Understanding the immunogenetic basis of coronavirus (CoV) susceptibility in major pathogen reservoirs, such as bats, is central to inferring their zoonotic potential. Members of the cryptic Hipposideros bat species complex differ in CoV susceptibility, but the underlying mechanisms remain unclear. The genes of the major histocompatibility complex (MHC) are the best understood genetic basis of pathogen resistance, and differences in MHC diversity are one possible reason for asymmetrical infection patterns among closely related species. Here, we aimed to link asymmetries in observed CoV (CoV-229E, CoV-2B and CoV-2Bbasal) susceptibility to immunogenetic differences amongst four Hipposideros bat species. From the 2072 bats assigned to their respective species using the mtDNA cytochrome b gene, members of the most numerous and ubiquitous species, Hipposideros caffer D, were most infected with CoV-229E and SARS-related CoV-2B. Using a subset of 569 bats, we determined that much of the existent allelic and functional (i.e. supertype) MHC DRB class II diversity originated from common ancestry. One MHC supertype shared amongst all species, ST12, was consistently linked to susceptibility with CoV-229E, which is closely related to the common cold agent HCoV-229E, and infected bats and those carrying ST12 had a lower body condition. The same MHC supertype was connected to resistance to CoV-2B, and bats with ST12 were less likely be co-infected with CoV-229E and CoV-2B. Our work suggests a role of immunogenetics in determining CoV susceptibility in bats. We advocate for the preservation of functional genetic and species diversity in reservoirs as a means of mitigating the risk of disease spillover.

Charité Universitätsmedizin Berlin Institute of Virology German Centre for Infection Research Berlin Germany

Department of Biological Sciences Macquarie University Sydney New South Wales Australia

Department of Wildlife and Range Management Kwame Nkrumah University of Science and Technology Kumasi Ghana

German Centre for Infection Research Berlin Germany

Institute of Evolutionary Ecology and Conservation Genomics Ulm University Ulm Germany

Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic

Zobrazit více v PubMed

Annan, A., Baldwin, H. J., Corman, V. M., Klose, S. M., Owusu, M., Nkrumah, E. E., Badu, E. K., Anti, P., Agbenyega, O., Meyer, B., Oppong, S., Sarkodie, Y. A., Kalko, E. K. V., Lina, P. H. C., Godlevska, E. V., Reusken, C., Seebens, A., Gloza-Rausch, F., Vallo, P., … Drexler, J. F. (2013). Human betacoronavirus 2c EMC/2012-related viruses in bats, Ghana and Europe. Emerging Infectious Diseases, 19(3), 456-459. https://doi.org/10.3201/eid1903.121503

Anthony, S. J., Johnson, C. K., Greig, D. J., Kramer, S., Che, X., Wells, H., Hicks, A. L., Joly, D. O., Wolfe, N. D., Daszak, P., Karesh, W., Lipkin, W. I., Morse, S. S., Mazet, J. A. K., & Goldstein, T. (2017). Global patterns in coronavirus diversity. Virus Evolution, 3(1), 12. https://doi.org/10.1093/ve/vex012

Anti, P., Owusu, M., Agbenyega, O., Annan, A., Badu, E. K., Nkrumah, E. E., Tschapka, M., Oppong, S., Adu-Sarkodie, Y., & Drosten, C. (2015). Human-bat interactions in rural west Africa. Emerging Infectious Diseases, 21(8), 1418-1421. https://doi.org/10.3201/eid2108.142015

Baldwin, H. J. (2015). Epidemiology and ecology of virus and host: Bats and coronaviruses in Ghana, West Africa. (Thesis). Macquarie University. p. 194.

Baldwin, H. J., Vallo, P., Gardner, M. G., Drosten, C., Tschapka, M., & Stow, A. J. (2014). Isolation and characterization of 11 novel microsatellite loci in a West African leaf-nosed bat, Hipposideros aff. ruber. BMC Research Notes, 7(1), 1-4. https://doi.org/10.1186/1756-0500-7-607

Baldwin, H. J., Vallo, P., Ruiz, A. T., Anti, P., Nkrumah, E. E., Badu, E. K., Oppong, S. K., Kalko, E. K. V., Tschapka, M., & Stow, A. J. (2021). Concordant patterns of genetic, acoustic, and morphological divergence in the West African Old World leaf-nosed bats of the Hipposideros caffer complex. Journal of Zoological Systematics and Evolutionary Research, 59(6), 1390-1407. https://doi.org/10.1111/JZS.12506

Banerjee, A., Baker, M. L., Kulcsar, K., Misra, V., Plowright, R., & Mossman, K. (2020). Novel insights into immune systems of bats. Frontiers in Immunology, 1, 26. https://doi.org/10.3389/fimmu.2020.00026

Banerjee, A., Kulcsar, K., Misra, V., Frieman, M., & Mossman, K. (2019). Bats and coronaviruses. Viruses, 11(1), 41. https://doi.org/10.3390/v11010041

Bartoń, K. (2009). MuMIn: Multi-model inference.

Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B: Methodological, 57(1), 289-300.

Bolnick, D. I., Snowberg, L. K., Caporaso, J. G., Lauber, C., Knight, R., & Stutz, W. E. (2014). Major histocompatibility complex class IIb polymorphism influences gut microbiota composition and diversity. Molecular Ecology, 23(19), 4831-4845. https://doi.org/10.1111/mec.12846

Boni, M. F., Lemey, P., Jiang, X., Tsan-Yuk Lam, T., Perry, B. W., Castoe, T. A., Rambaut, A., & Robertson, D. L. (2020). Evolutionary origins of the SARS-CoV-2 sarbecovirus lineage responsible for the COVID-19 pandemic. Nature Microbiology, 5, 1408-1417. https://doi.org/10.1038/s41564-020-0771-4

Bourgarel, M., Pfukenyi, D. M., Boué, V., Talignani, L., Chiweshe, N., Diop, F., Caron, A., Matope, G., Missé, D., & Liégeois, F. (2018). Circulation of Alphacoronavirus, Betacoronavirus and Paramyxovirus in Hipposideros bat species in Zimbabwe. Infection, Genetics and Evolution, 58, 253-257. https://doi.org/10.1016/J.MEEGID.2018.01.007

Brown, J. H., Jardetzky, T. S., Gorga, J. C., Stern, L. J., Urban, R. G., Strominger, J. L., & Wiley, D. C. (1993). Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature, 364(6432), 33-39. https://doi.org/10.1038/364033a0

Bruchez, A., Sha, K., Johnson, J., Chen, L., Stefani, C., McConnell, H., Gaucherand, L., Prins, R., Matreyek, K. A., Hume, A. J., Mühlberger, E., Schmidt, E. V., Olinger, G. G., Stuart, L. M., & Lacy-Hulbert, A. (2020). MHC class II transactivator CIITA induces cell resistance to Ebola virus and SARS-like coronaviruses. Science, 370(6513), 241-247. https://doi.org/10.1126/SCIENCE.ABB3753

Buchholz, R., Jones Dukes, M., Hecht, S., & Findley, A. M. (2004). Investigating the Turkey's “snood” as a morphological marker of heritable disease resistance. Journal of Animal Breeding and Genetics, 121, 176-185.

Cao, A. T., Yao, S., Gong, B., Elson, C. O., & Cong, Y. (2012). Th17 cells upregulate polymeric Ig receptor and intestinal IgA and contribute to intestinal homeostasis. The Journal of Immunology, 189(9), 4666-4673. https://doi.org/10.4049/jimmunol.1200955

Castelli, E. C., de Castro, M. V., Naslavsky, M. S., Scliar, M. O., Silva, N. S. B., Andrade, H. S., Souza, A. S., Pereira, R. N., Castro, C. F. B., Mendes-Junior, C. T., Meyer, D., Nunes, K., Matos, L. R. B., Silva, M. V. R., Wang, J. Y. T., Esposito, J., Coria, V. R., Bortolin, R. H., Hirata, M. H., … Zatz, M. (2021). MHC variants associated with symptomatic versus asymptomatic SARS-CoV-2 infection in highly exposed individuals. Frontiers in Immunology, 12, 742881. https://doi.org/10.3389/fimmu.2021.742881

Chu, H., Zhou, J., Ho-Yin Wong, B., Li, C., Cheng, Z. S., Lin, X., Kwok-Man Poon, V., Sun, T., Choi-Yi Lau, C., Fuk-Woo Chan, J., Kai-Wang To, K., Chan, K. H., Lu, L., Zheng, B. J., & Yuen, K. Y. (2014). Productive replication of Middle East respiratory syndrome coronavirus in monocyte-derived dendritic cells modulates innate immune response. Virology, 454-455(1), 197-205. https://doi.org/10.1016/J.VIROL.2014.02.018

Civitello, D. J., Cohen, J., Fatima, H., Halstead, N. T., Liriano, J., McMahon, T. A., Ortega, C. N., Sauer, E. L., Sehgal, T., Young, S., & Rohr, J. R. (2015). Biodiversity inhibits parasites: Broad evidence for the dilution effect. Proceedings of the National Academy of Sciences of the United States of America, 112(28), 8667-8671. https://doi.org/10.1073/pnas.1506279112

Corman, V. M., Baldwin, H. J., Tateno, A. F., Zerbinati, R. M., Annan, A., Owusu, M., Nkrumah, E. E., Maganga, G. D., Oppong, S., Adu-Sarkodie, Y., Vallo, P., da Silva Filho, L. V., Leroy, E. M., Thiel, V., van der Hoek, L., Poon, L. L., Tschapka, M., Drosten, C., & Drexler, J. F. (2015). Evidence for an ancestral association of human coronavirus 229E with bats. Journal of Virology, 89(23), 11858-11870. https://doi.org/10.1128/JVI.01755-15

Corman, V. M., Muth, D., Niemeyer, D., & Drosten, C. (2018). Hosts and sources of endemic human coronaviruses. Advances in Virus Research, 100, 163-188. https://doi.org/10.1016/BS.AIVIR.2018.01.001

Crossley, B. M., Mock, R. E., Callison, S. A., & Hietala, S. K. (2012). Identification and characterization of a novel Alpaca respiratory coronavirus most closely related to the human coronavirus 229E. Viruses, 4(12), 3689-3700. https://doi.org/10.3390/V4123689

Davies, C. S., Worsley, S. F., Maher, K. H., Komdeur, J., Burke, T., Dugdale, H. L., & Richardson, D. S. (2022). Immunogenetic variation shapes the gut microbiome in a natural vertebrate population. Microbiome, 10(1), 1-22. https://doi.org/10.1186/S40168-022-01233-Y/FIGURES/5

Dengjel, J., Schoor, O., Fischer, R., Reich, M., Kraus, M., Müller, M., Kreymborg, K., Altenberend, F., Brandenburg, J., Kalbacher, H., Brock, R., Driessen, C., Rammensee, H.-G., & Stevanovic, S. (2005). Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. www.ncbi.nih.govgeo

Doytchinova, I. A., Guan, P., & Flower, D. R. (2004). Identifiying human MHC supertypes using bioinformatic methods. Journal of Immunology, 172, 4314-4323. https://doi.org/10.4049/jimmunol.172.7.4314

Drexler, J. F., Corman, V. M., & Drosten, C. (2014). Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS. Antiviral Research, 101, 45-56.

Drexler, J. F., Corman, V. M., Müller, M. A., Maganga, G. D., Vallo, P., Binger, T., Gloza-Rausch, F., Rasche, A., Yordanov, S., Seebens, A., Oppong, S., Sarkodie, Y. A., Pongombo, C., Lukashev, A. N., Schmidt-Chanasit, J., Stöcker, A., Carneiro, A. J. B., Erbar, S., Maisner, A., … Drosten, C. (2012). Bats host major mammalian paramyxoviruses. Nature Communications, 3, 796. https://doi.org/10.1038/ncomms1796

Drexler, J. F., Kupfer, B., Petersen, N., Grotto, R. M. T., Rodrigues, S. M. C., Grywna, K., Panning, M., Annan, A., Silva, G. F., Douglas, J., Koay, E. C., Smuts, H., Netto, E. M., Simmonds, P., De Moura Campos Pardini, M. I., Roth, W. K., & Drosten, C. (2009). A novel diagnostic target in the hepatitis C virus genome. PLoS Medicine, 6(2), e1000031. https://doi.org/10.1371/JOURNAL.PMED.1000031

Dudek, K., Gaczorek, T. S., Zieliński, P., & Babik, W. (2019). Massive introgression of major histocompatibility complex (MHC) genes in newt hybrid zones. Molecular Ecology, 28(21), 4798-4810. https://doi.org/10.1111/mec.15254

Eby, P., Peel, A. J., Hoegh, A., Madden, W., Giles, J. R., Hudson, P. J., & Plowright, R. K. (2022). Pathogen spillover driven by rapid changes in bat ecology. Nature, 613(7943), 340-344. https://doi.org/10.1038/s41586-022-05506-2

Eizaguirre, C., Lenz, T. L., Kalbe, M., & Milinski, M. (2012a). Divergent selection on locally adapted major histocompatibility complex immune genes experimentally proven in the field. Ecology Letters, 15(7), 723-731. https://doi.org/10.1111/j.1461-0248.2012.01791.x

Eizaguirre, C., Lenz, T. L., Kalbe, M., & Milinski, M. (2012b). Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nature Communications, 3, 621. https://doi.org/10.1038/ncomms1632

Epstein, J. H., Anthony, S. J., Islam, A., Marm Kilpatrick, A., Khan, S. A., Balkey, M. D., Ross, N., Smith, I., Zambrana-Torrelio, C., Tao, Y., Islam, A., Quan, P. L., Olival, K. J., Salah Uddin Khan, M., Gurley, E. S., Jahangir Hossein, M., Field, H. E., Fielder, M. D., Briese, T., … Daszak, P. (2020). Nipah virus dynamics in bats and implications for spillover to humans. Proceedings of the National Academy of Sciences of the United States of America, 117(46), 29190-29201. https://doi.org/10.1073/pnas.2000429117

Fijarczyk, A., & Babik, W. (2015). Detecting balancing selection in genomes: Limits and prospects. Molecular Ecology, 24(14), 3529-3545. https://doi.org/10.1111/mec.13226

Fleischer, R., Schmid, D. W., Wasimuddin Brändel, S. D., Rasche, A., Corman, V. M., Drosten, C., Tschapka, M., & Sommer, S. (2022). Interaction between MHC diversity and constitution, gut microbiota and Astrovirus infections in a neotropical bat. Molecular Ecology, 31, 3342-3359. https://doi.org/10.1111/MEC.16491

Frank, H. K., Enard, D., & Boyd, S. D. (2022). Exceptional diversity and selection pressure on coronavirus host receptors in bats compared to other mammals. Proceedings of the Royal Society B: Biological Sciences, 289(1979), 20220193. https://doi.org/10.1098/RSPB.2022.0193

Frick, W. F., Pollock, J. F., Hicks, A. C., Langwig, K. E., Reynolds, D. S., Turner, G. G., Butchkoski, C. M., & Kunz, T. H. (2010). An emerging disease causes regional population collapse of a common North American bat species. Science, 329(5992), 679-682. https://doi.org/10.1126/science.1188594

Gaczorek, T. S., Marszałek, M., Dudek, K., Arntzen, J. W., Wielstra, B., & Babik, W. (2022). Interspecific introgression of MHC genes in Triturus newts: Evidence from multiple contact zones. Molecular Ecology, 32(4), 867-880. https://doi.org/10.1111/mec.16804

Gaigher, A., Burri, R., San-Jose, L. M., Roulin, A., & Fumagalli, L. (2019). Lack of statistical power as a major limitation in understanding MHC-mediated immunocompetence in wild vertebrate populations. Molecular Ecology, 28(23), 5115-5132. https://doi.org/10.1111/mec.15276

Gibb, R., Redding, D. W., Chin, K. Q., Donnelly, C. A., Blackburn, T. M., Newbold, T., & Jones, K. E. (2020). Zoonotic host diversity increases in human-dominated ecosystems. Nature, 584, 396-402. https://doi.org/10.1038/s41586-020-2562-8

Gillingham, M. A. F., Courtiol, A., Teixeira, M., Galan, M., Bechet, A., & Cezilly, F. (2016). Evidence of gene orthology and trans-species polymorphism, but not of parallel evolution, despite high levels of concerted evolution in the major histocompatibility complex of flamingo species. Journal of Evolutionary Biology, 29(2), 438-454. https://doi.org/10.1111/jeb.12798

Gillingham, M. A. F., Montero, B. K., Wihelm, K., Grudzus, K., Sommer, S., & Santos, P. S. C. (2021). A novel workflow to improve genotyping of multigene families in wildlife species: An experimental set-up with a known model system. Molecular Ecology Resources, 21(3), 982-998. https://doi.org/10.1111/1755-0998.13290

Giotis, E. S., Carnell, G., Young, E. F., Ghanny, S., Soteropoulos, P., Wang, L. F., Barclay, W. S., Skinner, M. A., & Temperton, N. (2019). Entry of the bat influenza H17N10 virus into mammalian cells is enabled by the MHC class II HLA-DR receptor. Nature Microbiology, 4(12), 2035-2038 https://doi.org/10.1038/s41564-019-0517-3

Gouilh, M. A., Puechmaille, S. J., Gonzalez, J. P., Teeling, E., Kittayapong, P., & Manuguerra, J. C. (2011). SARS-Coronavirus ancestor's foot-prints in South-East Asian bat colonies and the refuge theory. Infection, Genetics and Evolution, 11(7), 1690-1702. https://doi.org/10.1016/j.meegid.2011.06.021

Griffith, D. M., Veech, J. A., & Marsh, C. J. (2016). cooccur: Probabilistic species co-occurrence analysis in R. Journal of Statistical Software, 69(1), 1-17. https://doi.org/10.18637/JSS.V069.C02

Han, G., Luong, H., & Vaishnava, S. (2022). Low abundance members of the gut microbiome exhibit high immunogenicity. Gut Microbes, 14(1), 2104086. https://doi.org/10.1080/19490976.2022.2104086

Harman, A. N., Kraus, M., Bye, C. R., Byth, K., Turville, S. G., Tang, O., Mercier, S. K., Nasr, N., Stern, J. L., Slobedman, B., Driessen, C., & Cunningham, A. L. (2009). HIV-1-infected dendritic cells show 2 phases of gene expression changes, with lysosomal enzyme activity decreased during the second phase. Blood, 114(1), 85-94. https://doi.org/10.1182/blood-2008

Hayman, D. T. S., Yu, M., Crameri, G., Wang, L. F., Suu-Ire, R., Wood, J. L. N., & Cunningham, A. A. (2012). Ebola virus antibodies in fruit bats, Ghana, West Africa. Emerging Infectious Diseases, 18(7), 1207-1209. https://doi.org/10.3201/eid1807.111654

Hill, A. V., Allsopp, C. E., Kwiatkowski, D., Anstey, N. M., Twumasi, P., Rowe, P. A., Bennett, S., Brewster, D., McMichael, A. J., & Greenwood, B. M. (1991). Common west African HLA antigens are associated with protection from severe malaria. Nature, 352(6336), 595-600. https://doi.org/10.1038/352595a0

Hoffmann, M., Kleine-Weber, H., Schroeder, S., Krüger, N., Herrler, T., Erichsen, S., Schiergens, T. S., Herrler, G., Wu, N. H., Nitsche, A., Müller, M. A., Drosten, C., & Pöhlmann, S. (2020). SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell, 181(2), 271-280.e8. https://doi.org/10.1016/J.CELL.2020.02.052

Huus, K. E., Petersen, C., & Finlay, B. B. (2021). Diversity and dynamism of IgA−microbiota interactions. Nature Reviews Immunology, 21(8), 514-525. https://doi.org/10.1038/s41577-021-00506-1

Huynh, J., Li, S., Yount, B., Smith, A., Sturges, L., Olsen, J. C., Nagel, J., Johnson, J. B., Agnihothram, S., Gates, J. E., Frieman, M. B., Baric, R. S., & Donaldson, E. F. (2012). Evidence supporting a zoonotic origin of human coronavirus strain NL63. Journal of Virology, 86(23), 12816-12825. https://doi.org/10.1128/jvi.00906-12

Irving, A. T., Ahn, M., Goh, G., Anderson, D. E., & Wang, L. F. (2021). Lessons from the host defences of bats, a unique viral reservoir. Nature, 589(7842), 363-370. https://doi.org/10.1038/s41586-020-03128-0

Ithete, N. L., Stoffberg, S., Corman, V. M., Cottontail, V. M., Richards, L. R., Schoeman, M. C., Drosten, C., Drexler, J. F., & Preiser, W. (2013). Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerging Infectious Diseases, 19(10), 1697-1699.

Jombart, T., Devillard, S., & Balloux, F. (2010). Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genetics, 11(1), 1-15. https://doi.org/10.1186/1471-2156-11-94/FIGURES/9

Karakus, U., Thamamongood, T., Ciminski, K., Ran, W., Günther, S. C., Pohl, M. O., Eletto, D., Jeney, C., Hoffmann, D., Reiche, S., Schinköthe, J., Ulrich, R., Wiener, J., Hayes, M. G. B., Chang, M. W., Hunziker, A., Yángüez, E., Aydillo, T., Krammer, F., … Stertz, S. (2019). MHC class II proteins mediate cross-species entry of bat influenza viruses. Nature, 567, 109-112. https://doi.org/10.1038/s41586-019-0955-3

Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772-780. https://doi.org/10.1093/molbev/mst010

Kaufman, J. (2018a). Unfinished business: Evolution of the MHC and the adaptive immune system of jawed vertebrates. Annual Review of Immunology, 36(1), 383-409. https://doi.org/10.1146/annurev-immunol-051116-052450

Kaufman, J. (2018b). Generalists and specialists: A new view of how MHC class I molecules fight infectious pathogens. Trends in Immunology, 39(5), 367-379. https://doi.org/10.1016/j.it.2018.01.001

Kubinak, J. L., Stephens, W. Z., Soto, R., Petersen, C., Chiaro, T., Gogokhia, L., Bell, R., Ajami, N. J., Petrosino, J. F., Morrison, L., Potts, W. K., Jensen, P. E., O'Connell, R. M., & Round, J. L. (2015). MHC variation sculpts individualized microbial communities that control susceptibility to enteric infection. Nature Communications, 6, 8642. https://doi.org/10.1038/ncomms9642

Laing, E. D., Sterling, S. L., Weir, D. L., Beauregard, C. R., Smith, I. L., Larsen, S. E., Wang, L. F., Snow, A. L., Schaefer, B. C., & Broder, C. C. (2019). Enhanced autophagy contributes to reduced viral infection in black flying fox cells. Viruses, 11(3), 260. https://doi.org/10.3390/v11030260

Latinne, A., Hu, B., Olival, K. J., Zhu, G., Zhang, L., Li, H., Chmura, A. A., Field, H. E., Zambrana-Torrelio, C., Epstein, J. H., Li, B., Zhang, W., Wang, L.-F., Shi, Z.-L., & Daszak, P. (2020). Origin and cross-species transmission of bat coronaviruses in China. Nature Communications, 11(7), 4235. https://doi.org/10.1038/s41467-020-17687-3

Lau, S. K. P., Li, K. S. M., Huang, Y., Shek, C.-T., Tse, H., Wang, M., Choi, G. K. Y., Xu, H., Lam, C. S. F., Guo, R., Chan, K.-H., Zheng, B.-J., Woo, P. C. Y., & Yuen, K.-Y. (2010). Ecoepidemiology and complete genome comparison of different strains of severe acute respiratory syndrome-related Rhinolophus bat coronavirus in China reveal bats as a reservoir for acute, self-limiting infection that allows recombination events. Journal of Virology, 84(6), 2808-2819. https://doi.org/10.1128/JVI.02219-09

Lau, S. K. P., Li, K. S. M., Tsang, A. K. L., Shek, C.-T., Wang, M., Choi, G. K. Y., Guo, R., Wong, B. H. L., Poon, R. W. S., Lam, C. S. F., Wang, S. Y. H., Fan, R. Y. Y., Chan, K.-H., Zheng, B.-J., Woo, P. C. Y., & Yuen, K.-Y. (2012). Recent transmission of a novel alphacoronavirus, bat coronavirus HKU10, from Leschenault's rousettes to pomona leaf-nosed bats: first evidence of interspecies transmission of coronavirus between bats of different suborders. Journal of Virology, 86(21), 11906-11918. https://doi.org/10.1128/jvi.01305-12

Lenz, T. L., Eizaguirre, C., Kalbe, M., & Milinski, M. (2013). Evaluating patterns of convergent evolution and trans-species polymorphism at mhc immunogenes in two sympatric stickleback species. Evolution, 67(8), 2400-2412. https://doi.org/10.1111/evo.12124

Lenz, T. L., Wells, K., Pfeiffer, M., & Sommer, S. (2009). Diverse MHC IIB allele repertoire increases parasite resistance and body condition in the Long-tailed giant rat (Leopoldamys sabanus). BMC Evolutionary Biology, 9, 269. https://doi.org/10.1186/1471-2148-9-269

Leroy, E. M., Epelboin, A., Mondonge, V., Pourrut, X., Gonzalez, J. P., Muyembe-Tamfum, J. J., & Formenty, P. (2009). Human ebola outbreak resulting from direct exposure to fruit bats in Luebo, Democratic Republic of Congo, 2007. Vector Borne and Zoonotic Diseases, 9(6), 723-728. https://doi.org/10.1089/vbz.2008.0167

Letko, M., Seifert, S. N., Olival, K. J., Plowright, R. K., & Munster, V. J. (2020). Bat-borne virus diversity, spillover and emergence. Nature Reviews Microbiology, 18(8), 461-471. https://doi.org/10.1038/s41579-020-0394-z

Li, W., Shi, Z., Yu, M., Ren, W., Smith, C., Epstein, J. H., Wang, H., Crameri, G., Hu, Z., Zhang, H., Zhang, J., McEachern, J., Field, H., Daszak, P., Eaton, B. T., Zhang, S., & Wang, L. F. (2005). Bats are natural reservoirs of SARS-like coronaviruses. Science, 310(5748), 676-679. https://doi.org/10.1126/science.1118391

Li, X., Liu, T., Li, A., Zhang, L., Dai, W., Jin, L., Sun, K., & Feng, J. (2021). Genetic polymorphisms and the independent evolution of major histocompatibility complex class II-DRB in sibling bat species Rhinolophus episcopus and Rhinolophus siamensis. Journal of Zoological Systematics and Evolutionary Research, 59(4), 887-901. https://doi.org/10.1111/jzs.12462

Liang, S. C., Tan, X. Y., Luxenberg, D. P., Karim, R., Dunussi-Joannopoulos, K., Collins, M., & Fouser, L. A. (2006). Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. Journal of Experimental Medicine, 203(10), 2271-2279. https://doi.org/10.1084/jem.20061308

Lighten, J., Papadopulos, A. S. T., Mohammed, R. S., Ward, B. J., Paterson, I. G., Baillie, L., Bradbury, I. R., Hendry, A. P., Bentzen, P., & Van Oosterhout, C. (2017). Evolutionary genetics of immunological supertypes reveals two faces of the Red Queen. Nature Communications, 8(1), 1294. https://doi.org/10.1038/s41467-017-01183-2

Loyal, L., Braun, J., Henze, L., Kruse, B., Dingeldey, M., Reimer, U., Kern, F., Schwarz, T., Mangold, M., Unger, C., Dörfler, F., Kadler, S., Rosowski, J., Gürcan, K., Uyar-Aydin, Z., Frentsch, M., Kurth, F., Schnatbaum, K., Eckey, M., … Giesecke-Thiel, C. (2021). Cross-reactive CD4+ T cells enhance SARS-CoV-2 immune responses upon infection and vaccination. Science, 374(6564), eabh1823. https://doi.org/10.1126/science.abh1823

Luckey, D., Weaver, E. A., Osborne, D. G., Billadeau, D. D., & Taneja, V. (2019). Immunity to influenza is dependent on MHC II polymorphism: Study with 2 HLA transgenic strains. Scientific Reports, 9(1), 19061. https://doi.org/10.1038/s41598-019-55503-1

Lundberg, A. S., & McDevitt, H. O. (1992). Evolution of major histocompatibility complex class II allelic diversity: Direct descent in mice and humans. Immunology, 89, 6545-6549.

Maganga, G. D., Bourgarel, M., Vallo, P., Dallo, T. D., Ngoagouni, C., Drexler, J. F., Drosten, C., Nakouné, E. R., Leroy, E. M., & Morand, S. (2014). Bat distribution size or shape as determinant of viral richness in African bats. PLoS One, 9(6), e100172. https://doi.org/10.1371/journal.pone.0100172

Marques, D. A., Lucek, K., Sousa, V. C., Excoffier, L., & Seehausen, O. (2019). Admixture between old lineages facilitated contemporary ecological speciation in Lake Constance stickleback. Nature Communications, 10, 4240. https://doi.org/10.1038/s41467-019-12182-w

McKiernan, S. M., Hagan, R., Curry, M., McDonald, G. S. A., Kelly, A., Nolan, N., Walsh, A., Hegarty, J., Lawlor, E., & Kelleher, D. (2004). Distinct MHC class I and II alleles are associated with hepatitis C viral clearance, originating from a single source. Hepatology, 40(1), 108-114. https://doi.org/10.1002/hep.20261

Meyer, M., Schmid, D. W., Baldwin, H. J., Wilhelm, K., Nkrumah, E. E., Ebenezer, K. B., Oppong, S. K., Schwensow, N., Vallo, P., Corman, V. M., Tschapka, M., Drosten, C., & Sommer, S. (in review). Bat species assemblage predicts coronavirus prevalence.

Meyer-Lucht, Y., & Sommer, S. (2005). MHC diversity and the association to nematode parasitism in the yellow-necked mouse (Apodemus flavicollis). Molecular Ecology, 14(7), 2233-2243. https://doi.org/10.1111/j.1365-294X.2005.02557.x

Migliorini, F., Torsiello, E., Spiezia, F., Oliva, F., Tingart, M., & Maffulli, N. (2021). Association between HLA genotypes and COVID-19 susceptibility, severity and progression: a comprehensive review of the literature. European Journal of Medical Research, 26(1), 84. https://doi.org/10.1186/s40001-021-00563-1

Milinski, M., Griffiths, S., Wegner, K. M., Reusch, T. B. H., Haas-Assenbaum, A., & Boehm, T. (2005). Mate choice decisions of stickleback females predictably modified by MHC peptide ligands. Proceedings of the National Academy of Sciences, 102(12), 4414-4418. https://doi.org/10.1073/pnas.0408264102

Minias, P., Whittingham, L. A., & Dunn, P. O. (2017). Coloniality and migration are related to selection on MHC genes in birds. Evolution, 71(2), 432-441. https://doi.org/10.1111/EVO.13142

Monadjem, A., Taylor, P., Cotteri, F. P. D. W., Kityo, R., & Fahr, J. (2007). Conservation status of bats in sub-Saharan Africa. Bat Research News, 48(4), 267.

Montero, B. K., Wasimuddin Schwensow, N., Gillingham, M. A. F., Ratovonamana, Y. R., Rakotondranary, S. J., Corman, V. M., Drosten, C., Ganzhorn, J. U., & Sommer, S. (2021). Evidence of MHC class I and II influencing viral and helminth infection via the microbiome in a non − human primate. PLoS One, 17(11), e1009675. https://doi.org/10.1371/journal.ppat.1009675

Moreno Santillán, D. D., Lama, T. M., Gutierrez Guerrero, Y. T., Brown, A. M., Donat, P., Zhao, H., Rossiter, S. J., Yohe, L. R., Potter, J. H., Teeling, E. C., Vernes, S. C., Davies, K. T. J., Myers, E., Hughes, G. M., Huang, Z., Hoffmann, F., Corthals, A. P., Ray, D. A., & Dávalos, L. M. (2021). Large-scale genome sampling reveals unique immunity and metabolic adaptations in Bats. Molecular Ecology, 30(23), 6449-6467. https://doi.org/10.1111/mec.16027

Müller, M. A., Paweska, J. T., Leman, P. A., Drosten, C., Grywna, K., Kemp, A., Braack, L., Sonnenberg, K., Niedrig, M., & Swanepoel, R. (2007). Coronavirus antibodies in African bat species. Emerging Infectious Diseases, 13(9), 1367. https://doi.org/10.3201/EID1309.070342

Munster, V. J., Adney, D. R., van Doremalen, N., Brown, V. R., Miazgowicz, K. L., Milne-Price, S., Bushmaker, T., Rosenke, R., Scott, D., Hawkinson, A., de Wit, E., Schountz, T., & Bowen, R. A. (2016). Replication and shedding of MERS-CoV in Jamaican fruit bats (Artibeus jamaicensis). Scientific Reports, 6, 21878. https://doi.org/10.1038/SREP21878

Nadachowska-Brzyska, K., Zieliński, P., Radwan, J., & Babik, W. (2012). Interspecific hybridization increases MHC class II diversity in two sister species of newts. Molecular Ecology, 21(4), 887-906. https://doi.org/10.1111/j.1365-294X.2011.05347.x

Neefjes, J., Jongsma, M. L. M., Paul, P., & Bakke, O. (2011). Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nature Reviews Immunology, 11(12), 823-836. https://doi.org/10.1038/nri3084

Nicholls, J. A., Double, M. C., Rowell, D. M., & Magrath, R. D. (2000). The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae). Journal of Avian Biology, 31(2), 165-176.

Nkrumah, E. E., Baldwin, H. J., Kofi Badu, E., Anti, P., Vallo, P., Klose, S., Klara, E., Kalko, V., Oppong, S. K., & Tschapka, M. (2021). Diversity and conservation of cave-roosting bats in central Ghana. Tropical Conservation Science, 14, 1-10. https://doi.org/10.1177/19400829211034671

Ovsyannikova, I. G., Haralambieva, I. H., Crooke, S. N., Poland, G. A., Kennedy, R. B., & Richard Kennedy, C. B. (2020). The role of host genetics in the immune response to SARS-CoV-2 and COVID-19 susceptibility and severity. Immunological Reviews, 296, 205-219. https://doi.org/10.1111/imr.12897

Pathak, G. A., Singh, K., Miller-Fleming, T. W., Wendt, F. R., Ehsan, N., Hou, K., Johnson, R., Lu, Z., Gopalan, S., Yengo, L., Mohammadi, P., Pasaniuc, B., Polimanti, R., Davis, L. K., & Mancuso, N. (2021). Integrative genomic analyses identify susceptibility genes underlying COVID-19 hospitalization. Nature Communications, 12(1), 4569. https://doi.org/10.1038/s41467-021-24824-z

Pfefferle, S., Oppong, S., Drexler, J. F., Gloza-Rausch, F., Ipsen, A., Seebens, A., Müller, M. A., Annan, A., Vallo, P., Adu-Sarkodie, Y., Kruppa, T. F., & Drosten, C. (2009). Distant relatives of severe acute respiratory syndrome coronavirus and close relatives of human coronavirus 229E in bats, Ghana. Emerging Infectious Diseases, 15(9), 1377-1384. https://doi.org/10.3201/eid1509.090224

Phillips, K. P., Cable, J., Mohammed, R. S., Herdegen-Radwan, M., Raubic, J., Przesmycka, K. J., van Oosterhout, C., & Radwan, J. (2018). Immunogenetic novelty confers a selective advantage in host-pathogen coevolution. Proceedings of the National Academy of Sciences of the United States of America, 115(7), 1552-1557. https://doi.org/10.1073/pnas.1708597115

Pisanti, S., Deelen, J., Gallina, A. M., Caputo, M., Citro, M., Abate, M., Sacchi, N., Vecchione, C., & Martinelli, R. (2020). Correlation of the two most frequent HLA haplotypes in the Italian population to the differential regional incidence of Covid-19. Journal of Translational Medicine, 18(1), 1-16. https://doi.org/10.1186/S12967-020-02515-5/TABLES/7

Plowright, R. K., Field, H. E., Smith, C., Divljan, A., Palmer, C., Tabor, G., Daszak, P., & Foley, J. E. (2008). Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proceedings of the Royal Society B: Biological Sciences, 275(1636), 861-869. https://doi.org/10.1098/rspb.2007.1260

Quan, P. L., Firth, C., Street, C., Henriquez, J. A., Petrosov, A., Tashmukhamedova, A., Hutchison, S. K., Egholm, M., Osinubi, M. O. V., Niezgoda, M., Ogunkoya, A. B., Briese, T., Rupprecht, C. E., & Ian Lipkin, W. (2010). Identification of a severe acute respiratory syndrome coronavirus-like virus in a leaf-nosed bat in Nigeria. MBio, 1(4), 1-9. https://doi.org/10.1128/mBio.00208-10

Qurkhuli, T., Schwensow, N., Brändel, S. D., Tschapka, M., & Sommer, S. (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(8-9), 575-587. https://doi.org/10.1007/s00251-019-01128-7

Radwan, J., Babik, W., Kaufman, J., Lenz, T. L., & Winternitz, J. (2020). Advances in the evolutionary understanding of MHC polymorphism. Trends in Genetics, 36(4), 298-311. https://doi.org/10.1016/j.tig.2020.01.008

Roland, M. M., Mohammed, A. D., & Kubinak, J. L. (2020). How MHCII signaling promotes benign host-microbiota interactions. PLOS Pathogens, 16(6), e1008558. https://doi.org/10.1371/journal.ppat.1008558

Roved, J., Hansson, B., Stervander, M., Hasselquist, D., & Westerdahl, H. (2022). MHCtools - An R package for MHC high-throughput sequencing data: genotyping, haplotype and supertype inference, and downstream genetic analyses in non-model organisms. Molecular Ecology Resources, 22, 2775-2792. https://doi.org/10.1111/1755-0998.13645

Ruiz-Aravena, M., McKee, C., Gamble, A., Lunn, T., Morris, A., Snedden, C. E., Yinda, C. K., Port, J. R., Buchholz, D. W., Yeo, Y. Y., Faust, C., Jax, E., Dee, L., Jones, D. N., Kessler, M. K., Falvo, C., Crowley, D., Bharti, N., Brook, C. E., … Plowright, R. K. (2021). Ecology, evolution and spillover of coronaviruses from bats. Nature Reviews Microbiology, 20, 299-314. https://doi.org/10.1038/s41579-021-00652-2

Sagonas, K., Runemark, A., Antoniou, A., Lymberakis, P., Pafilis, P., Valakos, E. D., Poulakakis, N., & Hansson, B. (2018). Selection, drift, and introgression shape MHC polymorphism in lizards. Heredity, 122(4), 468-484. https://doi.org/10.1038/s41437-018-0146-2

Salmier, A., De Thoisy, B., Crouau-Roy, B., Lacoste, V., & Lavergne, A. (2016). Spatial pattern of genetic diversity and selection in the MHC class II DRB of three Neotropical bat species. BMC Evolutionary Biology, 16(1), 229. https://doi.org/10.1186/s12862-016-0802-1

Sandberg, M., Eriksson, L., Jonsson, J., Sjöström, M., & Wold, S. (1998). New chemical descriptors relevant for the design of biologically active peptides. A multivariate characterization of 87 amino acids. Journal of Medicinal Chemistry, 41(14), 2481-2491.

Schad, J., Dechmann, D., Voigt, C. C., & Sommer, S. (2011). MHC class II DRB diversity, selection pattern and population structure in a neotropical bat species, Noctilio albiventris. Heredity, 107, 115-126. https://doi.org/10.1038/hdy.2010.173

Schad, J., Dechmann, D. K. N., Voigt, C. C., & Sommer, S. (2012). Evidence for the “Good Genes” model: Association of MHC class II DRB alleles with ectoparasitism and reproductive state in the neotropical lesser bulldog bat, Noctilio albiventris. PLoS One, 7(5), e37101. https://doi.org/10.1371/journal.pone.0037101

Schwensow, N., Castro-Prieto, A., Wachter, B., & Sommer, S. (2019). Immunological MHC supertypes and allelic expression: How low is the functional MHC diversity in free-ranging Namibian cheetahs? Conservation Genetics, 20, 65-80. https://doi.org/10.1007/s10592-019-01143-x

Schwensow, N., Eberle, M., & Sommer, S. (2008). Compatibility counts: MHC-associated mate choice in a wild promiscuous primate. Proceedings of the Royal Society B, 275(1634), 555-564. https://doi.org/10.1098/rspb.2007.1433

Sepil, I., Lachish, S., & Sheldon, B. C. (2013). Mhc-linked survival and lifetime reproductive success in a wild population of great tits. Molecular Ecology, 22(2), 384-396. https://doi.org/10.1111/mec.12123

Silverman, M., Kua, L., Tanca, A., Pala, M., Palomba, A., Tanes, C., Bittinger, K., Uzzau, S., Benoist, C., & Mathis, D. (2017). Protective major histocompatibility complex allele prevents type 1 diabetes by shaping the intestinal microbiota early in ontogeny. Proceedings of the National Academy of Sciences of the United States of America, 114(36), 9671-9676. https://doi.org/10.1073/pnas.1712280114

Sommer, S. (2005). The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Frontiers in Zoology, 2, 16. https://doi.org/10.1186/1742-9994-2-16

Spurgin, L. G., & Richardson, D. S. (2010). How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proceedings of the Royal Society B: Biological Sciences, 277(1684), 979-988. https://doi.org/10.1098/rspb.2009.2084

Subudhi, S., Rapin, N., Bollinger, T. K., Hill, J. E., Donaldson, M. E., Davy, C. M., Warnecke, L., Turner, J. M., Kyle, C. J., Willis, C. K. R., & Misra, V. (2017). A persistently infecting coronavirus in hibernating Myotis lucifugus, the North American little brown bat. Journal of General Virology, 98, 2297-2309. https://doi.org/10.1099/jgv.0.000898

Suu-Ire, R., Obodai, E., Bel-Nono, S. O., Ampofo, W. K., Mazet, J. A. K., Goldstein, T., Johnson, C. K., Smith, B., Boaatema, L., Asigbee, T. W., Awuni, J., Opoku, E., & Kelly, T. R. (2022). Surveillance for potentially zoonotic viruses in rodent and bat populations and behavioral risk in an agricultural settlement in Ghana. One Health Outlook, 4, 6. https://doi.org/10.1186/S42522-022-00061-2

Takahata, N., & Nei, M. (1990). Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics, 124(4), 967-978.

Tay, J. H., Porter, A. F., Wirth, W., & Duchene, S. (2022). The emergence of SARS-CoV-2 variants of concern is driven by acceleration of the substitution rate. Molecular Biology and Evolution, 39(2), 1-9. https://doi.org/10.1093/molbev/msac013

Vallo, P., Guillén-Servent, A., Benda, P., Pires, D. B., & Koubek, P. (2008). Variation of mitochondrial DNA in the Hipposideros caffer complex (Chiroptera: Hipposideridae) and its taxonomic implications. Acta Chiropterologica, 10(2), 193-206. https://doi.org/10.3161/150811008X414782

Veech, J. A. (2013). A probabilistic model for analysing species co-occurrence. Global Ecology and Biogeography, 22, 252-260. https://doi.org/10.1111/j.1466-8238.2012.00789.x

Vietzen, H., Zoufaly, A., Traugott, M., Aberle, J., Aberle, S. W., & Puchhammer-Stöckl, E. (2021). Deletion of the NKG2C receptor encoding KLRC2 gene and HLA-E variants are risk factors for severe COVID-19. Genetics in Medicine, 23(5), 963-967. https://doi.org/10.1038/s41436-020-01077-7

Wacharapluesadee, S., Duengkae, P., Chaiyes, A., Kaewpom, T., Rodpan, A., Yingsakmongkon, S., Petcharat, S., Phengsakul, P., Maneeorn, P., & Hemachudha, T. (2018). Longitudinal study of age-specific pattern of coronavirus infection in Lyle's flying fox (Pteropus lylei) in Thailand. Virology Journal, 15, 38. https://doi.org/10.1186/s12985-018-0950-6

Wang, L. F., Gamage, A. M., Chan, W. O. Y., Hiller, M., & Teeling, E. C. (2021). Decoding bat immunity: The need for a coordinated research approach. Nature Reviews Immunology, 21(5), 269-271. https://doi.org/10.1038/s41577-021-00523-0

Wegner, K. M., Kalbe, M., Kurtz, J., Reusch, T., & Milinski, M. (2003). Parasite selection for immunogenetic optimality. Science, 301(5638), 1343. https://doi.org/10.1126/science.1088293

Westerdahl, H., Asghar, M., Hasselquist, D., & Bensch, S. (2012). Quantitative disease resistance: To better understand parasite-mediated selection on major histocompatibility complex. Proceedings of the Royal Society B: Biological Sciences, 279(1728), 577-584. https://doi.org/10.1098/rspb.2011.0917

Whittingham, L. A., Dunn, P. O., Freeman-Gallant, C. R., Taff, C. C., & Johnson, J. A. (2018). Major histocompatibility complex variation and blood parasites in resident and migratory populations of the common yellowthroat. Journal of Evolutionary Biology, 31(10), 1544-1557. https://doi.org/10.1111/JEB.13349

Xu, B., & Yang, Z. (2013). PamlX: A graphical user interface for PAML. Molecular Biology and Evolution, 13(12), 2723-2724. https://doi.org/10.1093/molbev/mst179

Yang, Z. (2007). PAML 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8), 1586-1591. https://doi.org/10.1093/molbev/msm088

Zeileis, A., Meyer, D., & Hornik, K. (2007). Residual-based shadings for visualizing (conditional) independence. Journal of Computational and Graphical Statistics, 16(3), 507-525. https://doi.org/10.1198/106186007X237856

Zhao, Y., Li, D., Xu, Y., & Zhu, Y. (2014). The genetic diversity and evolution of MHC classII-DRB genes in Rhinolophus sinicus. Acta Theriologica Sinica, 34(3), 262.

Zhou, P., Yang, X. L., Wang, X. G., Hu, B., Zhang, L., Zhang, W., Si, H. R., Zhu, Y., Li, B., Huang, C. L., Chen, H. D., Chen, J., Luo, Y., Guo, H., Di Jiang, R., Liu, M. Q., Chen, Y., Shen, X. R., Wang, X., … Shi, Z. L. (2020). A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature, 579(7798), 270-273. https://doi.org/10.1038/s41586-020-2012-7

Bat species assemblage predicts coronavirus prevalence

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