vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/VJ20.670vavilov-2818Research ArticleГЕНЕТИКА И СЕЛЕКЦИЯ РАСТЕНИЙ НА ИММУНИТЕТ, КАЧЕСТВО, ПРОДУКТИВНОСТЬ И СТРЕССОУСТОЙЧИВОСТЬANIMAL GENETICS AND BREEDINGCелекция продуктивности кур влияет на гены иммунной системыChickens productivity selection affects immune system geneshttps://orcid.org/0000-0002-1478-1261БородинА. М.BorodinА. М.

д. Березняки, Московская область

Нижний Новгород

Bereznyaki, Moscow Region

Nizhnii Novgorod

https://orcid.org/0000-0002-1696-7684АлексеевЯ. И.AlekseevYa. I.

Москва

Санкт-Петербург

Moscow

St. Petersburg

jalex@syntol.ruhttps://orcid.org/0000-0003-3945-4969ГерасимовК. Е.GerasimovK. E.

Москва

Moscow

https://orcid.org/0000-0003-4316-1077КоноваловаН. В.KonovalovaN. V.

Москва

Moscow

https://orcid.org/0000-0003-2777-0948TерентьеваЕ. В.ТerentjevaE. V.

Москва

Moscow

https://orcid.org/0000-0002-4152-2476ЕфимовД. Н.EfimovD. N.

д. Березняки, Московская область

Сергиев Посад, Московская область

Bereznyaki, Moscow Region

Sergiev Posad, Moscow Region

https://orcid.org/0000-0002-8855-2947ЕмануйловаЖ. В.EmanuilovaZh. V.

д. Березняки, Московская область

Bereznyaki, Moscow Region

https://orcid.org/0000-0002-6951-2843ТучемскийЛ. И.TuchemskiyL. I.

д. Березняки, Московская область

Bereznyaki, Moscow Region

https://orcid.org/0000-0002-1026-7513КомаровА. А.KomarovA. A.

д. Березняки, Московская область

Bereznyaki, Moscow Region

https://orcid.org/0000-0003-0081-6336ФисининВ. И.FisininV. I.

Сергиев Посад, Московская область

Bereznyaki, Moscow Region

Селекционно-генетический центр «Смена»; Институт медико-биологических исследованийРоссияBreeding and Genetic Center “Smena”; Institute of Medical and Biological ResearchRussian FederationООО «Синтол»; Институт аналитического приборостроения Российской академии наукРоссияLimited liability company “Syntol”; Institute for Analytical Instrumentation of the Russian Academy of SciencesRussian FederationООО «Синтол»РоссияLimited liability company “Syntol”Russian FederationСелекционно-генетический центр «Смена»; Федеральный научный центр «Всероссийский научно-исследовательский и технологический институт птицеводства» Российской академии наукРоссияBreeding and Genetic Center “Smena”; Federal Scientific Center ”All-Russian Research and Technological Poultry Institute” of the Russian Academy of Sciences, Sergiev PosadRussian FederationСелекционно-генетический центр «Смена»РоссияBreeding and Genetic Center “Smena”Russian FederationФедеральный научный центр «Всероссийский научно-исследовательский и технологический институт птицеводства» Российской академии наукРоссияFederal Scientific Center ”All-Russian Research and Technological Poultry Institute” of the Russian Academy of Sciences, Sergiev PosadRussian Federation202005122020247755760Copyright © Бородин А.М., Алексеев Я.И., Герасимов К.Е., Коновалова Н.В., Tерентьева Е.В., Ефимов Д.Н., Емануйлова Ж.В., Тучемский Л.И., Комаров А.А., Фисинин В.И., 20202020Бородин А.М., Алексеев Я.И., Герасимов К.Е., Коновалова Н.В., Tерентьева Е.В., Ефимов Д.Н., Емануйлова Ж.В., Тучемский Л.И., Комаров А.А., Фисинин В.И.Borodin А.М., Alekseev Y.I., Gerasimov K.E., Konovalova N.V., Тerentjeva E.V., Efimov D.N., Emanuilova Z.V., Tuchemskiy L.I., Komarov A.A., Fisinin V.I.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/2818

Локусы количественных признаков, связанные с иммунными свойствами кур, представляют интерес с точки зрения получения устойчивых к инфекционным агентам животных при помощи маркер-опосредованной (геномной) селекции. В процессе подбора маркеров для геномной селекции у кур бройлерного типа выявлена нестандартная частота аллеля гена RACK1 (SNP Gga_rs15788101) у кур линии Б5 мясного кросса селекции СГЦ «Смена» и возникло предположение о том, что этот ген вовлечен в селекцию. Поэтому было решено исследовать доступные полиморфизмы в трех генах, ответственных за титр IgY (DMA, RACK1 и CD1B). Молекулярное типирование однонуклеотидных полиморфизмов трех локусов показало приближение к фиксации неблагоприятных аллелей генов DMA (SNP Gga_rs15788237) и RACK1 и преобладание благоприятного аллеля гена CD1B (SNP Gga_rs16057130). При анализе гаплотипов выявлено сильное неравновесное сцепление этих генов. Это свидетельствует о том, что данные гены испытывают селекционное давление. Исследование белоккодирующих последовательностей генов CD1B и DMA различных пород кур продемонстрировало негативную селекцию этих генов. Для того чтобы понять, является ли фиксация изученных аллелей результатом направленной селекции кур линии Б5 мясного кросса СГЦ «Смена», проведен анализ аналогичных локусов у кур яичной селекции «Хайсекс белый». Частоты аллелей в локусах гена CD1B (Gga_rs16057130) и гена RACK1 (Gga_rs15788101) в геноме кур «Хайсекс белый» отличаются от частот аллелей, полученных для кур линии Б5 мясного кросса селекции СГЦ «Смена». Можно предположить, что фиксация аллеля в гене DMA (SNP Gga_rs15788237) связана с искусственным или естественным отбором, единым для кур мясной и яичной селекции. Изменения в локусах Gga_rs16057130 и Gga_rs15788101 у кур линии Б5 мясного кросса селекции СГЦ «Смена», скорее всего, связаны с искусственной селекцией признаков продуктивности бройлеров, которая в дальнейшем может привести к фиксации аллелей в этих локусах. Искусственная селекция кур ведет к деградации вариабельности генов, кодирующих элементы иммунной системы и, как следствие, уменьшению резистентности к различным заболеваниям. Изучение негативного влияния селекции хозяйственных признаков на иммунитет должно способствовать снижению отрицательных последствий и поиску способов получения резистентных к заболеваниям животных.

The quantitative trait loci associated with the immune properties of chickens are of interest from the point of view of obtaining animals resistant to infectious agents using marker-assisted selection. In the process of selecting markers for genomic selection in broiler-type chickens, a non-standard genotype frequency of the RACK1 gene allele (SNP Gga_rs15788101) in the B5 line of broiler-type chicken cross Smena 8 was identified and it was suggested that this gene was involved in selection. Therefore, it was decided to investigate the available polymorphisms in the three genes responsible for the IgY titer (DMA, RACK1 and CD1B). Molecular typing of single nucleotide polymorphisms of three loci revealed an approach to fixation of the unfavorable allele of the DMA gene (SNP Gga_rs15788237), an approach to fixation of the unfavorable allele of the RACK1 gene and the prevalence of the favorable CD1B gene allele (SNP Gga_rs16057130). Analysis of the haplotypes revealed a strong linkage disequilibrium of these genes. This suggests that these genes experience selection pressure. Analysis of the protein-coding sequences of the CD1B and DMA genes of various breeds of chickens revealed a negative selection of these genes. In order to understand whether the fixation of the studied alleles is the result of artificial selection of the B5 line of the cross Smena 8, an analysis of similar loci in layer chickens Hisex White was carried out. The frequencies of the alleles at the loci of the CD1B gene (Gga_rs16057130) and the RACK1 gene (Gga_rs15788101) in the Hisex White chicken genome differ from the frequencies of the alleles obtained for chickens of the B5 line of the cross Smena 8. It can be assumed that the fixation of the allele in the DMA gene (SNP Gga_rs15723) is associated with artificial or natural selection, consistent in broilers and layers. Changes in the loci Gga_rs16057130 and Gga_rs15788101 in the B5 line of the Smena 8 chickens are most likely associated with artificial selection of broiler productivity traits, which can subsequently lead to fixation of alleles at these loci. Artificial breeding of chickens leads to degradation of the variability of genes encoding elements of the immune system, which can cause a decrease in resistance to various diseases. The study of the negative impact of selection of economic traits on immunity should provide means to mitigate negative consequences and help find ways to obtain disease-resistant animals.

гены иммунной системы курфиксация аллелейнегативная селекцияchickens immune system genesallele fixationnegative selectionРабота выполнена по государственному заданию ФГБУ Селекционно-генетический центр «Смена» № 075-01297-20-00 от 18.12.2019.ReferencesAbplanalp H., Lowry D.C., Van Middelkoop J.H. Selection for increased incidence of double-yolked egg in white leghorn chickens. Br. Poult. Sci. 1977;18(5):585-595. DOI 10.1080/00071667708416407.Abplanalp H., Lowry D.C., Van Middelkoop J.H. Selection for increased incidence of double-yolked egg in white leghorn chickens. Br. Poult. Sci. 1977;18(5):585-595. DOI 10.1080/00071667708416407.Anoosha P., Sakthivel R., Gromiha M.M. Prediction of protein disorder on amino acid substitutions. Anal. Biochem. 2015;491:18-22. DOI 10.1016/j.ab.2015.08.028.Anoosha P., Sakthivel R., Gromiha M.M. Prediction of protein disorder on amino acid substitutions. Anal. Biochem. 2015;491:18-22. DOI 10.1016/j.ab.2015.08.028.Barral D.C., Brenner M.B. CD1 antigen presentation: how it works. Nat. Rev. Immunol. 2007;7(12):929-941. DOI 10.1038/nri2191.Barral D.C., Brenner M.B. CD1 antigen presentation: how it works. Nat. Rev. Immunol. 2007;7(12):929-941. DOI 10.1038/nri2191.Bosse M., Megens H.J., Derks M.F.L., de Cara Á.M.R., Groenen M.A.M. Deleterious alleles in the context of domestication, inbreeding, and selection. Evol. Appl. 2018;12(1):6-17. DOI 10.1111/eva.12691.Bosse M., Megens H.J., Derks M.F.L., de Cara Á.M.R., Groenen M.A.M. Deleterious alleles in the context of domestication, inbreeding, and selection. Evol. Appl. 2018;12(1):6-17. DOI 10.1111/eva.12691.Chazara O., Tixier-Boichard M., Morin V., Zoorob R., Bed’hom B. Organisation and diversity of the class II DM region of the chicken MHC. Mol. Immunol. 2011;48(9-10):1263-1271. DOI 10.1016/j.molimm.2011.03.009.Chazara O., Tixier-Boichard M., Morin V., Zoorob R., Bed’hom B. Organisation and diversity of the class II DM region of the chicken MHC. Mol. Immunol. 2011;48(9-10):1263-1271. DOI 10.1016/j.molimm.2011.03.009.Cheema M.A., Qureshi M.A., Havenstein G.B. A comparison of the immune response of a 2001 commercial broiler with a 1957 randombred broiler strain when fed representative 1957 and 2001 broiler diets. Poult. Sci. 2003;82(10):1519-1529. DOI 10.1093/ps/82.10.1519.Cheema M.A., Qureshi M.A., Havenstein G.B. A comparison of the immune response of a 2001 commercial broiler with a 1957 randombred broiler strain when fed representative 1957 and 2001 broiler diets. Poult. Sci. 2003;82(10):1519-1529. DOI 10.1093/ps/82.10.1519.Chen H., Blanchette M. Detecting non-coding selective pressure in coding regions. BMC Evol. Biol. 2007;7(Suppl 1):S9. DOI 10.1186/1471-2148-7-S1-S9.Chen H., Blanchette M. Detecting non-coding selective pressure in coding regions. BMC Evol. Biol. 2007;7(Suppl 1):S9. DOI 10.1186/1471-2148-7-S1-S9.Dias da Silva W., Tambourgi D.V. IgY: a promising antibody for use in immunodiagnostic and in immunotherapy. Vet. Immunol. Immunophatol. 2010;135(3-4):173-180. DOI 10.1016/j.vetimm.2009.12.011.Dias da Silva W., Tambourgi D.V. IgY: a promising antibody for use in immunodiagnostic and in immunotherapy. Vet. Immunol. Immunophatol. 2010;135(3-4):173-180. DOI 10.1016/j.vetimm.2009.12.011.Drake J.A, Bird C., Nemesh J., Thomas D.J., Newton-Cheh C., Reymond A., Excoffier L., Attar H., Antonarakis S.E., Dermitzakis E.T., Hirschhorn J.N. Conserved noncoding sequences are selectively constrained and not mutation cold spots. Nat. Genet. 2006;38(2): 223-227. DOI 10.1038/ng1710.Drake J.A, Bird C., Nemesh J., Thomas D.J., Newton-Cheh C., Reymond A., Excoffier L., Attar H., Antonarakis S.E., Dermitzakis E.T., Hirschhorn J.N. Conserved noncoding sequences are selectively constrained and not mutation cold spots. Nat. Genet. 2006;38(2): 223-227. DOI 10.1038/ng1710.Elferink M.G., Megens H.J., Vereijken A., Hu X., Crooijmans R.P.,Elferink M.G., Megens H.J., Vereijken A., Hu X., Crooijmans R.P.,Groenen M.A. Signatures of selection in the genomes of commercial and non-commercial chicken breeds. PLoS One. 2012;7(2):e32720.DOI 10.1371/journal.pone.0032720.Groenen M.A. Signatures of selection in the genomes of commercial and non-commercial chicken breeds. PLoS One. 2012;7(2):e32720.DOI 10.1371/journal.pone.0032720.Emam M., Mehrabani-Yeganeh H., Barjesteh N., Nikbakht G., Thompson-Crispi K., Charkhkar S., Mallard B. The influence of genetic background versus commercial breeding programs on chicken immunocompetence. Poult. Sci. 2014;93(1):77-84. DOI 10.3382/ps.2013-03475.Emam M., Mehrabani-Yeganeh H., Barjesteh N., Nikbakht G., Thompson-Crispi K., Charkhkar S., Mallard B. The influence of genetic background versus commercial breeding programs on chicken immunocompetence. Poult. Sci. 2014;93(1):77-84. DOI 10.3382/ps.2013-03475.Fleming D.S., Koltes J.E., Markey A.D., Schmidt C.J., Ashwell C.M., Rothschild M.F., Persia M.E., Reecy J.M., Lamont S.L. Genomic analysis of Ugandan and Rwandan chicken ecotypes using a 600 K genotyping array. BMC Genom. 2016;17:407. DOI 10.1186/s12864-016-2711-5.Fleming D.S., Koltes J.E., Markey A.D., Schmidt C.J., Ashwell C.M., Rothschild M.F., Persia M.E., Reecy J.M., Lamont S.L. Genomic analysis of Ugandan and Rwandan chicken ecotypes using a 600 K genotyping array. BMC Genom. 2016;17:407. DOI 10.1186/s12864-016-2711-5.Futuyma D.J. Evolution: Third Edition. Sunderland, MA: Sinauer Associates, Inc., 2013. 656 p.Futuyma D.J. Evolution: Third Edition. Sunderland, MA: Sinauer Associates, Inc., 2013. 656 p.Gaunt T.R., Rodrigues S., Day I.N. Cubic exact solutions for the estimation of pairwise haplotype frequencies: implications for linkage disequilibrium analyses and a web tool ‘CubeX’. BMC Bioinform. 2007;8:428. DOI 10.1186/1471-2105-8-428.Gaunt T.R., Rodrigues S., Day I.N. Cubic exact solutions for the estimation of pairwise haplotype frequencies: implications for linkage disequilibrium analyses and a web tool ‘CubeX’. BMC Bioinform. 2007;8:428. DOI 10.1186/1471-2105-8-428.Guo X., Fang Q., Ma C., Zhou B., Wan Y., Jiang R. Whole-genome resequencing of Xishuangbanna fighting chicken to identify signatures of selection. Genet. Sel. Evol. 2016;48(1):62. DOI 10.1186/s12711-016-0239-4.Guo X., Fang Q., Ma C., Zhou B., Wan Y., Jiang R. Whole-genome resequencing of Xishuangbanna fighting chicken to identify signatures of selection. Genet. Sel. Evol. 2016;48(1):62. DOI 10.1186/s12711-016-0239-4.Hedrick P.W., Garcia-Dorado A. Understanding Inbreeding Depression, Purging, and Genetic Rescue. Trends Ecol. Evol. 2016;31(12): 940-952. DOI 10.1016/j.tree.2016.09.005.Hedrick P.W., Garcia-Dorado A. Understanding Inbreeding Depression, Purging, and Genetic Rescue. Trends Ecol. Evol. 2016;31(12): 940-952. DOI 10.1016/j.tree.2016.09.005.Hocking P.M. Unexpected consequences of genetic selection in broilers and turkeys: problems and solutions. Br. Poult. Sci. 2014;55(1):1-12. DOI 10.1080/00071668.2014.877692.Hocking P.M. Unexpected consequences of genetic selection in broilers and turkeys: problems and solutions. Br. Poult. Sci. 2014;55(1):1-12. DOI 10.1080/00071668.2014.877692.Hurst L.D. Fundamental concepts in genetics: genetics and the understanding of selection. Nat. Rev. Genet. 2009;10(2):83-93. DOI 10.1038/nrg2506.Hurst L.D. Fundamental concepts in genetics: genetics and the understanding of selection. Nat. Rev. Genet. 2009;10(2):83-93. DOI 10.1038/nrg2506.Iglesias G.M., Canet Z.E., Cantaro H., Miquel M.C., Melo J.E., Miller M.M., Berres M.E., Fulton J.E. Mhc-B haplotypes in “Campero-Inta” chicken synthetic line. Poult. Sci. 2019;98(11):5281-5286. DOI 10.3382/ps/pez431.Iglesias G.M., Canet Z.E., Cantaro H., Miquel M.C., Melo J.E., Miller M.M., Berres M.E., Fulton J.E. Mhc-B haplotypes in “Campero-Inta” chicken synthetic line. Poult. Sci. 2019;98(11):5281-5286. DOI 10.3382/ps/pez431.Kaiser M.G., Deeb N., Lamont S.J. Microsatellite markers linked to Salmonella enterica serovar enteritidis vaccine response in young F1 broiler-cross chicks. Poult. Sci. 2002;81(2):193-201. DOI 10.1093/ps/81.2.193.Kaiser M.G., Deeb N., Lamont S.J. Microsatellite markers linked to Salmonella enterica serovar enteritidis vaccine response in young F1 broiler-cross chicks. Poult. Sci. 2002;81(2):193-201. DOI 10.1093/ps/81.2.193.Katzman S., Kern A.D., Bejerano G., Fewell G., Fulton L., Wilson R.K., Salama S.R., Haussler D. Human genome ultraconserved elements are ultraselected. Science. 2007;317(5840):915. DOI 10.1126/ science.1142430.Katzman S., Kern A.D., Bejerano G., Fewell G., Fulton L., Wilson R.K., Salama S.R., Haussler D. Human genome ultraconserved elements are ultraselected. Science. 2007;317(5840):915. DOI 10.1126/ science.1142430.Keller M.C., Visscher P.M., Goddard M.E. Quantification of inbreeding due to distant ancestors and its detection using dense single nucleotide polymorphism data. Genetics. 2011;189(1):237-249. DOI 10.1534/genetics.111.130922.Keller M.C., Visscher P.M., Goddard M.E. Quantification of inbreeding due to distant ancestors and its detection using dense single nucleotide polymorphism data. Genetics. 2011;189(1):237-249. DOI 10.1534/genetics.111.130922.Koenen M.E., Boonstra-Blom A.G., Jeurissen S.H. Immunological differences between layer and broiler type chickens. Vet. Immunol. Immunophatol. 2002;89(1-2):47-56. DOI 10.1016/S0165-2427(02) 00169-1.Koenen M.E., Boonstra-Blom A.G., Jeurissen S.H. Immunological differences between layer and broiler type chickens. Vet. Immunol. Immunophatol. 2002;89(1-2):47-56. DOI 10.1016/S0165-2427(02) 00169-1.Koonin E.V., Wolf Y.I. Constraints and plasticity in genome and molecular-phenome evolution. Nat. Rev. Genet. 2010;11(7):487-498. DOI 10.1038/nrg2810.Koonin E.V., Wolf Y.I. Constraints and plasticity in genome and molecular-phenome evolution. Nat. Rev. Genet. 2010;11(7):487-498. DOI 10.1038/nrg2810.Kosakovsky Pond S.L., Frost S.D. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 2005;22(5):1208-1222. DOI 10.1093/molbev/msi105.Kosakovsky Pond S.L., Frost S.D. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 2005;22(5):1208-1222. DOI 10.1093/molbev/msi105.Latorra D., Campbell K., Wolter A., Hurley J.M. Enhanced allele-specific PCR discrimination in SNP genotyping using 3′ locked nucleic acid (LNA) primers. Hum. Mutat. 2003;22(1):79-85. DOI 10.1002/humu.10228.Latorra D., Campbell K., Wolter A., Hurley J.M. Enhanced allele-specific PCR discrimination in SNP genotyping using 3′ locked nucleic acid (LNA) primers. Hum. Mutat. 2003;22(1):79-85. DOI 10.1002/humu.10228.Li J.J., Wang Y., Yang C.W., Ran J.S., Jiang X.S., Du H.R., Hu Y.D., Liu Y.P. Genotypes of IFIH1 and IFIT5 in seven chicken breeds indicated artificial selection for commercial traits influenced antiviral genes. Infect. Genet. Evol. 2017;56:54-61. DOI 10.1016/j.meegid.2017.10.019.Li J.J., Wang Y., Yang C.W., Ran J.S., Jiang X.S., Du H.R., Hu Y.D., Liu Y.P. Genotypes of IFIH1 and IFIT5 in seven chicken breeds indicated artificial selection for commercial traits influenced antiviral genes. Infect. Genet. Evol. 2017;56:54-61. DOI 10.1016/j.meegid.2017.10.019.Ma Y., Gu L., Yang L., Sun C., Xie S., Fang C., Gong Y., Li S. Identifying artificial selection signals in the chicken genome. PLoS One. 2018;13(4):e0196215. DOI 10.1371/journal.pone.0196215.Ma Y., Gu L., Yang L., Sun C., Xie S., Fang C., Gong Y., Li S. Identifying artificial selection signals in the chicken genome. PLoS One. 2018;13(4):e0196215. DOI 10.1371/journal.pone.0196215.Marchesi J.A.P., Buzanskas M.E., Cantão M.E., Ibelli A.M.G., Peixoto J.O., Joaquim L.B., Moreira G.C.M., Godoy T.F., Sbardella A.P., Figueiredo E.A.P., Coutinho L.L., Munari DP., Ledur M.C. Relationship of runs of homozygosity with adaptive and production traits in a paternal broiler line. Animal. 2018;12(6):1126-1134. DOI 10.1017/S1751731117002671.Marchesi J.A.P., Buzanskas M.E., Cantão M.E., Ibelli A.M.G., Peixoto J.O., Joaquim L.B., Moreira G.C.M., Godoy T.F., Sbardella A.P., Figueiredo E.A.P., Coutinho L.L., Munari DP., Ledur M.C. Relationship of runs of homozygosity with adaptive and production traits in a paternal broiler line. Animal. 2018;12(6):1126-1134. DOI 10.1017/S1751731117002671.McQuillan R., Leutenegger A.L., Abdel-Rahman R., Franklin C.S., Pericic M., Barac-Lauc L., Smolej-Narancic N., Janicijevic B., Polasek O., Tenesa A., Macleod A.K., Farrington S.M., Rudan P., Hayward C., Vitart V., Rudan I., Wild S.H., Dunlop M.G., Wright A.F., Campbell H., Wilson J.F. Runs of Homozygosity in European Populations. Am. J. Hum. Genet. 2008;83(3):359-372. DOI 10.1016/j.ajhg.2008.08.007.McQuillan R., Leutenegger A.L., Abdel-Rahman R., Franklin C.S., Pericic M., Barac-Lauc L., Smolej-Narancic N., Janicijevic B., Polasek O., Tenesa A., Macleod A.K., Farrington S.M., Rudan P., Hayward C., Vitart V., Rudan I., Wild S.H., Dunlop M.G., Wright A.F., Campbell H., Wilson J.F. Runs of Homozygosity in European Populations. Am. J. Hum. Genet. 2008;83(3):359-372. DOI 10.1016/j.ajhg.2008.08.007.Nguyen-Phuc H., Fulton J.E., Berres M.E. Genetic variation of major histocompatibility complex (MHC) in wild Red Junglefowl (Gallus gallus). Poult. Sci. 2016;95(2):400-411. DOI 10.3382/ps/pev364.Nguyen-Phuc H., Fulton J.E., Berres M.E. Genetic variation of major histocompatibility complex (MHC) in wild Red Junglefowl (Gallus gallus). Poult. Sci. 2016;95(2):400-411. DOI 10.3382/ps/pev364.Rozas J., Ferrer-Mata A., Sánchez-DelBarrio J.C., Guirao-Rico S., Librado P., Ramos-Onsins S.E., Sánchez-Gracia A. DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. Mol. Biol. Evol. 2017;34(12):3299-3302. DOI 10.1093/molbev/msx248.Rozas J., Ferrer-Mata A., Sánchez-DelBarrio J.C., Guirao-Rico S., Librado P., Ramos-Onsins S.E., Sánchez-Gracia A. DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. Mol. Biol. Evol. 2017;34(12):3299-3302. DOI 10.1093/molbev/msx248.Rubin C.-J., Zody M.C., Eriksson J., Meadows J.R., Sherwood E., Webster M.T., Jiang L., Ingman M., Sharpe T., Ka S., Hallböök F., Besnier F., Carlborg Ö., Bed’hom B., Tixier-Boichard M., Jensen P., Siegel P., Lindblad-Toh K., Andersson L. Whole-genome resequencing reveals loci under selection during chicken domestication. Nature. 2010;464(7288):587-591. DOI 10.1038/nature08832.Rubin C.-J., Zody M.C., Eriksson J., Meadows J.R., Sherwood E., Webster M.T., Jiang L., Ingman M., Sharpe T., Ka S., Hallböök F., Besnier F., Carlborg Ö., Bed’hom B., Tixier-Boichard M., Jensen P., Siegel P., Lindblad-Toh K., Andersson L. Whole-genome resequencing reveals loci under selection during chicken domestication. Nature. 2010;464(7288):587-591. DOI 10.1038/nature08832.Slawinska A., Siwek M. Meta - and combined - QTL analysis of different experiments on immune traits in chickens. J. Appl. Genet. 2013; 54(4):483-7. DOI 10.1007/s13353-013-0177-6.Slawinska A., Siwek M. Meta - and combined - QTL analysis of different experiments on immune traits in chickens. J. Appl. Genet. 2013; 54(4):483-7. DOI 10.1007/s13353-013-0177-6.Smith J.M., Haigh J. The hitch-hiking effect of a favorable gene. Genet. Res. 1974;23(1):23-35. DOI 10.1017/S0016672308009579. Waterhouse A., Bertoni M., Bienert S., Studer G., Tauriello G., Gumienny R., Heer F.T., de Beer T.A.P., Rempfer C., Bordoli L., Lepore R., Schwede T. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46(W1):W296-W303. DOI 10.1093/nar/gky427.Smith J.M., Haigh J. The hitch-hiking effect of a favorable gene. Genet. Res. 1974;23(1):23-35. DOI 10.1017/S0016672308009579. Waterhouse A., Bertoni M., Bienert S., Studer G., Tauriello G., Gumienny R., Heer F.T., de Beer T.A.P., Rempfer C., Bordoli L., Lepore R., Schwede T. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46(W1):W296-W303. DOI 10.1093/nar/gky427.Yonash N., Cheng H.H., Hillel J., Heller D.E., Cahaner A. DNA microsatellites linked to quantitative trait loci affecting antibody response and survival rate in meat-type chickens. Poult. Sci. 2001;80(1):22-28. DOI 10.1093/ps/80.1.22. You Y., Moreira B.G., BehLke M.A., Owczarzy R. Design of LNA probes that improve mismatch discrimination. Nucleic Acids Res. 2006;34(8):e60. DOI 10.1093/nar/gkl175.Yonash N., Cheng H.H., Hillel J., Heller D.E., Cahaner A. DNA microsatellites linked to quantitative trait loci affecting antibody response and survival rate in meat-type chickens. Poult. Sci. 2001;80(1):22-28. DOI 10.1093/ps/80.1.22. You Y., Moreira B.G., BehLke M.A., Owczarzy R. Design of LNA probes that improve mismatch discrimination. Nucleic Acids Res. 2006;34(8):e60. DOI 10.1093/nar/gkl175.Zekarias B., Ter Huurne A.A., Landman W.J., Rebel J.M., Pol J.M., Gruys E. Immunological basis of differences in disease resistance in the chicken. Vet. Res. 2002;33(2):109-125. DOI 10.1051/vetres:2002001.Zekarias B., Ter Huurne A.A., Landman W.J., Rebel J.M., Pol J.M., Gruys E. Immunological basis of differences in disease resistance in the chicken. Vet. Res. 2002;33(2):109-125. DOI 10.1051/vetres:2002001.Zerbino D.R., Achuthan P., Akanni W., Amode M.R., Barrell D., Bhai J., Billis K., Cummins C., Gall A., Girón C.G., Gil L., Gordon L., Haggerty L., Haskell E., Hourlier T., Izuogu O.G., Janacek S.H., Juettemann T., To J.K., Laird M.R., Lavidas I., Liu Z., Loveland J.E., Maurel T., McLaren W., Moore B., Mudge J., Murphy D.N., Newman V., Nuhn M., Ogeh D., Ong C.K., Parker A., Patricio M., Riat H.S., Schuilenburg H., Sheppard D., Sparrow H., Taylor K., Thormann A., Vullo A., Walts B., Zadissa A., Frankish A., Hunt S.E., Kostadima M., Langridge N., Martin F.J., Muffato M., Perry E., Ruffier M., Staines D.M., Trevanion S.J., Aken B.L., Cunningham F., Yates A., Flicek P. Ensembl 2018. Nucleic Acids Res. 2018;46(D1):D754-D761. DOI 10.1093/nar/gkx1098.Zerbino D.R., Achuthan P., Akanni W., Amode M.R., Barrell D., Bhai J., Billis K., Cummins C., Gall A., Girón C.G., Gil L., Gordon L., Haggerty L., Haskell E., Hourlier T., Izuogu O.G., Janacek S.H., Juettemann T., To J.K., Laird M.R., Lavidas I., Liu Z., Loveland J.E., Maurel T., McLaren W., Moore B., Mudge J., Murphy D.N., Newman V., Nuhn M., Ogeh D., Ong C.K., Parker A., Patricio M., Riat H.S., Schuilenburg H., Sheppard D., Sparrow H., Taylor K., Thormann A., Vullo A., Walts B., Zadissa A., Frankish A., Hunt S.E., Kostadima M., Langridge N., Martin F.J., Muffato M., Perry E., Ruffier M., Staines D.M., Trevanion S.J., Aken B.L., Cunningham F., Yates A., Flicek P. Ensembl 2018. Nucleic Acids Res. 2018;46(D1):D754-D761. DOI 10.1093/nar/gkx1098.Zhang L., Li P., Liu R., Zheng M., Sun Y., Wu D., Hu Y., Wen J., Zhao G. The identification of loci for immune traits in chickens using a genome-wide association study. PloS One. 2015;10(3):e0117269. DOI 10.1371/journal.pone.0117269.Zhang L., Li P., Liu R., Zheng M., Sun Y., Wu D., Hu Y., Wen J., Zhao G. The identification of loci for immune traits in chickens using a genome-wide association study. PloS One. 2015;10(3):e0117269. DOI 10.1371/journal.pone.0117269.

The authors declare that there are no conflicts of interest present.