nerrienet E., Rousset D., Mba S.A.S., Houze S., Fourment M., Le Bras J., Robert V., and Ariey F. Chimpanzee malaria parasites related to Plasmodium ovale in Africa. PLoS ONE 4 (2009) 35520
10. Escalante A.A., and 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
11. Fischer A., Wiebe V., Paabo S., and Przeworksi M. Evidence for a complex demographic history of chimpanzees. Mol. Biol. Evol. 21 (2004) 799-808
12. Flint J., Harding R.M., Boyce A.J., and Clegg J.B. The population genetics of the haemoglobinopathies. In: Higgs D.R., Weatherall D.J., et al. (Eds). Bailliere's Clinical Haemotology: Haemoglobinopathies (1998), Balliere Tindall, WB Saunders, London, England 1-51
13. Fu Y.-X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147 (1997) 915-925
14. Gagneux P., Wills C., Gerloff U., Tautz D., Morin P.A., Boesch C., Fruth B., Hohmann G., Ryder O.A., and Woodruff D.S. Mitochondrial sequences show diverse evolutionary histories of African hominoids. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 5077-5082
15. Gonder M.K., Oates J.F., Disotell T.R., Forstner M.R.J., Morales J.C., and Melnick D.J. A new West African chimpanzee subspecies. Nature 388 (1997) 337
16. Gonder, M.K., 2000. Evolutionary genetics of chimpanzees (Pan troglodytes) in Nigeria and Cameroon. PhD Thesis. New York, The City University of New York.
17. Haldane J.B.S. Disease and evolution. Ricerca Sci. 19 (1949) 3-10
18. Harding R.M., Fullerton S.M., Griffiths R.C., Bond J., Cox M.J., Schneider J.A., Moulin D.S., and Clegg J.B. Archaic African and Asian lineages in the genetic ancestry of modern humans. Am. J. Hum. Genet. 60 (1997) 772-789
19. Huisman T.H.J., Carver M.F.H., and Efremov G.D. A Syllabus of Human Hemoglobin Variants (1998), Sickle Cell Foundation, Augusta, GA
20. Kaessman H., Wiebe V., and Pääbo S. Extensive nuclear DNA sequence diversity among chimpanzees. Science (1999) 1159-1162
21. Livingstone F.B. Frequencies of Haemoglobin Variants: Thalassaemia, The Glucose-6-Phosphate Dehydrogenase Deficiency, G6PD Variants, and Ovalocytosis in Human Populations (1985), Oxford University Press, New York, NY
22. 3CR1. Mol. Biol. Evol. 26 (2009) 719-727
23. Martin M.J., Rayner J.C., Gagneux P., Barnwell J.W., and Varki A. Evolution of human-chimpanzee differences in malaria susceptibility: relationship to human genetic loss of N-glycolylneuraminic acid. PNAS 102 36 (2005) 12819-12824
24. Modiano D., Luoni G., Sirima B.S., Simpore J., Verra F., Konate A., Rastrelli E., Olivieri A., Calissano C., Paganotti G.M., D'Urbano L., Sanou I., Sawadogo A., Modiano G., and Coluzzi M. Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature 414 (2001) 305-308
25. Morin P.A., Moore J.J., Chakraborty R., Jin L., Goodall J., and Woodruff D.S. Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science 265 (1994) 1193-1201
26. Ollomo B., Karch S., Bureau P., Elissa N., Georges A.J., and Millet P. Lack of malaria parasite transmission between apes and humans in Gabon. Am. J. Trop. Med. Hyg. 56 (1997) 440-445
27. Sabeti P.C., Reich D.E., HIggins J.M., Levine H.Z., Richter D.J., Schaffner S.F., Gabriel S.B., Platko J.V., Patterson N.J., McDonald G.J., Ackerman H.C., Campbell S.J., Campbell S.J., Altshuler D., Cooper R., Kwiatkowski D., Ward R., and Lander E.S. Detecting recent positive selection in the human genome from haplotype structure. Nature 419 (2002) 832-837
28. Saunders M.A., Hammer M.F., and Nachman M.W. Nucleotide variability at G6PD and the signature of malarial selection in humans. Genetics 162 (2002) 1849-1861
29. Schneider S., Roessli D., and Excoffier L. Arlequin ver. 2.000 A Software for Population Genetics Data Analysis. Genetics and Biometry Laboratory (2000), University of Geneva, Switzerland
30. Stephens M., Smith N., and Donnelly P. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68 (2001) 978-989
31. Stephens M., and Scheet P. Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am. J. Hum. Genet. 76 (2005) 449-462
32. Stone A.C., Griffiths R.C., Zegura S.L., and Hammer M.F. High levels of Y-chromosome nucleotide diversity in the genus Pan. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 43-48
33. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 (1989) 585-595
34. Tishkoff S.A., Varkonyi R., Cahinhinan N., Abbes S., Argyropoulos G., Destro-Bisol G., Drousiotou A., Dangerfield B., Lefranc G., Loiselet J., Piro A., Stoneking M., Tagarelli A., Tagarelli G., Touma E.H., Williams S.M., and Clark A.G. Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science 293 (2001) 455-462
35. Verrelli B.C., McDonald J.H., Argyropoulos G., Destro-Bisol G., Froment A., Drousiotou A., Lefranc G., Helal A.N., Loiselet J., and Tishkoff S. Evidence for balancing selection from nucleotide sequence analyses of human G6PD. Am. J. Hum. Genet. 71 (2002) 1112-1128
36. Verrelli B.C., Tishkoff S.A., Stone A.C., and Touchman J.W. Contrasting histories of G6PD molecular evolution and malarial resistance in humans and chimpanzees. Mol. Biol. Evol. 23 (2006) 1592-1601
37. Weatherall D.J., and Clegg J.B. The Thalassaemia Syndromes. 4th ed. (2001), Blackwell Scientific, Oxford, England
38. Wise C.A., Sraml M., Rubinsztein D.C., and Easteal S. Comparative nuclear and mitochondrial genome diversity in humans and chimpanzees. Mol. Biol. Evol. 14 (1997) 707-716
39. Wooding S., Stone A.C., Dunn D.M., Mummidi S., Jorde L.B., Weiss R.K., Ahuja S., and Bamshad M.J. Contrasting effects of natural selection on human and chimpanzee CC chemokine receptor 5. Am. J. Hum. Genet. 76 (2005) 291-301
40. Yu N., Jensen-Seaman M.I., Chemnick L., Kidd J.R., Deinard A.S., Ryder O., Kidd K.K., and Li W.-H. Low nucleotide diversity in chimpanzees and bonobos. Genetics 164 (2003) 1511-1518