Skip to main content
SpringerLink
Log in

Structure, diversity and evolutionary patterns of expressed MHC class IIB genes in chub (Squalius cephalus), a cyprinid fish species from Europe

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

The polymorphism of exon 2 of the DAB genes (major histocompatibility complex [MHC] class IIB) was investigated for the first time in the freshwater cyprinid fish species, Squalius cephalus, in the wide range of its distribution in Europe. We identified 111 different MHC class IIB variants in 15 chub populations distributed from Finland to Spain. The sequence analysis showed that many structurally important amino acid sites that were conserved among tetrapods were also conserved in chub. The analysis of recombination indicated that it does not play an important role in producing and maintaining the variation of DAB genes analyzed in the present study. The exon 2 was shown to be subjected to intense positive selection. Phylogenetic analysis and sequence identities suggest the presence of two class IIB loci (DAB1-like and DAB3-like) in chub. Nevertheless, the presence of three DAB3-like sequence variants in several individuals indicates the duplication of the DAB3 gene. A contrasting selection pattern was found in DAB1-like and DAB3-like genes, which suggests the potential functional differences between these genes. Some DAB sequence variants were shared among the populations of different mtDNA lineages. The phylogenetic analyses did not confirm any biogeographical pattern of the genetic structure of MHC IIB in chub, which is in line with balancing selection and trans-species polymorphism in MHC genes. Nevertheless, cluster analysis based on the presence/absence of DAB sequence variants in the populations showed the phylogeophraphical pattern corresponding to the mtDNA lineages, which indicates that neutral selection can partially explain the MHC IIB evolution in chub.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agbali M, Reichard M, Bryjová A, Bryja J, Smith C (2010) Mate choice for nonadditive genetic benefits correlate with MHC dissimilarity in the rose bitterling (Rhodeus ocellatus). Evolution 64(6):1683–1696. doi:10.1111/j.1558-5646.2010.00961.x

    Article  CAS  PubMed  Google Scholar 

  • Aguilar A, Garza JC (2007) Patterns of historical balancing selection on the salmonid major histocompatibility complex class II beta gene. J Mol Evol 65(1):34–43. doi:10.1007/s00239-006-0222-8

    Article  CAS  PubMed  Google Scholar 

  • 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(11):2652–2665. doi:10.1111/j.1365-294X.2008.03791.x

    Article  CAS  PubMed  Google Scholar 

  • Anisimova M, Nielsen R, Yang ZH (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164(3):1229–1236

    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(3):363–377

    Article  CAS  PubMed  Google Scholar 

  • Bingulac-Popovic J, Figueroa F, Sato A, Talbot WS, Johnson SL, Gates M, Postlethwait JH, Klein J (1997) Mapping of Mhc class I and class II regions to different linkage groups in the zebrafish, Danio rerio. Immunogenetics 46(2):129–134. doi:10.1007/s002510050251

    Article  CAS  PubMed  Google Scholar 

  • Blais J, Rico C, van Oosterhout C, Cable J, Turner GF, Bernatchez L (2007) MHC adaptive divergence between closely related and sympatric African cichlids. PLoS ONE 2(8):e734. doi:10.1371/journal.pone.0000734

    Article  PubMed  Google Scholar 

  • Bos DH, Gopurenko D, Williams RN, DeWoody JA (2008) Inferring population history and demography using microsatellites, mitochondrial DNA, and major histocompatibility complex (MHC) genes. Evolution 62(6):1458–1468. doi:10.1111/j.1558-5646.2008.00364.x

    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(6432):33–39. doi:10.1038/364033a0

    Article  CAS  PubMed  Google Scholar 

  • 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(2–3):191–202. doi:10.1007/s00251-006-0085-6

    Article  CAS  PubMed  Google Scholar 

  • Bryja J, Charbonnel N, Berthier K, Galan M, Cosson JF (2007) Density-related changes in selection pattern for major histocompatibility complex genes in fluctuating populations of voles. Mol Ecol 16:5084–5097. doi:10.1111/j.1365-294X.2007.03584.x

    Article  CAS  PubMed  Google Scholar 

  • Čížková D, de Bellocq JD, Baird SJE, Piálek J, Bryja J (2010) Genetic structure and contrasting selection pattern at two major histocompatibility complex genes in wild house mouse populations. Heredity. doi:10.1038/hdy.2010.112

    PubMed  Google Scholar 

  • Clarke B, Kirby DRS (1966) Maintenance of histocompatibility polymorphisms. Nature 211(5052):999–1000. doi:10.1038/211999a0

    Article  CAS  PubMed  Google Scholar 

  • Dixon B, Nagelkerke LAJ, Sibbing FA, Egberts E, Stet RJM (1996) Evolution of MHC class II beta chain-encoding genes in the Lake Tana barbel species flock (Barbus intermedius complex). Immunogenetics 44(6):419–431. doi:10.1007/BF02602803

    CAS  PubMed  Google Scholar 

  • Durand JD, Persat H, Bouvet Y (1999) Phylogeography and postglacial dispersion of the chub (Leuciscus cephalus) in Europe. Mol Ecol 8(6):989–997

    Article  CAS  PubMed  Google Scholar 

  • Durand JD, Unlu E, Doadrio I, Pipoyan S, Templeton AR (2000) Origin, radiation, dispersion and allopatric hybridization in the chub Leuciscus cephalus. Proc R Soc B Biol Sci 267(1453):1687–1697

    Article  CAS  Google Scholar 

  • Figueroa F, Gutknecht J, Tichy H, Klein J (1990) Class II Mhc genes in rodent evolution. Immunol Rev 113:27–46

    Article  CAS  PubMed  Google Scholar 

  • Graser R, O'hUigin C, Vincek V, Meyer A, Klein J (1996) Trans-species polymorphism of class II Mhc loci in danio fishes. Immunogenetics 44(1):36–48

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Hammer Ř, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1): 9pp. http://palaeo-electronica.org/2001_1/past/issue1_01.htm

    Google Scholar 

  • Hänfling B, Brandl R (1998) Genetic and morphological variation in a common European cyprinid, Leuciscus cephalus within and across Central European drainages. J Fish Biol 52(4):706–715

    Google Scholar 

  • Hashimoto K, Nakanishi T, Kurosawa Y (1990) Isolation of carp genes encoding major histocompatibility complex antigens. Proc Natl Acad Sci USA 87:6863–6867

    Article  CAS  PubMed  Google Scholar 

  • Hill WG, Robertson (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226–231. doi:10.1007/BF01245622

    Article  Google Scholar 

  • Huchard E, Weill M, Cowlishaw G, Raymond M, Knapp LA (2008) Polymorphism, haplotype composition, and selection in the Mhc-DRB of wild baboons. Immunogenetics 60(10):585–598. doi:10.1007/s00251-008-0319-x

    Article  CAS  PubMed  Google Scholar 

  • Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hughes AL, Nei M (1992) Maintenance of MHC polymorphism. Nature 355:402–403. doi:10.1038/355402b0

    Article  CAS  PubMed  Google Scholar 

  • Kanagawa T (2003) Bias and artifacts in multitemplate polymerase chain reactions (PCR). J Biosci Bioeng 96(4):317–323. doi:10.1016/S1389-1723(03)90130-7

    CAS  PubMed  Google Scholar 

  • Karlin S, Altschul SF (1990) Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. Proc Natl Acad Sci USA 87:2264–2268

    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. doi:10.1006/smim.1994.1050

    Article  CAS  PubMed  Google Scholar 

  • Kennedy LJ, Ryvar R, Gaskell RM, Addie DD, Willoughby K, Carter SD et al (2002) Sequence analysis of MHC DRB alleles in domestic cats from the United Kingdom. Immunogenetics 54:348–352. doi:10.1007/s00251-002-0465-5

    Article  CAS  PubMed  Google Scholar 

  • Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19:155–162. doi:10.1016/0198-8859(87)90066-8

    Article  CAS  PubMed  Google Scholar 

  • Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER et al (1990) Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics 31:217–219. doi:10.1007/BF00204890

    CAS  PubMed  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW (2005) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22(5):1208–1222. doi:10.1093/molbev/msi105

    Article  PubMed  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW, Muse SV (2005) Hyphy: hypothesis testing using phylogenies. Bioinformatics 21(5):676–679. doi:10.1093/bioinformatics/bti079

    Article  Google Scholar 

  • Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW (2006) Gard: a genetic algorithm for recombination detection. Bioinformatics 22(24):3096–3098. doi:10.1093/bioinformatics/btl474

    Article  PubMed  Google Scholar 

  • Kruiswijk CP, Hermsen T, Fujiki K, Dixon B, Savelkoul HFJ, Stet RJM (2004) Analysis of genomic and expressed major histocompatibility class Ia and class II genes in a hexaploid Lake Tana African 'large' barb individual (Barbus intermedius). Immunogenetics 55(11):770–781. doi:10.1007/s00251-003-0635-0

    Article  CAS  PubMed  Google Scholar 

  • Kruiswijk CP, Hermsen T, van Heerwaarden J, Dixon B, Savelkoul HFJ, Stet RJM (2005) Major histocompatibility genes in the Lake Tana African large barb species flock: evidence for complete partitioning of class II B, but not class I, genes among different species. Immunogenetics 56(12):894–908. doi:10.1007/s00251-005-0767-5

    Article  CAS  PubMed  Google Scholar 

  • Kurtz J, Wegner KM, Kalbe M, Reusch TBH, Schaschl H, Hasselquist D, Milinski M (2006) MHC genes and oxidative stress in sticklebacks: an immuno-ecological approach. Proc R Soc B Biol Sci 273(1592):1407–1414. doi:10.1098/rspb.2005.3450

    Article  CAS  Google Scholar 

  • Landry C, Bernatchez L (2001) Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Mol Ecol 10(10):2525–2539

    Article  CAS  PubMed  Google Scholar 

  • Laroche J, Durand JD, Bouvet Y, Guinand B, Brohon B (1999) Genetic structure and differentiation among populations of two cyprinids, Leuciscus cephalus and Rutilus rutilus, in a large European river. Can J Fish Aquat Sci 56(9):1659–1667

    Article  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology, 2nd English edn. Elsevier, Amsterdam

    Google Scholar 

  • Lenz TL, Becker S (2008) Simple approach to reduce PCR artefact formation leads to reliable genotyping of MHC and other highly polymorphic loci—implications for evolutionary analysis. Gene 427(1–2):117–123. doi:10.1016/j.gene.2008.09.013

    Article  CAS  PubMed  Google Scholar 

  • Lewontin RC (1964) The interaction of selection and linkage: I. Genetic considerations; heterotic models. Genetics 49:49–67

    CAS  PubMed  Google Scholar 

  • Luetkemeier ES, Malhi RS, Beever JE, Schook LB (2009) Diversification of porcine MHC class II genes: evidence for selective advantage. Immunogenetics 61(2):119–129. doi:10.1007/s00251-008-0348-5

    Article  CAS  PubMed  Google Scholar 

  • Miller KM, Withler RE (1996) Sequence analysis of a polymorphic Mhc class II gene in Pacific salmon. Immunogenetics 43(6):337–351

    Article  CAS  PubMed  Google Scholar 

  • Murray BW, Shintani S, Sültmann H, Klein J (2000) Major histocompatibility complex class II A genes in cichlid fishes: identification, expression, linkage relationships, and haplotype variation. Immunogenetics 51:576–586

    Article  CAS  PubMed  Google Scholar 

  • Ono H, Klein D, Vincek V, Figueroa F, O'hUigin C, Tichy H, Klein J (1992) Major histocompatibility complex class-II genes of zebrafish. P Natl Acad Sci USA 89(24):11886–11890

    Article  CAS  Google Scholar 

  • Ono H, O'hUigin C, Vincek V, Klein J (1993a) Exon-intron organization of fish major histocompatibility complex class IIB genes. Immunogenetics 38(3):223–234

    Article  CAS  PubMed  Google Scholar 

  • Ono H, O'hUigin C, Vincek V, Stet RJM, Figueroa F, Klein J (1993b) New beta-chain-encoding MHC class-II genes in the carp. Immunogenetics 38(2):146–149

    Article  CAS  PubMed  Google Scholar 

  • Ottová E, Šimková A, Martin JF, de Bellocq JG, Gelnar M, Allienne JF, Morand S (2005) Evolution and trans-species polymorphism of MHC class II beta genes in cyprinid fish. Fish Shellfish Immunol 18(3):199–222. doi:10.1016/j.fsi.2004.07.004

    PubMed  Google Scholar 

  • Ottová E, Šimková A, Morand S (2007) The role of major histocompatibility complex diversity in vigour of fish males (Abramis brama L.) and parasite selection. Biol J Linn Soc 90(3):525–538

    Article  Google Scholar 

  • Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153(2):145–164

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14(9):817–818

    Article  CAS  PubMed  Google Scholar 

  • Rakus KL, Wiegertjes GF, Stet RJM, Savelkoul HFJ, Pilarczyk A, Irnazarow I (2003) Polymorphism of major histocompatibility class II B genes in different lines of the common carp (Cyprinus carpio). Aquat Living Resour 16:432–437. doi:10.1016/S0990-7440(03)00057-3

    Article  Google Scholar 

  • Rakus KL, Wiegertjes GF, Jurecka P, Walker PD, Pilarczyk A, Irnazarow I (2009) Major histocompatibility (MH) class II B gene polymorphism influences disease resistance of common carp (Cyprinus carpio L.). Aquaculture 288(1–2):44–50. doi:10.1016/j.aquaculture.2008.11.016

    Article  CAS  Google Scholar 

  • 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(3):623–641. doi:10.1016/s0022-2836(03)00750-2

    Article  CAS  PubMed  Google Scholar 

  • Reusch TBH, Langefors A (2005) Inter- and intralocus recombination drive MHC class IIB gene diversification in a teleost, the three-spined stickleback Gasterosteus aculeatus. J Mol Evol 61(4):531–545. doi:10.1007/s00239-004-0340-0

    Article  CAS  PubMed  Google Scholar 

  • Richman AD, Herrera LG, Nash D, Schierup MH (2003) Relative roles of mutation and recombination in generating allelic polymorphism at an MHC class II locus in Peromyseus maniculatus. Genet Res 82(2):89–99. doi:10.1017/s0016672303006347

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues PNS, Hermsen TT, van Maanen A, Taverne-Thiele AJ, Rombout J, Dixon B, Stet RJM (1998) Expression of MhcCyca class I and class II molecules in the early life history of the common carp (Cyprinus carpio L.). Dev Comp Immunol 22(5–6):493–506

    Article  CAS  PubMed  Google Scholar 

  • Sawyer SA (1999) GENECONV: a computer package for the statistical detection of gene conversion, Distributed by the author, Department of Mathematics, Washington University in St. Louis. Available at http://www.math.wustl.edu/~sawyer.

  • Seifertová M, Vyskočilová M, Morand S, Šimková A (2008) Metazoan parasites of freshwater cyprinid fish (Leuciscus cephalus): testing biogeographical hypotheses of species diversity. Parasitology 135:1417–1435. doi:10.1017/S0031182008004812

    Article  PubMed  Google Scholar 

  • Stet RJM, Dixon B, vanErp SHM, van Lierop MJC et al (1996) Inference of structure and function of fish Major Histocompatibility Complex (MHC) molecules from expressed genes. Fish Shellfish Immun 6:305–318. doi:10.1006/fsim.1996.0031

  • Stet RJM, Johnston R, Parham P, Weigertjes GF (1997) The unMHC of teleostean fish: segregation analysis in common carp and Atlantic salmon. Hereditas 127:169–170

    Google Scholar 

  • Stet RJM, de Vries B, Mudde K, Hermsen T, van Heerwaarden J, Shum BP et al (2002) Unique haplotypes of co-segregating major histocompatibility class IIA and class IIB alleles in Atlantic salmon (Salmo salar) give rise to diverse class II genotypes. Immunogenetics 54:320–331. doi:10.1007/s00251-002-0477-1

    Article  CAS  PubMed  Google Scholar 

  • Sültmann H, Mayer WE, Figueroa F, O'hUigin C, Klein J (1994) Organization of MHC class II B genes in the zebrafish (Brachydanio rerio). Genomics 23(1):1–14

    Article  PubMed  Google Scholar 

  • Summers K, Roney KE, da Silva J, Capraro G, Cuthbertson BJ, Kazianis S, Rosenthal GG, Ryan MJ, McConnell TJ (2009) Divergent patterns of selection on the DAB and DXB MHC class II loci in Xiphophorus fishes. Genetica 135(3):379–390. doi:10.1007/s10709-008-9284-4

    Article  PubMed  Google Scholar 

  • Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, MA

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599. doi:10.1093/molbev/msm092

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Valdar WSJ (2002) Scoring residue conservation. Proteins Struct Funct Bioinformatics 48(2):227–241. doi:10.1002/prot.10146

    Article  CAS  Google Scholar 

  • vanErp SHM, Egberts E, Stet RJM (1996) Characterization of class II A and B genes in a gynogenetic carp clone. Immunogenetics 44(3):192–202

    Article  CAS  Google Scholar 

  • Wegner KM (2008) Historical and contemporary selection of teleost MHC genes: did we leave the past behind? J Fish Biol 73(9):2110–2132. doi:10.1111/j.1095-8649.2008.02051.x

    Article  Google Scholar 

  • Wegner KM, Reusch TBH, Kalbe M (2003) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evol Biol 16(2):224–232

    Article  CAS  PubMed  Google Scholar 

  • Wegner KM, Kalbe M, Rauch G, Kurtz J, Schaschl H, Reusch TBH (2006) Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks. Mol Ecol 15(4):1153–1164. doi:10.1111/j.1365-294X.2006.02855.x

    Article  CAS  PubMed  Google Scholar 

  • Wiegertjes GF, Bongers ABJ, Voorthuis P, Doulabi BZ, Groeneveld A, VanMuiswinkel WB, Stet RJM (1996) Characterization of isogenic carp (Cyprinus carpio L.) lines with a genetically determined high or low antibody production. Anim Genet 27(5):313–319

    Article  CAS  PubMed  Google Scholar 

  • Wilson DJ, McVean G (2006) Estimating diversifying selection and functional constraint in the presence of recombination. Genetics 172:1411–1425

    Article  CAS  PubMed  Google Scholar 

  • Yang ZH (2007) PAML4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591. doi:10.1093/molbev/msm088

    Article  CAS  PubMed  Google Scholar 

  • Yang ZH, Nielsen R, Goldman N, Pedersen AMK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155(1):431–449

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was founded by the by the Czech Science Foundation, Project No. 524/07/0188. The travel costs for the different field studies and material collections were funded by the by Research Project of the Masaryk University, Brno, Project No.: MSM 0021622 416, and also supported by the Ichthyoparasitology, Centre of Excellence, Project No. LC 522, funded by Ministry of Education, Youth and Sports of the Czech Republic. We would like to thank the group from the Department of Fish Ecology, Institute of Vertebrate Biology, Academy of Sciences (Czech Republic), Teodora Trichkova and Milen Vassilev from the Institute of Zoology, Bulgarian Academy of Sciences (Bulgaria), Alexis Ribas Salvador from the Laboratory of Parasitology, University of Barcelona and Antoni Arrizabalaga, responsible for the Museu de Granollers Ciències Naturals ‘La Tela’ (Spain), André Gilles, René Chappaz and their co-workers from Université de Provence Aix–Marseille 1 (France), Paolo Galli from Department of Biotechnology and Biosciences, University of Milano–Bicocca (Italy), Jussi Pennanen, Finnish Game and Fisheries Research Institute, Helsinki (Finland), Miroslaw Przybylski, Grziegorz Zieba from University of Lodz, Lodz (Poland) for their help with fish sampling in the different sampling localities and the opportunity to use their laboratories. We also thank Martina Vyskočilová, Kristýna Hejlová and Kristína Civáňová from the Laboratory of Parasitology, Faculty of Science, Masaryk University, Brno (Czech Republic), for their help with molecular techniques. We are very grateful to Gregor Speas for the English revision of the first draft and to Matthew Nicholls for the English revision of the final version.

Author information

Authors and Affiliations

  1. Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 61137, Brno, Czech Republic

    Mária Seifertová & Andrea Šimková

Authors
  1. Mária Seifertová
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Šimková
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea Šimková.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Tab. S1

Results of the likelihood ratio tests of positive selection on exon 2 of MHC class IIB in Squalius cephalus. A test statistic was computed as 2(L b−L a), where L a and L b are the log-likelihood value for each of the nested models being compared (M0 and M3; M1a and M2a; M7 and M8). PSS positive selected site, n number of sequences in the analysed alignment. (PDF 68.1 kb)

Tab. S2

Geographical distribution of Sqce-DAB1 and Sqce-DAB3 sequences found in 15 populations of Squalius cephalus collected from European Rivers. (PDF 223 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seifertová, M., Šimková, A. Structure, diversity and evolutionary patterns of expressed MHC class IIB genes in chub (Squalius cephalus), a cyprinid fish species from Europe. Immunogenetics 63, 167–181 (2011). https://doi.org/10.1007/s00251-010-0495-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-010-0495-3

Keywords

Search

Navigation