MHC heterozygosity and survival in red junglefowl

Molecular Ecology

Volumn 19, Issue 15, 2010, Pages 3064-3075

  Worley, Kirsty ^a,b   Collet, Julie ^b   Spurgin, Lewis G ^a   Cornwallis, Charlie ^b   Pizzari, Tommaso ^b   Richardson, David S ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Heterozygote advantage; Junglefowl; Major histocompatibility complex; Overdominance; Survival

Indexed keywords

MICROSATELLITE DNA;

ANIMAL; ARTICLE; BIRD DISEASE; CHICKEN; COCCIDIOSIS; FEMALE; GENETIC VARIABILITY; GENETICS; HETEROZYGOTE; HOMOZYGOTE; IMMUNOLOGY; INNATE IMMUNITY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MORTALITY; REGRESSION ANALYSIS; STATISTICAL MODEL;

ANIMALS; BIRD DISEASES; CHICKENS; COCCIDIOSIS; FEMALE; GENETIC VARIATION; HETEROZYGOTE; HOMOZYGOTE; IMMUNITY, INNATE; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MICROSATELLITE REPEATS; MODELS, STATISTICAL; REGRESSION ANALYSIS;

AVES; GALLUS; GALLUS GALLUS; VERTEBRATA;

EID: 77954854198     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2010.04724.x     Document Type: Article

References (87)

1. Apanius V, Penn D, Slev PR et al. (1997) The nature of selection on the major histocompatibility complex. Critical Reviews in Immunology, 17, 179 224.
2. Aparicio JM, Ortego J, Cordero PJ (2006) What should we weigh to estimate heterozygosity, alleles or loci? Molecular Ecology, 15, 4659 4665.
3. Arkush (2002) Resistance to three pathogens in the endangered winter run Chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibility complex genotypes. Canadian Journal of Fisheries and Aquatic Sciences, 59, 966 975.
4. Bacon LD, Witter RL, Crittenden LB et al. (1981) B-haplotype influence on Marek's disease, Rous sarcoma, and lymphoid leukosis virus-induced tumors in chickens. Poultry Science, 60, 1132 1139.
5. Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations? Molecular Ecology, 13, 3021 3031.
6. Barribeau SM, Villinger J, Waldman B (2008) Major histocompatibility complex based resistance to a common bacterial pathogen of amphibians. PLoS ONE, 3, 2692.
7. Biedrzycka A, Radwan J (2008) Population fragmentation and major histocompatibility complex variation in the spotted suslik, Spermophilus suslicus. Molecular Ecology, 17, 4801 4811.
8. Bodmer W (1972) Evolutionary significance of the HL-A system. Nature, 237, 139 145.
9. Boyce WM, Hedrick PW, MuggliCockett NE et al. (1997) Genetic variation of major histocompatibility complex and microsatellite loci: a comparison in bighorn sheep. Genetics, 145, 421 433.
10. Briles WE, Briles RW, Taffs RE, Stone HA (1983) Resistance to a malignant-lymphoma in chickens is mapped to subregion of major histocompatibility (B) complex. Science, 219, 977 979.
11. Brouwer L, Komdeur J, Richardson DS (2007) Heterozygosity-fitness correlations in a bottlenecked island species: a case study on the Seychelles warbler. Molecular Ecology, 16, 3134 3144.
12. Bryja J, Charbonnel N, Berthier K et al. (2007) Density related changes in selection pattern for major histocompatibility complex genes in fluctuating populations of voles. Molecular Ecology, 16, 5084 5097.
13. Caron LA, Abplanalp H, Taylor RL (1997) Resistance, susceptibility, and immunity to Eimeria tenella in major histocompatibility (B) complex congenic lines. Poultry Science, 76, 677 682.
14. Carrington M, Nelson GW, Martin MP et al. (1999) HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science, 283, 1748 1752.
15. Cheng HH, Crittendon LB (1994) Microsatellite markers for genetic mapping in the chicken. Poultry Science, 73, 539 546.
16. Collins WM, Briles WE, Zsigray RM et al. (1977) B locus (MHC) in chicken-association with fate of RSV-induced tumors. Immunogenetics, 5, 333 343.
17. Coltman DW, Bowen WD, Wright JM (1998) Birth weight and neonatal survival of harbour seal pups ape positively correlated with genetic variation measured by microsatellites. Proceedings of the Royal Society of London Series B: Biological Sciences, 265, 803 809.
18. Croisetiere S, Tarte PD, Bernatchez L, Belhumeur P (2008) Identification of MHC class II beta resistance/susceptibility alleles to Aeromonas salmonicida in brook charr (Salvelinus fontinalis). Molecular Immunology, 45, 3107 3116.
19. Crooijmans RPMA, van Oers PAM, Strijk JA et al. (1996) Preliminary linkage map of the chicken (Gallus domesticus) genome based on microsatellite markers: 77 new markers mapped. Poultry Science, 75, 746 754.
20. Crooijmans RPMA, Dijkhof RJM, van der Poel JJ, Groenen MAM (1997) New microsatellite markers in chicken optimized for automated fluorescent genotyping. Animal Genetics, 28, 427 437.
21. Dawson D, McConnell S, Wardle A et al. (1998) Characterisation and mapping of 15 novel chicken microsatellite loci. Animal Genetics, 29, 159 160.
22. Dawson DA, Horsburgh GJ, Küpper C et al. (2010) New methods to identify conserved microsatellite loci and develop primer sets of high cross-species utility; as demonstrated for birds. Molecular Ecology Resources, 10, 475 494.
23. De Boer RJ, Borghans JAM, van Boven M et al. (2004) Heterozygote advantage fails to explain the high degree of polymorphism of the MHC. Immunogenetics, 55, 725 731.
24. Dionne M, Miller KM, Dodson JJ, Bernatchez L (2009) MHC standing genetic variation and pathogen resistance in wild Atlantic salmon. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences, 364, 1555 1565.
25. Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature, 256, 50 52.
26. Etches RJ (1996) Reproduction in Poultry. CAB International and Oxford University Press
27. Froeschke G, Sommer S (2005) MHC class II DRB variability and parasite load in the striped mouse (Rhabdomys pumilio) in the southern Kalahari. Molecular Biology and Evolution, 22, 1254 1259.
28. Fumihito A, Miyake T, Takada M et al. (1996) Monophyletic origin and unique dispersal patterns of domestic fowls. Proceedings of the National Academy of Sciences, USA, 93, 6792 6795.
29. Gibbs M, Dawson DA, McCamley C et al. (1997) Chicken microsatellite markers isolated from libraries enriched for simple tandem repeats. Animal Genetics, 28, 401 417.
30. Gillingham MAF, Richardson DS, Løvlie H et al. (2009) Cryptic preference for MHC dissimilar females in male red junglefowl, Gallus gallus. Proceedings of the Royal Society of London Series B: Biological Sciences, 276, 1083 1092.
31. Guillemot F, Billault A, Pourquie O et al. (1988) A molecular map of the chicken major histocompatibility complex: The class II β genes are closely linked to the class I genes and the nucleolar organiser. EMBO Journal, 7, 2775 2785.
32. Hala K, Vilhelmova M, Schulmannova J, Plachy J (1979) A new recombinant allele in the B-complex of the chicken. Folia Biologica (Praha), 25, 323 324.
33. Hala K, Chausse A, Bourlet Y et al. (1988) Attempt to detect recombination between B-F and B-L genes within the chicken B complex by serological typing, in vitro MLR, and RFLP analyses. Immunogenetics, 28, 433 438.
34. Hansson B, Richardson DS (2005) Genetic variation in two endangered Acrocephalus species compared to a widespread congener: estimates based on coding and non-coding loci. Animal Conservation, 8, 83 90.
35. Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Molecular Ecology, 11, 2467 2474.
36. Hedrick PW, Thomson G, Klitz W (1987) Evolutionary genetics and HLA: another classic example. Biological Journal of the Linnean Society, 31, 311 331.
37. Hedrick PW, Kim TJ, Parker KM (2001) Parasite resistance and genetic variation in the endangered Gila topminnow. Animal Conservation, 4, 103 109.
38. Hill AVS, Allsopp CEM, Kwiatkowski D, Anstey NM, Twumasi P, Rowe PA, Bennett S, Brewster D, McMichael AJ, Greenwood BM (1991) Common West African HLA antigens are associated with protection from severe malaria. Nature, 352, 595 600.
39. Hughes AL, Nei M (1992) Models of host-parasite interaction and MHC polymorphism. Genetics, 132, 863 864.
40. Ilmonen P, Penn DJ, Damjanovich K, Morrison L, Ghotbi L, Potts WK (2007) Major histocompatibility complex heterozygosity reduces fitness in experimentally infected mice. Genetics, 176, 2501 2508.
41. Jacob JP, Milne S, Beck S, Kaufman J (2000) The major and minor class II β-chain (B-LB) gene flank the Tapasin gene in the B-F/B-L region of the chicken major histocompatibility complex. Immunogenetics, 51, 138 147.
42. Jeffery KJ, Bangham CR (2000) Review: Do infectious diseases drive MHC diversity? Microbes and Infection, 2, 1335 1341.
43. Kaufman J, Volk H, Wallny H-J (1995) A 'minimal essential MHC' and an 'unrecognised MHC': two extremes in selection for polymorphism. Immunological Reviews, 143, 63 88.
44. Kaufman J, Jacob J, Shaw I et al. (1999a) Gene organisation determines evolution of function in the chicken MHC. Immunological Reviews, 167, 101 117.
45. Kaufman J, Milne S, Gobel TWF et al. (1999b) The chicken B locus is a minimal essential major histocompatibility complex. Nature, 401, 923 925.
46. Kekäläinen J, Vallunen JA, Primmer CR et al. (2009) Signals of major histocompatibility complex overdominance in a wild salmonid population. Proceedings of the Royal Society of London Series B: Biological Sciences, 276, 3133 3140.
47. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends in Ecology and Evolution, 17, 230 241.
48. Kempenaers B (2007) Mate choice and genetic quality: a review of the heterozygosity theory. Advances in the Study of Behavior, 37, 189 278.
49. Kenta T, Gratten J, Haigh NS et al. (2008) Multiplex SNP-SCALE: a cost-effective medium-throughput single nucleotide polymorphism genotyping method. Molecular Ecology Notes, 8, 1230 1238.
50. Kim DK, Lillehoj HS, Hong YH et al. (2008) Immune-related gene expression in two B-Complex disparate genetically inbred Fayoumi chicken lines following Eimeria maxima infection. Poultry Science, 87, 433 443.
51. Klein J (1986) Natural History of the Major Histocompatibility Complex. John Wiley and Sons
52. Koch C, Skjødt K, Toivanen A, Toivanen P (1983) New recombinants within the MHC (B-complex) of the chicken. Tissue Antigens, 21, 129 137.
53. Langefors A, Lohm J, Grahn M, Andersen O, von Schantz T (2001) Association between major histocombatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proceedings of the Royal Society of London Series B: Biological Sciences, 268, 479 485.
54. Loiseau C, Zoorob R, Garnier S et al. (2008) Antagonistic effects of a Mhc class I allele on malaria-infected house sparrows. Ecology Letters, 11, 258 265.
55. Mainguy J, Worley K, Cote SD, Coltman DW (2007) Low MHC DRB class II diversity in the mountain goat: past bottlenecks and possible role of pathogens and parasites. Conservation Genetics, 8, 885 891.
56. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology, 7, 639 655.
57. McClelland EE, Granger DL, Potts WK (2003a) Major histocompatibility complex-dependent susceptibility to Cryptococcus neoformans in mice. Infection and Immunity, 71, 4815 4817.
58. McClelland EE, Penn DJ, Potts WK (2003b) Major histocompatibility complex heterozygote superiority during coinfection. Infection and Immunity, 71, 2079 2086.
59. McConnell SKJ, Dawson DA, Wardle A, Burke TA (1999) The isolation and mapping of 19 tetranucleotide microsatellite markers in the chicken. Animal Genetics, 30, 183 189. (Pubitemid 29355057)
60. McDonald V, Shirley MW (2009) Past and future: vaccination against Eimeria. Parasitology, 136, 1477 1489.
61. McDougald LR (2008) In: Diseases of Poultry, 12th edn (ed. Saif YM). Wiley-Blackwell
62. Meyer D, Thomson G (2001) How selection shapes variation of the human major histocompatibility complex: a review. Annals of Human Genetics, 65, 1 26.
63. Meyer-Lucht Y, Sommer S (2005) MHC diversity and the association to nematode parasitism in the yellow-necked mouse (Apodemus flavicollis). Molecular Ecology, 14, 2233 2243.
64. Miller HC, Miller KM, Daugherty CH (2008) Reduced MHC variation in a threatened tuatara species. Animal Conservation, 11, 206 214.
65. Navarro P, Visscher PM, Knott SA et al. (2005) Mapping of quantitative trait loci affecting organ weights and blood variables in a broiler layer cross. British Poultry Science, 46, 430 442.
66. Oliver MK, Telfer S, Piertney SB (2009) Major histocompatibility complex (MHC) heterozygote superiority to natural multi-parasite infections in the water vole (Arvicola terrestris). Proceedings of the Royal Society of London Series B: Biological Sciences, 276, 1119 1128.
67. van Oosterhout C, Joyce DA, Cummings SM et al. (2006) Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulate). Evolution, 60, 2562 2574.
68. Paterson S, Wilson K, Pemberton JM (1998) Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Evolution, 95, 3714 3719.
69. Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility genes. The American Naturalist, 153, 145 164.
70. Penn DJ, Damjanovich K, Potts WK (2002) MHC heterozygosity confers a selective advantage against multiple-strain infections. Proceedings of the National Academy of Sciences, USA, 99, 11260 11264.
71. Quinnell RJ, Kennedy LJ, Barnes A et al. (2003) Susceptibility to visceral Leishmaniasis in the domestic dog is associated with MHC class II polymorphism. Immunogenetics, 55, 23 28.
72. Raymond M, Rousset F (1995) GENEPOP (Version-1.2)-population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248 249.
73. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conservation Biology, 17, 230 237.
74. Richardson DS, Westerdahl H (2003) MHC diversity in two Acrocephalus species: The outbred great reed warbler and the inbred Seychelles warbler. Molecular Ecology, 12, 3523 3529.
75. Richardson DS, Komdeur J, Burke TA, von Schantz T (2005) MHC based patterns of social and extra pair mate choice in the Seychelles warbler. Proceedings of the Royal Society of London Series B: Biological Sciences, 272, 759 767.
76. Schierman LW, Watanabe DH, McBride RA (1977) Genetic control of Rous sarcoma regression in chickens: linkage with the major histocompatibility complex. Immunogenetics, 5, 325 332.
77. Shaw I, Powell TA, Marston DA et al. (2007) Different evolutionary histories of the two classical class I gene BF1 and BF2 illustrate drift and selection within the stable MHC haplotypes of chickens. Journal of Immunology, 178, 5744 5752.
78. Skjødt K, Koch C, Crone M, Simonsen M (1985) Analysis of chickens for recombination with the MHC (B complex). Tissue Antigens, 25, 278 282.
79. Slate J, David P, Dodds KG et al. (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: Theoretical expectations and empirical data. Heredity, 93, 255 265.
80. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proceedings of the Royal Society of London Series B: Biological Sciences, 277, 979 988.
81. Sunnocks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution, 13, 510 524.
82. Takahata N, Nei M (1990) Allelic genealogy under overdominant and frequency dependent selection and polymorphism of major histocompatibility complex loci. Genetics, 124, 967 978.
83. Thursz MR, Thomas HC, Greenwood BM, Hill AV (1997) Heterozygote advantage for HLA class-II type in hepatitis B virus infection. Nature Genetics, 17, 11 12.
84. Wallny H-J, Avila D, Hunt LG et al. (2006) Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC-determined response to Rous sarcoma virus in chickens. Proceedings of the National Academy of Sciences, USA, 103, 1434 1439.
85. Wedekind C, Walker M, Little T (2005) The course of malaria in mice: Major histocompatibility complex (MHC) effects, but no general MHC heterozygote advantage in single-strain infections. Genetics, 170, 1427 1430.
86. Westerdahl H, Hansson B, Bensch S, Hasselquist D (2004) Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? Journal of Evolutionary Biology, 17, 485 492.
87. Worley K, Gillingham M, Jensen P et al. (2008) Single locus typing of MHC class I and class II B loci in a population of red junglefowl. Immunogenetics, 60, 233 247.