Analyze Diet
Scientific reports2019; 9(1); 6095; doi: 10.1038/s41598-019-42640-w

The horse Y chromosome as an informative marker for tracing sire lines.

Abstract: Analysis of the Y chromosome is the best-established way to reconstruct paternal family history in humans. Here, we applied fine-scaled Y-chromosomal haplotyping in horses with biallelic markers and demonstrate the potential of our approach to address the ancestry of sire lines. We de novo assembled a draft reference of the male-specific region of the Y chromosome from Illumina short reads and then screened 5.8 million basepairs for variants in 130 specimens from intensively selected and rural breeds and nine Przewalski's horses. Among domestic horses we confirmed the predominance of a young'crown haplogroup' in Central European and North American breeds. Within the crown, we distinguished 58 haplotypes based on 211 variants, forming three major haplogroups. In addition to two previously characterised haplogroups, one observed in Arabian/Coldblooded and the other in Turkoman/Thoroughbred horses, we uncovered a third haplogroup containing Iberian lines and a North African Barb Horse. In a genealogical showcase, we distinguished the patrilines of the three English Thoroughbred founder stallions and resolved a historic controversy over the parentage of the horse 'Galopin', born in 1872. We observed two nearly instantaneous radiations in the history of Central and Northern European Y-chromosomal lineages that both occurred after domestication 5,500 years ago.
Publication Date: 2019-04-15 PubMed ID: 30988347PubMed Central: PMC6465346DOI: 10.1038/s41598-019-42640-wGoogle Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research conducted Y-chromosome investigations on horses to reveal paternal lineages and explore the ancestry of sire lines. Findings indicate three main haplogroups among domestic horses, contributing to the identification of specific patrilines and resolving historical discrepancies in horses’ parentage.

Methodology

  • The researchers de novo assembled a draft reference of the male-specific region of the Y chromosome using Illumina short reads. This method involves building genome sequences from scratch, without guidance from a reference genome. It’s particularly useful in studying species or individuals for which no reference genome exists or to detect significant structural variants.
  • The team screened 5.8 million base pairs for variations in 130 specimens. These included horses from intensively selected breeds, rural breeds, and nine Przewalski’s horses, which are a rare and endangered subspecies of wild horse.

Results

  • The study confirmed the predominance of a relatively young ‘crown haplogroup’ in Central European and North American breeds. A haplogroup is a group of similar haplotypes that share a common ancestor with a single-nucleotide polymorphism mutation. In this case, the ‘crown’ refers to the most recent common ancestor of a particular group.
  • The team distinguished 58 haplotypes based on 211 variants. These formed three major haplogroups among domestic horses. A Haplotype is a group of genes within an organism that was inherited together from a single parent.
  • Two of these groups had been previously characterised: one observed in Arabian/Coldblooded horses, and the other in Turkoman/Thoroughbred horses. The newly uncovered third group contained Iberian lines and a North African Barb Horse, expanding our understanding of sire lines in different breeds.

Genealogical Showcase

  • The researchers successfully distinguished the patrilines of the three English Thoroughbred founder stallions. This not only verifies the effectiveness of their Y-chromosomal haplotyping approach but also highlights its utility in practical horse breeding and lineage verification scenarios.
  • The study resolved a longstanding controversy over the parentage of the horse ‘Galopin,’ born in 1872, by identifying its appropriate lineage through the analysis of Y-chromosomal lineages.

Historical Radiations

  • The study observed two nearly instantaneous radiations in the history of Central and Northern European Y-chromosomal lineages that both occurred after domestication around 5,500 years ago. These ‘radiations’ indicate periods when species rapidly diversify in a relatively short amount of time, relating here to the spread and variety in horse breeds after the advent of domestication.

Cite This Article

APA
Felkel S, Vogl C, Rigler D, Dobretsberger V, Chowdhary BP, Distl O, Fries R, Jagannathan V, Janečka JE, Leeb T, Lindgren G, McCue M, Metzger J, Neuditschko M, Rattei T, Raudsepp T, Rieder S, Rubin CJ, Schaefer R, Schlötterer C, Thaller G, Tetens J, Velie B, Brem G, Wallner B. (2019). The horse Y chromosome as an informative marker for tracing sire lines. Sci Rep, 9(1), 6095. https://doi.org/10.1038/s41598-019-42640-w

Publication

ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 9
Issue: 1
Pages: 6095

Researcher Affiliations

Felkel, Sabine
  • Institute of Animal Breeding and Genetics, University of Veterinary Medicine Vienna, Vienna, 1210, Austria.
  • Vienna Graduate School of Population Genetics, Vienna, Austria.
Vogl, Claus
  • Institute of Animal Breeding and Genetics, University of Veterinary Medicine Vienna, Vienna, 1210, Austria.
Rigler, Doris
  • Institute of Animal Breeding and Genetics, University of Veterinary Medicine Vienna, Vienna, 1210, Austria.
Dobretsberger, Viktoria
  • Institute of Animal Breeding and Genetics, University of Veterinary Medicine Vienna, Vienna, 1210, Austria.
Chowdhary, Bhanu P
  • United Arab Emirates University, 15551, Al Ain, UAE.
Distl, Ottmar
  • Institute for Animal Breeding and Genetics, University of Veterinary Medicine Hannover, Hannover, 30559, Germany.
Fries, Ruedi
  • Lehrstuhl fuer Tierzucht, Technische Universitaet Muenchen, Freising, 85354, Germany.
Jagannathan, Vidhya
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern, 3001, Switzerland.
Janečka, Jan E
  • Department of Biological Sciences, Duquesne University, Pittsburgh, 15282, USA.
Leeb, Tosso
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern, 3001, Switzerland.
Lindgren, Gabriella
  • Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Uppsala, 75007, Sweden.
  • Department of Biosystems, KU Leuven, Leuven, 3001, Belgium.
McCue, Molly
  • Veterinary Population Medicine Department, University of Minnesota, St. Paul, MN, 55108, USA.
Metzger, Julia
  • Institute for Animal Breeding and Genetics, University of Veterinary Medicine Hannover, Hannover, 30559, Germany.
Neuditschko, Markus
  • Agroscope, Swiss National Stud Farm, Avenches, 1580, Switzerland.
Rattei, Thomas
  • Department of Microbiology and Ecosystem Science, Division of Computational Systems Biology, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria.
Raudsepp, Terje
  • Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX, 77843-4458, USA.
Rieder, Stefan
  • Agroscope, Swiss National Stud Farm, Avenches, 1580, Switzerland.
Rubin, Carl-Johan
  • Department of Medical Biochemistry and Microbiology, Science for Life Laboratory, Uppsala University, Uppsala, 75123, Sweden.
Schaefer, Robert
  • Agroscope, Swiss National Stud Farm, Avenches, 1580, Switzerland.
Schlötterer, Christian
  • Institut fuer Populationsgenetik, University of Veterinary Medicine Vienna, Vienna, 1210, Austria.
Thaller, Georg
  • Institute of Animal Breeding and Husbandry, University of Kiel, Kiel, 24098, Germany.
Tetens, Jens
  • Institute of Animal Breeding and Husbandry, University of Kiel, Kiel, 24098, Germany.
  • Functional Breeding Group, Department of Animal Sciences, Georg-August-University Göttingen, Göttingen, 37077, Germany.
Velie, Brandon
  • Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Uppsala, 75007, Sweden.
  • School of Life and Environmental Sciences, University of Sydney, Sydney, 2006, Australia.
Brem, Gottfried
  • Institute of Animal Breeding and Genetics, University of Veterinary Medicine Vienna, Vienna, 1210, Austria.
Wallner, Barbara
  • Institute of Animal Breeding and Genetics, University of Veterinary Medicine Vienna, Vienna, 1210, Austria. barbara.wallner@vetmeduni.ac.at.

MeSH Terms

  • Animals
  • Breeding
  • Domestication
  • Female
  • Genetic Variation
  • Haplotypes
  • Horses / genetics
  • Male
  • Pedigree
  • Phylogeny
  • Y Chromosome / genetics

Grant Funding

  • W 1225 / Austrian Science Fund FWF

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 77 references
  1. Kelekna P. The Horse in Human History. .
  2. FAOSTAT www.fao.org/faostat. Accessed 2019 March 24 (2017).
  3. Rischkowsky B, Pilling D. The State of the World’s Animal Genetic Resources for Food and Agriculture. .
  4. Gaunitz C. Ancient genomes revisit the ancestry of domestic and Przewalski’s horses. Science 2018;360:111–114.
    doi: 10.1126/science.aao3297pubmed: 29472442google scholar: lookup
  5. Librado P. Ancient genomic changes associated with domestication of the horse. Science 2017;445:442–445.
    doi: 10.1126/science.aam5298pubmed: 28450643google scholar: lookup
  6. Peters JR. Römische Tierhaltung und Tierzucht: eine Synthese aus archäozoologischer Untersuchung und schriftlich-bildlicher Überlieferung. .
  7. Wutke S. Spotted phenotypes in horses lost attractiveness in the Middle Ages. Sci Rep 2016;7(6):38548.
    doi: 10.1038/srep38548pmc: PMC5141471pubmed: 27924839google scholar: lookup
  8. Lippold S. Discovery of lost diversity of paternal horse lineages using ancient DNA. Nat Commun 2011;2:450.
    doi: 10.1038/ncomms1447pubmed: 21863017google scholar: lookup
  9. Librado P. The Evolutionary Origin and Genetic Makeup of Domestic Horses. Genetics 2016;204:423–434.
    doi: 10.1534/genetics.116.194860pmc: PMC5068837pubmed: 27729493google scholar: lookup
  10. Hendricks BL. International Encyclopedia of Horse Breeds. .
  11. Poznik GD. Punctuated bursts in human male demography inferred from 1,244 worldwide Y-chromosome sequences. Nat. Genet. 2016;12:809–809.
    pmc: PMC4884158pubmed: 27111036
  12. Jobling MA, Tyler-Smith C. Human Y-chromosome variation in the genome-sequencing era. Nat. Rev. Genet. 2017;18:485–497.
    doi: 10.1038/nrg.2017.36pubmed: 28555659google scholar: lookup
  13. Edwards CJ. Dual origins of dairy cattle farming–evidence from a comprehensive survey of European Y-chromosomal variation. PLoS One 2011;6:e15922.
  14. Guirao-Rico S. Porcine Y-chromosome variation is consistent with the occurrence of paternal gene flow from non-Asian to Asian populations. Heredity (Edinb) 2018;120:1–14.
    doi: 10.1038/s41437-017-0002-9pmc: PMC5837104pubmed: 29234173google scholar: lookup
  15. Vidal O. Differential distribution of Y-chromosome haplotypes in Swiss and Southern European goat breeds. Sci. Rep. 2017;7:1–6.
    doi: 10.1038/s41598-016-0028-xpmc: PMC5701018pubmed: 29170508google scholar: lookup
  16. Ding Z-LL. Origins of domestic dog in Southern East Asia is supported by analysis of Y-chromosome DNA. Heredity (Edinb) 2012;108:507–514.
    doi: 10.1038/hdy.2011.114pmc: PMC3330686pubmed: 22108628google scholar: lookup
  17. King TE, Jobling MA. What’s in a name? Y chromosomes, surnames and the genetic genealogy revolution. Trends Genet. 2009;25:351–360.
    doi: 10.1016/j.tig.2009.06.003pubmed: 19665817google scholar: lookup
  18. Kayser M. Forensic use of Y-chromosome DNA: a general overview. Hum. Genet. 2017;136:621–635.
    doi: 10.1007/s00439-017-1776-9pmc: PMC5418305pubmed: 28315050google scholar: lookup
  19. Lindgren G. Limited number of patrilines in horse domestication. Nat Genet 2004;36:335–336.
    doi: 10.1038/ng1326pubmed: 15034578google scholar: lookup
  20. Kreutzmann N, Brem G, Wallner B. The domestic horse harbours Y-chromosomal microsatellite polymorphism only on two widely distributed male lineages. Anim Genet 2014;45:460.
    doi: 10.1111/age.12149pubmed: 24684376google scholar: lookup
  21. Wallner B, Piumi F, Brem G, Müller M, Achmann R. Isolation of Y chromosome-specific microsatellites in the horse and cross-species amplification in the genus Equus. J Hered 2004;95:158–164.
    doi: 10.1093/jhered/esh020pubmed: 15073232google scholar: lookup
  22. Wallner B. Identification of Genetic Variation on the Horse Y Chromosome and the Tracing of Male Founder Lineages in Modern Breeds. PLoS One 8 (2013).
    pmc: PMC3616054pubmed: 23573227
  23. Wallner B. Y Chromosome Uncovers the Recent Oriental Origin of Modern Stallions. Curr Biol Jul 10. 2017;27:2029–2035.
    doi: 10.1016/j.cub.2017.05.086pubmed: 28669755google scholar: lookup
  24. Felkel S. Asian horses deepen the MSY phylogeny. Anim. Genet. 2018;49:90–93.
    doi: 10.1111/age.12635pubmed: 29333704google scholar: lookup
  25. Frischknecht M. Imputation of sequence level genotypes in the Franches-Montagnes horse breed. Genet. Sel. Evol. 2014;46:1–8.
    doi: 10.1186/s12711-014-0063-7pmc: PMC4180851pubmed: 25927638google scholar: lookup
  26. Jun J. Whole genome sequence and analysis of the Marwari horse breed and its genetic origin. BMC Genomics 2014;15:S4.
    doi: 10.1186/1471-2164-15-S9-S4pmc: PMC4290615pubmed: 25521865google scholar: lookup
  27. Huang J. Analysis of horse genomes provides insight into the diversification and adaptive evolution of karyotype. Sci. Rep. 2014;4:1–8.
    pmc: PMC4021364pubmed: 24828444
  28. Schaefer RJ. Developing a 670k genotyping array to tag ~2M SNPs across 24 horse breeds. BMC Genomics 2017;18:1–18.
    doi: 10.1186/s12864-017-3943-8pmc: PMC5530493pubmed: 28750625google scholar: lookup
  29. Metzger J. Next generation sequencing gives an insight into the characteristics of highly selected breeds versus non-breed horses in the course of domestication. BMC Genomics 2014;15:562.
    doi: 10.1186/1471-2164-15-562pmc: PMC4097168pubmed: 24996778google scholar: lookup
  30. Rafati N. Large Deletions at the SHOX Locus in the Pseudoautosomal Region Are Associated with Skeletal Atavism in Shetland Ponies. G36 2016;2213–2223.
    pmc: PMC4938674pubmed: 27207956
  31. Andersson LSL. Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice. Nature 2012;488:642–646.
    doi: 10.1038/nature11399pmc: PMC3523687pubmed: 22932389google scholar: lookup
  32. Finno CJ. SERPINB11 Frameshift Variant Associated with Novel Hoof Specific Phenotype in Connemara Ponies. PLoS Genet. 2015;11:1–17.
  33. Der Sarkissian C. Evolutionary genomics and conservation of the endangered Przewalski’s horse. Curr. Biol. 2015;25:2577–2583.
    doi: 10.1016/j.cub.2015.08.032pmc: PMC5104162pubmed: 26412128google scholar: lookup
  34. Doan R. Whole-Genome sequencing and genetic variant analysis of a quarter Horse mare. BMC Genomics 2012;13:78.
    doi: 10.1186/1471-2164-13-78pmc: PMC3309927pubmed: 22340285google scholar: lookup
  35. Bauer A. A Nonsense Variant in the ST14 Gene in Akhal-Teke Horses with Naked Foal Syndrome. G3 (Bethesda) 2017;7:1315–1321.
    doi: 10.1534/g3.117.039511pmc: PMC5386879pubmed: 28235824google scholar: lookup
  36. Gómez-Sánchez D, Schlötterer C. ReadTools: A universal toolkit for handling sequence data from different sequencing platforms. Mol. Ecol. Resour. 2018;18:676–680.
    doi: 10.1111/1755-0998.12741pubmed: 29171165google scholar: lookup
  37. Paria N. A gene catalogue of the euchromatic male-specific region of the horse y chromosome: comparison with human and other mammals. PLoS One 2011;6:e21374.
  38. Li H, Durbin R. Fast and accurate short read alignment with Burrows – Wheeler transform. Bioinformatics 2009;25:1754–1760.
  39. Li H. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009;25:2078–2079.
  40. Bankevich A. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J. Comput. Biol. 2012;19:455–477.
    doi: 10.1089/cmb.2012.0021pmc: PMC3342519pubmed: 22506599google scholar: lookup
  41. Hunt M. REAPR: A universal tool for genome assembly evaluation. Genome Biol. 14 (2013).
    pmc: PMC3798757pubmed: 23710727
  42. Python Software Foundation. Python v3.5.1. .
  43. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010;26:841–842.
  44. Team RC. R: A language and environment for statistical computing. Foundation for Statistical Computing, Vienna, Austria. (2014).
  45. Camacho C. BLAST+: architecture and applications. BMC Bioinformatics 2009;15:521.
    pmc: PMC2803857pubmed: 20003500
  46. Janečka JE. Horse Y chromosome assembly displays unique evolutionary features, putative stallion fertility genes and horizontal transfer. Nat. Commun. 2018;9:2945.
    doi: 10.1038/s41467-018-05290-6pmc: PMC6063916pubmed: 30054462google scholar: lookup
  47. McKenna A. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297–303.
    doi: 10.1101/gr.107524.110pmc: PMC2928508pubmed: 20644199google scholar: lookup
  48. Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): High-performance genomics data visualization and exploration. Brief. Bioinform. 2013;14:178–192.
    doi: 10.1093/bib/bbs017pmc: PMC3603213pubmed: 22517427google scholar: lookup
  49. DL S. Phylogenetic analysis using parsimony and other methods version 4.0 beta version. 2002.
  50. Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30:1312–1313.
  51. Rambaut A. FigTree v1.4.2. .
  52. Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 1999;16:37–48.
  53. . CLC Genomics Workbench 7.7.1. © QIAGEN 2018.
  54. Suchard MA. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 2018;4:1–5.
    doi: 10.1093/ve/vey016pmc: PMC6007674pubmed: 29942656google scholar: lookup
  55. Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL. Datamonkey 2010: A suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010;26:2455–2457.
  56. Renaud G. Improved de novo genomic assembly for the domestic donkey. Sci. Adv. 2018;4:1–11.
    doi: 10.1126/sciadv.aaq0392pmc: PMC5938232pubmed: 29740610google scholar: lookup
  57. Tomaszkiewicz M. A time- and cost-effective strategy to sequence mammalian Y chromosomes: An application to the de novo assembly of gorilla Y. Genome Res. 2016;26:530–540.
    doi: 10.1101/gr.199448.115pmc: PMC4817776pubmed: 26934921google scholar: lookup
  58. Skaletsky H. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 2003;423:825–837.
    doi: 10.1038/nature01722pubmed: 12815422google scholar: lookup
  59. Treangen TJ, Salzberg SL. Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet. 2013;13:36–46.
    doi: 10.1038/nrg3117pmc: PMC3324860pubmed: 22124482google scholar: lookup
  60. Smeds L. Evolutionary analysis of the female-specific avian W chromosome. Nat. Commun. 6 (2015).
    pmc: PMC4468903pubmed: 26040272
  61. Hall AB. Six novel Y chromosome genes in Anopheles mosquitoes discovered by independently sequencing males and females. BMC Genomics 14 (2013).
    pmc: PMC3660176pubmed: 23617698
  62. Hammer M. A nomenclature system for the tree of human Y-Chromosomal binary haplogroups. Genome Res. 2002;12:339–348.
    doi: 10.1101/gr.217602pmc: PMC155271pubmed: 11827954google scholar: lookup
  63. Royo LJ. The origins of Iberian horses assessed via mitochondrial DNA. J. Hered. 2005;96:663–669.
    doi: 10.1093/jhered/esi116pubmed: 16251517google scholar: lookup
  64. Cunningham EP, Dooley JJ, Splan RK, Bradley DG. Microsatellite diversity, pedigree relatedness and the contributions of founder lineages to thoroughbred horses. Anim Genet. 2001;32:360–364.
  65. Richardson, C. In The New Book of the Horse, Volume 1 628 (Funk & Wagnalls Company 1911).
  66. Wall, J. F. In Famous Running Horses: Their Forbears and Descendants Sportsman’s Press book 313 (Infantry Journal Press 1949).
  67. Moorhouse, E. In The history and romance of the Derby, Vol 2 (Biogr. Press 1911).
  68. Larmuseau MHD, Van Geystelen A, Kayser M, van Oven M, Decorte R. Towards a consensus Y-chromosomal phylogeny and Y-SNP set in forensics in the next-generation sequencing era. Forensic Sci. Int. Genet. 2015;15:39–42.
    doi: 10.1016/j.fsigen.2014.11.012pubmed: 25488610google scholar: lookup
  69. Librado P. Tracking the origins of Yakutian horses and the genetic basis for their fast adaptation to subarctic environments. Proc. Natl. Acad. Sci. 2015;112:201513696.
    doi: 10.1073/pnas.1513696112pmc: PMC4687531pubmed: 26598656google scholar: lookup
  70. Peterlin B, Kunej T, Hristovski D. Diagnostic test for Y chromosome microdeletion screening in male infertility. Genet. Test. 2004;8:45–49.
    doi: 10.1089/109065704323016021pubmed: 15140373google scholar: lookup
  71. Toure A. A New Deletion of the Mouse Y Chromosome Long Arm Associated with the Loss of Ssty Expression, Abnormal Sperm Development and Sterility. Genetics 2004;166:901–912.
    doi: 10.1534/genetics.166.2.901pmc: PMC1470733pubmed: 15020475google scholar: lookup
  72. Raudsepp T. Molecular heterogeneity of XY sex reversal in horses. Anim. Genet. 2010;41:41–52.
  73. Achilli A. Mitochondrial genomes from modern horses reveal the major haplogroups that underwent domestication. Proc. Natl. Acad. Sci. 2012;109:2449–2454.
    doi: 10.1073/pnas.1111637109pmc: PMC3289334pubmed: 22308342google scholar: lookup
  74. Lippold S, Matzke NJ, Reissmann M, Hofreiter M. Whole mitochondrial genome sequencing of domestic horses reveals incorporation of extensive wild horse diversity during domestication. BMC Evol Biol. 2011;11:328.
    doi: 10.1186/1471-2148-11-328pmc: PMC3247663pubmed: 22082251google scholar: lookup
  75. Trombetta B, Cruciani F, Underhill Pa, Sellitto D, Scozzari R. Footprints of X-to-Y Gene Conversion in Recent Human Evolution. Mol. Biol. Evol. 2010;27:714–725.
    doi: 10.1093/molbev/msp231pubmed: 19812029google scholar: lookup
  76. Kong A. Rate of de novo mutations and the importance of father’s age to disease risk. Nature 2012;488:471–475.
    doi: 10.1038/nature11396pmc: PMC3548427pubmed: 22914163google scholar: lookup
  77. Wutke S. Decline of genetic diversity in ancient domestic stallions in Europe. Sci. Adv. 4 (2018).
    pmc: PMC5906072pubmed: 29675468

Citations

This article has been cited 29 times.
  1. Crooijmans RPMA, Gonzalez Prendes R, Colli L, Del Corvo M, Barbato M, Somenzi E, Tosser-Klopp G, Meszaros G, Ajmone-Marsan P, Weigend S, Wallner B, McCue ME, Orlando L, Bradley D, Hiemstra SJ, Schokker D, Peynot N, Stella A, Restoux G, Groenen MAM, Tixier-Boichard M. IMAGE001: A new livestock multispecies SNP array to characterize genomic variation in European livestock gene bank collections. Anim Genet 2025 Oct;56(5):e70039.
    doi: 10.1111/age.70039pubmed: 40965185google scholar: lookup
  2. Sharif MB, Mohaseb AF, Orlando L, Saliari K, Kunst GK, Czeika S, Mashkour M, Cucchi T, Peters J, Trixl S, Mohandesan E. Late Iron Age and Roman equine breeding north of the Alps: Genetic insights and cultural implications. iScience 2025 Sep 19;28(9):113224.
    doi: 10.1016/j.isci.2025.113224pubmed: 40837235google scholar: lookup
  3. Lira Garrido J, Tressières G, Chauvey L, Schiavinato S, Calvière-Tonasso L, Seguin-Orlando A, Southon J, Shapiro B, Bataille C, Birgel J, Wagner S, Khan N, Liu X, Rodanés JM, Picazo Millán JV, Giralt J, Alonso N, Aguilera I, Orsingher A, Trentacoste A, Payà X, Morán M, Iborra Eres MP, Albizuri S, Valenzuela Lamas S, Mestres Santandreu I, Duran Caixal M, Principal J, Farré Huguet J, Esteve X, Pedro Pasqual M, Sala N, Pablos A, Martín P, Vergès JM, Portero R, Arias P, Ontañón Peredo R, Detry C, Luís C, Cardoso JL, Maeir AM, Valente MJ, Grau E, Estall I Poles V, Alfonso Llorens J, Miguélez González A, Gardeisen A, Cupitò M, Tecchiati U, Bradley DG, Kolska Horwitz L, Rodríguez González E, Nieto Espinet A, Bover P, Ruiz Entrecanales R, Garcés Estallo I, Jiménez Fragoso J, Celestino S, Orlando L. The genomic history of Iberian horses since the last Ice Age. Nat Commun 2025 Aug 2;16(1):7098.
    doi: 10.1038/s41467-025-62266-zpubmed: 40753154google scholar: lookup
  4. More KD, Lebrasseur O, Garrido JL, Seguin-Orlando A, Discamps E, Estrada O, Tonasso-Calvière L, Chauvey L, Tressières G, Schiavinato S, Gibert M, Padula H, Chiavazza H, Fernández PM, Guardia NM, Borges C, Bertani S, Contreras-Mancilla J, Allccarima-Crisóstomo D, Fhon M, Barrey E, Charliquart L, Robbe E, de Noblet T, Zhumatayev R, Shakenov S, Vila E, Berthon R, Mashkour M, Khazaeli R, Nikgoftar A, Vahdati AA, Kosintsev P, Houle JL, Bayarsaikhan J, Wilczynski J, Moskal-Del Hoyo M, Nowak M, Taylor W, Bălășescu A, Dobrescu R, Benecke N, Arbuckle B, Steadman S, McMahon G, Šikanjić PR, Buric M, Vukičević TT, Alvarez N, Castel JC, Boudadi-Maligne M, Star B, Post-Melbye JR, Rødsrud CL, Stanton DWG, Charlton S, Mullin VE, Daly KG, Burgos NS, Pablos A, Dalen L, Bradley DG, Frantz L, Larson G, Orlando L. Validating a Target-Enrichment Design for Capturing Uniparental Haplotypes in Ancient Domesticated Animals. Mol Ecol Resour 2025 Oct;25(7):e14112.
    doi: 10.1111/1755-0998.14112pubmed: 40202701google scholar: lookup
  5. Radovic L, Remer V, Rigler D, Bozlak E, Allen L, Brem G, Reissman M, Brockmann GA, Ropka-Molik K, Stefaniuk-Szmukier M, Kalinkova L, Kalashnikov VV, Zaitev AM, Raudsepp T, Castaneda C, von Butler-Wemken I, Patterson Rosa L, Brooks SA, Novoa-Bravo M, Kostaras N, Abdurasulov A, Antczak DF, Miller DC, Lopes MS, da Câmara Machado A, Lindgren G, Juras R, Cothran G, Wallner B. The global spread of Oriental Horses in the past 1,500 years through the lens of the Y chromosome. Proc Natl Acad Sci U S A 2024 Dec 3;121(49):e2414408121.
    doi: 10.1073/pnas.2414408121pubmed: 39556761google scholar: lookup
  6. Bailey E, Finno CJ, Cullen JN, Kalbfleisch T, Petersen JL. Analyses of whole-genome sequences from 185 North American Thoroughbred horses, spanning 5 generations. Sci Rep 2024 Oct 2;14(1):22930.
    doi: 10.1038/s41598-024-73645-9pubmed: 39358442google scholar: lookup
  7. Gmel AI, Mikko S, Ricard A, Velie BD, Gerber V, Hamilton NA, Neuditschko M. Using high-density SNP data to unravel the origin of the Franches-Montagnes horse breed. Genet Sel Evol 2024 Jul 10;56(1):53.
    doi: 10.1186/s12711-024-00922-6pubmed: 38987703google scholar: lookup
  8. Musiał AD, Radović L, Stefaniuk-Szmukier M, Bieniek A, Wallner B, Ropka-Molik K. Mitochondrial DNA and Y chromosome reveal the genetic structure of the native Polish Konik horse population. PeerJ 2024;12:e17549.
    doi: 10.7717/peerj.17549pubmed: 38912049google scholar: lookup
  9. Fegraeus K, Rosengren MK, Naboulsi R, Orlando L, Åbrink M, Jouni A, Velie BD, Raine A, Egner B, Mattsson CM, Lång K, Zhigulev A, Björck HM, Franco-Cereceda A, Eriksson P, Andersson G, Sahlén P, Meadows JRS, Lindgren G. An endothelial regulatory module links blood pressure regulation with elite athletic performance. PLoS Genet 2024 Jun;20(6):e1011285.
    doi: 10.1371/journal.pgen.1011285pubmed: 38885195google scholar: lookup
  10. Bozlak E, Pokharel K, Weldenegodguad M, Paasivaara A, Stammler F, Røed KH, Kantanen J, Wallner B. Inferences about the population history of Rangifer tarandus from Y chromosome and mtDNA phylogenies. Ecol Evol 2024 Jun;14(6):e11573.
    doi: 10.1002/ece3.11573pubmed: 38863721google scholar: lookup
  11. Librado P, Tressières G, Chauvey L, Fages A, Khan N, Schiavinato S, Calvière-Tonasso L, Kusliy MA, Gaunitz C, Liu X, Wagner S, Der Sarkissian C, Seguin-Orlando A, Perdereau A, Aury JM, Southon J, Shapiro B, Bouchez O, Donnadieu C, Collin YRH, Gregersen KM, Jessen MD, Christensen K, Claudi-Hansen L, Pruvost M, Pucher E, Vulic H, Novak M, Rimpf A, Turk P, Reiter S, Brem G, Schwall C, Barrey É, Robert C, Degueurce C, Horwitz LK, Klassen L, Rasmussen U, Kveiborg J, Johannsen NN, Makowiecki D, Makarowicz P, Szeliga M, Ilchyshyn V, Rud V, Romaniszyn J, Mullin VE, Verdugo M, Bradley DG, Cardoso JL, Valente MJ, Telles Antunes M, Ameen C, Thomas R, Ludwig A, Marzullo M, Prato O, Bagnasco Gianni G, Tecchiati U, Granado J, Schlumbaum A, Deschler-Erb S, Mráz MS, Boulbes N, Gardeisen A, Mayer C, Döhle HJ, Vicze M, Kosintsev PA, Kyselý R, Peške L, O'Connor T, Ananyevskaya E, Shevnina I, Logvin A, Kovalev AA, Iderkhangai TO, Sablin MV, Dashkovskiy PK, Graphodatsky AS, Merts I, Merts V, Kasparov AK, Pitulko VV, Onar V, Öztan A, Arbuckle BS, McColl H, Renaud G, Khaskhanov R, Demidenko S, Kadieva A, Atabiev B, Sundqvist M, Lindgren G, López-Cachero FJ, Albizuri S, Trbojević Vukičević T, Rapan Papeša A, Burić M, Rajić Šikanjić P, Weinstock J, Asensio Vilaró D, Codina F, García Dalmau C, Morer de Llorens J, Pou J, de Prado G, Sanmartí J, Kallala N, Torres JR, Maraoui-Telmini B, Belarte Franco MC, Valenzuela-Lamas S, Zazzo A, Lepetz S, Duchesne S, Alexeev A, Bayarsaikhan J, Houle JL, Bayarkhuu N, Turbat T, Crubézy É, Shingiray I, Mashkour M, Berezina NY, Korobov DS, Belinskiy A, Kalmykov A, Demoule JP, Reinhold S, Hansen S, Wallner B, Roslyakova N, Kuznetsov PF, Tishkin AA, Wincker P, Kanne K, Outram A, Orlando L. Widespread horse-based mobility arose around 2200 BCE in Eurasia. Nature 2024 Jul;631(8022):819-825.
    doi: 10.1038/s41586-024-07597-5pubmed: 38843826google scholar: lookup
  12. Giontella A, Cardinali I, Sarti FM, Silvestrelli M, Lancioni H. Y-Chromosome Haplotype Report among Eight Italian Horse Breeds. Genes (Basel) 2023 Aug 9;14(8).
    doi: 10.3390/genes14081602pubmed: 37628653google scholar: lookup
  13. Bozlak E, Radovic L, Remer V, Rigler D, Allen L, Brem G, Stalder G, Castaneda C, Cothran G, Raudsepp T, Okuda Y, Moe KK, Moe HH, Kounnavongsa B, Keonouchanh S, Van NH, Vu VH, Shah MK, Nishibori M, Kazymbet P, Bakhtin M, Zhunushov A, Paul RC, Dashnyam B, Nozawa K, Almarzook S, Brockmann GA, Reissmann M, Antczak DF, Miller DC, Sadeghi R, von Butler-Wemken I, Kostaras N, Han H, Manglai D, Abdurasulov A, Sukhbaatar B, Ropka-Molik K, Stefaniuk-Szmukier M, Lopes MS, da Câmara Machado A, Kalashnikov VV, Kalinkova L, Zaitev AM, Novoa-Bravo M, Lindgren G, Brooks S, Rosa LP, Orlando L, Juras R, Kunieda T, Wallner B. Refining the evolutionary tree of the horse Y chromosome. Sci Rep 2023 Jun 2;13(1):8954.
    doi: 10.1038/s41598-023-35539-0pubmed: 37268661google scholar: lookup
  14. Liu X, Seguin-Orlando A, Chauvey L, Tressières G, Schiavinato S, Tonasso-Calvière L, Aury JM, Perdereau A, Wagner S, Clavel P, Estrada O, Pan J, Ma Y, Enk J, Devault A, Klunk J, Lepetz S, Clavel B, Jiang L, Wincker P, Collin YRH, Sarkissian C, Orlando L. DNA methylation-based profiling of horse archaeological remains for age-at-death and castration. iScience 2023 Mar 17;26(3):106144.
    doi: 10.1016/j.isci.2023.106144pubmed: 36843848google scholar: lookup
  15. Cardinali I, Giontella A, Tommasi A, Silvestrelli M, Lancioni H. Unlocking Horse Y Chromosome Diversity. Genes (Basel) 2022 Dec 2;13(12).
    doi: 10.3390/genes13122272pubmed: 36553539google scholar: lookup
  16. Sharif MB, Fitak RR, Wallner B, Orozco-terWengel P, Frewin S, Fremaux M, Mohandesan E. Reconstruction of the Major Maternal and Paternal Lineages in the Feral New Zealand Kaimanawa Horses. Animals (Basel) 2022 Dec 12;12(24).
    doi: 10.3390/ani12243508pubmed: 36552427google scholar: lookup
  17. Suminda GGD, Ghosh M, Son YO. The Innovative Informatics Approaches of High-Throughput Technologies in Livestock: Spearheading the Sustainability and Resiliency of Agrigenomics Research. Life (Basel) 2022 Nov 15;12(11).
    doi: 10.3390/life12111893pubmed: 36431028google scholar: lookup
  18. Radovic L, Remer V, Krcal C, Rigler D, Brem G, Rayane A, Driss K, Benamar M, Machmoum M, Piro M, Krischke D, Butler-Wemken IV, Wallner B. Y Chromosome Haplotypes Enlighten Origin, Influence, and Breeding History of North African Barb Horses. Animals (Basel) 2022 Sep 27;12(19).
    doi: 10.3390/ani12192579pubmed: 36230320google scholar: lookup
  19. Castaneda C, Radović L, Felkel S, Juras R, Davis BW, Cothran EG, Wallner B, Raudsepp T. Copy number variation of horse Y chromosome genes in normal equine populations and in horses with abnormal sex development and subfertility: relationship of copy number variations with Y haplogroups. G3 (Bethesda) 2022 Dec 1;12(12).
    doi: 10.1093/g3journal/jkac278pubmed: 36227030google scholar: lookup
  20. Remer V, Bozlak E, Felkel S, Radovic L, Rigler D, Grilz-Seger G, Stefaniuk-Szmukier M, Bugno-Poniewierska M, Brooks S, Miller DC, Antczak DF, Sadeghi R, Cothran G, Juras R, Khanshour AM, Rieder S, Penedo MC, Waiditschka G, Kalinkova L, Kalashnikov VV, Zaitsev AM, Almarzook S, Reißmann M, Brockmann GA, Brem G, Wallner B. Y-Chromosomal Insights into Breeding History and Sire Line Genealogies of Arabian Horses. Genes (Basel) 2022 Jan 26;13(2).
    doi: 10.3390/genes13020229pubmed: 35205275google scholar: lookup
  21. Ayad A, Almarzook S, Besseboua O, Aissanou S, Piórkowska K, Musiał AD, Stefaniuk-Szmukier M, Ropka-Molik K. Investigation of Cerebellar Abiotrophy (CA), Lavender Foal Syndrome (LFS), and Severe Combined Immunodeficiency (SCID) Variants in a Cohort of Three MENA Region Horse Breeds. Genes (Basel) 2021 Nov 26;12(12).
    doi: 10.3390/genes12121893pubmed: 34946842google scholar: lookup
  22. Librado P, Khan N, Fages A, Kusliy MA, Suchan T, Tonasso-Calvière L, Schiavinato S, Alioglu D, Fromentier A, Perdereau A, Aury JM, Gaunitz C, Chauvey L, Seguin-Orlando A, Der Sarkissian C, Southon J, Shapiro B, Tishkin AA, Kovalev AA, Alquraishi S, Alfarhan AH, Al-Rasheid KAS, Seregély T, Klassen L, Iversen R, Bignon-Lau O, Bodu P, Olive M, Castel JC, Boudadi-Maligne M, Alvarez N, Germonpré M, Moskal-Del Hoyo M, Wilczyński J, Pospuła S, Lasota-Kuś A, Tunia K, Nowak M, Rannamäe E, Saarma U, Boeskorov G, Lōugas L, Kyselý R, Peške L, Bălășescu A, Dumitrașcu V, Dobrescu R, Gerber D, Kiss V, Szécsényi-Nagy A, Mende BG, Gallina Z, Somogyi K, Kulcsár G, Gál E, Bendrey R, Allentoft ME, Sirbu G, Dergachev V, Shephard H, Tomadini N, Grouard S, Kasparov A, Basilyan AE, Anisimov MA, Nikolskiy PA, Pavlova EY, Pitulko V, Brem G, Wallner B, Schwall C, Keller M, Kitagawa K, Bessudnov AN, Bessudnov A, Taylor W, Magail J, Gantulga JO, Bayarsaikhan J, Erdenebaatar D, Tabaldiev K, Mijiddorj E, Boldgiv B, Tsagaan T, Pruvost M, Olsen S, Makarewicz CA, Valenzuela Lamas S, Albizuri Canadell S, Nieto Espinet A, Iborra MP, Lira Garrido J, Rodríguez González E, Celestino S, Olària C, Arsuaga JL, Kotova N, Pryor A, Crabtree P, Zhumatayev R, Toleubaev A, Morgunova NL, Kuznetsova T, Lordkipanize D, Marzullo M, Prato O, Bagnasco Gianni G, Tecchiati U, Clavel B, Lepetz S, Davoudi H, Mashkour M, Berezina NY, Stockhammer PW, Krause J, Haak W, Morales-Muñiz A, Benecke N, Hofreiter M, Ludwig A, Graphodatsky AS, Peters J, Kiryushin KY, Iderkhangai TO, Bokovenko NA, Vasiliev SK, Seregin NN, Chugunov KV, Plasteeva NA, Baryshnikov GF, Petrova E, Sablin M, Ananyevskaya E, Logvin A, Shevnina I, Logvin V, Kalieva S, Loman V, Kukushkin I, Merz I, Merz V, Sakenov S, Varfolomeyev V, Usmanova E, Zaibert V, Arbuckle B, Belinskiy AB, Kalmykov A, Reinhold S, Hansen S, Yudin AI, Vybornov AA, Epimakhov A, Berezina NS, Roslyakova N, Kosintsev PA, Kuznetsov PF, Anthony D, Kroonen GJ, Kristiansen K, Wincker P, Outram A, Orlando L. The origins and spread of domestic horses from the Western Eurasian steppes. Nature 2021 Oct;598(7882):634-640.
    doi: 10.1038/s41586-021-04018-9pubmed: 34671162google scholar: lookup
  23. Liu S, Fu C, Yang Y, Zhang Y, Ma H, Xiong Z, Ling Y, Zhao C. Current genetic conservation of Chinese indigenous horses revealed with Y-chromosomal and mitochondrial DNA polymorphisms. G3 (Bethesda) 2021 Feb 9;11(2).
    doi: 10.1093/g3journal/jkab008pubmed: 33604674google scholar: lookup
  24. Cosgrove EJ, Sadeghi R, Schlamp F, Holl HM, Moradi-Shahrbabak M, Miraei-Ashtiani SR, Abdalla S, Shykind B, Troedsson M, Stefaniuk-Szmukier M, Prabhu A, Bucca S, Bugno-Poniewierska M, Wallner B, Malek J, Miller DC, Clark AG, Antczak DF, Brooks SA. Genome Diversity and the Origin of the Arabian Horse. Sci Rep 2020 Jun 16;10(1):9702.
    doi: 10.1038/s41598-020-66232-1pubmed: 32546689google scholar: lookup
  25. Liu S, Yang Y, Pan Q, Sun Y, Ma H, Liu Y, Wang M, Zhao C, Wu C. Ancient Patrilineal Lines and Relatively High ECAY Diversity Preserved in Indigenous Horses Revealed With Novel Y-Chromosome Markers. Front Genet 2020;11:467.
    doi: 10.3389/fgene.2020.00467pubmed: 32508879google scholar: lookup
  26. Raudsepp T, Finno CJ, Bellone RR, Petersen JL. Ten years of the horse reference genome: insights into equine biology, domestication and population dynamics in the post-genome era. Anim Genet 2019 Dec;50(6):569-597.
    doi: 10.1111/age.12857pubmed: 31568563google scholar: lookup
  27. Orlando L, Librado P. Origin and Evolution of Deleterious Mutations in Horses. Genes (Basel) 2019 Aug 28;10(9).
    doi: 10.3390/genes10090649pubmed: 31466279google scholar: lookup
  28. Castaneda C, Juras R, Khanshour A, Randlaht I, Wallner B, Rigler D, Lindgren G, Raudsepp T, Cothran EG. Population Genetic Analysis of the Estonian Native Horse Suggests Diverse and Distinct Genetics, Ancient Origin and Contribution from Unique Patrilines. Genes (Basel) 2019 Aug 20;10(8).
    doi: 10.3390/genes10080629pubmed: 31434327google scholar: lookup
  29. Felkel S, Wallner B, Chuluunbat B, Yadamsuren A, Faye B, Brem G, Walzer C, Burger PA. A First Y-Chromosomal Haplotype Network to Investigate Male-Driven Population Dynamics in Domestic and Wild Bactrian Camels. Front Genet 2019;10:423.
    doi: 10.3389/fgene.2019.00423pubmed: 31178891google scholar: lookup