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Abdelmanova A.S., Kharzinova V.R., Fornara M.S., Chinarov R.Yu., Boronetskaya O.I., Sermyagin A.A., Trukhachev V.I., Zinovieva N.A. Estimation of genetic relationships of black-and-white cattle breeds with ancestral populations based of genome-wide SNP-genotyping of modern and museum samples. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2024, Vol. 59, № 4, p. 605-619.
(how to cite this article)

doi: 10.15389/agrobiology.2024.4.605eng

UDC: 636.2:57.082.133:577.2

Acknowledgements:
The equipment of the Center for Collective Use «Bioresources and bioengineering of farm animals» (Ernst Federal Research Center for Animal Husbandry) was used.
Supported financially by the Russian Science Foundation, project No. 19-76-20012

 

ESTIMATION OF GENETIC RELATIONSHIPS OF BLACK-AND-WHITE CATTLE BREEDS WITH ANCESTRAL POPULATIONS BASED OF GENOME-WIDE SNP-GENOTYPING OF MODERN AND MUSEUM SAMPLES

A.S. Abdelmanova1 ✉, V.R. Kharzinova1, M.S. Fornara1,
R.Yu. Chinarov1, O.I. Boronetskaya2, A.A. Sermyagin1,
V.I. Trukhachev2, N.A. Zinovieva1

1Ernst Federal Research Center for Animal Husbandry, 60, pos. Dubrovitsy, Podolsk District, Moscow Province, 142132 Russia, e-mail abdelmanova@vij.ru (✉ corresponding author), veronika0784@mail.ru, margaretfornara@gmail.com, roman_chinarov@mail.ru, alex_sermyagin85@mail.ru, n_zinovieva@mail.ru;
2Timiryazev Russian State Agrarian University—Moscow Agrarian Academy, 49, ul. Timiryazevskaya, Moscow, 127550 Russia, e-mail: liskun@rgau-msha.ru, rector@rgau-msha.ru

ORCID:
Abdelmanova A.S. orcid.org/0000-0003-4752-0727
Boronetskaya O.I. orcid.org/0000-0001-8389-5572
Kharzinova V.R. orcid.org/0000-0002-8067-0404
Sermyagin A.A. orcid.org/0000-0002-1799-6014
Fornara M.S. orcid.org/0000-0002-8844-177X
Trukhachev V.I. orcid.org/0000-0003-4676-5407
Chinarov R.Yu. orcid.org/0000-0001-6511-5341
Zinovieva N.A. orcid.org/0000-0003-4017-6863

Final revision received  May 04, 2024
Accepted June 07, 2024

 

Kholmogor and Yaroslavl cattle are the most widespread among Russian local breeds. However, the history of their origin and development is still a matter of debate and requires clarification. The large-scale use of Holstein bulls for improvement could lead to a significant alterations in the allele pool of local breeds. The inclusion of museum samples in the analyses allows shed the light on the history of creation and development of the breeds and to assess whether ancestral components are preserved in the modern Kholmogor and Yaroslavl breeds. For the first time in this work describes the results of analyses of genetic diversity and structure of modern Black-and-White cattle in comparison with ancestral populations using high-density DNA microarray, and assesses the influence of imported breeds on the formation of the gene pool of Kholmogor and Yaroslavl cattle in the end XIX—early XX century. The aim of our work was to analyze the genetic relationships between ancestral and modern populations of Black-and-White cattle, to estimate the proportion of ancestral components in modern breeds, to clarify the history of origin and development of the Kholmogor and Yaroslavl breeds of cattle based on genotyping data using a high-density DNA microarray. DNA extraction from museum samples was carried out using the COrDIS Extract Decalcine kit (GORDIZ LLC, Russia) with some modifications (increased lysis time and volume of reagents per sample) of the DNA extraction protocol recommended by the manufacturer. Whole-genome analysis of 68 museum samples using a high-density DNA microarray (Bovine GGP HD BeadChip, Illumina, Inc., USA) containing about 150,000 SNPs was carried out using the iScan system (Illumina, Inc., USA). The obtained SNP-genotypes were used to generate a combined dataset including SNP-genotypes of 31 museum (Kholmogor breed, H_KHLM, n = 17; Yaroslavl breed, H_YRSL, n = 12; Great Russian cattle, H_GRUS, n = 1; East Friesian cattle, H_OFRZ, n = 1) and 132 modern samples (Yaroslavl, YRSL, n = 53; Kholmogor, KHLM, n = 26; Holstein, HLST, n = 54). To estimate genetic diversity in each breed, observed (HO) and unbiased expected (UHE) heterozygosity, inbreeding coefficient (UFIS) and allelic diversity adjusted for sample size (AR) were calculated using the R package ‘diveRsity’.  Genetic differences between breeds were estimated in PLINK v1.90 by principal component analysis (PCA) visualised using the R package ‘ggplot2’. Pairwise distances for identical-by-state (identical-by-state, IBS) fragments were used to construct a ‘neighbourhood network’ dendrogram in SplitsTree 4.14.5 software. Pairwise FST values were calculated in the R-package ‘diveRsity’ and used to construct ‘neighbourhood network’ dendrograms in SplitsTree 4.14.5 software. The cluster structure of populations was investigated in ADMIXTURE v1.23 software. Visualisation of the analysis results was performed using the R package ‘BITE’. To assess the presence and degree of introgression between breeds, D-statistics and F4-statistics were calculated using the R package ‘admixr’. To assess the degree of population divergence and extent of gene exchange between breeds, TreeMix 1.12 software was used. Yakut breed was used as an outgroup in the construction of TreeMix maximum likelihood (ML) tree. The results of our studies indicate more significant changes in the gene pool of the Yaroslavl breed over the XX century compared to the Kholmogor breed, both due to the breeding process and using limited number of bull sires because of a decrease in the population. It was found that allelic diversity (AR) in ancestral populations of Kholmogor and Yaroslavl cattle was significantly (p < 0.001) higher compared to modern populations of these breeds: 1.959 vs. 1.936 and 1.981 vs. 1.917 for Kholmogor and Yaroslavl cattle, respectively. The H_KHLM and KHLM populations had greater genetic similarity to each other (FST = 0.040; D = 0.257) compared to their counterparts for H_YRSL and YRSL (FST = 0.099; D = 0.353). The results of introgression analysis using D- and F-statistics and TreeMix analysis confirmed the genetic relationships between H_GRUS and H_YRSL. The presence of some proportion of East Friesian cattle genomic components in historical samples of Kholmogor and Yaroslavl breeds was shown which confirms the use of imported foreign breeds in breeding of Russian local cattle at the turn of the XIX-XX centuries. The modern populations of Kholmogor and Yaroslavl breeds almost have no introgression of Holstein breed, but they retain genomic components of ancestral populations.

Keywords: cattle, museum samples, Yaroslavl breed, Kholmogor breed, SNP-genotyping, DNA-array.

 

REFERENCES

  1. Promyshlennaya revolyutsiya [Industrial revolution]. Available: https://old.bigenc.ru/world_history/text/3180201. Accessed: 11.04.2024 (in Russ.).
  2. Ernst L.K., Dmitriev N.G., Paronyan I.A. Geneticheskie resursy sel’skokhozyaystvennykh zhivotnykh v Rossii i sopredel’nykh stranakh [Genetic resources of agricultural animals in Russia and neighboring countries]. St. Petersburg, 1994 (in Russ.).
  3. Middendorf A.F. Issledovanie sovremennogo sostoyaniya skotovodstva v Rossii. Vypusk I. Rogatyy skot [Research of the current state of cattle breeding in Russia. Issue I. Horned cattle]. Moscow, 1884: 226-260 Available: https://elibrary.tambovlib.ru/?ebook=4383. Accessed: 04/11/2024 (in Russ.).
  4. Diomidov A.M., Zhirkovich E.F. Razvedenie i porody krupnogo rogatogo skota [Сattl breeding and breeds]. Moscow, 1934 (in Russ.).
  5. Sabaneev L.P. Ocherki Zaural’ya i stepnoe khozyaystvo na bashkirskikh zemlyakh [Essays on the Trans-Urals and the steppe economy on the Bashkir lands]. Moscow, 1873 Available: https://elibrary.orenlib.ru/index.php?dn=down&to=avtoropen&id=3546. Accessed: 04/11/2024 (in Russ.).
  6. Felius M. Cattle breeds — an encyclopedia. Misset, Doetinchem, Netherlands, 1995.
  7. Liskun E.F. Otechestvennye porody krupnogo rogatogo skota [Domestic breeds of cattle]. Moscow, 1949 (in Russ.).
  8. Kolesnikov P.A. Severnaya Rus’. Vypusk 2. Arkhivnye istochniki istorii Evropeyskogo Severa Rossii XVIII v. [Northern Rus'. Issue 2. Archival sources of the history of the European North of Russia in the 18th century]. Vologda, 1973. Available: https://www.booksite.ru/fulltext/754332/text.pdf. Accessed: 04/12/2024 (in Russ.).
  9. Otchet o Pervoy Vserossiyskoy vystavke rogatogo skota 1869 goda, sostavlennyy s soizvoleniya Ego Imperatorskogo Vysochestva Gosudarya Velikogo Knyazya Nikolaya Nikolaevicha Starshego, komissiey po ustroystvu vystavki [Report on the First All-Russian Cattle Exhibition of 1869, compiled with the permission of His Imperial Highness the Sovereign Grand Duke Nikolai Nikolaevich the Elder, by the exhibition organization commission]. St. Petersburg, 1869. Available: https://kp.rusneb.ru/item/reader/otchet-o-pervoy-vserossiyskoy-vystavke-rogatogo-skota-1869-goda. Accessed: 04/12/2024 (in Russ.).
  10. Sermyagin A.A., Naryshkina E.N., Nedashkovskiy I.S., Ermilov A.N., Bogdanova T.V. AgroZooTekhnika, 2018, 1(3): 1 CrossRef (in Russ.).
  11. Abdelmanova A.S., Kharzinova V.R., Volkova V.V., Mishina A.I., Dotsev A.V., Sermyagin A.A., Boronetskaya O.I., Petrikeeva L.V., Chinarov R.Y., Brem G., Zinovieva N.A. Genetic diversity of historical and modern populations of russian cattle breeds revealed by microsatellite analysis. Genes, 2020, 11(8): 940 CrossRef
  12. Volkova V.V., Koshkina O.A., Khozhokov A.A. Trudy Kubanskogo gosudarstvennogo agrarnogo universiteta, 2022, 98: 163-171 CrossRef (in Russ.).
  13. Stolpovsky Yu.A., Beketov S.V., Solodneva E.V., Absalikov V.M., Abdelmanova A.S., Gladyr E.A., Zinovieva N.A.. The population-genetic structure of native tagil cattle by STR- and SNP-markers. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2021, 56(6): 1123-1133 CrossRef
  14. Abdel’manova A.S., Sermyagin A.A., Dotsev A.V., Rodionov A.N., Stolpovskiy Yu.A., Zinov’eva N.A. Genetika, 2022, 58(7): 786-797 CrossRef (in Russ.).
  15. Abdelmanova A.S., Volkova V.V., Kharzinova V.R., Fornara M.S., Chinarov R.Yu., Boronetskaya O.I., Trukhachev V.I., Brem G., Zinovieva N.A. Determination of consensus genotypes by microsatellites for museum accessions of cattle (Vos taurus). Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2023, 58(6): 1035-1045 CrossRef
  16. Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M.A., Bender D., Maller J., Sklar P., de Bakker P.I., Daly M.J., Sham P.C. PLINK: a tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics, 2007, 81(3): 559-575 CrossRef
  17. Nei M. Estimation of average heterozygosity and genetic distance from small number of individuals. Genetics, 1978, 89(3): 583-590 CrossRef
  18. Weir B.S., Cockerham C.C. Estimating F-Statistics for the analysis of population structure. Evolution, 1984, 38(6): 1358-1370 CrossRef
  19. Kalinowski S.T. Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conservation Genetics, 2004, 5: 539-543 CrossRef
  20. Keenan K., McGinnity P., Cross T.F., Crozier W.W., Prodöhl P.A. diveRsity: An R package for the estimation of population genetics parameters and their associated errors. Methods in Ecology and Evolution, 2013, 4(8): 782-788 CrossRef
  21. Wickham H. ggplot2: elegant graphics for data analysis. Springer, New York, 2009.
  22. Huson D.H., Bryant D. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 2006, 23(2): 254-267 CrossRef
  23. Alexander D.H., Novembre J., Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res., 2009, 19: 1655-1664 CrossRef
  24. Milanesi M., Capomaccio S., Vajana E., Bomba L., Garcia J.F., Ajmone-Marsan P., Colli L. BITE: an R package for biodiversity analyses. bioRxiv, 2017 CrossRef
  25. Green R.E., Krause J., Briggs A.W., Maricic T., Stenzel U., Kircher M., Patterson N., Li H., Zhai W., Fritz M.H., Hansen N.F., Durand E.Y., Malaspinas A.S., Jensen J.D., Marques-Bonet T., Alkan C., Prüfer K., Meyer M., Burbano H.A., Good J.M., Schultz R., Aximu-Petri A., Butthof A., Höber B., Höffner B., Siegemund M., Weihmann A., Nusbaum C., Lander ES., Russ C., Novod N., Affourtit J., Egholm M., Verna C., Rudan P., Brajkovic D., Kucan Ž., Gušic I., Doronichev V.B., Golovanova L.V., Lalueza-Fox C., de la Rasilla M., Fortea J., Rosas A., Schmitz R.W., Johnson P.L.F., Eichler E.E., Falush D., Birney E., Mullikin J.C., Slatkin M., Nielsen R., Kelso J., Lachmann M., Reich D., Pääbo S. A draft sequence of the Neandertal genome. Science, 2010, 328(5979): 710-722 CrossRef
  26. Patterson N., Moorjani P., Luo Y. Mallick S., Rohland N., Zhan Y., Genschoreck T., Webster T., Reich D. Ancient admixture in human history. Genetics, 2012, 192(3): 1065-1093 CrossRef
  27. Petr M., Vernot B., Kelso J. admixr — R package for reproducible analyses using ADMIXTOOLS. Bioinformatics, 2019, 35(17): 3194-3195 CrossRef
  28. Pickrell J.K., Pritchard J.K. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genetics, 2012, 8: e1002967 CrossRef
  29. Dabney J., Meyer M., Pääbo S. Ancient DNA damage. Cold Spring Harbor Perspectives in Biology, 2013, 5(7): a012567 CrossRef
  30. Gorden E. M., Sturk-Andreaggi K., Marshall C. Repair of DNA damage caused by cytosine deamination in mitochondrial DNA of forensic case samples. Forensic Science International: Genetics, 2018, 34: 257-264 CrossRef
  31. Bailey J.F., Richards M.B., Macaulay V.A., Colson I.B., James I.T., Bradley D.G., Hedges R.E., Sykes B.C. Ancient DNA suggests a recent expansion of European cattle from a diverse wild progenitor species. Proceedings of the Royal Society of London. Series B: Biological Sciences, 1996, 263(1376): 1467-1473 CrossRef
  32. Beja-Pereira A., Caramelli D., Lalueza-Fox C., Vernesi C., Ferrand N., Casoli A., Goyache F., Royo LJ., Conti S., Lari M., Martini A., Ouragh L., Magid A., Atash A., Zsolnai A., Boscato P., Triantaphylidis C., Ploumi K., Sineo L., Mallegni F., Taberlet P., Erhardt G., Sampietro L., Bertranpetit J., Barbujani G., Luikart G., Bertorelle G. The origin of European cattle: evidence from modern and ancient DNA. Proceedings of the National Academy of Sciences, 2006, 103(21): 8113-8118 CrossRef
  33. Delsol N., Stucky B.J., Oswald J.A., Cobb C.R., Emery K.F., Guralnick R. Ancient DNA confirms diverse origins of early post-Columbian cattle in the Americas. Sci. Rep., 2023, 13(1): 12444 CrossRef
  34. Edwards C.J., Connellan J., Wallace P.F., Park S.D.E., McCormick F.M., Olsaker I., Eythórsdóttir E., MacHugh D.E., Bailey J.F., Bradley D.G. Feasibility and utility of microsatellite markers in archaeological cattle remains from a Viking Age settlement in Dublin. Animal Genetics, 2003, 34(6): 410-416 CrossRef
  35. Gargani M., Pariset L., Lenstra J.A., De Minicis E., European Cattle Genetic Diversity Consortium, Valentini A. Microsatellite genotyping of medieval cattle from central Italy suggests an old origin of Chianina and Romagnola cattle. Front. Genet., 2015, 6: 68 CrossRef
  36. Glazko V.I., Kosovsky G.Yu., Glazko T.T., Fedorova L.M. DNA markers and microsatellite code (review). Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2023, 58(2): 223-248 CrossRef

 

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