Abstract
Duplicates of genes for major histocompatibility complex (MHC) molecules can be subjected to selection independently and vary markedly in their evolutionary rates, sequence polymorphism, and functional roles. Therefore, without a thorough understanding of their copy number variation (CNV) in the genome, the MHC-dependent fitness consequences within a species could be misinterpreted. Studying the intra-specific CNV of this highly polymorphic gene, however, has long been hindered by the difficulties in assigning alleles to loci and the lack of high-quality genomic data. Here, using the high-quality genome of the Siamese fighting fish (Betta splendens), a model for mate choice studies, and the whole-genome sequencing (WGS) data of 17 Betta species, we achieved locus-specific amplification of their three classical MHC class II genes — DAB1, DAB2, and DAB3. By performing quantitative PCR and depth-of-coverage analysis using the WGS data, we revealed intra-specific CNV at the DAB3 locus. We identified individuals that had two allelic copies (i.e., heterozygous or homozygous) or one allele (i.e., hemizygous) and individuals without this gene. The CNV was due to the deletion of a 20-kb-long genomic region harboring both the DAA3 and DAB3 genes. We further showed that the three DAB genes were under different modes of selection, which also applies to their corresponding DAA genes that share similar pattern of polymorphism. Our study demonstrates a combined approach to study CNV within a species, which is crucial for the understanding of multigene family evolution and the fitness consequences of CNV.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Information of raw read sequences (including their NCBI Sequence Read Archive accession numbers) used in this study were detailed in the supplementary file 1. The DNA sequences of Betta splendens exon 2 alleles were assigned to GenBank accession numbers: MW863583 – MW863612.
Code availability
Not applicable.
Change history
06 June 2022
A Correction to this paper has been published: https://doi.org/10.1007/s00251-022-01267-4
References
Aguilar A, Edwards SV, Smith TB et al (2006) Patterns of variation in MHC Class II β loci of the Little Greenbul (Andropadus virens) with comments on MHC evolution in birds. J. Hered 97:133-142. https://doi.org/10.1093/jhered/esj013
Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics, Babraham Institute, Cambridge, United Kingdom
Anisimova M, Nielsen R, Yang Z (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229–1236. https://doi.org/10.1093/genetics/164.3.1229
Babik W (2010) Methods for MHC genotyping in non-model vertebrates. Mol Ecol Resour 10:237–251. https://doi.org/10.1111/j.1755-0998.2009.02788.x
Bentkowski P, Radwan J (2019) Evolution of major histocompatibility complex gene copy number. PLoS Comput Biol 15:e1007015. https://doi.org/10.1371/journal.pcbi.1007015
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. https://doi.org/10.1046/j.1420-9101.2003.00531.x
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bollmer JL, Dunn PO, Whittingham LA et al (2010) Extensive MHC Class II B gene duplication in a passerine, the common yellowthroat (Geothlypis trichas). J Hered 101:448-460. https://doi.org/10.1093/jhered/esq018
Braasch I, Gehrke AR, Smith JJ et al (2016) The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nat Genet 48:427–437. https://doi.org/10.1038/ng.3526
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. https://doi.org/10.1038/364033a0
Burri R, Salamin N, Studer RA et al (2010) Adaptive divergence of ancient gene duplicates in the avian MHC class II β. Mol Biol Evol 27:2360–2374. https://doi.org/10.1093/molbev/msq120
Chain FJJ, Feulner PGD, Panchal M et al (2014) Extensive copy-number variation of young genes across stickleback populations. PLoS Genet 10:e1004830. https://doi.org/10.1371/journal.pgen.1004830
Cheng Y, Stuart A, Morris K et al (2012) Antigen-presenting genes and genomic copy number variations in the Tasmanian devil MHC. BMC Genomics 13:87. https://doi.org/10.1186/1471-2164-13-87
Clotfelter ED, Curren LJ, Murphy CE (2006) Mate choice and spawning success in the fighting fish Betta splendens: the importance of body size, display behavior and nest size. Ethology 112:1170-1178. https://doi.org/10.1111/j.1439-0310.2006.01281.x
Cram RA, Lawrence JM, Dzieweczynski TL (2019) Mating under the influence: male Siamese fighting fish prefer EE2-exposed females. Ecotoxicology 28:201–211. https://doi.org/10.1007/s10646-018-02012-y
Darriba D, Taboada GL, Doallo R et al (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772. https://doi.org/10.1038/nmeth.2109
Dearborn DC, Gager AB, McArthur AG et al (2016) Gene duplication and divergence produce divergent MHC genotypes without disassortative mating. Mol Ecol 25:4355–4367. https://doi.org/10.1111/mec.13747
Delport W, Poon AFY, Frost SDW et al (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455–2457. https://doi.org/10.1093/bioinformatics/btq429
Dijkstra JM, Grimholt U (2018) Major histocompatibility complex (MHC) fragment numbers alone - in Atlantic cod and in general - do not represent functional variability. F1000Res 7:963. https://doi.org/10.12688/f1000research.15386.2
Dijkstra JM, Grimholt U, Leong J et al (2013) Comprehensive analysis of MHC class II genes in teleost fish genomes reveals dispensability of the peptide-loading DM system in a large part of vertebrates. BMC Evol Biol 13:260. https://doi.org/10.1186/1471-2148-13-260
Dijkstra JM, Kiryu I, Yoshiura Y et al (2006) Polymorphism of two very similar MHC class Ib loci in rainbow trout (Oncorhynchus mykiss). Immunogenetics 58:152–167. https://doi.org/10.1007/s00251-006-0086-5
Dirscherl H, Yoder JA (2015) A nonclassical MHC class I U lineage locus in zebrafish with a null haplotypic variant. Immunogenetics 67:501–513. https://doi.org/10.1007/s00251-015-0862-1
Dobin A, Davis CA, Schlesinger F et al (2012) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21. https://doi.org/10.1093/bioinformatics/bts635
Dubin A, Jørgensen TE, Moum T et al (2019) Complete loss of the MHC II pathway in an anglerfish. Lophius Piscatorius Biol Lett 15:20190594. https://doi.org/10.1098/rsbl.2019.0594
Dzieweczynski TL, Russell AM, Forrette LM et al (2014) Male behavioral type affects female preference in Siamese fighting fish. Behav Ecol 25:136–141. https://doi.org/10.1093/beheco/art095
Eizaguirre C, Lenz TL, Sommerfeld RD et al (2011) Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes. Evol Ecol 25:605–622. https://doi.org/10.1007/s10682-010-9424-z
Eizaguirre C, Lenz TL, Traulsen A et al (2009) Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes. Ecol Lett 12:5–12. https://doi.org/10.1111/j.1461-0248.2008.01247.x
Ekblom R, Wolf JBW (2014) A field guide to whole-genome sequencing, assembly and annotation. Evol Appl 7:1026–1042. https://doi.org/10.1111/eva.12178
Fremont DH, Monnaie D, Nelson CA et al (1998) Crystal structure of I-Ak in complex with a dominant epitope of lysozyme. Immunity 8:305–317. https://doi.org/10.1016/S1074-7613(00)80536-1
Gamazon ER, Stranger BE (2015) The impact of human copy number variation on gene expression. Brief Funct Genom 14:352–357. https://doi.org/10.1093/bfgp/elv017
Gerdol M, Lucente D, Buonocore F et al (2019) Molecular and structural characterization of MHC class II β genes reveals high diversity in the cold-adapted icefish Chionodraco hamatus. Sci Rep 9:5523. https://doi.org/10.1038/s41598-019-42003-5
Gómez D, Conejeros P, Marshall SH et al (2010) MHC evolution in three salmonid species: a comparison between class II alpha and beta genes. Immunogenetics 62:531–542. https://doi.org/10.1007/s00251-010-0456-x
Grimholt U (2016) MHC and Evolution in Teleosts Biology 5:6. https://doi.org/10.3390/biology5010006
He K, Minias P, Dunn PO (2021) Long-read genome assemblies reveal extraordinary variation in the number and structure of MHC loci in birds. Genome Biol. Evol. 13:evaa270. https://doi.org/10.1093/gbe/evaa270
Hoover B, Alcaide M, Jennings S et al (2018) Ecology can inform genetics: disassortative mating contributes to MHC polymorphism in Leach’s storm-petrels (Oceanodroma leucorhoa). Mol Ecol 27:3371–3385. https://doi.org/10.1111/mec.14801
Horton R, Wilming L, Rand V et al (2004) Gene map of the extended human MHC. Nat Rev Genet 5:889–899. https://doi.org/10.1038/nrg1489
Huson DH, Bryant D (2005) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030
Jeon H-B, Won H, Suk HY (2019) Polymorphism of MHC class IIB in an acheilognathid species, Rhodeus sinesis shaped by historical selection and recombination. BMC Genet. 20:74. https://doi.org/10.1186/s12863-019-0775-3
Kaufman J (2018) Generalists and specialists: a new view of how MHC class I molecules fight infectious pathogens. Trends Immunol 39:367–379. https://doi.org/10.1016/j.it.2018.01.001
Klein J, Bontrop RE, Dawkins RL et al (1990) Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics 31:217–219. https://doi.org/10.1007/BF00204890
Klein J, Sato A, Nagl S et al (1998) Molecular trans-species polymorphism. Annu Rev Ecol Syst 29:1–21. https://doi.org/10.1146/annurev.ecolsys.29.1.1
Kosakovsky Pond SL, Posada D, Gravenor MB et al (2006) GARD: a genetic algorithm for recombination detection. Bioinformatics 22:3096–3098. https://doi.org/10.1093/bioinformatics/btl474
Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li H, Handsaker B, Wysoker A et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Li W, Sun W, Hu J et al (2014) Molecular characterization, polymorphism and expression analysis of swamp eel major histocompatibility complex class II B gene, after infection by Aeromonas Hydrophilia. J Anim Plant Sci 24:481–491
Lighten J, van Oosterhout C, Bentzen P (2014a) Critical review of NGS analyses for de novo genotyping multigene families. Mol Ecol 23:3957–3972. https://doi.org/10.1111/mec.12843
Lighten J, van Oosterhout C, Paterson IG et al (2014b) Ultra-deep Illumina sequencing accurately identifies MHC class IIb alleles and provides evidence for copy number variation in the guppy (Poecilia reticulata). Mol Ecol Resour 14:753–767. https://doi.org/10.1111/1755-0998.12225
Liu H-Y, Xue F, Gong J et al (2017) Limited polymorphism of the functional MHC class II B gene in the black-spotted frog (Pelophylax nigromaculatus) identified by locus-specific genotyping. Ecol Evol 7:9860–9868. https://doi.org/10.1002/ece3.3408
Llaurens V, McMullan M, van Oosterhout C (2012) Cryptic MHC polymorphism revealed but not explained by selection on the class IIB peptide-binding region. Mol Biol Evol 29:1631–1644. https://doi.org/10.1093/molbev/mss012
Loehlin DW, Carroll SB (2016) Expression of tandem gene duplicates is often greater than twofold. Proc Natl Acad Sci 113:5988–5992. https://doi.org/10.1073/pnas.1605886113
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155. https://doi.org/10.1126/science.290.5494.1151
Maccari G, Robinson J, Bontrop RE et al (2018) IPD-MHC: nomenclature requirements for the non-human major histocompatibility complex in the next-generation sequencing era. Immunogenetics 70:619–623. https://doi.org/10.1007/s00251-018-1072-4
Málaga-Trillo E, Zaleska-Rutczynska Z, McAndrew B et al (1998) Linkage relationships and haplotype polymorphism among cichlid Mhc class II B loci. Genetics 149:1527–1537. https://doi.org/10.1093/genetics/149.3.1527
Malmstrøm M, Matschiner M, Tørresen OK et al (2016) Evolution of the immune system influences speciation rates in teleost fishes. Nat Genet 48:1204–1210. https://doi.org/10.1038/ng.3645
Migalska M, Sebastian A, Radwan J (2019) Major histocompatibility complex class I diversity limits the repertoire of T cell receptors. Proc Natl Acad Sci 116:5021–5026. https://doi.org/10.1073/pnas.1807864116
Miller KM, Li S, Ming TJ et al (2006) The salmonid MHC class I: more ancient loci uncovered. Immunogenetics 58:571-589. https://doi.org/10.1007/s00251-006-0125-2
Minias P, Pikus E, Whittingham LA et al (2019) Evolution of copy number at the MHC varies across the avian tree of life. Genome Biol Evol 11:17–28. https://doi.org/10.1093/gbe/evy253
Minias P, Włodarczyk R, Remisiewicz M et al (2021) Distinct evolutionary trajectories of MHC class I and class II genes in Old World finches and buntings. Heredity. https://doi.org/10.1038/s41437-021-00427-8
Monvises A, Nuangsaeng B, Sriwattanarothai N et al (2009) The Siamese fighting fish: well-known generally but little-known scientifically. ScienceAsia 35:8–16. https://doi.org/10.2306/scienceasia1513-1874.2009.35.008
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426. https://doi.org/10.1093/oxfordjournals.molbev.a040410
Nei M, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci 94:7799–7806. https://doi.org/10.1073/pnas.94.15.7799
Nielsen R, Paul JS, Albrechtsen A et al (2011) Genotype and SNP calling from next-generation sequencing data. Nat Rev Genet 12:443–451. https://doi.org/10.1038/nrg2986
Niimura Y, Matsui A, Touhara K (2014) Extreme expansion of the olfactory receptor gene repertoire in African elephants and evolutionary dynamics of orthologous gene groups in 13 placental mammals. Genome Res 24:1485–1496. https://doi.org/10.1101/gr.169532.113
Nonaka MI, Nonaka M (2010) Evolutionary analysis of two classical MHC class I loci of the medaka fish, Oryzias latipes: haplotype-specific genomic diversity, locus-specific polymorphisms, and interlocus homogenization. Immunogenetics 62:319–332. https://doi.org/10.1007/s00251-010-0426-3
Nowak MA, Tarczy-Hornoch K, Austyn JM (1992) The optimal number of major histocompatibility complex molecules in an individual. Proc Natl Acad Sci 89:10896–10899. https://doi.org/10.1073/pnas.89.22.10896
O’Connor EA, Westerdahl H (2021) Trade-offs in expressed major histocompatibility complex diversity seen on a macroevolutionary scale among songbirds. Evolution 75:1061–1069. https://doi.org/10.1111/evo.14207
O’Connor EA, Westerdahl H, Burri R et al (2019) Avian MHC evolution in the era of genomics: phase 1.0. Cells 8:1152. https://doi.org/10.3390/cells8101152
Panijpan B, Kowasupat C, Laosinchai P et al (2014) Southeast Asian mouth-brooding Betta fighting fish (Teleostei: Perciformes) species and their phylogenetic relationships based on mitochondrial COI and nuclear ITS1 DNA sequences and analyses. Meta Gene 2:862–879. https://doi.org/10.1016/j.mgene.2014.10.007
Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21. https://doi.org/10.1038/sj.hdy.6800724
Pond SLK, Frost SDW, Muse SV (2004) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679. https://doi.org/10.1093/bioinformatics/bti079
Qurkhuli T, Schwensow N, Brändel SD et al (2019) Can extreme MHC class I diversity be a feature of a wide geographic range? The example of Seba’s short-tailed bat (Carollia perspicillata). Immunogenetics 71:575–587. https://doi.org/10.1007/s00251-019-01128-7
R Core Team (2020) R: a language and environment for statistical computing.
Radwan J, Babik W, Kaufman J et al (2020) Advances in the evolutionary understanding of MHC polymorphism. Trends Genet 36:298–311. https://doi.org/10.1016/j.tig.2020.01.008
Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544. https://doi.org/10.1016/j.biocon.2009.07.026
Radwan J, Kuduk K, Levy E et al (2014) Parasite load and MHC diversity in undisturbed and agriculturally modified habitats of the ornate dragon lizard. Mol Ecol 23:5966–5978. https://doi.org/10.1111/mec.12984
Rambaut A (2018) FigTree v1.4.4.
Reusch TBH, Schaschl H, Wegner KM (2004) Recent duplication and inter-locus gene conversion in major histocompatibility class II genes in a teleost, the three-spined stickleback. Immunogenetics 56:427–437. https://doi.org/10.1007/s00251-004-0704-z
Rinker DC, Specian NK, Zhao S et al (2019) Polar bear evolution is marked by rapid changes in gene copy number in response to dietary shift. Proc Natl Acad Sci 116:13446–13451. https://doi.org/10.1073/pnas.1901093116
Roche PA, Furuta K (2015) The ins and outs of MHC class II-mediated antigen processing and presentation. Nat Rev Immunol 15:203–216. https://doi.org/10.1038/nri3818
Ronquist F, Teslenko M, Van Der Mark P et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Roth O, Solbakken MH, Tørresen OK et al (2020) Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes. Proc Natl Acad Sci 117:9431–9439. https://doi.org/10.1073/pnas.1916251117
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC et al (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Rüber L, Britz R, Tan HH et al (2004) Evolution of mouthbrooding and life-history correlates in the fighting fish genus Betta. Evolution 58:799–813. https://doi.org/10.1111/j.0014-3820.2004.tb00413.x
Sammut B, Marcuz A, Pasquier LD (2002) Correction, Vol. 32(6) 2002, pp 1593–1604 The fate of duplicated major histocompatibility complex class Ia genes in a dodecaploid amphibian. Xenopus Ruwenzoriensis Eur J Immunol 32:2698–2709. https://doi.org/10.1002/1521-4141(200209)32:9%3c2698::AID-IMMU2698%3e3.0.CO;2-U
Sato A, Dongak R, Hao L et al (2012) Organization of Mhc class II A and B genes in the tilapiine fish Oreochromis. Immunogenetics 64:679–690. https://doi.org/10.1007/s00251-012-0618-0
Sato A, Figueroa F, Murray BW et al (2000) Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 51:108–116. https://doi.org/10.1007/s002510050019
Sedlazeck FJ, Rescheneder P, von Haeseler A (2013) NextGenMap: fast and accurate read mapping in highly polymorphic genomes. Bioinformatics 29:2790–2791. https://doi.org/10.1093/bioinformatics/btt468
Shiina T, Dijkstra JM, Shimizu S et al (2005) Interchromosomal duplication of major histocompatibility complex class I regions in rainbow trout (Oncorhynchus mykiss), a species with a presumably recent tetraploid ancestry. Immunogenetics 56:878-893. https://doi.org/10.1007/s00251-004-0755-1
Shand R, Dixon B (2001) Teleost major histocompatibility genes: diverse but not complex. Mod Asp Immunobiol 2:66–72
Sin SYW, Cloutier A, Nevitt G et al (2021) Olfactory receptor subgenome and expression in a highly olfactory procellariiform seabird. Genetics. https://doi.org/10.1093/genetics/iyab210
Sin YW, Annavi G, Dugdale HL et al (2014) Pathogen burden, co-infection and major histocompatibility complex variability in the European badger (Meles meles). Mol Ecol 23:5072–5088. https://doi.org/10.1111/mec.12917
Sin YW, Annavi G, Newman C et al (2015) MHC class II-assortative mate choice in European badgers (Meles meles). Mol Ecol 24:3138–3150. https://doi.org/10.1111/mec.13217
Sin YW, Dugdale HL, Newman C et al (2012a) Evolution of MHC class I genes in the European badger (Meles meles). Ecol Evol 2:1644–1662. https://doi.org/10.1002/ece3.285
Sin YW, Dugdale HL, Newman C et al (2012b) MHC class II genes in the European badger (Meles meles): characterization, patterns of variation, and transcription analysis. Immunogenetics 64:313–327. https://doi.org/10.1007/s00251-011-0578-9
Song K, Li L, Zhang G (2016) Coverage recommendation for genotyping analysis of highly heterologous species using next-generation sequencing technology. Sci. Rep. 6:35736. https://doi.org/10.1038/srep35736
Spielmann M, Lupiáñez DG, Mundlos S (2018) Structural variation in the 3D genome. Nat Rev Genet 19:453–467. https://doi.org/10.1038/s41576-018-0007-0
Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc Royal Soc B 277:979–988. https://doi.org/10.1098/rspb.2009.2084
Stervander M, Dierickx EG, Thorley J et al (2020) High MHC gene copy number maintains diversity despite homozygosity in a critically endangered single-island endemic bird, but no evidence of MHC-based mate choice. Mol Ecol 19:3578–3592. https://doi.org/10.1111/mec.15471
Stet RJ, Kruiswijk CP, Dixon B (2003) Major histocompatibility lineages and immune gene function in teleost fishes: the road not taken. Crit Rev Immunol 23:441–471. https://doi.org/10.1615/critrevimmunol.v23.i56.50
Sudmant PH, Rausch T, Gardner EJ et al (2015) An integrated map of structural variation in 2,504 human genomes. Nature 526:75–81. https://doi.org/10.1038/nature15394
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 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
Thorvaldsdóttir H, Robinson JT, Mesirov JP (2012) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192. https://doi.org/10.1093/bib/bbs017
Völker M, Backström N, Skinner BM et al (2010) Copy number variation, chromosome rearrangement, and their association with recombination during avian evolution. Genome Res 20:503–511. https://doi.org/10.1101/gr.103663.109
Weaver S, Dube S, Mir A et al (2010) Taking qPCR to a higher level: analysis of CNV reveals the power of high throughput qPCR to enhance quantitative resolution. Methods 50:271–276. https://doi.org/10.1016/j.ymeth.2010.01.003
Wegner KM, Kalbe M, Kurtz J et al (2003) Parasite selection for immunogenetic optimality. Science 301:1343–1343. https://doi.org/10.1126/science.1088293
Winternitz JC, Minchey SG, Garamszegi LZ et al (2013) Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism. Proc Royal Soc B 280:20131605. https://doi.org/10.1098/rspb.2013.1605
Woelfing B, Traulsen A, Milinski M et al (2009) Does intra-individual major histocompatibility complex diversity keep a golden mean? Philos. Trans. R. Soc. Lond., B. Biol Sci 364:117–128. https://doi.org/10.1098/rstb.2008.0174
Wu Y, Zhang N, Hashimoto K et al (2021) Structural comparison between MHC classes I and II; in Evolution, a Class-II-Like Molecule Probably Came First. Front Immunol 12:621153. https://doi.org/10.3389/fimmu.2021.621153
Yamaguchi T, Dijkstra JM (2019) Major histocompatibility complex (MHC) genes and disease resistance in fish. Cells 8:378. https://doi.org/10.3390/cells8040378
Zarrei M, MacDonald JR, Merico D et al (2015) A copy number variation map of the human genome. Nat Rev Genet 16:172–183. https://doi.org/10.1038/nrg3871
Zhai T, Yang H-Q, Zhang R-C et al (2017) Effects of population bottleneck and balancing selection on the Chinese alligator are revealed by locus-specific characterization of MHC genes. Sci Rep 7:5549. https://doi.org/10.1038/s41598-017-05640-2
Zhang F, Gu W, Hurles ME et al (2009) Copy number variation in human health, disease, and evolution. Annu Rev Genom Hum Genet 10:451–481. https://doi.org/10.1146/annurev.genom.9.081307.164217
Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298. https://doi.org/10.1016/S0169-5347(03)00033-8
Zhang W, Wang H, Brandt DYC et al (2021) The genetic architecture of phenotypic diversity in the betta fish (Betta splendens). bioRxiv https://doi.org/10.1101/2021.05.10.443352
Zhao M, Wang Q, Wang Q et al (2013) Computational tools for copy number variation (CNV) detection using next-generation sequencing data: features and perspectives. BMC Bioinform 14:S1. https://doi.org/10.1186/1471-2105-14-S11-S1
Zagalska-Neubauer M, Babik W, Sttuglik M et al (2010) 454 sequencing reveals extreme complexity of the class II major histocompatibility complex in the collared flycatcher. BMC Evol Biol 10:395. https://doi.org/10.1186/1471-2148-10-395
Acknowledgements
The computations were performed using research computing facilities offered by the Information Technology Services, the University of Hong Kong.
Funding
This research was supported by the start-up fund (the University of Hong Kong) granted to SYWS.
Author information
Authors and Affiliations
Contributions
S.Y.W.S. and A.T.C.W. designed research; A.T.C.W., D.K.L., E.S.K.P., D.T.C.C. and S.Y.W.S. performed research; A.T.C.W. analyzed data; A.T.C.W. wrote the paper and all authors contributed to revised versions.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original online version of this article was revised: The correct Supplementary materials has been uploaded.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wong, A.T.C., Lam, D.K., Poon, E.S.K. et al. Intra-specific copy number variation of MHC class II genes in the Siamese fighting fish. Immunogenetics 74, 327–346 (2022). https://doi.org/10.1007/s00251-022-01255-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00251-022-01255-8