Evolutionary genetics of MHC class II beta genes in the brown hare, Lepus europaeus
Tóm tắt
The genes of the major histocompatibility complex (MHC) are attractive candidates for investigating the link between adaptive variation and individual fitness. High levels of diversity at the MHC are thought to be the result of parasite-mediated selection and there is growing evidence to support this theory. Most studies, however, target just a single gene within the MHC and infer any evidence of selection to be representative of the entire gene region. Here we present data from three MHC class II beta genes (DPB, DQB, and DRB) for brown hares in two geographic regions and compare them against previous results from a class II alpha-chain gene (DQA). We report moderate levels of diversity and high levels of population differentiation in the DQB and DRB genes (Na = 11, D
est = 0.071 and Na = 15, D
est = 0.409, respectively), but not for the DPB gene (Na = 4, D
est = 0.00). We also detected evidence of positive selection within the peptide binding region of the DQB and DRB genes (95% CI, ω > 1.0) but found no signature of selection for DPB. Mutation and recombination were both found to be important processes shaping the evolution of the class II genes. Our findings suggest that while diversifying selection is a significant contributor to the generally high levels of MHC diversity, it does not act in a uniform manner across the entire MHC class II region. The beta-chain genes that we have characterized provide a valuable set of MHC class II markers for future studies of the evolution of adaptive variation in Leporids.
Tài liệu tham khảo
Acevedo-Whitehouse K, Cunningham AA (2006) Is MHC enough for understanding wildlife immunogenetics? Trends Ecol Evol 21:433–438
Aguilar A, Roemer G, Debenham S et al (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 101:3490–3494
Alcaide M, Edwards SV, Negro JJ, Serrano D, Tella JL (2008) Extensive polymorphism and geographical variation at a positively selected MHC class II B gene of the lesser kestrel (Falco naumanni). Mol Ecol 17:2652–2665
Amills M, Ramirez O, Tomas A, Obexer-Ruff G, Vidal O (2008) Positive selection on mammalian MHC-DQ genes revisited from a multispecies perspective. Genes Immunol 9:651
Anmarkrud JA, Johnsen A, Bachmann L, Lifjeld JT (2010) Ancestral polymorphism in exon 2 of bluethroat (Luscinia svecica) MHC class II B genes. J Evol Biol 23:1206–1217
Averdam A, McClure G, Suraj V et al (1992) Polymorphism, recombination, and linkage disequilibrium within the HLA class II region. J Immunol 148:249–258
Averdam A, Kuschal C, Otto N et al (2010) Sequence analysis of the grey mouse lemur (Microcebus murinus) MHC class II DQ and DR region. Immunogenetics 63:1–9
Awadalla P, Eyre-Walker A, Smith JM (1999) Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science 286:2524–2525
Begovich A, McClure G, Suraj V et al (1992) Polymorphism, recombination, and linkage disequilibrium within the HLA class II region. J Immunol 148:249–258
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
Bodmer JG, Marsh SGE, Albert ED et al (1999) Nomenclature for factors of the HLA system, 1998. Tissue Antigens 53:407–446
Bondinas G, Moustakas A, Papadopoulos G (2007) The spectrum of HLA-DQ and HLA-DR alleles, 2006: a listing correlating sequence and structure with function. Immunogenetics 59:539–553
Brown JH, Jardetzky TS, Gorga JC et al (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33–39
Bryja J, Galan M, Charbonnel N, Cosson JF (2006) Duplication, balancing selection and trans-species evolution explain the high levels of polymorphism of the DQA MHC class II gene in voles (Arvicolinae). Immunogenetics 58:191–202
Campos JL, Bellocq JGd, Schaschl H, Suchentrunk F (2011) MHC class II DQA gene variation across cohorts of brown hares (Lepus europaeus) from eastern Austria: testing for different selection hypotheses. Mamm Biol Z Saugetierkunde 76:251–257
Chouchane L, Kindt T (1992) Mapping of the rabbit MHC reveals that class I genes are adjacent to the DR subregion and defines an insertion/deletion-related polymorphism in the class II region. J Immunol 149:1216–1222
Čížková D, Goüy de Bellocq J, Baird SJE, Piálek J, Bryja J (2011) Genetic structure and contrasting selection pattern at two major histocompatibility complex genes in wild house mouse populations. Heredity 106(5):727–740
Evans ML, Neff BD, Heath DD (2010) MHC genetic structure and divergence across populations of Chinook salmon (Oncorhynchus tshawytscha). Heredity 104:449–459
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resourc 10:564–567
Fearnhead P, Donnelly P (2001) Estimating recombination rates from population genetic data. Genetics 159:1299–1318
Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722
Gomez D, Conejeros P, Marshall SH, Consuegra S (2010) MHC evolution in three salmonid species: a comparison between class II alpha and beta genes. Immunogenetics 62:531–542
Göritz F, Faßbender M, Broich A et al (2001) Untersuchungen zur reproduktiven Fitness lebender weiblicher Feldhasen aus unterschiedlichen Habitaten. Z Jagdwissenschft 47:92
Goüy de Bellocq J, Suchentrunk F, Baird S, Schaschl H (2009) Evolutionary history of an MHC gene in two leporid species: characterisation of Mhc-DQA in the European brown hare and comparison with the European rabbit. Immunogenetics 61:131–144
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis rogram for Windows 95/98/NT. Nucl. Acids. Symp. Ser. 41:95–98
Hartl GB, Suchentrunk F, Willing R, Petznek R (1995) Allozyme heterozygosity and fluctuating asymmetry in the brown hare (Lepus europaeus): a test of the developmental homeostasis hypothesis. Philos Trans R Soc Lond B Biol Sci 350:313–323
Hudson RR (2001) Two-locus sampling distributions and their application. Genetics 159:1805–1817
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026
Kasapidis P, Suchentrunk F, Magoulas A, Kotoulas G (2005) The shaping of mitochondrial DNA phylogeographic patterns of the brown hare (Lepus europaeus) under the combined influence of Late Pleistocene climatic fluctuations and anthropogenic translocations. Mol Phylogenet Evol 34:55–66
Klein J, Kasahara M, Gutknecht J, Figueroa F (1990) Origin and function of mhc polymorphism. Chem Immunol 49:35–50
Ladle RJ (1992) Parasites and sex: catching the red queen. Trends Ecol Evol 7:405–408
Loiseau C, Richard M, Garnier S et al (2009) Diversifying selection on MHC class I in the house sparrow (Passer domesticus). Mol Ecol 18:1331–1340
McVean G, Awadalla P, Fearnhead P (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231–1241
Oliver MK, Piertney SB (2006) Isolation and characterization of a MHC class II DRB locus in the European water vole (Arvicola terrestris). Immunogenetics 58:390–395
Petersdorf EW, Gooley T, Malkki M et al (2001) The biological significance of HLA-DP gene variation in haematopoietic cell transplantation. Br J Haematol 112:988–994
Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21
Rousset F (2008) GENEPOP'007: A complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8:103–106
Schad J, Sommer S, Ganzhorn JU (2004) MHC variability of a small lemur in the littoral forest fragments of southeastern Madagascar. Conservation Genetics 5:299–309
Schaschl H, Wandeler P, Suchentrunk F, Obexer-Ruff G, Goodman SJ (2006) Selection and recombination drive the evolution of MHC class II DRB diversity in ungulates. Heredity 97:427–437
Schaschl H, Tobler M, Plath M, Penn DJ, Schlupp I (2008) Polymorphic MHC loci in an asexual fish, the amazon molly (Poecilia formosa; Poeciliidae). Mol Ecol 17:5220–5230
Smith S, Mang T, Goüy de Bellocq J et al (2010) Homozygosity at a class II MHC locus depresses female reproductive ability in European brown hares. Mol Ecol 19:4131–4143
Stamatis C, Suchentrunk F, Moutou KA et al (2009) Phylogeography of the brown hare (Lepus europaeus) in Europe: a legacy of south-eastern Mediterranean refugia? J Biogeogr 36:515–528
Stern LJ, Brown JH, Jardetzky TS et al (1994) Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza virus peptide. Nature 368:215–221
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24:1596–1599
Trowsdale J (1995) ‘Both man and bird and beast’: comparative organization of MHC genes. Immunogenetics 41:1–17
Wibbelt G, Frölich K (2005) Infectious diseases in European brown hare (Lepus europaeus). Wildl Biol Pract 1:86–93
Wilson DJ, McVean G (2006) Estimating diversifying selection and functional constraint in the presence of recombination. Genetics 172:1411–1425