Advertisement

Immunogenetics

, Volume 69, Issue 1, pp 49–61 | Cite as

Egernia stokesii (gidgee skink) MHC I positively selected sites lack concordance with HLA peptide binding regions

  • Sarah K. Pearson
  • C. Michael Bull
  • Michael G. Gardner
Original Article

Abstract

Genes of the major histocompatibility complex (MHC) play an important role in vertebrate disease resistance, kin recognition and mate choice. Mammalian MHC is the most widely characterised of all vertebrates, and attention is often given to the peptide binding regions of the MHC because they are presumed to be under stronger selection than non-peptide binding regions. For vertebrates where the MHC is less well understood, researchers commonly use the amino acid positions of the peptide binding regions of the human leukocyte antigen (HLA) to infer the peptide binding regions within the MHC sequences of their taxon of interest. However, positively selected sites within MHC have been reported to lack correspondence with the HLA in fish, frogs, birds and reptiles including squamates. Despite squamate diversity, the MHC has been characterised in few snakes and lizards. The Egernia group of scincid lizards is appropriate for investigating mechanisms generating MHC variation, as their inclusion will add a new lineage (i.e. Scincidae) to studies of selection on the MHC. We aimed to identify positively selected sites within the MHC of Egernia stokesii and then determine if these sites corresponded with the peptide binding regions of the HLA. Six positively selected sites were identified within E. stokesii MHC I, only two were homologous with the HLA. E. stokesii positively selected sites corresponded more closely to non-lizard than other lizard taxa. The characterisation of the MHC of more intermediate taxa within the squamate order is necessary to understand the evolution of the MHC across all vertebrates.

Keywords

MHC Peptide binding region Positively selected sites Squamata Scincidae Egernia stokesii 

Notes

Acknowledgments

We thank volunteers for assistance with field surveys; Kathy Saint and Terry Bertozzi for assistance with laboratory work; and Katina Krasnec for assistance with bioinformatics. We undertook laboratory components of this work at the South Australian Research Facility for Molecular Ecology and Evolution, Adelaide. Funding from The Field Naturalists Society of South Australia and the Sir Mark Mitchell Research Foundation supported this work.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution at which the studies were conducted.

References

  1. Acevedo-Whitehouse K, Cunningham AA (2006) Is MHC enough for understanding wildlife immunogenetics? TRENDS Ecol Evolut 21:433–438CrossRefGoogle Scholar
  2. Alcaide M, Liu M, Edwards SV (2013) Major histocompatibility complex class I evolution in songbirds: universal primers, rapid evolution and base compositional shifts in exon 3. PeerJ 1:e86CrossRefPubMedPubMedCentralGoogle Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi: 10.1016/S0022-2836(05)80360-2 CrossRefPubMedGoogle Scholar
  4. Ansari TH (2016) The distribution of genetic variation in sleepy lizards. Flinders University of South Australia, AdelaideGoogle Scholar
  5. Ansari TH, Bertozzi T, Miller RD, Gardner MG (2015) MHC in a monogamous lizard—characterization of class I MHC genes in the Australian skink Tiliqua rugosa. Dev Comp Immunol 53:320–327CrossRefPubMedGoogle Scholar
  6. Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17:179–224CrossRefPubMedGoogle Scholar
  7. Babik W (2010) Methods for MHC genotyping in non-model vertebrates. Mol Ecol Resour 10:237–251CrossRefPubMedGoogle Scholar
  8. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300Google Scholar
  9. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377CrossRefPubMedGoogle Scholar
  10. 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. doi: 10.1007/s00251-007-0224-8 CrossRefPubMedGoogle Scholar
  11. Bonneaud C, Sorci G, Morin V, Westerdahl H, Zoorob R, Wittzell H (2004) Diversity of Mhc class I and IIB genes in house sparrows (Passer domesticus). Immunogenetics 55:855–865. doi: 10.1007/s00251-004-0648-3 CrossRefPubMedGoogle Scholar
  12. Bull CM, Griffith SC, Lanham EJ, Johnston GR (2000) Recognition of pheromones from group members in a gregarious lizard, Egernia stokesii. J Herpetol 34:92–99CrossRefGoogle Scholar
  13. Chelvanayagam G (1996) A roadmap for HLA-A, HLA-B, and HLA-C peptide binding specificities. Immunogenet 45:15–26CrossRefGoogle Scholar
  14. Cogger HG (1983) Reptiles and amphibians of Australia. AH & AW Reed Pty Ltd, SydneyGoogle Scholar
  15. Consuegra S, Megens HJ, Leon K, Stet RJM, Jordan WC (2005) Patterns of variability at the major histocompatability class II alpha locus in Atlantic salmon constrast with those at the class I locus. Immunogenetics 57:16–24CrossRefPubMedGoogle Scholar
  16. Consuegra S, de Eyto E, McGinnity P, Stet RJM, Jordan WC (2011) Contrasting responses to selection in class I and class IIα major histocompatibility-linked markers in salmon. Heredity 107:143–154CrossRefPubMedPubMedCentralGoogle Scholar
  17. Díez-Rivero CM, Reche P (2009) Discovery of conserved epitopes through sequence variability analyses. In: Bioinformatics for immunomics. Springer, New York, pp. 95–101Google Scholar
  18. Duffield GA, Bull CM (1996) Host location by larvae of the reptile tick Amblyomma vikirri (Acari: Ixodidae). Exp Appl Acarol 20:575–582CrossRefGoogle Scholar
  19. Duffield GA, Bull CM (2002) Stable aggregations in an Australian lizard, Egernia stokesii. Naturwissenschaften 89:424–427CrossRefPubMedGoogle Scholar
  20. Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305–311. doi: 10.1016/s0169-5347(98)01416-5 CrossRefPubMedGoogle Scholar
  21. Eimes JA, Townsend AK, Sepil I, Nishiumi I, Satta Y (2015) Patterns of evolution of MHC class II genes of crows (Corvus) suggest trans-species polymorphism. PeerJ 3:e853CrossRefPubMedPubMedCentralGoogle Scholar
  22. Elbers JP, Taylor SS (2016) Major histocompatibility complex polymorphism in reptile conservation. Herpetol Conserv Biol 11:1–12Google Scholar
  23. Fenner AL, Bull CM (2008) The impact of nematode parasites on the behaviour of an Australian lizard, the gidgee skink Egernia stokesii. Ecol Res 23:897–903CrossRefGoogle Scholar
  24. Galan M, Guivier E, Caraux G, Charbonnel N, Cosson J-F (2010) A 454 multiplex sequencing method for rapid and reliable genotyping of highly polymorphic genes in large-scale studies. BMC Genomics 11:296CrossRefPubMedPubMedCentralGoogle Scholar
  25. Garcia-Boronat M, Diez-Rivero CM, Reinherz EL, Reche PA (2008) PVS: a web server for protein sequence variability analysis tuned to facilitate conserved epitope discovery. Nucleic Acids Res 36:W35–W41CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gardner MG, Bull CM, Cooper JB, Duffied GA (2001) Genetic evidence for a family structure in stable social aggregations of the Australian lizard Egernia stokesii. Mol Ecol 10:175–183CrossRefPubMedGoogle Scholar
  27. Gardner MG, Bull CM, Cooper SJB (2002) High levels of genetic monogamy in the group-living Australian lizard Egernia stokesii. Mol Ecol 11:1787–1794CrossRefPubMedGoogle Scholar
  28. Gardner MG, Bull CM, Fenner A, Murray K, Donnellan SC (2007) Consistent social structure within aggregations of the Australian lizard, Egernia stokesii across seven disconnected rocky outcrops. J Ethol 25:263–270CrossRefGoogle Scholar
  29. Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722. doi: 10.1111/j.0014-3820.2003.tb00580.x CrossRefPubMedGoogle Scholar
  30. Glaberman S, Caccone A (2008) Species-specific evolution of class I MHC genes in iguanas (Order: Squamata; Subfamily: Iguaninae). Immunogenetics 60:371–382CrossRefPubMedGoogle Scholar
  31. Glaberman S, Moreno MA, Caccone A (2009) Characterization and evolution of MHC class II B genes in Galapagos marine iguanas (Amblyrhynchus cristatus). Dev Comp Immunol 33:939–947CrossRefPubMedGoogle Scholar
  32. Godfrey SS, Bull CM, Gardner MG (2006) Associations between blood parasite infection and a mircosatellite DNA allele in an Australian scincid lizard (Egernia stokesii). Parasitol Res 100:109–109CrossRefGoogle Scholar
  33. Godfrey SS, Bull CM, James R, Murray K (2009) Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii. Behav Ecol Sociobiol 63:1045–1056CrossRefGoogle Scholar
  34. Hallas G, Bull CM, Bursey CR (2005) Pharyngodon tiliquae and Thelandros trachysauri (Nematoda: Pharyngodonidae), new parasite records for Egernia stokesii (Scincidae) from Australia. Comp Parasitol 72:119–120CrossRefGoogle Scholar
  35. Herdegen M, Babik W, Radwan J (2014) Selective pressures on MHC class II genes in the guppy (Poecilia reticulata) as inferred by hierarchical analysis of population structure. J Evol Biol 27:2347–2359CrossRefPubMedGoogle Scholar
  36. Huchard E, Albrecht C, Schliehe-Diecks S, Baniel A, Roos C, Peter PMK, Brameier M (2012) Large-scale MHC class II genotyping of a wild lemur population by next generation sequencing. Immunogenetics 64:895–913CrossRefPubMedPubMedCentralGoogle Scholar
  37. Hughes AL (2007) Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level. Heredity 99:364–373CrossRefPubMedGoogle Scholar
  38. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167–170CrossRefPubMedGoogle Scholar
  39. Hughes AL, Yeager M (1998) Natural selection at major histocompatibilty complex loci of vertebrates. Annu Rev Genet 321:415–435CrossRefGoogle Scholar
  40. Hung A (2013) MHC and mate choice in Anolis sagrei. Dissertation, The University of New Mexico, AlbuquerqueGoogle Scholar
  41. Hurvich CM, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika 76:297–307. doi: 10.2307/2336663 CrossRefGoogle Scholar
  42. Jaratlerdsiri W, Isberg SR, Higgins DP, Ho SY, Salomonsen J, Skjodt K, Miles LG, Gongora J (2014) Evolution of MHC class I in the Order Crocodylia. Immunogenetics 66:53–65CrossRefPubMedGoogle Scholar
  43. Keirans JE, Bull CM, Duffield GA (1996) Amblyomma vikkiri n. sp. (Acari: Ixodida: Ixodidae), a parasite of the gidgee skink Egernia stokesii (Reptilia: Scincidae) from South Australia. Syst Parasitol 34:1–9CrossRefGoogle Scholar
  44. Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683–695CrossRefPubMedGoogle Scholar
  45. Kiemnec-Tyburczy K, Richmond J, Savage A, Lips K, Zamudio K (2012) Genetic diversity of MHC class I loci in six non-model frogs is shaped by positive selection and gene duplication. Heredity 109:146–155CrossRefPubMedPubMedCentralGoogle Scholar
  46. Klein J, Satta Y, O’hUigin C (1993) The molecular descent of the major histocompatibility complex. Annu Rev Immunol 11:269–295CrossRefPubMedGoogle Scholar
  47. Knapp LA (2005) The ABCs of MHC. Evol Anthropol: Issu, News, Rev 14:28–37CrossRefGoogle Scholar
  48. Kryazhimskiy S, Plotkin JB (2008) The population genetics of dN/dS. PLoS Genet 4:e1000304CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kuduk K, Johanet A, Allainé D, Cohas A, Radwan J (2012) Contrasting patterns of selection acting on MHC class I and class II DRB genes in the Alpine marmot (Marmota marmota). J Evol Biol 25:1686–1693. doi: 10.1111/j.1420-9101.2012.02537.x CrossRefPubMedGoogle Scholar
  50. Madsen T, Ujvari B (2006) MHC class I variation associates with parasite resistance and longevity in tropical pythons. J Evol Biol 19:1973–1978CrossRefPubMedGoogle Scholar
  51. Main AR, Bull CM (1996) Mother-offspring recognition in two Australian lizards, Tiliqua rugosa and Egernia stokesii. Anim Behav 52:193–200CrossRefGoogle Scholar
  52. Meyer M, Kircher M (2010) Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb Protoc 2010:t5448CrossRefGoogle Scholar
  53. Milinski M (2006) The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol Syst 37:159–186CrossRefGoogle Scholar
  54. Miller HC, Belov K, Daugherty CH (2006) MHC class I genes in the tuatara (Sphenodon spp.): evolution of the MHC in an ancient reptilian order. Mol Biol Evol 23:949–956CrossRefPubMedGoogle Scholar
  55. Miller HC, Andrews-Cookson M, Daugherty CH (2007) Two patterns of variation among MHC class I loci in tuatara (Sphenodon punctatus). J Hered 98:666–677CrossRefPubMedGoogle Scholar
  56. Miller HC, O’Meally DO, Ezaz T, Amemiya C, Marshall-Graves JA, Edwards S (2015) Major histocompatibility complex genes map to two chromosomes in an evolutionarily ancient reptile, the tuatara Sphenodon punctatus. G3: Genes, Genomes, Genetics doi: 10.1534/g3.115.017467
  57. Neefjes J, Jongsma ML, Paul P, Bakke O (2011) Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol 11:823–836PubMedGoogle Scholar
  58. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  59. Pechouskova E, Dammhahn M, Brameier M, Fichtel C, Kappeler PM, Huchard E (2015) MHC class II variation in a rare and ecological specialist mouse lemur reveals lower allelic richness and contrasting selection patterns compared to a generalist and widespread sympatric congener. Immunogenet 67:229–245CrossRefGoogle Scholar
  60. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21PubMedGoogle Scholar
  61. Pokorny I, Sharma R, Goyal S, 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. doi: 10.1007/s00251-010-0475-7 CrossRefPubMedGoogle Scholar
  62. Posada D, Buckley T (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808. doi: 10.1080/10635150490522304 CrossRefPubMedGoogle Scholar
  63. Pyron RA, Burbrink FT, Wiens JJ (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 13:1CrossRefGoogle Scholar
  64. Radwan J, Zagalska-Neubauer M, Cichon M, Sendecka J, Kulma K, Gustafsson L, Babik W (2012) MHC diversity, malaria and lifetime reproductive success in collared flycatchers. Mol Ecol 21:2469–2479CrossRefPubMedGoogle Scholar
  65. Radwan J, Kuduk K, Levy E, Lebas N, Babik W (2014) Parasite load and MHC diversity in undisturbed and agriculturally modified habitats of the ornate dragon lizard. Mol Ecol 23:5966–5978. doi: 10.1111/mec.12984 CrossRefPubMedGoogle Scholar
  66. Reche PA, Reinherz EL (2003) Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphisms. J Mol Biol 331:623–641. doi: 10.1016/s0022-2836(03)00750-2 CrossRefPubMedGoogle Scholar
  67. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16. doi: 10.1186/1742-9994-2-16 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sommer S, Courtiol A, Mazzoni CJ (2013) MHC genotyping of non-model organisms using next-generation sequencing: a new methodology to deal with artefacts and allelic dropout. BMC Genomics 14. doi: 10.1186/1471-2164-14-542
  69. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B Biol Sci 277:979–988CrossRefGoogle Scholar
  70. Stein J (1999) An ecological study of the blood parasites of E. stokesii. Dissertation, Flinders University of South Australia, AdelaideGoogle Scholar
  71. Stein J, Dyce AL (2002) Field observations on the phlebotomine sand fly Australophlebotomus mackerrasi Lewis and Dyce feeding on the Gidgee skink Egernia stokesii Gray. Parasitol Res 88:278–279. doi: 10.1007/s00436-001-0541-z CrossRefPubMedGoogle Scholar
  72. Strandh M, Lannefors M, Bonadonna F, Westerdahl H (2011) Characterization of MHC class I and II genes in a subantarctic seabird, the blue petrel, Halobaena caerulea (Procellariiformes). Immunogenet 63:653–666CrossRefGoogle Scholar
  73. Strandh M, Westerdahl H, Pontarp M, Canback B, Dubois M-P, Miquel C, Taberlet P, Bonadonna F (2012) Major histocompatibility complex class II compatibility, but not class I, predicts mate choice in a bird with highly developed olfaction. Proc R Soc Lond Ser B Biol Sci 279:4457–4463CrossRefGoogle Scholar
  74. Stuglik MT, Radwan J, Babik W (2011) jMHC: software assistant for multilocus genotyping of gene families using next-generation amplicon sequencing. Mol Ecol Resour 11:739–742. doi: 10.1111/j.1755-0998.2011.02997.x CrossRefPubMedGoogle Scholar
  75. Sun Y, Xi D, Li G, Hao T, Chen Y, Yang Y (2014) Genetic characterization of MHC class II DQB exon 2 variants in gayal (Bos frontalis). Biotechnol Biotechnol Equip 28:827–833CrossRefPubMedPubMedCentralGoogle Scholar
  76. Sutton J, Robertson B, Grueber C, Stanton J-A, Jamieson I (2013) Characterization of MHC class II B polymorphism in bottlenecked New Zealand saddlebacks reveals low levels of genetic diversity. Immunogenet 65:619–633. doi: 10.1007/s00251-013-0708-7 CrossRefGoogle Scholar
  77. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi: 10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Telford SR, Stein J (2000) Two malaria parasites (Apicomplexa: Plasmodiidae) of the Australian skink Egernia stokesii. J Parasitol 86:395–406CrossRefPubMedGoogle Scholar
  79. The Reptile Database (2015) http://www.reptile-database.org. Accessed 3 Jun 2016
  80. Uetz P (2015) (editor) The Reptile Database. http://www.reptile-database.org. Accessed 3 Jun 2016
  81. Wang D, Zhong L, Wei Q, Gan X, He S (2010) Evolution of MHC class I genes in two ancient fish, paddlefish (Polyodon spathula) and Chinese sturgeon (Acipenser sinensis). FEBS Lett 584:3331–3339CrossRefPubMedGoogle Scholar
  82. Wedekind C, Penn D (2000) MHC genes, body odours, and odour preferences. Nephrol Dial Transplant 15:1269–1271CrossRefPubMedGoogle Scholar
  83. Wegner KM (2008) Historical and contemporary selection of teleost MHC genes: did we leave the past behind? J Fish Biol 73:2110–2132CrossRefGoogle Scholar
  84. Winternitz JC, Minchey SG, Garamszegi LZ, Huang S, Stephens PR, Altizer S (2013) Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism. Proc R Soc Lond Ser B Biol Sci 280:20131605. doi: 10.1098/rspb.2013.1605 CrossRefGoogle Scholar
  85. Wu TT, Kabat EA (1970) An analysis of the sequences of the variable regions of Bence Jones proteins and myeloma light chains and their implications for antibody complementarity. J Exp Med 132:211–250CrossRefPubMedPubMedCentralGoogle Scholar
  86. Xu B, Yang Z (2013) PAMLX: a graphical user interface for PAML. Mol Biol Evol 30:2723–2724. doi: 10.1093/molbev/mst179 CrossRefPubMedGoogle Scholar
  87. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591. doi: 10.1093/molbev/msm088 CrossRefPubMedGoogle Scholar
  88. Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118. doi: 10.1093/molbev/msi097 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Sarah K. Pearson
    • 1
  • C. Michael Bull
    • 1
  • Michael G. Gardner
    • 1
    • 2
  1. 1.School of Biological SciencesFlinders University of South AustraliaAdelaideAustralia
  2. 2.Evolutionary Biology UnitSouth Australian MuseumAdelaideAustralia

Personalised recommendations