Abstract
Ducks (Anatidae) are often vectors for the spread of pathogens because of their long-distance migrations. These migrations also expose ducks to a wide variety of pathogens in their wintering and breeding grounds, and, as a consequence, we might expect strong selection on their immune genes. Here, we studied exons 2 and 3 of the MHC class I in four species of Anas ducks (A. platyrhynchos, A. poecilorhyncha, A. formosa, and A. querquedula) using Illumina-sequencing. Both exons 2 and 3 code for the peptide-binding region of class I molecules; however, most previous studies of birds have only focused on exon 3. Here, we found stronger positive selection on exon 2 than exon 3, as indicated by more species with dN/dS > 1 and higher Wu-Kabat values. There was little evidence that divergence time influenced polymorphism, the numbers of identical alleles (partial α1 or α2 regions) among four Anas, or selection, suggesting that these widespread species might share similar levels of selection from pathogens. The high similarity of allele numbers, positively selected sites (PSS), conserved motifs, and variable protein sites (VPS) supported the persistence of trans-species polymorphism in Anas for at least 10 million years. Our study revealed exon 2 as a relatively unexplored source of variation in avian MHC class I, which should be considered in future studies.
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source of these alleles, respectively. The selected reference sequences were UAA-UEA from AY885227 amino acid alleles
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Data availability
The raw sequence reads generated in this study deposited in the NCBI Sequence Read Archive (SRA) database (BioProject ID: PRJNA718702).
References
Alcaide M, Edwards SV, CadahíaJuan L, Negro JJ (2009) MHC class I genes of birds of prey: isolation, polymorphism and diversifying selection. Conserv Genet 10:1349
Campbell LK, Magor KE (2020) Pattern recognition receptor signaling and innate responses to influenza A viruses in the Mallard Duck, compared to humans and chickens. Front Cell Infect Microbiol 10
Chan WF, Parks-Dely JA, Magor BG, Magor KE (2016) The minor MHC class I gene UDA of ducks is regulated by Let-7 microRNA. J Immunol 197:1212
Chappell PE, Meziane EK, Harrison M, Magiera Ł, Hermann C, Mears L, Wrobel AG, Durant C, Nielsen LL, Buus S, Ternette N, Mwangi W, Butter C, Nair V, Ahyee T, Duggleby R, Madrigal A, Roversi P, Lea SM, Kaufman J (2015) Expression levels of MHC class I molecules are inversely correlated with promiscuity of peptide binding. eLife 4:e05345
Drews A, Westerdahl H (2019) Not all birds have a single dominantly expressed MHC-I gene: Transcription suggests that siskins have many highly expressed MHC-I genes. Sci Rep 9:19506
Dunn PO, Bollmer JL, Freeman-Gallant CR, Whittingham LA (2013) MHC variation is related to a sexually selected ornament, survival, and parasite resistance in common yellowthroats. Evolution: International Journal of Organic Evolution 67:679–687
Evseev, Danyel, Magor, Katharine E (2019) Innate immune responses to avian influenza viruses in ducks and chickens. Vet Sci
Fleming-Canepa X, Jensen SM, Mesa CM, Diaz-Satizabal L, Roth AJ, Parks-Dely JA, Moon DA, Wong JP, Evseev D, Gossen DA (2016) Extensive allelic diversity of MHC class I in wild mallard ducks. J Immunol 783
Galan M, Guivier E, Caraux G, Charbonnel N, Cosson JFO (2010) A 454 multiplex sequencing method for rapid and reliable genotyping of highly polymorphic genes in large-scale studies. BMC Genomics 11:296–296
He K, Piotr M, Dunn PO (2020) Long-read genome assemblies reveal extraordinary variation in the number and structure of MHC loci in birds. Genome Biol Evol 13. https://doi.org/10.1093/gbe/evaa1270
Hosomichi K, Shiina T, Suzuki S, Tanaka M, Shimizu S, Iwamoto S, Hara H, Yoshida Y, Kulski JK, Inoko H (2006) The major histocompatibility complex (Mhc) class IIB region has greater genomic structural flexibility and diversity in the quail than the chicken. BMC Genomics 7:322
Jones MR, Cheviron ZA, Carling MD (2015) Spatially variable coevolution between a haemosporidian parasite and the MHC of a widely distributed passerine. Ecol Evol 5:1045–1060
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649
Kikkawa E, Tanaka M, Naruse TK, Tsuda TT, Kimura A (2016) Diversity of MHC class I alleles in Spheniscus humboldti. Immunogenetics 69:1–12
Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19:155–162
Klein J (1986) Natural history of the major histocompatibility complex
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Lobkovsky AE, Levi L, Wolf YI, Maiers M, Gragert L, Alter I, Louzoun Y, Koonin EV (2019) Multiplicative fitness, rapid haplotype discovery, and fitness decay explain evolution of human MHC. Proc Natl Acad Sci 116:14098–14104
Martin Ti, Michal V (2015) Trans-Species Polymorphism in Immune Genes: General Pattern or MHC-Restricted Phenomenon? J Immunol Res 2015:838035
Mesa CM, Thulien KJ, Moon DA, Veniamin SM, Magor KE (2004) The dominant MHC class I gene is adjacent to the polymorphic TAP2 gene in the duck, Anas platyrhynchos. Immunogenetics 56:192–203
Minias P, Bateson ZW, Whittingham LA, Johnson JA, Oyler-Mccance S, Dunn PO (2016) Contrasting evolutionary histories of MHC class I and class II loci in grouse--effects of selection and gene conversion. Heredity
Minias P, Pikus E, Whittingham LA, Dunn PO (2018a) Evolution of copy number at the MHC varies across the avian tree of life. Genome Biol Evol 11:17–28
Minias P, Bateson ZW, Whittingham LA, Johnson JA, Oyler-Mccance S, Dunn PO (2018b) Extensive shared polymorphism at non-MHC immune genes in recently diverged North American prairie grouse. Immunogenetics
Minias P, Gutiérrez JS, Dunn PO (2020) Avian major histocompatibility complex copy number variation is associated with helminth richness. Biol Lett 16:20200194
Minias P, He K, Dunn PO (2021) The strength of selection is consistent across both domains of the MHC class I peptide-binding groove in birds. BMC Ecology and Evolution 21:80
Minias P, Pikus E, Anderwald D (2019) Allelic diversity and selection at the MHC class I and class II in a bottlenecked bird of prey, the White-tailed Eagle. BMC Evol Biol 19:2
Minias P, Pikus E, Whittingham LA, Dunn PO (2018c) A global analysis of selection at the avian MHC. Evolution 72:1278–1293
Minias P, Whittingham LA, Dunn PO (2017) Coloniality and migration are related to selection on MHC genes in birds. Evolution 71:432–441
Moon DA, Veniamin SM, Parks-Dely JA, Magor KE (2005) The MHC of the duck (Anas platyrhynchos) contains five differentially expressed class I genes. J Immunol 175:6702–6712
Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus ADME, Fouchier RAM (2006) Global Patterns of Influenza A Virus in Wild Birds. Science 312:384–388
Radwan J, Kuduk K, Levy E, Lebas N, Babik WA (2015) Parasite load and MHC diversity in undisturbed and agriculturally modified habitats of the ornate dragon lizard. Mol Ecol 23:5966–5978
Sebastian A, Herdegen M, Migalska M, Radwan J (2015) AMPLISAS: a web server for multilocus genotyping using next-generation amplicon sequencing data. Mol Ecol Resour 16
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
Sudhir K, Glen S, Li M, Christina K, Koichiro T (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 6
Sun Z, Pan T, Hu C, Sun L, Zhang B (2017) Rapid and recent diversification patterns in Anseriformes birds: Inferred from molecular phylogeny and diversification analyses. Plos One 12:e0184529
Wallny H-J, Avila D, Hunt LG, Powell TJ, Riegert P, Salomonsen J, Skjødt K, Vainio O, Vilbois F, Wiles MV, Kaufman J (2006) Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC-determined response to Rous sarcoma virus in chickens. Proc Natl Acad Sci 103:1434–1439
Whittingham LA, Dunn PO, Freeman‐Gallant CR, Taff CC, Johnson JA (2018) Major histocompatibility complex variation and blood parasites in resident and migratory populations of the common yellowthroat. J Evol Biol
Wickham H (2009) Ggplot2: elegant graphics for data analysis. Springer Publishing Company, Incorporated
Yu S, Wu J, Bai J, Ding Y, Zhang L (2019) Polymorphic analysis of peptide binding domain of major histocompatibility complex class I in domestic ducks. Pol J Vet Sci 22:415–422
Zeng QQ, He K, Sun DD, Ma MY, Ge YF, Fang SG, Wan QH (2016) Balancing selection and recombination as evolutionary forces caused population genetic variations in golden pheasant MHC class I genes. BMC Evol Biol 16:42
Zhang L, Liu WJ, Wu JQ, Xu ML, Kong Z (2017) Characterization of duck (Anas platyrhynchos) MHC class I gene in two duck lines. J Genet 96:371
Funding
This work was supported by National Natural Science Foundation of China (No. 31600292) and Zhejiang Major Scientific and Technological Projects for Breeding of New Breed of Livestock and Poultry (No. 2016C02054).
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K.H and S.D.Q conceived the study; S.D.Q, H.Y.L, and Y.Y collected and analyzed the data; K.H. and P.O.D. wrote the initial draft; and all authors contributed to and approved the final manuscript.
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No individuals were expressly killed for this study, and this study was approved by ethics committee of Zhejiang A&F University.
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251_2021_1222_MOESM1_ESM.pdf
Supplementary file1 Figure S1 The alignment of 77 (exon 2, A) and 94 (exon 3, B) amino acid sequences found in four Anas. UAA*31 from Fleming-Canepa et al. (2016) was taken as reference sequence, the sequences of top line are consensus sequences generated with Geneious with 25% threshold level of amino acid similarity. Sequences with the same amino acid are indicated by dots (PDF 14171 KB)
251_2021_1222_MOESM2_ESM.pdf
Supplementary file2 Figure S2 The distribution of MHC class I alleles in four Anas: (A) nucleotide alleles of exon 2, (B) amino acid alleles of exon 2, (C) nucleotide alleles of exon 3, and (D) amino acid alleles of exon 3. NT = nucleotide, and AA = amino acid (PDF 2322 KB)
251_2021_1222_MOESM3_ESM.pdf
Supplementary file3 Figure S3 The Wu-Kubat index scores of MHC class I (A) exon 2 and (B) exon 3. Only the aimed regions are listed in the figure. The consensus amino acid sequences inferred by the whole allele of four Anas are listed under the X-axis (PDF 1324 KB)
251_2021_1222_MOESM4_ESM.pdf
Supplementary file4 Figure S4 Phylogenetic tree of MHC class I exon 2 (A) and exon 3 (B) in Anas, based on nucleotide sequences. Clades with supporting values > 70% were marked with an asterisk. Alleles with shade and circles next to some alleles suggested these alleles were detected in more than 2 individuals and can be found in two species, respectively. The 22 selected reference sequences were GU245788.1; GU245871.1; GU245812.2; GU245773.1; KX118679.1; MH218828.1; MH218826.1; GU245810.1; GU245797.1; GU245793.1; GU245849.1; GU245805.1; GU245832.1; GU245874.1; KX118673.1; KX118677.1; KX118684.1) and UAA-UEA from AY885227 (PDF 8687 KB)
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Qin, S., Dunn, P.O., Yang, Y. et al. Polymorphism and varying selection within the MHC class I of four Anas species. Immunogenetics 73, 395–404 (2021). https://doi.org/10.1007/s00251-021-01222-9
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DOI: https://doi.org/10.1007/s00251-021-01222-9