Cheetah paradigm revisited: MHC diversity in the world's largest free-ranging population

Molecular Biology and Evolution

Volumn 28, Issue 4, 2011, Pages 1455-1468

  Castro Prieto, Aines ^a   Wachter, Bettina ^a   Sommer, Simone ^a  

^a LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

Author keywords

Acinonyx jubatus; diversity; free ranging cheetahs; MHC class I; MHC class II DRB; positive selection

Indexed keywords

GENOMIC DNA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ALLELE; ARTICLE; CHEETAH; CLONING; COMPARATIVE STUDY; DISEASE PREDISPOSITION; EXON; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; IMMUNOGENETICS; INTRON; NAMIBIA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; SINGLE STRAND CONFORMATION POLYMORPHISM;

ACINONYX; AMINO ACID SEQUENCE; ANIMALS; DISEASE SUSCEPTIBILITY; GENES, MHC CLASS II; GENETIC VARIATION; GENETICS, POPULATION; GENOTYPE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT;

ACINONYX JUBATUS; FELIDAE; MAMMALIA;

EID: 79952849168     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq330     Document Type: Article

References (118)

1. Acevedo-Whitehouse K, Cunningham AA. 2006. Is MHC enough for understanding wildlife immunogenetics? Trends Ecol. Evol. 21: 433-438. (Pubitemid 44066618)
2. Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne R. 2004. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA. 101:3490-3494. (Pubitemid 38338222)
3. Altizer S, Foufopoulos J, Gager A. 2001. Conservation and diseases. In: Levin SA editor. Encyclopedia of Biodiversity. San Diego (CA): Academic Press. p. 109-126.
4. Altizer S, Harvell D, Friedle E. 2003. Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol Evol. 18:589-596. (Pubitemid 37240485)
5. Amos W, Harwood J. 1998. Factors affecting levels of genetic diversity in natural populations. Philos Trans R Soc Lond Ser B. 353:177-186. (Pubitemid 128713029)
6. Axtner J, Sommer S. 2009. Validation of internal reference genes for quantitative real-time PCR in a non-model organism, the yellow-necked mouse, Apodemus flavicollis. BMC Res. Notes 2:264.
7. Babik W, Durka W, Radwan J. 2005. Sequence diversity of the MHC DRB gene in the Eurasian beaver (Castor fiber). Mol Ecol. 14: 4249-4257. (Pubitemid 44943707)
8. Bernatchez L, Landry C. 2003. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol. 16:363-377. (Pubitemid 36567968)
9. Bjorkman PJ, Parham P. 1990. Structure, function, and diversity of classi major histocompatibility complex-molecules. Annu Rev Biochem. 59:253-288.
10. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC. 1987. The foreign antigen-binding site and T-Cell recognition regions of classi histocompatibility antigens. Nature 329:512-518. (Pubitemid 17131094)
11. Bowen L, Aldridge B, Beckmen K, Gelatt T, Rea L, Burek K, Pitcher K, Stott JL. 2006. Differential expression of immune response genes in Steller sea lions (Eumetopias jubatus): an indicator of ecosystem health? Ecohealth 3:109-113. (Pubitemid 44198394)
12. Bowen L, Aldridge BM, Gulland F, Van Bonn W, DeLong R, Melin S, Lowenstine LJ, Stott JL, Johnson ML. 2004. Class II multiformity generated by variable MHC-DRB region configurations in the California sea lion (Zalophus californianus). Immunogenetics 56: 12-27. (Pubitemid 38626418)
13. Brandley MC, Schmitz A, Reeder TW. 2005. Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Syst Biol. 54:373-390. (Pubitemid 41040438)
14. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC. 1993. Three-dimensional structure of the human classiI histocompatibility antigen HLA-DR1. Nature 364:33-39. (Pubitemid 23233452)
15. Caro TM. 1994. Cheetahs of the Serengeti plains: group living in an asocial species. Chicago: The University of Chicago Press.
16. Caro TM, Laurenson MK. 1994. Ecological and genetic-factors in conservation-a cautionary tale. Science 263:485-486.
17. Caughley G. 1994. Directions in conservation biology. J Anim Ecol. 63:215-244.
18. Cereb N, Hughes AL, Yang SY. 1997. Locus-specific conservation of the HLA class I introns by intra-locus homogenization. Immu-nogenetics 47:30-36. (Pubitemid 28062031)
19. Cereb N, Kong Y, Lee S, Maye P, Yang SY. 1996. Nucleotide sequences of MHC class I introns 1, 2, and 3 in humans and intron 2 in nonhuman primates. Tissue Antigens. 47:498-511. (Pubitemid 26184117)
20. Doherty PC, Zinkernagel RM. 1975. Biological role for major histocompatibility antigens. Lancet 1:1406-1409.
21. Drake GJC, Kennedy LJ, Auty HK, Ryvar R, Ollier WER, Kitchener AC, Freeman AR, Radford AD. 2004. The use of reference strand-mediated conformational analysis for the study of cheetah (Acinonyx jubatus) feline leucocyte antigen class II DRB polymorphisms. Mol Ecol. 13:221-229. (Pubitemid 38119098)
22. Driscoll CA, Menotti-Raymond M, Nelson G, Goldstein D, O'Brien SJ. 2002. Genomic microsatellites as evolutionary chronometers: a test in wild cats. Genome Res. 12:414-423. (Pubitemid 34233016)
23. Edwards S, Potts W. 1996. Polymorphism of genes in the major histocompatibility complex: implications for conservation genetics of vertebrates. In: Smith T, Wayne R, editors. Molecular genetic approaches in conservation. New York: Oxford University Press. p. 214-237.
24. Ejsmond MJ, Radwan J. 2009. Mhc diversity in bottlenecked populations: a simulation model. Conserv Genet. doi:10.1007/s10592-009-9998-6.
25. Ellegren H, Hartman G, Johansson M, Andersson L. 1993. Major histocompatibility complex monomorphism and low-levels of DNA-fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proc Natl Acad Sci USA. 90: 8150-8153. (Pubitemid 23260873)
26. Evermann JF, Heeney JL, Roelke ME, Mckeirnan AJ, O'Brien SJ. 1988. Biological and pathological consequences of feline infectious peritonitis virusinfection in the cheetah. Arch Virol. 102:155-171.
27. Frankham R. 1995a. Effective population size/adult sizes ratios in wildlife: a review. Genet Res. 66:95-107.
28. Frankham R. 1995b. Inbreeding and extinction-a threshold effect. Conserv Biol. 9:792-799.
29. Frankham R, Ballou JD, Briscoe DA. 2002. Introduction to Conservation Genetics. Cambridge. Cambridge University Press.
30. Freeman AR, Machugh DE, McKeown S, Walzer C, McConnell DJ, Bradley DG. 2001. Sequence variation in the mitochondrial DNA control region of wild African cheetahs (Acinonyx jubatus). Heredity 86:355-362. (Pubitemid 32722475)
31. Froeschke G, Sommer S. 2005. MHC class II DRB variability and parasite load in the striped mouse (Rhabdomys pumilio) in the Southern Kalahari. Mol Biol Evol. 22:1254-1259. (Pubitemid 40577763)
32. Garrigan D, Hedrick PW. 2003. Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707-1722. (Pubitemid 37096389)
33. Giese AR, Hedrick PW. 2003. Genetic variation and resistance to a bacterial infection in the endangered Gila topminnow. Anim Conserv. 6:369-377. (Pubitemid 40281163)
34. Gutierrez-Espeleta GA, Hedrick PW, Kalinowski ST, Garrigan D, Boyce WM. 2001. Is the decline of desert bighorn sheep from infectious disease the result of low MHC variation? Heredity 86:439-450. (Pubitemid 32745305)
35. Hanssen L, Stander P. 2004. Namibia Large Carnivore Atlas Report vol. 1. Windhoek (Namibia): Predator Conservation Trust, Ministry of Environment and Tourism, Division of Speciality Support Services.
36. Hedrick PW. 1994. Evolutionary genetics of the major histocom-patibility complex. Am Nat. 143:945-964. (Pubitemid 2107801)
37. Hedrick PW. 2002. Pathogen resistance and genetic variation at MHC loci. Evolution. 56:1902-1908. (Pubitemid 35302002)
38. Hedrick PW. 2003a. A heterozygote advantage. Science 302:57.
39. Hedrick PW. 2003b. The major histocompatibility complex (MHC) in declining populations: an example of adaptive variation. In: Holt W, Pickard A, Rodger J, Wildt D, editors. Reproduction science and integrated conservation. Cambridge: Cambridge University Press. p. 97-113.
40. Hedrick PW, Lee RN, Garrigan D. 2002. Major histocompatibility complex variation in red wolves: evidence for common ancestry with coyotes and balancing selection. Mol Ecol. 11:1905-1913.
41. Hedrick PW, Lee RN, Parker KM. 2000. Major histocompatibility complex (MHC) variation in the endangered Mexican wolf and related canids. Heredity 85:617-624. (Pubitemid 32200620)
42. Hedrick PW, Parker KM, Gutierrez-Espeleta GA, Rattink A, Lievers K. 2000. Major histocompatibility complex variation in the Arabian oryx. Evolution 54:2145-2151. (Pubitemid 32113840)
43. Heeney JL, Evermann JF, McKeirnan AJ, Marker-Kraus L, Roelke ME, Bush M, Wildt DE, Meltzer DG, Colly L, Lukas J. 1990. Prevalence and implications of feline coronavirus infections of captive and free-ranging cheetahs (Acinonyx jubatus). J Virol. 64:1964-1972. (Pubitemid 20148437)
44. Hill AVS. 1998. The immunogenetics of human infectious diseases. Annu Rev Immunol. 16:593-617.
45. Hughes AL. 2000. Evolution of introns and exons of class II major histocompatibility complex genes of vertebrates. Immunogenet-ics 51:473-486. (Pubitemid 30265038)
46. Hughes AL, Nei M. 1988. Pattern of nucleotide substitution at major histocompatibility complex classi loci reveals overdominant selection. Nature 335:167-170.
47. Hughes AL, Nei M. 1989. Nucleotide substitution at major histocompatibility complex classiI loci-evidence for over-dominant selection. Proc Natl Acad Sci USA. 86:958-962. (Pubitemid 19056271)
48. Jarvi SI, Tarr CL, McIntosh CE, Atkinson CT, Fleischer RC. 2004. Natural selection of the major histocompatibility complex (MHC) in Hawaiian honeycreepers (Drepanidinae). Mol Ecol. 13: 2157-2168. (Pubitemid 38946407)
49. Jepson A, Banya W, SisayJoof F, HassanKing M, Nunes C, Bennett S, Whittle H. 1997. Quantification of the relative contribution of major histocompatibility complex (MHC) and non-MHC genes to human immune responses to foreign antigens. Infect Immun. 65:872-876. (Pubitemid 27087984)
50. Jukes TH, Cantor CR. 1969. Evolution of protein molecules. In: Munro HN, editor. Mammalian protein metabolism. New York: Academic Press. p. 21-132.
51. Kelly MJ, Laurenson MK, FitzGibbon CD, Collins DA, Durant SM, Frame GW, Bertram BCR, Caro TM. 1998. Demography of the Serengeti cheetah (Acinonyx jubatus) population: the first 25 years. J Zool. 244:473-488. (Pubitemid 28235923)
52. Kelley J, Walter R, Trowsdale J. 2005. Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683-695. (Pubitemid 40174963)
53. Kennedy LJ, Angles JM, Barnes A, Carmichael LF, Radford AD, Ollier WER, Happ GM. 2007. DLA-DRBI, DQAI, and DQBI alleles and haplotypes in North American gray wolves. J Hered. 98: 491-499. (Pubitemid 47357591)
54. Klein J. 1986. Natural History of the Major Histocompatibility Complex. New York: Wiley.
55. Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI. 1990. Nomenclature for the major histocompatibility complexes of different species-a proposal. Immunogenetics 31:217-219. (Pubitemid 20132749)
56. Klein J, Sato A, Nagl S, O'hUiǵn C. 1998. Molecular trans-species polymorphism. Annu. Rev. Ecol. Syst. 29:1-21. (Pubitemid 29033024)
57. Klein J, Sato A, OhUigin C. 1998. Evolution by gene duplication in the major histocompatibility complex. Cytogenet. Cell Genet. 80: 123-127. (Pubitemid 28330371)
58. Kumar S, Tamura K, Nei M. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinformatics. 5:150-163.
59. Laurenson MK, Caro TM, Gros P, Wielebnowski N. 1995. Controversial cheetahs? Nature 377:392.
60. 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. Conserv Genet. 8: 885-891. (Pubitemid 47104533)
61. Marker-Kraus LL, Kraus D, Barnett D, Hurlbut S. 1996. Cheetah survival on Namibian farmlands. Windhoek (Namibia): Cheetah Conservation Fund.
62. Marker LL, Mills MGL, Macdonald DW. 2003. Factors influencing perceptions of conflict and tolerance towards cheetahs on Namibian farmlands. Conserv Biol. 17:1290-1298. (Pubitemid 37250069)
63. Marker LL, Wilkerson AJP, Sarno RJ, Martenson J, Breitenmoser- Würsten C, O'Brien SJ, Warren EJ. 2008. Molecular genetic insights on cheetah (Acinonyx jubatus) ecology and conservation in Namibia. J Hered. 99:2-13. (Pubitemid 351261483)
64. Marsden CD, Mable BK, Woodroffe R, Rasmussen GSA, Cleaveland S, McNutt JW, Emmanuel M, Thomas R, Kennedy LJ. 2009. Highly endangered African wild dogs (Lycaon pictus) lack variation at the major histocompatibility complex. J Hered. 100:S54-S65.
65. May RM. 1995. The cheetah controversy. Nature 374:309-310.
66. Menotti-Raymond M, O'Brien SJ. 1993. Dating the genetic bottleneck of the African cheetah. Proc Natl Acad Sci USA. 90:3172-3176. (Pubitemid 23111327)
67. Menotti-Raymond MA, O'Brien SJ. 1995. Evolutionary conservation of ten microsatellite loci in four species of Felidae. J Hered. 86: 319-322.
68. Merola M. 1994. A reassessment of homozygosity and the case for inbreeding depression in the cheetah, Acinonyx jubatus: implications for conservation. Conserv Biol. 8:961-971.
69. Meyer-Lucht Y, Sommer S. 2005. MHC diversity and the association to nematode parasitism in the yellow-necked mouse (Apodemus flavicollis). Mol Ecol. 14:2233-2243. (Pubitemid 40772435)
70. Mikko S, Andersson L. 1995. Low major histocompatibility complex classiI diversity in European and North-American moose. Proc Natl Acad Sci USA. 92:4259-4263.
71. Mikko S, Roed K, Schmutz S, Andersson L. 1999. Monomorphism and polymorphism at MHC DRB loci in domestic and wild ruminants. Immunol Rev. 167:169-178. (Pubitemid 29178979)
72. Miller HC, Lambert DM. 2004. Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol Ecol. 13:3709-3721. (Pubitemid 39569048)
73. Monaghan MT, Inward DJG, Hunt T, Vogler AP. 2007. A molecular phylogenetic analysis of the Scarabaeinae (dung beetles). Mol Phylogenet Evol. 45:674-692. (Pubitemid 47532746)
74. Munson L, Marker L, Dubovi E, Spencer JA, Evermann JF, O'Brien SJ. 2004. Serosurvey of viral infections in free-ranging Namibian cheetahs (Acinonyx jubatus). J Wildl Dis. 40:23-31. (Pubitemid 39026751)
75. Munson L, Terio KA, Worley M, Jago M, Bagot-Smith A, Marker L. 2005. Extrinsic factors significantly affect patterns of disease in free-ranging and captive cheetah (Acinonyx jubatus) populations. J Wildl Dis. 41:542-548. (Pubitemid 41622858)
76. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 3:418-426. (Pubitemid 16010523)
77. Nichols R. 2001. Gene trees and species trees are not the same. Trends Ecol Evol. 16:358-364. (Pubitemid 32525776)
78. O'Brien SJ. 1994. The cheetah's conservation controversy. Conserv Biol. 8:1153-1155.
79. O'Brien SJ, Evermann JF. 1988. Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol. 3:254-259.
80. O'Brien SJ, Roelke ME, Marker L, Newman A, Winkler CA, Meltzer D, Colly L, Evermann JF, Bush M, Wildt DE. 1985. Genetic basis for species vulnerability in the cheetah. Science 227:1428-1434.
81. O'Brien SJ, Wildt DE, Bush M. 1986. The cheetah in genetic peril. Sci Am. 254:84-92.
82. O'Brien SJ, Wildt DE, Bush M, Caro TM, Fitzgibbon C, Aggundey I, Leakey RE. 1987. East-African cheetahs-evidence for two population bottlenecks. Proc Natl Acad Sci USA. 84:508-511. (Pubitemid 17006224)
83. O'Brien SJ, Wildt DE, Goldman D, Merril CR, Bush M. 1983. The cheetah is depauperate in genetic variation. Science 221: 459-462.
84. O'Brien SJ, Yuhki N. 1999. Comparative genome organization of the major histocompatibility complex: lessons from the Felidae. Immunol Rev. 167:133-144. (Pubitemid 29178976)
85. Orita M, Iwahana H, Kanazawa H, Hayashi K, Sekiya T. 1989. Detection of polymorphisms of human DNA by gel electropho-resis as single-strand conformation polymorphisms. Proc Natl Acad Sci USA. 86:2766-2770. (Pubitemid 19112622)
86. Piertney SB, Oliver MK. 2006. The evolutionary ecology of the major histocompatibility complex. Heredity 96:7-21.
87. Pokorny I, Sharma R, Goyal SP, Mishra S, Tiedemann R. 2010. MHC class I and MHC class II DRB gene variability in wild and captive Bengal tigers (Panthera tigris tigris). Immunogenetics 62:667-679.
88. Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818. (Pubitemid 28552116)
89. Radwan J, Biedrzycka A, Babik W. 2010. Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv. 143:537-544.
90. Radwan J, Kawalko A, Wójcik JM, Babik W. 2007. MHC-DRB3 variation in a free-living population of the European bison, Bison bonasus. Mol Ecol. 16:531-540. (Pubitemid 46161077)
91. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. (Pubitemid 37038874)
92. Sachdev M, Sankaranarayanan R, Reddanna P, Thangaraj K, Singh L. 2005. Major histocompatibility complex class I polymorphism in Asiatic lions. Tissue Antigens. 66:9-18. (Pubitemid 40942708)
93. Satta Y. 1993. How the ratio of nonsynonymous to synonymous pseudogene substitutions can be less than one. Immunogenetics 38:450-454. (Pubitemid 23290973)
94. Satta Y, Ohuigin C, Takahata N, Klein J. 1994. Intensity of natural selection at the major histocompatibility complex loci. Proc Natl Acad Sci USA. 91:7184-7188. (Pubitemid 24226827)
95. Schad J, Sommer S. 2005. Parasite burden and constitution of major histocompatibility complex in the Malagasy mouse lemur. Microcebus murinus. Evolution 59:439-450. (Pubitemid 40356055)
96. Siddle HV, Kreiss A, Eldridge MDB, Noonan E, Clarke CJ, Pyecroft S, Woods GM, Belov K. 2007. Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc Natl Acad Sci USA. 104:16221-16226. (Pubitemid 350099388)
97. Sommer S. 2003. Effects of habitat fragmentation and changes of dispersal behaviour after a recent decline on the genetic variability of noncoding and coding DNA of a monogamous Malagasy rodent. Mol Ecol. 12:2845-2851. (Pubitemid 37195919)
98. Sommer S. 2005. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool. 2:16.
99. Sommer S, Schwab D, Ganzhorn JU. 2002. MHC diversity of endemic Malagasy rodents in relation to geographic range and social system. Behav Ecol Sociobiol. 51:214-221. (Pubitemid 36064238)
100. Stern LJ, Wiley DC. 1994. Antigenic peptide binding by classi and classiI histocompatibility proteins. Structure 2:245-251.
101. Storz JF, Ramakrishnan U, Alberts SC. 2002. Genetic effective size of a wild primate population: influence of current and historical demography. Evolution 54:817-829. (Pubitemid 34519792)
102. Trachtenberg E, Vinson M, Hayes E, Hsu YM, Houtchens K, Erlich H, Klitz W, Hsia Y, Hollenbach J. 2007. HLA class I (A, B, C) and class II (DRB1, DQA1, DQB1, DPB1) alleles and haplotypes in the Han from southern China. Tissue Antigens. 70:455-463. (Pubitemid 350075785)
103. Sunnucks P, Wilson ACC, Beheregaray LB, Zenger K, French J, Taylor AC. 2000. SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology. Mol Ecol. 9:1699-1710.
104. Swofford DL. 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sunderland (MA): Sinauer Associates.
105. Terio KA, Marker L, Munson L. 2004. Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function. J Wildl Dis. 40:259-266. (Pubitemid 39047944)
106. Thalwitzer S, Wachter B, Robert N, Wibbelt G, Muller T, Lonzer J, Meli ML, Bay G, Hofer H. 2010. Seroprevalences to viral pathogens in free-ranging and captive cheetahs (Acinonyx jubatus) on Namibian farmland. Clin Vaccine Immunol. 17:232-238.
107. Wakeland EK, Boehme S, She JX, Lu CC, McIndoe RA, Cheng I, Ye Y, Potts WK. 1990. Ancestral polymoprhisms of MHC class II genes: divergent allele advantage. Immunol Res. 9:115-122. (Pubitemid 20109685)
108. Wang X, Wei K, Zhang Z, Xu X, Zhang W, Shen F, Zhang L, Yue B. 2009. Major histocompatibility complex class II DRB exon-2 diversity of the Eurasian lynx (Lynx lynx) in China. J Nat Hist. 43:245-257.
109. Weber DS, Stewart BS, Schienman J, Lehman N. 2004. Major histocompatibility complex variation at three class II loci in the northern elephant seal. Mol Ecol. 13:711-718. (Pubitemid 38260951)
110. Weyrich A, Axtner J, Sommer S. 2010. Selection and validation of reference genes for real-time RT-PCR studies in the non-model species Delomys sublineatus, an endemic Brazilian roedent. Biochem Biophys Res Commun. 392:145-149.
111. Yuhki N, Beck T, Stephens R, Neelam B, O'Brien SJ. 2007. Comparative genomic structure of human, dog, and cat MHC: HLA, DLA, and FLA. J Hered. 98:390-399. (Pubitemid 47357595)
112. Yuhki N, Heidecker GF, O'Brien SJ. 1989. Characterization of MHC cDNA clones in the domestic cat - diversity and evolution of classi genes. J Immunol. 142:3676-3682. (Pubitemid 19137506)
113. Yuhki N, Mullikin JC, Beck T, Stephens R, O'Brien SJ. 2008. Sequences, annotation and single nucleotide polymorphism of the major histocompatibility complex in the domestic cat. PLoS One. 3:e2674.
114. Yuhki N, O'Brien SJ. 1990a. DNA recombination and natural selection pressure sustain genetic sequence diversity of the Feline MHC classi genes. J Exp Med. 172:621-630. (Pubitemid 20248403)
115. Yuhki N, O'Brien SJ. 1990b. DNA variation of the mammalian major histocompatibility complex reflects genomic diversity and population history. Proc Natl Acad Sci USA. 87:836-840. (Pubitemid 20051466)
116. Yuhki N, O'Brien SJ. 1994. Exchanges of short polymorphic DNA segments predating speciation in feline major histocompatibility complex classi genes. J Mol Evol. 39:22-33. (Pubitemid 24181121)
117. Yuhki N, O'Brien SJ. 1997. Nature and origin of polymorphism in feline MHC class II DRA and DRB genes. J Immunol. 158: 2822-2833. (Pubitemid 127470542)
118. Zhang C, Anderson A, DeLisi C. 1998. Structural principles that govern the peptide-binding motifs of class I MHC molecules. J Mol Biol. 281:929-947. (Pubitemid 28408439)