Genetic Structure Analysis of 155 Transboundary and Local Populations of Cattle (Bos taurus, Bos indicus and Bos grunniens) Based on STR Markers

Every week, 1–2 breeds of farm animals, including local cattle, disappear in the world. As the keepers of rare allelic variants, native breeds potentially expand the range of genetic solutions to possible problems of the future, which means that the study of the genetic structure of these breeds is an urgent task. Providing nomadic herders with valuable resources necessary for life, domestic yaks have also become an important object of study. In order to determine the population genetic characteristics, and clarify the phylogenetic relationships of modern representatives of 155 cattle populations from different regions of the world, we collected a large set of STR data (10,250 individuals), including unique native cattle, 12 yak populations from Russia, Mongolia and Kyrgyzstan, as well as zebu breeds. Estimation of main population genetic parameters, phylogenetic analysis, principal component analysis and Bayesian cluster analysis allowed us to refine genetic structure and provided insights in relationships of native populations, transboundary breeds and populations of domestic yak. Our results can find practical application in conservation programs of endangered breeds, as well as become the basis for future fundamental research.

[1]  Yongfu La,et al.  Transcriptome-Wide Study of mRNAs and lncRNAs Modified by m6A RNA Methylation in the Longissimus Dorsi Muscle Development of Cattle-Yak , 2022, Cells.

[2]  D. Larkin,et al.  Copy Number Variants in Two Northernmost Cattle Breeds Are Related to Their Adaptive Phenotypes , 2022, Genes.

[3]  T. Sonstegard,et al.  Genome-wide local ancestry and evidence for mitonuclear coadaptation in African hybrid cattle populations , 2022, iScience.

[4]  F. J. Navas González,et al.  Do Pharaohs’ cattle still graze the Nile Valley? Genetic characterization of the Egyptian Baladi cattle breed , 2021, Animal biotechnology.

[5]  G. Brem,et al.  Comparative Study of the Genetic Diversity of Local Steppe Cattle Breeds from Russia, Kazakhstan and Kyrgyzstan by Microsatellite Analysis of Museum and Modern Samples , 2021, Diversity.

[6]  O. Hanotte,et al.  Population differentiated copy number variation of Bos taurus, Bos indicus and their African hybrids , 2021, BMC genomics.

[7]  L. Colli,et al.  On the origin and diversification of Podolian cattle breeds: testing scenarios of European colonization using genome-wide SNP data , 2021, Genetics Selection Evolution.

[8]  P. Bork,et al.  Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation , 2021, Nucleic Acids Res..

[9]  A. Graphodatsky,et al.  Demographic History, Adaptation, and NRAP Convergent Evolution at Amino Acid Residue 100 in the World Northernmost Cattle from Siberia , 2021, Molecular biology and evolution.

[10]  Hong Chen,et al.  Mitochondrial genomes from modern and ancient Turano-Mongolian cattle reveal an ancient diversity of taurine maternal lineages in East Asia , 2021, Heredity.

[11]  C. Maria,et al.  Phenotypic characterization of the Guaymi breed in conservation centers of Panama , 2021 .

[12]  G. Brem,et al.  PSXII-21 Genome-wide search for genomic regions under putative selection in two Russian native cattle breeds using high-density SNP Bead Chip , 2020 .

[13]  G. Brem,et al.  Selection signatures in two oldest Russian native cattle breeds revealed using high-density single nucleotide polymorphism analysis , 2020, PloS one.

[14]  Choongwon Jeong,et al.  The mosaic genome of indigenous African cattle as a unique genetic resource for African pastoralism , 2020, Nature Genetics.

[15]  E. Ciani,et al.  Refining the genetic structure and relationships of European cattle breeds through meta-analysis of worldwide genomic SNP data, focusing on Italian cattle , 2020, Scientific Reports.

[16]  G. Svishcheva,et al.  Microsatellite Diversity and Phylogenetic Relationships among East Eurasian Bos taurus Breeds with an Emphasis on Rare and Ancient Local Cattle , 2020, Animals : an open access journal from MDPI.

[17]  E. Ciani,et al.  Fifteen Shades of Grey: Combined Analysis of Genome-Wide SNP Data in Steppe and Mediterranean Grey Cattle Sheds New Light on the Molecular Basis of Coat Color , 2020, Genes.

[18]  A. Zsolnai,et al.  Genetic position of Hungarian Grey among European cattle and identification of breed-specific markers. , 2020, Animal : an international journal of animal bioscience.

[19]  R. Crooijmans,et al.  Adaptive introgression from indicine cattle into white cattle breeds from Central Italy , 2020, Scientific Reports.

[20]  Andrea Alves do Egito,et al.  The genetic ancestry of American Creole cattle inferred from uniparental and autosomal genetic markers , 2019, Scientific Reports.

[21]  Benjamin S. Arbuckle,et al.  Ancient cattle genomics, origins, and rapid turnover in the Fertile Crescent , 2019, Science.

[22]  M. Bruford,et al.  Genome‐wide differential DNA methylation in tropically adapted Creole cattle and their Iberian ancestors , 2018, Animal genetics.

[23]  P. Orozco‐terWengel,et al.  Domestication of cattle: Two or three events? , 2018, Evolutionary applications.

[24]  R. Lyons,et al.  Sequencing the mosaic genome of Brahman cattle identifies historic and recent introgression including polled , 2018, Scientific Reports.

[25]  G. Svishcheva,et al.  Study of Genetic Diversity and Population Structure of the Yak (Bos grunniens) in the Sayan-Altai Region , 2018, Russian Journal of Genetics.

[26]  S. Ahlawat,et al.  Cattle microsatellite markers successfully established diversity status of Arunachali yak (only registered yak breed of India) , 2018, The Indian Journal of Animal Sciences.

[27]  D. Larkin,et al.  Scans for signatures of selection in Russian cattle breed genomes reveal new candidate genes for environmental adaptation and acclimation , 2018, Scientific Reports.

[28]  G. Brem,et al.  Whole-genome SNP analysis elucidates the genetic structure of Russian cattle and its relationship with Eurasian taurine breeds , 2018, Genetics Selection Evolution.

[29]  Hong Chen,et al.  Whole-genome resequencing reveals world-wide ancestry and adaptive introgression events of domesticated cattle in East Asia , 2018, Nature Communications.

[30]  R. Nielsen,et al.  Pervasive introgression facilitated domestication and adaptation in the Bos species complex , 2018, Nature Ecology & Evolution.

[31]  A. Achilli,et al.  Mitochondrial DNA variants of Podolian cattle breeds testify for a dual maternal origin , 2018, PloS one.

[32]  C. V. Van Tassell,et al.  Signatures of Selection for Environmental Adaptation and Zebu × Taurine Hybrid Fitness in East African Shorthorn Zebu , 2017, Front. Genet..

[33]  H. Blum,et al.  Whole-genome analysis of introgressive hybridization and characterization of the bovine legacy of Mongolian yaks , 2017, Nature Genetics.

[34]  Yixue Li,et al.  Genomic Analysis Reveals Hypoxia Adaptation in the Tibetan Mastiff by Introgression of the Gray Wolf from the Tibetan Plateau , 2016, Molecular biology and evolution.

[35]  D. A. Magee,et al.  Genetic origin, admixture and population history of aurochs (Bos primigenius) and primitive European cattle , 2016, Heredity.

[36]  D. Larkin,et al.  Genome-wide genotyping uncovers genetic profiles and history of the Russian cattle breeds , 2017, Heredity.

[37]  J. Decker,et al.  Insight into the genetic composition of South African Sanga cattle using SNP data from cattle breeds worldwide , 2016, Genetics Selection Evolution.

[38]  A. Martínez,et al.  Molecular Study of the Amazonian Macabea Cattle History , 2016, PloS one.

[39]  T. Iso-Touru,et al.  Genetic diversity and genomic signatures of selection among cattle breeds from Siberia, eastern and northern Europe. , 2016, Animal genetics.

[40]  D. Villalba,et al.  Corrigendum to: Comparison of B-splines and non-linear functions to describe growth patterns and predict mature weight of female beef cattle , 2016 .

[41]  O. Hanotte,et al.  African Indigenous Cattle: Unique Genetic Resources in a Rapidly Changing World , 2015, Asian-Australasian journal of animal sciences.

[42]  J. Lenstra,et al.  Microsatellite genotyping of medieval cattle from central Italy suggests an old origin of Chianina and Romagnola cattle , 2015, Front. Genet..

[43]  D. Fisher,et al.  The roles of microphthalmia-associated transcription factor and pigmentation in melanoma. , 2014, Archives of biochemistry and biophysics.

[44]  A. Evsyukov,et al.  Comparative analysis of ISSR marker polymorphism in populations of yak (Bos mutus) and in F1 hybrids between yak and cattle in the Sayan-Altai region , 2014, Russian Journal of Genetics.

[45]  Asan,et al.  Altitude adaptation in Tibet caused by introgression of Denisovan-like DNA , 2014, Nature.

[46]  Aaron T. Adamack,et al.  PopGenReport: simplifying basic population genetic analyses in R , 2014 .

[47]  Hong Chen,et al.  When and how did Bos indicus introgress into Mongolian cattle? , 2014, Gene.

[48]  Zhian N. Kamvar,et al.  Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction , 2014, PeerJ.

[49]  T. Mipam,et al.  Isolation and characterization of polymorphic microsatellites in the genome of Yak (Bos grunniens) , 2014, Molecular Biology Reports.

[50]  R. Nielsen,et al.  Classic Selective Sweeps Revealed by Massive Sequencing in Cattle , 2014, PLoS genetics.

[51]  M. P. Heaton,et al.  Worldwide Patterns of Ancestry, Divergence, and Admixture in Domesticated Cattle , 2013, PLoS genetics.

[52]  M. Pla La Raça Bruna dels Pirineus, patrimoni boví autòcton català , 2014 .

[53]  J. Lenstra,et al.  Revisiting AFLP fingerprinting for an unbiased assessment of genetic structure and differentiation of taurine and zebu cattle , 2014, BMC Genetics.

[54]  V. Stepanov,et al.  Gene pool of Buryats: Clinal variability and territorial subdivision based on data of Y-chromosome markers , 2014, Russian Journal of Genetics.

[55]  Thomas F. Cross,et al.  diveRsity: An R package for the estimation and exploration of population genetics parameters and their associated errors , 2013 .

[56]  E. J. McTavish,et al.  New World cattle show ancestry from multiple independent domestication events , 2013, Proceedings of the National Academy of Sciences.

[57]  G. Bittante,et al.  Genetic relationships among Italian and Croatian Podolian cattle breeds assessed by microsatellite markers , 2012 .

[58]  I. Martín-Burriel,et al.  Genetic Footprints of Iberian Cattle in America 500 Years after the Arrival of Columbus , 2012, PloS one.

[59]  A. Torroni,et al.  Origin and Spread of Bos taurus: New Clues from Mitochondrial Genomes Belonging to Haplogroup T1 , 2012, PloS one.

[60]  Vladimir Makarenkov,et al.  T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks , 2012, Nucleic Acids Res..

[61]  Theunis Piersma,et al.  The interplay between habitat availability and population differentiation , 2012 .

[62]  J. Lenstra,et al.  On the Breeds of Cattle—Historic and Current Classifications , 2011 .

[63]  O. Hanotte,et al.  Domesticating Animals in Africa: Implications of Genetic and Archaeological Findings , 2011 .

[64]  Ole Tange,et al.  GNU Parallel: The Command-Line Power Tool , 2011, login Usenix Mag..

[65]  A. Torroni,et al.  The Enigmatic Origin of Bovine mtDNA Haplogroup R: Sporadic Interbreeding or an Independent Event of Bos primigenius Domestication in Italy? , 2010, PloS one.

[66]  M. Mariotti,et al.  Relationships between Podolic cattle breeds assessed by single nucleotide polymorphisms (SNPs) genotyping. , 2010, Journal of animal breeding and genetics = Zeitschrift fur Tierzuchtung und Zuchtungsbiologie.

[67]  Mathieu Gautier,et al.  Insights into the Genetic History of French Cattle from Dense SNP Data on 47 Worldwide Breeds , 2010, PloS one.

[68]  Paolo Ajmone-Marsan,et al.  On the origin of cattle: How aurochs became cattle and colonized the world , 2010 .

[69]  A. Beja-Pereira,et al.  Y-specific microsatellites reveal an African subfamily in taurine (Bos taurus) cattle. , 2010, Animal genetics.

[70]  J. Rege,et al.  Assessment of cattle genetic introgression into domestic yak populations using mitochondrial and microsatellite DNA markers , 2010, Animal genetics.

[71]  J. Kantanen,et al.  Genetic structure of Eurasian cattle (Bos taurus) based on microsatellites: clarification for their breed classification. , 2010, Animal genetics.

[72]  J. Delgado,et al.  Origins and genetic diversity of New World Creole cattle: inferences from mitochondrial and Y chromosome polymorphisms. , 2010, Animal genetics.

[73]  Robert D Schnabel,et al.  Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics , 2009, Proceedings of the National Academy of Sciences.

[74]  S. Thessler,et al.  Maternal and paternal genealogy of Eurasian taurine cattle (Bos taurus) , 2009, Heredity.

[75]  A. V. Kushnir,et al.  Gray Ukrainian cattle and their closely related forms , 2009, Contemporary Problems of Ecology.

[76]  Robert D Schnabel,et al.  Genome-Wide Survey of SNP Variation Uncovers the Genetic Structure of Cattle Breeds , 2009, Science.

[77]  W. V. Haeringen,et al.  Population studies of 16 bovine STR loci for forensic purposes , 2009, International Journal of Legal Medicine.

[78]  J. Cañón,et al.  Ancestral matrilineages and mitochondrial DNA diversity of the Lidia cattle breed. , 2008, Animal genetics.

[79]  M. B. Leite,et al.  Bos indicus or Bos taurus mitochondrial DNA - comparison of productive and reproductive breeding values in a Guzerat dairy herd. , 2008, Genetics and molecular research : GMR.

[80]  Thibaut Jombart,et al.  adegenet: a R package for the multivariate analysis of genetic markers , 2008, Bioinform..

[81]  S. Davis Zooarchaeological evidence for Moslem and Christian improvements of sheep and cattle in Portugal , 2008 .

[82]  S. Yu The challenges and progress in the management of reproduction in yaks. , 2019, Society of Reproduction and Fertility supplement.

[83]  D. Grattapaglia,et al.  Microsatellite based genetic diversity and relationships among ten Creole and commercial cattle breeds raised in Brazil , 2007, BMC Genetics.

[84]  J. Vilkki,et al.  The genetic structure of cattle populations (Bos taurus) in northern Eurasia and the neighbouring Near Eastern regions: implications for breeding strategies and conservation , 2007, Molecular ecology.

[85]  Noah A. Rosenberg,et al.  CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure , 2007, Bioinform..

[86]  L. Cavalli-Sforza,et al.  The mystery of Etruscan origins: novel clues from Bos taurus mitochondrial DNA , 2007, Proceedings of the Royal Society B: Biological Sciences.

[87]  S. Lai,et al.  Mitochondrial DNA sequence diversity and origin of Chinese domestic yak. , 2007, Animal genetics.

[88]  J. Lenstra,et al.  Differentiation of European cattle by AFLP fingerprinting. , 2007, Animal genetics.

[89]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[90]  Yoshio Tateno,et al.  Accuracy of estimated phylogenetic trees from molecular data , 1983, Journal of Molecular Evolution.

[91]  M. R. Goe,et al.  Application of bovine microsatellite markers for genetic diversity analysis of Swiss yak (Poephagus grunniens). , 2005, Animal genetics.

[92]  D. Bradley,et al.  Microsatellite diversity suggests different histories for Mediterranean and Northern European cattle populations , 2005, Proceedings of the Royal Society B: Biological Sciences.

[93]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[94]  H. Ellegren,et al.  Prehistoric contacts over the Straits of Gibraltar indicated by genetic analysis of Iberian Bronze Age cattle. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[95]  Henner Simianer,et al.  Decision making in livestock conservation , 2005 .

[96]  O. Hanotte,et al.  Genetic diversity and differentiation of Mongolian and Russian yak populations. , 2005, Journal of animal breeding and genetics = Zeitschrift fur Tierzuchtung und Zuchtungsbiologie.

[97]  J. Goudet HIERFSTAT , a package for R to compute and test hierarchical F -statistics , 2005 .

[98]  D. Bradley,et al.  Independent mitochondrial origin and historical genetic differentiation in North Eastern Asian cattle. , 2004, Molecular phylogenetics and evolution.

[99]  J. Piedrafita,et al.  Characterisation of young bulls of the Bruna dels Pirineus cattle breed (selected from old Brown Swiss) in relation to carcass, meat quality and biochemical traits. , 2004, Meat science.

[100]  S. Moore,et al.  Characterization of 65 bovine microsatellites , 1994, Mammalian Genome.

[101]  W. Barendse,et al.  Physically mapped, cosmid-derived microsatellite markers as anchor loci on bovine chromosomes , 1993, Mammalian Genome.

[102]  A. Sánchez,et al.  Genetic characterization of southwestern European bovine breeds: a historical and biogeographical reassessment with a set of 16 microsatellites. , 2003, The Journal of heredity.

[103]  C. Spinage,et al.  Cattle Plague , 2003, Springer US.

[104]  C. You Diversity of Chinese yellow cattle breeds and their conservation , 2001 .

[105]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[106]  O. Hanotte,et al.  Geographic distribution and frequency of a taurine Bos taurus and an indicine Bos indicus Y specific allele amongst sub‐Saharan African cattle breeds , 2000, Molecular ecology.

[107]  R. Lôbo,et al.  Is the American Zebu really Bos indicus , 1999 .

[108]  Y. Zhang,et al.  Mitochondrial DNA variation in cattle of south China: origin and introgression. , 1999, Animal genetics.

[109]  J. Rege,et al.  The state of African cattle genetic resources II. Geographical distribution, characteristics and uses of present-day breeds and strains , 1999 .

[110]  D. Bradley,et al.  Mitochondrial sequence variation suggests an African influence in Portuguese cattle , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[111]  M. Shriver,et al.  Microsatellite DNA variation and the evolution, domestication and phylogeography of taurine and zebu cattle (Bos taurus and Bos indicus). , 1997, Genetics.

[112]  Y. Hotta,et al.  Fertility investigations in the F1 hybrid and backcross progeny of cattle (Bos taurus) and yak (B. grunniens) in Mongolia. , 1997, Cytogenetics and cell genetics.

[113]  M. Georges,et al.  A genetic linkage map of the bovine genome , 1994, Nature Genetics.

[114]  A. Eggen,et al.  Isolation and mapping of polymorphic microsatellites in cattle. , 2009, Animal genetics.

[115]  J. Keele,et al.  A highly polymorphic bovine microsatellite locus: BM2113. , 2009, Animal genetics.

[116]  S. Kemp,et al.  ILSTS006: a polymorphic bovine microsatellite. , 2009, Animal genetics.

[117]  S. Moore,et al.  Dinucleotide polymorphism at the bovine calmodulin independent adenylcyclase locus. , 2009, Animal genetics.

[118]  J. Zilhão The Spread of Agro-Pastoral Economies across Mediterranean Europe: A View from the Far West , 1993 .

[119]  Y. Tikochinsky,et al.  Large restriction fragments containing poly-TG are highly polymorphic in a variety of vertebrates. , 1990, Nucleic acids research.

[120]  D. Tautz Hypervariability of simple sequences as a general source for polymorphic DNA markers. , 1989, Nucleic acids research.

[121]  R. Willham Genetic improvement of beef cattle in the United States: cattle, people and their interaction. , 1982, Journal of animal science.