Factors shaping genetic variation in the MHC of natural non-human primate populations

Tissue Antigens

Volumn 70, Issue 5, 2007, Pages 398-411

  Bonhomme, M ^a,b   Blancher, A ^b   Jalil, M F ^c,d   Crouau Roy, B ^a  

^a École Nationale de Formation Agronomique   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d UNIVERSITI MALAYSIA SABAH   (Malaysia)

Author keywords

Demographic history; Linkage disequilibrium; Macaca fascicularis; Macaque populations; MHC region; Microsatellites; Selection

Indexed keywords

ARTICLE; BORNEO; CHINA; CONTROLLED STUDY; DEMOGRAPHY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC SELECTION; GENETIC VARIABILITY; HAPLOTYPE; HOMOZYGOSITY; HYBRIDIZATION; KAPOK; MACACA; MAJOR HISTOCOMPATIBILITY COMPLEX; MAURITIUS; MICROSATELLITE MARKER; NONHUMAN; PHILIPPINES; PLASMODIUM; PLASMODIUM COATNEYI; PLASMODIUM KNOWLESI; POPULATION DIFFERENTIATION; PRIORITY JOURNAL; SOUTHEAST ASIA;

ANIMALS; ASIA, SOUTHEASTERN; GENETICS, POPULATION; HAPLOTYPES; HUMANS; LINKAGE DISEQUILIBRIUM; MACACA FASCICULARIS; MACACA MULATTA; MAJOR HISTOCOMPATIBILITY COMPLEX; MALARIA; PARASITEMIA; PLASMODIUM KNOWLESI; VARIATION (GENETICS);

MACACA FASCICULARIS; MACACA MULATTA; PLASMODIUM COATNEYI; PLASMODIUM KNOWLESI; PRIMATES;

EID: 35148848701     PISSN: 00012815     EISSN: 13990039     Source Type: Journal    
DOI: 10.1111/j.1399-0039.2007.00925.x     Document Type: Article

References (83)

1. Klein J. Natural History of the Major Histocompatibility Complex. New York : John Wiley, 1986.
2. Hughes AL, Nei M. Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci U S A 1989 : 86 : 958 62.
3. Hedrick PW. Evolutionary genetics of the major histocompatibility complex. Am Nat 1994 : 143 : 945 64.
4. Meyer D, Thomson G. How selection shapes variation of the human major histocompatibility complex: a review. Ann Hum Genet 2001 : 65 : 1 26.
5. Bernatchez L, Landry C. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 2003 : 16 : 363 77.
6. Garrigan D, Hedrick PW. Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 2003 : 57 : 1707 22.
7. Klein J, O'hUigin C. MHC polymorphism and parasites. Philos Trans R Soc Lond B Biol Sci 1994 : 346 : 351 8.
8. Weatherall D, Clegg J, Kwiatkowski D. The role of genomics in studying genetic susceptibility to infectious disease. Genome Res 1997 : 7 : 967 73.
9. Hill AV. The immunogenetics of human infectious diseases. Annu Rev Immunol 1998 : 16 : 593 617.
10. Tishkoff SA, Verrelli BC. Patterns of human genetic diversity: implications for human evolutionary history and disease. Annu Rev Genomics Hum Genet 2003 : 4 : 293 340.
11. Sommer S. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2005 : 2 : 1 18.
12. Piertney SB, Oliver MK. The evolutionary ecology of the major histocompatibility complex. Heredity 2006 : 96 : 7 21.
13. Wright S. Evolution in Mendelian populations. Genetics 1931 : 16 : 97 159.
14. Wright S. Isolation by distance. Genetics 1943 : 28 : 114 38.
15. Slatkin M. Isolation by distance in equilibrium and nonequilibrium populations. Evolution 1993 : 47 : 264 79.
16. Cornuet JM, Luikart G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 1996 : 144 : 2001 14.
17. Beaumont MA. Detecting population expansion or decline using microsatellites. Genetics 1999 : 153 : 2013 29.
18. Garza JC, Williamson EG. Detection of reduction in population size using data from microsatellite loci. Mol Ecol 2001 : 10 : 305 18.
19. O'Connor DH. Chinese rhesus and cynomolgus macaques in HIV vaccine and pathogenesis research. Future Virol 2006 : 1 : 165 72.
20. Borie D, Hausen B, Larson M et al. A life-supporting technique of renal allotransplantation in Macaca fascicularis to evaluate novel immunosuppressive drugs in nonhuman primates. J Surg Res 2002 : 107 : 64 74.
21. Fooden J. Systematic review of Philippine macaques (primates, cercopithecidae: Macaca fascicularis subspp). Fieldiana: Zool 1991 : 64 : 1 44.
22. Fooden J. Systematic review of southeast asian longtail macaques, Macaca fascicularis [Raffles, (1821)]. Fieldiana: Zool 1995 : 81 : 1 206.
23. Schmidt LH, Fradkin R, Harrison J, Rossan RN. Differences in the virulence of Plasmodium knowlesi for Macaca irus (fascicularis) of Philippine and Malayan origins. Am J Trop Med Hyg 1977 : 26 : 612 22.
24. Collins WE, Skinner JC, Broderson JR et al. Susceptibility of Macaca fascicularis to different species of Plasmodium. J Parasitol 1992 : 78 : 505 11.
25. Migot-Nabias F, Ollomo B, Dubreuil G et al. Plasmodium coatneyi: differential clinical and immune responses of two populations of Macaca fascicularis from different origins. Exp Parasitol 1999 : 91 : 30 9.
26. Tattersall I, Dunaif A, Sussman RW, Jamieson R. Hematological and serum biochemical values in free-ranging Macaca fascicularis of Mauritius: possible diabetes mellitus and correlation with nutrition. Am J Primatol 1981 : 1 : 413 9.
27. Dunaif A, Tattersall I. Prevalence of glucose intolerance in free-ranging Macaca fascicularis of Mauritius. Am J Primatol 1987 : 13 : 435 42.
28. Menninger K, Wieczorek G, Riesen S et al. The origin of cynomolgus monkey affects the outcome of kidney allografts under neoral immunosuppression. Transplant Proc 2002 : 34 : 2887 8.
29. Terao K, Fujimoto K, Cho F, Honjo S. Inheritance and distribution of human-type A-B-O blood groups in cynomolgus monkeys. J Med Primatol 1981 : 10 : 72 80.
30. Nozawa K, Shotake T, Ohkura Y, Tanabe Y. Genetic variations within and between species of Asian macaques. Jpn J Genet 1977 : 52 : 15 30.
31. Kondo M, Kawamoto Y, Nozawa K et al. Population genetics of crab-eating macaques (Macaca fascicularis) on the island of Mauritius. Am J Primatol 1993 : 29 : 167 82.
32. Harihara S, Saitou N, Hirai M et al. Differentiation of mitochondrial DNA types in Macaca fascicularis. Primates 1988 : 29 : 117 27.
33. Lawler SH, Sussman RW, Taylor LL. Mitochondrial DNA of the mauritian macaques (Macaca fascicularis): an example of the founder effect. Am J Phys Anthropol 1995 : 96 : 133 41.
34. Tosi AJ, Morales JC, Melnick DJ. Y-chromosome and mitochondrial markers in Macaca fascicularis indicate introgression with indochinese M. mulatta and a biogeographic barrier in the isthmus of Kra. Int J Primatol 2002 : 23 : 161 78.
35. Tosi AJ, Morales JC, Melnick DJ. Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution 2003 : 57 : 1419 35.
36. Tosi AJ, Coke CS. Comparative phylogenetics offer new insights into the biogeographic history of Macaca fascicularis and the origin of the Mauritian macaques. Mol Phylogenet Evol 2007 : 42 : 498 504.
37. Blancher A, Tisseyre P, Dutaur M et al. Study of cynomolgus monkey (Macaca fascicularis) MhcDRB (Mafa-DRB) polymorphism in two populations. Immunogenetics 2006 : 58 : 269 82.
38. Fooden J. Tail length variation in Macaca fascicularis and Macaca mulatta. Primates 1997 : 38 : 221 32.
39. Fooden J. Rhesus and crab-eating macaques: intergradation in Thailand. Science 1964 : 143 : 363 5.
40. Otting N, de Groot NG, Doxiadis GGM, Bontrop RE. Extensive Mhc-DQB variation in humans and non-human primate species. Immunogenetics 2002 : 54 : 230 9.
41. Uda A, Tanabayashi K, Yamada YK et al. Detection of 14 alleles derived from the MHC class I A locus in cynomolgus monkeys. Immunogenetics 2004 : 56 : 155 63.
42. Uda A, Tanabayashi K, Fujita O, Hotta A, Terao K, Yamada A. Identification of the MHC class I B locus in cynomolgus monkeys. Immunogenetics 2005 : 57 : 189 97.
43. Doxiadis GGM, Rouweler AJM, de Groot NG et al. Extensive sharing of MHC class II alleles between rhesus and cynomolgus macaque. Immunogenetics 2006 : 10 : 1 10.
44. Krebs KC, Jin Z, Rudersdorf R, Hughes AL, O'Connor DH. Unusually high frequency MHC class I alleles in Mauritian origin cynomolgus macaques. J Immunol 2005 : 175 : 5230 9.
45. Leuchte N, Berry N, Köhler B et al. MhcDRB-sequences from cynomolgus macaque (Macaca fascicularis) of different origin. Tissue Antigens 2004 : 63 : 529 37.
46. Sano K, Shiina T, Kohara S et al. Novel cynomolgus macaque MHC-DPB1 polymorphisms in three South East Asian populations. Tissue Antigens 2006 : 67 : 297 306.
47. Penedo MCT, Bontrop RE, Heijmans CMC et al. Microsatellite typing of the rhesus macaque MHC region. Immunogenetics 2005 : 57 : 198 209.
48. Crouau-Roy B. Trans-speciation maintenance in the MHC region of a polymorphism which includes a polymorphic dinucleotide locus, and the de novo arisal of a polymorphic tetranucleotide microsatellite. Tissue Antigens 1999 : 54 : 560 4.
49. Hardy OJ, Charbonnel N, Freville H, Heuertz M. Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 2003 : 163 : 1467 82.
50. Sussman RW, Tattersall I. Behavior and ecology of Macaca fascicularis in Mauritius: a preliminary study. Primates 1981 : 22 : 192 205.
51. Stumpf MP, Goldstein DB. Demography, recombination hotspot intensity, and the block structure of linkage disequilibrium. Curr Biol 2003 : 13 : 1 8.
52. Bonhomme M, Blancher A, Crouau-Roy B. Multiplexed microsatellites for rapid identification and characterization of individuals and populations of cercopithecidae. Am J Primatol 2005 : 67 : 385 91.
53. Taberlet P, Griffin S, Goossens B et al. Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 1996 : 24 : 3189 94.
54. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F. GENETIX Version 4.05, Logiciel sous Windows TM pour la génétique des Populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000. France : université Montpellier II, Montpellier, 2004.
55. Raymond M, Rousset F. Genepop (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 1995 : 86 : 248 9.
56. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P. Microchecker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 2004 : 4 : 535 8.
57. Slatkin M. A measure of population subdivision based on microsatellite allele frequencies. Genetics 1995 : 139 : 457 62.
58. Goodman SJ. RST CALC: a collection of computer programs for calculating unbiased estimates of genetic differentiation and determining their significance for microsatellite data. Mol Ecol 1997 : 6 : 881 5.
59. Landry PA, Koskinen MT, Primmer CR. Deriving evolutionary relationships among populations using microsatellites and (deltamu)(2): all loci are equal, but some are more equal than others. Genetics 2002 : 161 : 1339 47.
60. Felsenstein J. PHYLIP (Phylogeny Inference Package) Version 3.6. Seattle : Distributed by the author Department of Genome Sciences, University of Washington, 2004.
61. Schneider S, Roessli D, Excoffier L. Arlequin Ver. 2.000: A Software for Population Genetics Data Analysis. Switzerland : Genetics and Biometry Laboratory, University of Geneva, 2000.
62. Slatkin M. Linkage disequilibrium in growing and stable populations. Genetics 1994 : 137 : 331 6.
63. Excoffier L, Slatkin M. Maximum-likelihood estimation of molecular haplotype frequencies in a diploid population. Mol Biol Evol 1995 : 12 : 921 7.
64. Slatkin M, Excoffier L. Testing for linkage disequilibrium in genotypic data using the EM algorithm. Heredity 1996 : 76 : 377 83.
65. Stephens M, Smith NJ, Donnelly P. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 2001 : 68 : 978 89.
66. Stephens M, Scheet P. Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet 2005 : 76 : 449 62.
67. Watterson GA. Homozygosity test of neutrality. Genetics 1978 : 88 : 405 17.
68. Piry S, Luikart G, Cornuet JM. Bottleneck: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 1999 : 90 : 502 3.
69. Beaumont MA, Nichols RA. Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B 1996 : 263 : 1619 26.
70. Vitalis R, Dawson K, Boursot P. Interpretation of variation across loci as evidence for selection. Genetics 2001 : 158 : 1811 23.
71. Vitalis R, Dawson K, Boursot P, Belkhir K. DetSel 1.0: a computer program to detect markers responding to selection. J Hered 2003 : 94 : 429 31.
72. Sussman RW, Tattersall I. Distribution, abundance, and putative ecological strategy of Macaca fascicularis on the island of Mauritius, southwestern indian ocean. Folia Primatol 1986 : 46 : 28 43.
73. Excoffier L, Slatkin M. Incorporating genotypes of relatives into a test of linkage disequilibrium. Am J Hum Genet 1998 : 62 : 171 80.
74. Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne RK. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci U S A 2004 : 101 : 3490 4.
75. Wiseman RW, Wojcechowskyj JA, Greene JM et al. Simian immunodeficiency virus SIVmac239 infection of major histocompatibility complex-identical cynomolgus macaques from Mauritius. J Virol 2007 : 81 : 349 61.
76. Fortin A, Stevenson MM, Gros P. Susceptibility to malaria as a complex trait: big pressure from a tiny creature. Hum Mol Genet 2002 : 11 : 2469 78.
77. Frodsham AJ, Hill AVS. Genetics of infectious diseases. Hum Mol Genet 2004 : 13 : 187 94.
78. Wheatley BP. Malaria as a possible selective factor in the speciation of macaques. J Mammal 1980 : 61 : 307 11.
79. Collins WE. Primate malarias. Adv Vet Sci Comp Med 1974 : 18 : 1 23.
80. Doxiadis GGM, Otting N, de Groot NG et al. Evolutionary stability of MHC class II haplotypes in diverse rhesus macaque populations. Immunogenetics 2003 : 55 : 540 51.
81. Crouau-Roy B, Service S, Slatkin M, Freimer N. A fine-scale comparison of the human and chimpanzee genomes: linkage, linkage disequilibrium and sequence analysis. Hum Mol Genet 1996 : 5 : 1131 7.
82. Crouau-Roy B, Clayton J. Testing two possible mechanisms for gametic association in human: frozen haplotypes and segregation distortion. Genetica 2002 : 114 : 17 23.
83. Allendorf FW, Leary RF, Spruell P, Wenburg JK. The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 2001 : 16 : 613 22.