PLOS ONE RESEARCH ARTICLE Selection signatures in two oldest Russian native cattle breeds revealed using high- density single nucleotide polymorphism analysis Natalia Anatolievna Zinovieva1*, Arsen Vladimirovich Dotsev1, Alexander Alexandrovich Sermyagin1, Tatiana Evgenievna Deniskova1, Alexandra 1 1 2 Sergeevna Abdelmanova , Veronika Ruslanovna KharzinovaID , Johann SoÈ lkner , a1111111111 Henry Reyer3, Klaus Wimmers3, Gottfried Brem1,4 a1111111111 a1111111111 1 L.K. Ernst Federal Science Center for Animal Husbandry, Federal Agency of Scientific Organizations, settl. Dubrovitzy, Podolsk Region, Moscow Province, Russia, 2 Division of Livestock Sciences, University of a1111111111 Natural Resources and Life Sciences, Vienna, Austria, 3 Institute of Genome Biology, Leibniz Institute for a1111111111 Farm Animal Biology [FBN], Dummerstorf, Germany, 4 Institute of Animal Breeding and Genetics, University of Veterinary Medicine [VMU], Vienna, Austria * [email protected] OPEN ACCESS Citation: Zinovieva NA, Dotsev AV, Sermyagin AA, Abstract Deniskova TE, Abdelmanova AS, Kharzinova VR, et al. (2020) Selection signatures in two oldest Native cattle breeds can carry specific signatures of selection reflecting their adaptation to Russian native cattle breeds revealed using high- the local environmental conditions and response to the breeding strategy used. In this density single nucleotide polymorphism analysis. study, we comprehensively analysed high-density single nucleotide polymorphism (SNP) PLoS ONE 15(11): e0242200. https://doi.org/ genotypes to characterise the population structure and detect the selection signatures in 10.1371/journal.pone.0242200 Russian native Yaroslavl and Kholmogor dairy cattle breeds, which have been little influ- Editor: Gyaneshwer Chaubey, Banaras Hindu enced by introgression with transboundary breeds. Fifty-six samples of pedigree-recorded University, INDIA purebred animals, originating from different breeding farms and representing different sire Received: May 29, 2020 lines, of the two studied breeds were genotyped using a genome-wide bovine genotyping Accepted: October 29, 2020 array (Bovine HD BeadChip). Three statistical analysesÐcalculation of fixation index (FST) Published: November 16, 2020 for each SNP for the comparison of the pairs of breeds, hapFLK analysis, and estimation of Peer Review History: PLOS recognizes the the runs of homozygosity (ROH) islands shared in more than 50% of animalsÐwere com- benefits of transparency in the peer review bined for detecting the selection signatures in the genome of the studied cattle breeds. We process; therefore, we enable the publication of confirmed nine and six known regions under putative selection in the genomes of Yaroslavl all of the content of peer review and author and Kholmogor cattle, respectively; the flanking positions of most of these regions were elu- responses alongside final, published articles. The editorial history of this article is available here: cidated. Only two of the selected regions (localised on BTA 14 at 24.4±25.1 Mbp and on https://doi.org/10.1371/journal.pone.0242200 BTA 16 at 42.5±43.5 Mb) overlapped in Yaroslavl, Kholmogor and Holstein breeds. In addi- Copyright: © 2020 Zinovieva et al. This is an open tion, we detected three novel selection sweeps in the genome of Yaroslavl (BTA 4 at 4.74± access article distributed under the terms of the 5.36 Mbp, BTA 15 at 17.80±18.77 Mbp, and BTA 17 at 45.59±45.61 Mbp) and Kholmogor Creative Commons Attribution License, which breeds (BTA 12 at 82.40±81.69 Mbp, BTA 15 at 16.04±16.62 Mbp, and BTA 18 at 0.19± permits unrestricted use, distribution, and reproduction in any medium, provided the original 1.46 Mbp) by using at least two of the above-mentioned methods. We expanded the list of author and source are credited. candidate genes associated with the selected genomic regions and performed their func- Data Availability Statement: We deposited our tional annotation. We discussed the possible involvement of the identified candidate genes Dataset files in the Dryad Digital Repository. in artificial selection in connection with the origin and development of the breeds. Our Zinovieva, Natalia et al. (2020), Selection PLOS ONE | https://doi.org/10.1371/journal.pone.0242200 November 16, 2020 1 / 30 PLOS ONE Selection signatures in native cattle breeds signatures in two oldest Russian native cattle findings on the Yaroslavl and Kholmogor breeds obtained using high-density SNP genotyp- breeds revealed using high-density single ing and three different statistical methods allowed the detection of novel putative genomic nucleotide polymorphism analysis, Dryad, Dataset, https://doi.org/10.5061/dryad.vt4b8gtq9. regions and candidate genes that might be under selection. These results might be useful for the sustainable development and conservation of these two oldest Russian native cattle Funding: This work was supported by the Russian Science Foundation within Project No. 19-76- breeds. 20012 (SNP genotyping) and the Russian Ministry of Science and Higher Education within theme 0445-2019-0024 (DNA collection and partly SNP genotyping). The URLshttp://grant.rscf.ru. Grant receiver no. 19-76-20012 is Zinovieva NA. The Introduction https://minobrnauki.gov.ru. Theme supervisor is National livestock genetic resources are the most important carriers of the unique forms of Dotsev A.V. The funder had no role in study design, data collection and analysis, decision to publish, or variability; they are necessary to ensure the sustainability of local agricultural production sys- preparation of the manuscript. tems [1]. In Russia, over a long period, various cattle breeds have formed, which are character- ised by good adaptation to the local environmental conditions and better suitability for the Competing interests: The authors have declared that no competing interests exist. development of geographic production systems [2]. Among the Black-and-White cattle breeds, Kholmogor and Yaroslavl dairy cattle have remarkable importance for animal husbandry in the Central and Northern regions of European Russia. Both breeds originated from small-stat- ure Great Russian Cattle (height at withers is 105±110 cm, body weight up to 325±390 kg [3, 4]. The first records of the presence of cattle on the islands in the upper reaches of the North- ern Dvina River near the Kholmogory town in Northern Russia date back to the sixteenth cen- tury (the breed was named after this town) [5]. Over a long history, the good pastures and hayfields in the Kholmogor breeding zone have contributed to the development of the tall cat- tle breed well suited for dairy production. In the 18th±19th centuries, the Kholmogor cattle were well-known in Russia and abroad owing to their high productivity and excellent quality of dairy products. Cattle breeding began to develop in the Yaroslavl region (near Moscow), based on which the breed is named, in the seventeenth and eighteenth centuries [5]. The Yaroslavl cattle were selected for adaptability, high feed efficiency and good reproductive ability even in poor forage conditions during win- ter. Moreover, this breed was in great demand among peasants and small cattle holders [4]. Most researchers suggested that foreign breeds, including Holsteins contributed little in the development of the Yaroslavl and Kholmogor cattle populations [6, 7], which was subse- quently confirmed by molecular genetics studies [8±10]. The studies of the historical speci- mens of Yaroslavl and Kholmogor cattle, dated from the end of 19th to the first half of 20th century using microsatellites, indicated that Russian breeds and Holsteins were developed from different ancestral populations [11]. In the 1960s, the number of Kholmogor and Yaro- slavl cattle was close to million individuals (993 and 951 thousand, respectively) each; in con- trast, in 2015, their census population size remarkably decreased to 222.9 and 50.5 thousand heads, respectively [12]. During the last decade, along with the remarkable decrease in popula- tion size, crossbreeding has been actively used in the remaining purebred animals, which could lead to the loss of genetic distinctness. Several molecular genetic studies have attempted to characterise the demographic history and population structure of the modern populations of Yaroslavl and Kholmogor breeds and their relationship to other taurine breeds [9, 10, 13, 14], but their results were, in some cases, controversial. By using microsatellite-based clustering, Li and Kantanen [13] suggested the composite origin of these breeds. Whole-genome studies performed using medium-density SNP chips showed that Yaroslavl and Kholmogor cattle are valuable national genetic resources, which have been little influenced by introgression with non-Russian breeds [9, 10]. The main- tenance of a visible part of historical components in the modern populations both of Yaroslavl and Kholmogor breeds was confirmed by the study of historical specimens [11]. Further PLOS ONE | https://doi.org/10.1371/journal.pone.0242200 November 16, 2020 2 / 30 PLOS ONE Selection signatures in native cattle breeds elucidation of the genetic architecture of these two breeds and more precise identification of genomic regions that are affected by putative selection may be achieved by using more power- ful molecular genetic tools such as bovine high-density SNP BeadChip (Illumina Inc., USA) which contains 777,962 SNPs. Several studies have explored the genome diversity and adaptation of cattle breeds by using high-density DNA arrays [15±17].