Diverse MHC IIB allele repertoire increases parasite resistance and body condition in the long-tailed giant rat (Leopoldamys sabanus)

BMC Evolutionary Biology

Volumn 9, Issue 1, 2009, Pages

  Lenz, Tobias L ^a,b   Wells, Konstans ^c   Pfeiffer, Martin ^c   Sommer, Simone ^a,d  

^a UNIVERSITY OF HAMBURG   (Germany)

^b MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

^c UNIVERSITY OF ULM   (Germany)

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

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2B; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ALLELE; ANIMAL EXPERIMENT; ANIMAL PARASITOSIS; ARTICLE; BODY CONSTITUTION; BORNEO; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOTE; INFECTION RESISTANCE; LEOPOLDAMYS SABANUS; MURIDAE; NONHUMAN; NUCLEOTIDE SEQUENCE; RAT; ANIMAL; DNA SEQUENCE; GENE; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; HOST PARASITE INTERACTION; INNATE IMMUNITY; MOLECULAR EVOLUTION; MURINAE; PARASITE IDENTIFICATION; PARASITOLOGY; SINGLE STRAND CONFORMATION POLYMORPHISM;

LEOPOLDAMYS; LEOPOLDAMYS SABANUS; RATTUS; VERMES; VERTEBRATA;

ALLELES; ANIMALS; BORNEO; EVOLUTION, MOLECULAR; GENES, MHC CLASS II; HETEROZYGOTE; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; MURINAE; PARASITE EGG COUNT; POLYMORPHISM, GENETIC; POLYMORPHISM, SINGLE-STRANDED CONFORMATIONAL; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 72149127649     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-9-269     Document Type: Article

References (93)

1. Sexual reproduction as an adaptation to resist parasites (a review). WD Hamilton R Axelrod R Tanese, Proc Natl Acad Sci USA 1990 87 9 3566 3573 10.1073/pnas.87.9.3566 2185476
2. Sex against virulence: the coevolution of parasitic diseases. D Ebert WD Hamilton, Trends Ecol Evol 1996 11 2 79 82 10.1016/0169-5347(96)81047-0
3. The nature of selection on the major histocompatibility complex. V Apanius D Penn PR Slev LR Ruff WK Potts, Crit Rev Immunol 1997 17 2 179 224 9094452
4. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years. L Bernatchez C Landry, J Evol Biol 2003 16 3 363 377 10.1046/j.1420-9101.2003.00531.x 14635837
5. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. S Sommer, Front Zool 2005 2 1 16 10.1186/1742-9994-2-16 16242022
6. The major histocompatibility complex, sexual selection, and mate choice. M Milinski, Annu Rev Ecol Evol Syst 2006 37 1 159 186 10.1146/annurev.ecolsys. 37.091305.110242 (Pubitemid 44907616)
7. J Klein, Natural history of the major histocompatibility complex 1986
8. The evolutionary ecology of the major histocompatibility complex. SB Piertney MK Oliver, Heredity 2005 96 1 7 21
9. Evolution of diversity at the major histocompatibility complex. WK Potts EK Wakeland, Trends Ecol Evol 1990 5 6 181 187 10.1016/0169-5347(90)90207-T
10. Evolution and ecology of MHC molecules: From genomics to sexual selection. SV Edwards PW Hedrick, Trends Ecol Evol 1998 13 8 305 311 10.1016/S0169-5347(98)01416-5 (Pubitemid 28368430)
11. Parasitic exploitation as an engine of diversity. K Summers S McKeon J Sellars M Keusenkothen J Morris D Gloeckner C Pressley B Price H Snow, Biol Rev 2003 78 639 675 10.1017/S146479310300616X 14700394
12. Maintenance of histocompatibility polymorphisms. B Clarke DRS Kirby, Nature 1966 211 5052 999 1000 10.1038/211999a0 6007869
13. Evolutionary significance of the HL-A system. WF Bodmer, Nature 1972 237 5351 139 183 10.1038/237139a0 4113158
14. Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. N Takahata M Nei, Genetics 1990 124 4 967 978 2323559
15. A new evolutionary law. L Van Valen, Evol Theor 1973 1 1 30
16. Common west African HLA antigens are associated with protection from severe malaria. AV Hill CE Allsopp D Kwiatkowski NM Anstey P Twumasi PA Rowe S Bennett D Brewster AJ McMichael BM Greenwood, Nature 1991 352 6336 595 600 10.1038/352595a0 1865923
17. Association between an MHC class II allele and clearance of hepatitis B virus in the Gambia. MR Thursz D Kwiatkowski CE Allsopp BM Greenwood HC Thomas AV Hill, N Engl J Med 1995 332 16 1065 1069 10.1056/NEJM199504203321604 7898524
18. Association between major histocompatibility complex class II DRB alleles and parasite load in the hairy-footed gerbil, Gerbillurus paeba, in the southern Kalahari. R Harf S Sommer, Mol Ecol 2005 14 85 91 10.1111/j.1365-294X. 2004.02402.x 15643953
19. MHC diversity and the association to nematode parasitism in the yellow-necked mouse (Apodemus flavicollis). Y Meyer-Lucht S Sommer, Mol Ecol 2005 14 7 2233 2243 10.1111/j.1365-294X.2005.02557.x 15910340
20. Associations between malaria and MHC genes in a migratory songbird. H Westerdahl J Waldenstrom B Hansson D Hasselquist T von Schantz S Bensch, Proc R Soc Lond B Biol Sci 2005 272 1571 1511 1518 10.1098/rspb.2005.3113 (Pubitemid 41414709)
21. Inverse associations of human leukocyte antigen and malaria parasite types in two West African populations. K Young A Frodsham OK Doumbo S Gupta A Dolo JT Hu KJH Robson A Crisanti AVS Hill SC Gilbert, Infect Immun 2005 73 2 953 955 10.1128/IAI.73.2.953-955.2005 15664937
22. Neutral versus adaptive genetic variation in parasite resistance: importance of major histocompatibility complex supertypes in a free-ranging primate. N Schwensow J Fietz KH Dausmann S Sommer, Heredity 2007 99 265 277 10.1038/sj.hdy.6800993 17519969
23. Antagonistic effects of a Mhc class I allele on malaria-infected house sparrows. C Loiseau R Zoorob S Garnier J Birard P Federici R Julliard G Sorci, Ecol Lett 2008 11 3 258 265 10.1111/j.1461-0248.2007.01141.x 18070099
24. Enhanced immunological surveillance in mice heterozygous at H-2 gene complex. PC Doherty RM Zinkernagel, Nature 1975 256 5512 50 52 10.1038/256050a0 1079575
25. Evolution of the Major Histocompatibility Complex. J Klein F Figueroa, Crit Rev Immunol 1986 6 4 295 386 3536303
26. MHC heterozygosity confers a selective advantage against multiple-strain infections. DJ Penn K Damjanovich WK Potts, Proc Natl Acad Sci USA 2002 99 17 11260 11264 10.1073/pnas.162006499 12177415
27. Parasite selection for immunogenetic optimality. KM Wegner M Kalbe J Kurtz TBH Reusch M Milinski, Science 2003 301 5638 1343 1343 10.1126/science.1088293 12958352
28. The course of malaria in mice: Major histocompatibility complex (MHC) effects, but no general MHC heterozygote advantage in single-strain infections. C Wedekind M Walker TJ Little, Genetics 2005 170 3 1427 1430 10.1534/genetics.105.040683 15911576
29. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. AL Hughes M Nei, Nature 1988 335 6186 167 170 10.1038/335167a0 3412472
30. Nucleotide substitution at major histocompatibility complex class-II loci - evidence for overdominant selection. AL Hughes M Nei, Proc Natl Acad Sci USA 1989 86 3 958 962 10.1073/pnas.86.3.958 2492668
31. Effect of human leukocyte antigen heterozygosity on infectious disease outcome: the need for allele-specific measures. M Lipsitch CT Bergstrom R Antia, BMC Med Genet 2003 4 2 10.1186/1471-2350-4-2 12542841
32. Major histocompatibility complex heterozygosity reduces fitness in experimentally infected mice. P Ilmonen DJ Penn K Damjanovich L Morrison L Ghotbi WK Potts, Genetics 2007 176 4 2501 2508 10.1534/genetics.107.074815 17603099
33. Heterozygote advantage fails to explain the high degree of polymorphism of the MHC. RJ De Boer JA Borghans M van Boven C Kesmir FJ Weissing, Immunogenetics 2004 55 11 725 731 10.1007/s00251-003-0629-y 14722686
34. Ancestral polymorphisms of MHC class-II genes - divergent allele advantage. EK Wakeland S Boehme JX She CC Lu RA McIndoe I Cheng Y Ye WK Potts, Immunol Res 1990 9 2 115 122 10.1007/BF02918202 2189934
35. Global patterns in biodiversity. KJ Gaston, Nature 2000 405 6783 220 227 10.1038/35012228 10821282
36. Movement trajectories and habitat partitioning of small mammals in logged and unlogged rain forests on Borneo. K Wells M Pfeiffer MB Lakim EKV Kalko, J Anim Ecol 2006 75 5 1212 1223 10.1111/j.1365-2656.2006.01144.x 16922857
37. Diverstiy, dynamics and spacing patterns of a small mammal community in a primary rainforest in Sabah, Malaysia. Comparing an arboreal and terrestrial habitat. K Wells, MSc-thesis Würzburg: Julius-Maximilian-University 2002
38. Distribution, relative abundance, food habits, and parasite patterns of giant rats (Rattus) in West Malaysia. BL Lim, J Mammal 1970 51 4 730 740 10.2307/1378298 5530310
39. Effects of rain forest logging on species richness and assemblage composition of small mammals in Southeast Asia. K Wells EKV Kalko MB Lakim M Pfeiffer, J Biogeogr 2007 34 6 1087 1099 10.1111/j.1365-2699.2006.01677.x (Pubitemid 47074543)
40. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman, Nucl Acids Res 1997 25 17 3389 3402 10.1093/nar/25.17.3389 9254694
41. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. JH Brown TS Jardetzky JC Gorga LJ Stern RG Urban JL Strominger DC Wiley, Nature 1993 364 6432 33 39 10.1038/364033a0 8316295
42. Statistical tests of selective neutrality in the age of genomics. R Nielsen, Heredity 2001 86 641 647 10.1046/j.1365-2540.2001.00895.x 11595044
43. Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level. AL Hughes, Heredity 2007 99 4 364 373 10.1038/sj.hdy.6801031 17622265
44. Ensembl: Dog Genome release 52. http://dec2008.archive.ensembl.org/Canis- familiaris/
45. Frequent segmental sequence exchanges and rapid gene duplication characterize the MHC class I genes in lemurs. Y Go Y Satta Y Kawamoto G Rakotoarisoa A Randrianjafy N Koyama H Hirai, Immunogenetics 2003 55 7 450 461 10.1007/s00251-003-0613-6 14530885
46. Recent duplication and inter-locus gene conversion in major histocompatibility class II genes in a teleost, the three-spined stickleback. TB Reusch H Schaschl KM Wegner, Immunogenetics 2004 56 6 427 437 10.1007/s00251-004-0704-z 15322775
47. Linkage relationships and haplotype polymorphism among cichlid Mhc class II B loci. E Malaga-Trillo Z Zaleska-Rutczynska B McAndrew V Vincek F Figueroa H Sultmann J Klein, Genetics 1998 149 3 1527 1537 9649539
48. Major histocompatibility complex class II polymorphisms in primates. RE Bontrop N Otting NG de Groot GGM Doxiadis, Immunol Rev 1999 167 1 339 350 10.1111/j.1600-065X.1999.tb01403.x 10319272
49. Variation analysis and gene annotation of eight MHC haplotypes: The MHC haplotype project. R Horton R Gibson P Coggill M Miretti RJ Allcock J Almeida S Forbes JGR Gilbert K Halls JL Harrow, et al. Immunogenetics 2008 60 1 1 18 10.1007/s00251-007-0262-2 18193213
50. Class II multiformity generated by variable MHC-DRB region configurations in the California sea lion (Zalophus californianus). L Bowen BM Aldridge F Gulland W Bonn R DeLong S Melin LJ Lowenstine JL Stott ML Johnson, Immunogenetics 2004 56 1 12 27 10.1007/s00251-004-0655-4 14997355
51. Unprecedented polymorphism of MHC-DRB region configurations in rhesus macaques. GGM Doxiadis N Otting NG de Groot R Noort RE Bontrop, J Immunol 2000 164 6 3193 3199 10706710
52. HLA DNA Typing. HA Erlich TL Bugawan, PCR Protocols New York: Academic Press, Innis MA, Gelfand DH, Sninsky JJ, White TJ, 1990 261 271
53. MHC variability of a small lemur in the littoral forest fragments of Southeastern Madagascar. J Schad S Sommer JU Ganzhorn, Conserv Genet 2004 5 3 299 309 10.1023/B:COGE.0000031137.50239.d3 (Pubitemid 38983078)
54. MHC class II DRB variability and parasite load in the striped mouse (Rhabdomys pumilio) in the southern Kalahari. G Froeschke S Sommer, Mol Biol Evol 2005 22 5 1254 1259 10.1093/molbev/msi112 15703235
55. Major histocompatibility complex variation in Talas Tuco-Tucos: The influence of demography on selection. AP Cutrera EA Lacey, J Mammal 2006 87 4 706 716 10.1644/05-MAMM-A-383R1.1 (Pubitemid 44353347)
56. Gene duplication, allelic diversity, selection processes and adaptive value of MHC class II DRB genes of the bank vole, Clethrionomys glareolus. J Axtner S Sommer, Immunogenetics 2007 59 5 417 426 10.1007/s00251-007-0205-y 17351770
57. The genomic sequence and comparative analysis of the rat major histocompatibility complex. P Hurt L Walter R Sudbrak S Klages I Muller T Shiina H Inoko H Lehrach E Gunther R Reinhardt, et al. Genome Res 2004 14 4 631 639 10.1101/gr.1987704 15060004
58. Coevolutionary relationship between helminth diversity and MHC class II polymorphism in rodents. J Goüy De Bellocq N Charbonnel S Morand, J Evol Biol 2008 21 4 1144 1150 10.1111/j.1420-9101.2008.01538.x 18462313
59. MHC class II beta sequence diversity in the deer mouse (Peromyscus maniculatus): Implications for models of balancing selection. AD Richman LG Herrera D Nash, Mol Ecol 2001 10 12 2765 2773 11903890
60. 'Good genes as heterozygosity': The major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). C Landry D Garant P Duchesne L Bernatchez, Proc R Soc Lond B Biol Sci 2001 268 1473 1279 1285 10.1098/rspb.2001.1659 (Pubitemid 32622382)
61. MHC-mediated mate choice increases parasite resistance in salmon. S Consuegra C Garcia de Leaniz, Proc R Soc Lond B Biol Sci 2008 275 1641 1397 1403 10.1098/rspb.2008.0066 (Pubitemid 351653009)
62. Compatibility counts: MHC-associated mate choice in a wild promiscuous primate. N Schwensow M Eberle S Sommer, Proc R Soc Lond B Biol Sci 2008 275 1634 555 564 10.1098/rspb.2007.1433 (Pubitemid 351156528)
63. The MHC and non-random mating in a captive population of Chinook salmon. BD Neff SR Garner JW Heath DD Heath, Heredity 2008 101 2 175 185 10.1038/hdy.2008.43 18506203
64. HLA supertypes and supermotifs: a functional perspective on HLA polymorphism. A Sette J Sidney, Curr Opin Immunol 1998 10 4 478 482 10.1016/S0952-7915(98)80124-6 9722926
65. Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. A Langefors J Lohm M Grahn O Andersen T von Schantz, Proc R Soc Lond B Biol Sci 2001 268 1466 479 485 10.1098/rspb.2000.1378 (Pubitemid 32250783)
66. Major histocompatibility alleles associated with local resistance to malaria in a passerine. C Bonneaud J Perez-Tris P Federici O Chastel G Sorci, Evolution 2006 60 2 383 389 16610328
67. MHC polymorphism under host-pathogen coevolution. JA Borghans JB Beltman RJ De Boer, Immunogenetics 2004 55 11 732 739 10.1007/s00251-003-0630-5 14722687
68. Impact of rain-forest logging on helminth assemblages in small mammals (Muridae, Tupaiidae) from Borneo. K Wells LR Smales EKV Kalko M Pfeiffer, J Trop Ecol 2007 23 35 43 10.1017/S0266467406003804 (Pubitemid 46095780)
69. Guidelines of the American Socitey of Mammalogists for the use of wild animals in research. WL Gannon RS Sikes The animal care and use committee of the American Society of Mammalogists, J Mammal 2007 88 3 809 823 10.1644/06-MAMM-F-185R1.1 (Pubitemid 47001236)
70. D Thienpont F Rochette O Vanparijs, Diagnosing helminthiasis by coprological examination Beerse, Belgium: Janssen Research Foundation 1986
71. Parasitism, predation and survival of hen red grouse Lagopus lagopus scoticus in spring. R Moss IB Trenholm A Watson R Parr, J Anim Ecol 1990 59 2 631 642 10.2307/4885
72. Life-history covariation in intestinal nematodes of mammals. A Skorping AF Read AE Keymer, Oikos 1991 60 3 365 372 10.2307/3545079
73. Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. LJ Seivwright SM Redpath F Mougeot L Watt PJ Hudson, J Helminthol 2004 78 1 69 76 10.1079/JOH2003220 14972040
74. Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. T Gillespie, Int J Primatol 2006 27 4 1129 1143 10.1007/s10764-006-9064-x (Pubitemid 44610615)
75. PCR-SSCP: A method for detection of mutations. K Hayashi, Genet Anal: Tech Appl 1992 9 3 73 79 1476794
76. Screening techniques for detecting allelic variation in DNA sequences. EP Lessa G Applebaum, Mol Ecol 1993 2 2 119 129 10.1111/j.1365-294X.1993.tb00006.x 8180734
77. SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology. P Sunnucks ACC Wilson LB Beheregaray K Zenger J French AC Taylor, Mol Ecol 2000 9 11 1699 1710 10.1046/j.1365-294x.2000.01084.x 11091307
78. Major histocompatibility complex (MHC) class II polymorphism and paternity in the monogamous Hypogeomys antimena, the endangered, largest endemic Malagasy rodent. S Sommer H Tichy, Mol Ecol 1999 8 1259 1272 10.1046/j.1365-294X.1999.00687.x 10447867
79. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. TB Reusch MA Haberli PB Aeschlimann M Milinski, Nature 2001 414 6861 300 302 10.1038/35104547 11713527
80. MHC variability, life-traits and parasite diversity of European cyprinid fish. A Simkova E Ottova S Morand, Evol Ecol 2006 20 5 465 477
81. DNA sequencing with chain-terminating inhibitors. F Sanger S Nicklen AR Coulson, Proc Natl Acad Sci USA 1977 74 12 5463 5467 10.1073/pnas.74.12.5463 271968
82. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. T Hall, Nucleic Acids Symp Ser 1999 41 95 98
83. Statistical tests for detecting gene conversion. S Sawyer, Mol Biol Evol 1989 6 5 526 538 2677599
84. Evaluation of methods for detecting recombination from DNA sequences: Empirical data. D Posada, Mol Biol Evol 2002 19 5 708 717 11961104
85. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. K Tamura J Dudley M Nei S Kumar, Mol Biol Evol 2007 24 8 1596 1599 10.1093/molbev/msm092 17488738
86. Prospects of inferring very large phylogenies by using the neighbor-joining method. K Tamura M Nei S Kumar, Proc Natl Acad Sci USA 2004 101 11030 11035 10.1073/pnas.0404206101 15258291
87. Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. K Tamura M Nei, Mol Biol Evol 1993 10 3 512 526 8336541
88. PAML 4: Phylogenetic Analysis by Maximum Likelihood. Z Yang, Mol Biol Evol 2007 24 8 1586 1591 10.1093/molbev/msm088 17483113
89. Statistical methods for detecting molecular adaptation. ZH Yang JP Bielawski, Trends Ecol Evol 2000 15 12 496 503 10.1016/S0169-5347(00)01994-7 11114436
90. Restitution of mass-size residuals: Validating body condition indices. AI Schulte-Hostedde B Zinner JS Millar GJ Hickling, Ecology 2005 86 1 155 163 10.1890/04-0232
91. Condition indices for conservation: new uses for evolving tools. RD Stevenson WA Woods Jr, Integr Comp Biol 2006 46 6 1169 1190 10.1093/icb/icl052 (Pubitemid 44739903)
92. R Development Core Team, R: A language and environment for statistical computing Vienna, Austria: R Foundation for Statistical Computing 2007
93. W Venables B Ripley, Modern Applied Statistics with S New York: Springer 4 2002