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MHC class I and MHC class II DRB gene variability in wild and captive Bengal tigers (Panthera tigris tigris)

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An Erratum to this article was published on 14 December 2010

Abstract

Bengal tigers are highly endangered and knowledge on adaptive genetic variation can be essential for efficient conservation and management. Here we present the first assessment of allelic variation in major histocompatibility complex (MHC) class I and MHC class II DRB genes for wild and captive tigers from India. We amplified, cloned, and sequenced alpha-1 and alpha-2 domain of MHC class I and beta-1 domain of MHC class II DRB genes in 16 tiger specimens of different geographic origin. We detected high variability in peptide-binding sites, presumably resulting from positive selection. Tigers exhibit a low number of MHC DRB alleles, similar to other endangered big cats. Our initial assessment—admittedly with limited geographic coverage and sample size—did not reveal significant differences between captive and wild tigers with regard to MHC variability. In addition, we successfully amplified MHC DRB alleles from scat samples. Our characterization of tiger MHC alleles forms a basis for further in-depth analyses of MHC variability in this illustrative threatened mammal.

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References

  • Amadou C (1999) Evolution of the MHC class I region: the framework hypothesis. Immunogenetics 49:362–367

    Article  CAS  PubMed  Google Scholar 

  • Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on major histocompatibility complex. Crit Rev Immunol 17:179–224

    CAS  PubMed  Google Scholar 

  • Beck TW, Menninger J, Voigt G, Newmann K, Nishigaki Y, Nash WG, Stephens RM, Wang Y, de Jong P, O’Brien SJ, Yuhki N (2001) Comparative feline genomics: a BAC/PAC contig map of the major histocompatibility class II region. Genomics 71:282–295

    Article  CAS  PubMed  Google Scholar 

  • Beck TW, Menninger J, Murphy WJ, Nash WG, O’Brien SJ, Yuhki N (2005) The feline major histocompatibility complex is rearranged by an inversion with a breakpoint in the distal class I region. Immunogenetics 56:702–709

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bjorkman PM, Parham P (1990) Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem 59:253–288

    Article  CAS  PubMed  Google Scholar 

  • Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33–39

    Article  CAS  PubMed  Google Scholar 

  • Casola C, Hahn MW (2009) Gene conversion among paralogs results in moderate false detection of positive selection using likelihood methods. J Mol Evol 68:679–687

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Graumann MB, DeRose SA, Ostrander EA, Storb R (1998) Polymorphism analysis of four canine MHC class I genes. Tissue Antigens 51:374–381

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hedrick PW (1994) Evolutionary genetics of the major histocompatibility complex. Am Nat 143:945–964

    Article  Google Scholar 

  • Hedrick PW (2002) Pathogen resistance and genetic variation at MHC loci. Evolution 56:1902–1908

    PubMed  Google Scholar 

  • Hendrickson SL, Mayer GC, Wallen EP, Quigley K (2000) Genetic variability and geographic structure of three subspecies of tigers (Panthera tigris) based on MHC class I variation. Anim Conserv 3:135–143

    Article  Google Scholar 

  • Herrington S (1987) Subspecies and the conservation of Panthera tigris. In: Tilson RL, Seal US (eds) Tigers of the world: the biology, biopolitics, management and conservation of an endangered species. Noyes, Park Ridge, pp 51–60

    Google Scholar 

  • Hughes AL, Hughes MK (1995) Natural selection on the peptide-binding regions of major histocompatibility complex molecules. Immunogenetics 42:233–243

    Article  CAS  PubMed  Google Scholar 

  • Hughes AL, Nei M (1989a) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Nat Acad Sci USA 86:958–962

    Article  CAS  PubMed  Google Scholar 

  • Hughes AL, Nei M (1989b) Evolution of the major histocompatibility complex: independent origin of nonclassical class I genes in different groups of mammals. Mol Biol Evol 6:559–579

    CAS  PubMed  Google Scholar 

  • Huson DH (1998) SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73

    Article  CAS  PubMed  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267, www.splitstree.org

    Article  CAS  PubMed  Google Scholar 

  • Jackson P (1997) The status of the tiger in 1997 and threats in the future. Cat News 27:8–10

    CAS  Google Scholar 

  • Jhala YV, Gopal R, Qureshi Q (2008) Status of the tigers, co-predators, and prey in India. National Tiger Conservation Authority, Government of India, New Dehli, Wildlife Institute of India Dehradun, TR 08/001, 151

  • Judo MSB, Wedel AB, Wilson C (1998) Stimulation and suppression of PCR-mediated recombination. Nucleic Acids Res 26:1819–1825

    Article  CAS  PubMed  Google Scholar 

  • Kaufman J, Salomonsen J, Flajnik M (1994) Evolutionary conservation of MHC class I and class II molecules—different yet the same. Semin Immunol 6:411–424

    Article  CAS  PubMed  Google Scholar 

  • Kennedy LJ, Ryvar R, Gaskell RM, Addie DD, Willoughby K, Carter SD, Thomson W, Ollier WER, Radford AD (2002) Sequence analysis of MHC DRB alleles in domestic cats from the United Kingdom. Immunogenetics 54:348–352

    Article  CAS  PubMed  Google Scholar 

  • Kennedy LJ, Ryvar R, Brown JJ, Ollier WER, Radford AD (2003) Resolution of complex feline leukocyte antigen DRB loci by reference strand-mediated conformational analysis (RSCA). Tissue Antigens 62:313–323

    Article  CAS  PubMed  Google Scholar 

  • Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York

    Google Scholar 

  • Klein J (1997) Immunology. Blackwell Science, Oxford

    Google Scholar 

  • Klein J, Bontrop RE, Dawkins RL et al (1990) Nomenclature for the major histocompatibility complex in different species: a proposal. Immunogenetics 31:217–219

    CAS  PubMed  Google Scholar 

  • Knapp LA (2005) Facts, faeces and setting the standards for the study of MHC genes using noninvasive samples. Mol Ecol 14:1597–1599

    Article  CAS  PubMed  Google Scholar 

  • Korber B (2000) HIV Signature and sequence variation analysis. In: Rodrigo AG, Learn GH (eds) Computational analysis of HIV molecular sequences, chapter 4. Kluwer Academic, The Netherlands, pp 55–72

    Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  PubMed  Google Scholar 

  • Kuwahara Y, Kitoh K, Kobayashi R, Iwata J, Ohne R, Hosokawa-Kanai T, Matsumoto Y, Kitagawa H, Sasaki Y (2000) Genotyping of feline MHC (FLA) class II DRB by PCR-RFLP method using group-specific primers. J Vet Med Sci 62:1283–1289

    Article  CAS  PubMed  Google Scholar 

  • Lenz TL, Becker S (2008) Simple approach to reduce PCR artifact formation leads to reliable genotyping of MHC and other highly polymorphic loci—implications for evolutionary analysis. Gene 427:117–123

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lukas D, Vigilant L (2005) Reply: facts, faeces and setting the standards for the study of MHC genes using noninvasive samples. Mol Ecol 14:1601–1602

    Article  Google Scholar 

  • Lukas D, Bradley BJ, Nsubuga AM, Doran-Sheehy D, Robbins MM, Vigilant L (2004) Major histocompatibility complex and microsatellite variation in two populations of wild gorillas. Mol Ecol 13:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Luo SJ, Kim JH, Johnson WE et al (2004) Phylogeography and genetic ancestry of tigers (Panthera tigris). PLoS Biol 2:2275–2293

    CAS  Google Scholar 

  • Mazak V (1981) Panthera tigris. Mamm Species 152:1–8

    Article  Google Scholar 

  • Meyers LA, Bull JJ (2002) Fighting change with change: adaptive variation in an uncertain world. Trends Ecol Evol 17:551–557

    Article  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Nielson R, Yang Z (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929–936

    Google Scholar 

  • O’Brien SJ, Yuhki N (1999) Comparative genome organization of the major histocompatibility complex: lessons from the Felidae. Immunol Rev 167:133–144

    Article  PubMed  Google Scholar 

  • O’Brien SJ, Wildt DE, Goldman D, Merril CR, Bush M (1983) The cheetah is depauperate in genetic variation. Science 221:459–462

    Article  PubMed  Google Scholar 

  • Ouborg NJ, Pertoldi C, Loeschcke V, Bijlsma R, Hedrick PW (2010) Conservation genetics in transition to conservation genomics. Trends Genet 26:177–187

    Article  CAS  PubMed  Google Scholar 

  • Pääbo S, Irwin DM, Wilson AC (1990) DNA damage promotes jumping between templates during enzymatic amplification. J Biol Chem 265:4718–47121

    PubMed  Google Scholar 

  • Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sharma R, Stuckas H, Bhaskar R, Rajput S, Khan I, Goyal SP, Tiedemann R (2009) mtDNA indicates profound population structure in Indian tiger (Panthera tigris tigris). Conserv Genet 10:909–914

    Article  CAS  Google Scholar 

  • Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:1–18

    Article  Google Scholar 

  • Wan QH, Zhu L, Wu H, Fang SG (2006) Major histocompatibility complex class II variation in giant panda (Ailuropoda melanoleuca). Mol Ecol 15:2441–2450

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Wu X, Yan P, Zheng S (2008) Sequence variability analysis on major histocompatibility complex class II DRB alleles in three felines. Front Biol China 3:55–62

    Article  Google Scholar 

  • Wei K, Zhang Z, Wang X, Zhang W, Xu X, Shen F, Yue B (2010) Lineage pattern, trans-species polymorphism, and selection pressure among major lineages of feline MHC-DRB peptide-binding region. Immunogenetics 62:307–317

    Article  CAS  PubMed  Google Scholar 

  • Wong WS, Yang Z, Goldman N, Nielsen R (2004) Accuracy and power of statistical methods detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168:1041–1051

    Article  CAS  PubMed  Google Scholar 

  • Yang Z (2000) Phylogenetic analysis by maximum likelihood (PAML), version 3.0. University College London, London, http://abacus.gene.ucl.ac.uk/software/paml.html

    Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  CAS  PubMed  Google Scholar 

  • Yuhki N, O’Brien SJ (1990a) DNA variation of the mammalian major histocompatibility complex reflects genomic diversity and population history. Proc Natl Acad Sci USA 87:836–840

    Article  CAS  PubMed  Google Scholar 

  • Yuhki N, O’Brien SJ (1990b) DNA recombination and natural selection pressure sustain genetic sequence diversity of the feline MHC class I genes. J Exp Med 172:621–630

    Article  CAS  PubMed  Google Scholar 

  • Yuhki N, O’Brien SJ (1994) Exchanges of short polymorphic DNA segments predating speciation in feline major histocompatibility complex class I genes. J Mol Evol 39:22–33

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Yuhki N, Beck T, Stephens RM, Nishigaki Y, Newmann K, O’Brien SJ (2003) Comparative genome organization of human, murine, and feline MHC class II region. Genome Res 13:1169–1179

    Article  CAS  PubMed  Google Scholar 

  • Yuhki N, Mullikin JC, Beck T, Stephens R, O’Brien SJ (2008) Sequences, annotation and single nucleotide polymorphism of major histocompatibility complex in the domestic cat. PLoS ONE 3(7):e2674. doi:10.1371/journal.pone.0002674

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Carolin Doering, Madlen Stange, and Fanny Wegner for laboratory help. Financial support is acknowledged from the University of Potsdam. We would like to express sincere thanks to Shri P.R. Sinha, Director and Dr. V.B. Mathur, Dean of the Wildlife Institute of India for providing all required support for the work on tiger genetics. We thank two anonymous reviewers for helpful comments on the manuscript.

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Correspondence to Ralph Tiedemann.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s00251-010-0496-2

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Pokorny, I., Sharma, R., Goyal, S.P. et al. MHC class I and MHC class II DRB gene variability in wild and captive Bengal tigers (Panthera tigris tigris). Immunogenetics 62, 667–679 (2010). https://doi.org/10.1007/s00251-010-0475-7

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