Analyze Diet
Frontiers in genetics2020; 11; 467; doi: 10.3389/fgene.2020.00467

Ancient Patrilineal Lines and Relatively High ECAY Diversity Preserved in Indigenous Horses Revealed With Novel Y-Chromosome Markers.

Abstract: Extremely low nucleotide diversity of modern horse Y-chromosome has been reported, and only poor phylogenetic resolution could be resulted from limited Y-chromosome markers. In this study, three types of horse Y-chromosome markers, including Single-nucleotide polymorphisms (SNPs), copy number variants (CNVs), and allele-specific CNVs, were developed by screening more than 300 male horses from 23 indigenous Chinese horse populations and 4 imported horse breeds. Fourteen segregating sites including a novel SNP in the AMELY gene were found in approximately 53 kb of male-specific Y-chromosome sequences. CNVs were detected at 11 of 14 sites, while allele-specific CNVs at 6 polymorphic sites in repeated fragments were also determined. The phylogenetic analyses with the SNPs identified in this study and previously published 51 SNPs obtained mainly from European horses showed that indigenous Chinese horses exhibit much deeper divergence than European and Middle Eastern horses, while individuals of Chinese horses with the C allele of the AMELY gene constituted the most ancient group. Via SNPs, CNVs, and allele-specific CNVs, much higher diversity of paternal lines can be detected than those identified with merely SNPs. Our results indicated that there are ancient paternal horse lines preserved in southwestern China, which sheds new light on the domestication and immigration of horses, and suggest that the priorities of the conservation should be given to the ancient and rare paternal lines. These three marker types provided finer phylogenetic resolution of horse patrilineal lines, and the strategies used in the present study also provide valuable reference for the genetic studies of other mammalian patrilineages.
Publication Date: 2020-05-21 PubMed ID: 32508879PubMed Central: PMC7253630DOI: 10.3389/fgene.2020.00467Google 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

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.

This study reveals that indigenous Chinese horses show more diversity from a genetic standpoint than their European and Middle Eastern counterparts. Through advanced genetic testing methods, previously unidentified ancient patrilineal lines were discovered, providing greater insight into the domestication and migration history of horses.

Research Methodology

  • The research involved a comprehensive screening of over 300 male horses. The subjects were divided into 23 indigenous Chinese horse populations and 4 imported horse breeds.
  • The screening focused on three types of horse Y-chromosome markers. These markes are:
    • Single-nucleotide polymorphisms (SNPs), which involve changes in individual genetic building blocks.
    • Copy number variants (CNVs), referring to regions of the genome where the number of copies of a particular section varies between individuals.
    • Allele-specific CNVs, which involve differences observed in the same genetic locus.
  • The researchers identified 14 segregating sites, including an unidentified SNP in the AMELY gene (found on male-specific Y-chromosomes). CNVs were detected at 11 of these sites, with allele-specific CNVs present in 6 polymorphic areas of repeated fragments.

Research Findings

  • The phylogenetic analyses (study of evolutionary relationships) was executed, using both the SNPs identified in this study, and 51 SNPs previously derived mostly from European horses.
  • The study revealed that indigenous Chinese horses show a deeper genetic divergence than European and Middle Eastern horses. A group of Chinese horses with a specific genetic trait (the C allele of the AMELY gene) were identified as the most ancient group.
  • Through the combination of SNPs, CNVs, and allele-specific CNVs, a higher diversity of paternal horse lines was identified.
  • Powerful evidence was identified for the existence of ancient paternal horse lines in southwestern China, shining new light on horse domestication and migration history.

Implications and Further Studies

  • The study suggests that conservation priorities should be reoriented towards protecting these ancient and rare paternal lines.
  • The techniques and strategies utilised in this study could be used to gain further understandings in genetic studies of other mammalian patrilineages, indicating the potential of these methods for broader use.

Cite This Article

APA
Liu S, Yang Y, Pan Q, Sun Y, Ma H, Liu Y, Wang M, Zhao C, Wu C. (2020). Ancient Patrilineal Lines and Relatively High ECAY Diversity Preserved in Indigenous Horses Revealed With Novel Y-Chromosome Markers. Front Genet, 11, 467. https://doi.org/10.3389/fgene.2020.00467

Publication

ISSN: 1664-8021
NlmUniqueID: 101560621
Country: Switzerland
Language: English
Volume: 11
Pages: 467
PII: 467

Researcher Affiliations

Liu, Shuqin
  • College of Animal Science and Technology, China Agricultural University, Beijing, China.
  • Equine Center, China Agricultural University, Beijing, China.
Yang, Yunzhou
  • College of Animal Science and Technology, China Agricultural University, Beijing, China.
  • Equine Center, China Agricultural University, Beijing, China.
Pan, Qingjie
  • School of Animal Science and Technology, Qingdao Agricultural University, Shandong, China.
Sun, Yujiang
  • School of Animal Science and Technology, Qingdao Agricultural University, Shandong, China.
Ma, Hongying
  • College of Animal Science and Technology, China Agricultural University, Beijing, China.
  • Equine Center, China Agricultural University, Beijing, China.
Liu, Yu
  • College of Animal Science and Technology, China Agricultural University, Beijing, China.
  • Equine Center, China Agricultural University, Beijing, China.
Wang, Min
  • College of Animal Science and Technology, China Agricultural University, Beijing, China.
  • Equine Center, China Agricultural University, Beijing, China.
Zhao, Chunjiang
  • College of Animal Science and Technology, China Agricultural University, Beijing, China.
  • Equine Center, China Agricultural University, Beijing, China.
  • National Engineering Laboratory for Animal Breeding, Beijing, China.
  • Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture, Beijing, China.
  • Beijing Key Laboratory for Animal Genetic Improvement, Beijing, China.
Wu, Changxin
  • College of Animal Science and Technology, China Agricultural University, Beijing, China.
  • Equine Center, China Agricultural University, Beijing, China.
  • National Engineering Laboratory for Animal Breeding, Beijing, China.
  • Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture, Beijing, China.
  • Beijing Key Laboratory for Animal Genetic Improvement, Beijing, China.

References

This article includes 48 references
  1. Achilli A, Olivieri A, Soares P, Lancioni H, Hooshiar Kashani B, Perego UA, Nergadze SG, Carossa V, Santagostino M, Capomaccio S, Felicetti M, Al-Achkar W, Penedo MC, Verini-Supplizi A, Houshmand M, Woodward SR, Semino O, Silvestrelli M, Giulotto E, Pereira L, Bandelt HJ, Torroni A. Mitochondrial genomes from modern horses reveal the major haplogroups that underwent domestication.. Proc Natl Acad Sci U S A 2012 Feb 14;109(7):2449-54.
    doi: 10.1073/pnas.1111637109pmc: PMC3289334pubmed: 22308342google scholar: lookup
  2. Bidon T, Janke A, Fain SR, Eiken HG, Hagen SB, Saarma U, Hallström BM, Lecomte N, Hailer F. Brown and polar bear Y chromosomes reveal extensive male-biased gene flow within brother lineages.. Mol Biol Evol 2014 Jun;31(6):1353-63.
    doi: 10.1093/molbev/msu109pubmed: 24667925google scholar: lookup
  3. Brandariz-Fontes C, Leonard JA, Vega-Pla JL, Backström N, Lindgren G, Lippold S, Rico C. Y-chromosome analysis in Retuertas horses.. PLoS One 2013;8(5):e64985.
    doi: 10.1371/journal.ponepmc: PMC3669082pubmed: 23741439google scholar: lookup
  4. Cai D. W., Tang Z. W., Han L., Speller C. F., Yang D. Y. Y., Ma X. L.. Ancient DNA provides new insights into the origin of the Chinese domestic horse. J. Archaeol. Sci. 36 835–842.
    doi: 10.1016/j.jas.2008.11.006google scholar: lookup
  5. Chang H.. Animal Genetic Resources in China-Horses, Donkeys, and Camels. .
  6. Cieslak M, Pruvost M, Benecke N, Hofreiter M, Morales A, Reissmann M, Ludwig A. Origin and history of mitochondrial DNA lineages in domestic horses.. PLoS One 2010 Dec 20;5(12):e15311.
  7. Cortes O, Tupac-Yupanqui I, Dunner S, Fernández J, Cañón J. Y chromosome genetic diversity in the Lidia bovine breed: a highly fragmented population.. J Anim Breed Genet 2011 Dec;128(6):491-6.
  8. Cunningham EP, Dooley JJ, Splan RK, Bradley DG. Microsatellite diversity, pedigree relatedness and the contributions of founder lineages to thoroughbred horses.. Anim Genet 2001 Dec;32(6):360-4.
  9. 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. The horse Y chromosome as an informative marker for tracing sire lines.. Sci Rep 2019 Apr 15;9(1):6095.
    doi: 10.1038/s41598-019-42640-wpmc: PMC6465346pubmed: 30988347google scholar: lookup
  10. Felkel S, Vogl C, Rigler D, Jagannathan V, Leeb T, Fries R, Neuditschko M, Rieder S, Velie B, Lindgren G, Rubin CJ, Schlötterer C, Rattei T, Brem G, Wallner B. Asian horses deepen the MSY phylogeny.. Anim Genet 2018 Feb;49(1):90-93.
    doi: 10.1111/age.12635pubmed: 29333704google scholar: lookup
  11. Freire-Aradas A, Fondevila M, Kriegel AK, Phillips C, Gill P, Prieto L, Schneider PM, Carracedo A, Lareu MV. A new SNP assay for identification of highly degraded human DNA.. Forensic Sci Int Genet 2012 May;6(3):341-9.
    doi: 10.1016/j.fsigen.2011.07.010pubmed: 21908243google scholar: lookup
  12. Hallast P, Jobling MA. The Y chromosomes of the great apes.. Hum Genet 2017 May;136(5):511-528.
    doi: 10.1007/s00439-017-1769-1768pubmed: 28265767google scholar: lookup
  13. Hamilton CK, Favetta LA, Di Meo GP, Floriot S, Perucatti A, Peippo J, Kantanen J, Eggen A, Iannuzzi L, King WA. Copy number variation of testis-specific protein, Y-encoded (TSPY) in 14 different breeds of cattle (Bos taurus).. Sex Dev 2009;3(4):205-13.
    doi: 10.1159/000228721pubmed: 19752600google scholar: lookup
  14. Han H, Wallner B, Rigler D, MacHugh DE, Manglai D, Hill EW. Chinese Mongolian horses may retain early domestic male genetic lineages yet to be discovered.. Anim Genet 2019 Aug;50(4):399-402.
    doi: 10.1111/age.12780pubmed: 31073991google scholar: lookup
  15. Han H, Zhang Q, Gao K, Yue X, Zhang T, Dang R, Lan X, Chen H, Lei C. Y-Single Nucleotide Polymorphisms Diversity in Chinese Indigenous Horse.. Asian-Australas J Anim Sci 2015 Aug;28(8):1066-74.
    doi: 10.5713/ajas.14.0784pmc: PMC4478473pubmed: 26104513google scholar: lookup
  16. He K. Y.. A tentative study of origin of Chinese domestic horses. Chengdu Archaeol. Res. 2008 714–723.
  17. Hendricks B. L.. International Encyclopedia of Horse Breeds. .
  18. Hou W. T.. A brief analysis of the origin and development of the pony in China. Agric. Archaeol. 1 340–344.
  19. Janečka JE, Davis BW, Ghosh S, Paria N, Das PJ, Orlando L, Schubert M, Nielsen MK, Stout TAE, Brashear W, Li G, Johnson CD, Metz RP, Zadjali AMA, Love CC, Varner DD, Bellott DW, Murphy WJ, Chowdhary BP, Raudsepp T. Horse Y chromosome assembly displays unique evolutionary features and putative stallion fertility genes.. Nat Commun 2018 Jul 27;9(1):2945.
  20. Jansen T, Forster P, Levine MA, Oelke H, Hurles M, Renfrew C, Weber J, Olek K. Mitochondrial DNA and the origins of the domestic horse.. Proc Natl Acad Sci U S A 2002 Aug 6;99(16):10905-10.
    doi: 10.1073/pnas.152330099pmc: PMC125071pubmed: 12130666google scholar: lookup
  21. Jiang Q, Wei Y, Huang Y, Jiang H, Guo Y, Lan G, Liao J. The complete mitochondrial genome and phylogenetic analysis of the Debao pony (Equus caballus).. Mol Biol Rep 2011 Jan;38(1):593-9.
    doi: 10.1007/s11033-010-0145-148pubmed: 20390359google scholar: lookup
  22. Kreutzmann N, Brem G, Wallner B. The domestic horse harbours Y-chromosomal microsatellite polymorphism only on two widely distributed male lineages.. Anim Genet 2014 Jun;45(3):460.
    doi: 10.1111/age.12149pubmed: 24684376google scholar: lookup
  23. Langaee T, Hamadeh I, Chapman AB, Gums JG, Johnson JA. A novel simple method for determining CYP2D6 gene copy number and identifying allele(s) with duplication/multiplication.. PLoS One 2015;10(1):e0113808.
  24. Lau AN, Peng L, Goto H, Chemnick L, Ryder OA, Makova KD. Horse domestication and conservation genetics of Przewalski's horse inferred from sex chromosomal and autosomal sequences.. Mol Biol Evol 2009 Jan;26(1):199-208.
    doi: 10.1093/molbev/msn239pubmed: 18931383google scholar: lookup
  25. Lei CZ, Su R, Bower MA, Edwards CJ, Wang XB, Weining S, Liu L, Xie WM, Li F, Liu RY, Zhang YS, Zhang CM, Chen H. Multiple maternal origins of native modern and ancient horse populations in China.. Anim Genet 2009 Dec;40(6):933-44.
  26. Levine M. A.. Botai and the origins of horse domestication. J. Anthropol. Archaeol. 18 29–78.
    doi: 10.1006/jaar.1998.0332google scholar: lookup
  27. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.. Bioinformatics 2009 Jun 1;25(11):1451-2.
    doi: 10.1093/bioinformatics/btp187pubmed: 19346325google scholar: lookup
  28. Lindgren G, Backström N, Swinburne J, Hellborg L, Einarsson A, Sandberg K, Cothran G, Vilà C, Binns M, Ellegren H. Limited number of patrilines in horse domestication.. Nat Genet 2004 Apr;36(4):335-6.
    doi: 10.1038/ng1326pubmed: 15034578google scholar: lookup
  29. Ling YH, Ma YH, Guan WJ, Cheng YJ, Wang YP, Han JL, Mang L, Zhao QJ, He XH, Pu YB, Fu BL. Evaluation of the genetic diversity and population structure of Chinese indigenous horse breeds using 27 microsatellite markers.. Anim Genet 2011 Feb;42(1):56-65.
  30. Ling Y, Ma Y, Guan W, Cheng Y, Wang Y, Han J, Jin D, Mang L, Mahmut H. Identification of Y chromosome genetic variations in Chinese indigenous horse breeds.. J Hered 2010 Sep-Oct;101(5):639-43.
    doi: 10.1093/jhered/esq047pubmed: 20497969google scholar: lookup
  31. Lippold S, Knapp M, Kuznetsova T, Leonard JA, Benecke N, Ludwig A, Rasmussen M, Cooper A, Weinstock J, Willerslev E, Shapiro B, Hofreiter M. Discovery of lost diversity of paternal horse lineages using ancient DNA.. Nat Commun 2011 Aug 23;2:450.
    doi: 10.1038/ncomms1447pubmed: 21863017google scholar: lookup
  32. Lira J, Linderholm A, Olaria C, Brandström Durling M, Gilbert MT, Ellegren H, Willerslev E, Lidén K, Arsuaga JL, Götherström A. Ancient DNA reveals traces of Iberian Neolithic and Bronze Age lineages in modern Iberian horses.. Mol Ecol 2010 Jan;19(1):64-78.
  33. Lister A., Kadwell M., Kaagen L. M., Richards M. B., Stanley H. F.. Ancient and modern DNA in a study of horse domestication. Ancient Biomol. 2 267–280.
  34. Márquez GC, Speidel SE, Enns RM, Garrick DJ. Genetic diversity and population structure of American Red Angus cattle.. J Anim Sci 2010 Jan;88(1):59-68.
    doi: 10.2527/jas.2008-1292pubmed: 19783699google scholar: lookup
  35. Pierce MD, Dzama K, Muchadeyi FC. Corrigendum: Genetic Diversity of Seven Cattle Breeds Inferred Using Copy Number Variations.. Front Genet 2018;9:252.
    doi: 10.3389/fgene.2018.00252pmc: PMC6053618pubmed: 30038636google scholar: lookup
  36. Rafeie F., Amirinia C., Javaremi A. N., Mirhoseini S. Z., Amirmozafari N.. A study of patrilineal genetic diversity in Iranian indigenous horse breeds. Afr. J. Biotechnol. 10 17347–17352.
    doi: 10.5897/Ajb11.1430google scholar: lookup
  37. Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH, Andrews TD, Fiegler H, Shapero MH, Carson AR, Chen W, Cho EK, Dallaire S, Freeman JL, González JR, Gratacòs M, Huang J, Kalaitzopoulos D, Komura D, MacDonald JR, Marshall CR, Mei R, Montgomery L, Nishimura K, Okamura K, Shen F, Somerville MJ, Tchinda J, Valsesia A, Woodwark C, Yang F, Zhang J, Zerjal T, Zhang J, Armengol L, Conrad DF, Estivill X, Tyler-Smith C, Carter NP, Aburatani H, Lee C, Jones KW, Scherer SW, Hurles ME. Global variation in copy number in the human genome.. Nature 2006 Nov 23;444(7118):444-54.
    doi: 10.1038/nature05329pmc: PMC2669898pubmed: 17122850google scholar: lookup
  38. Subramanian S.. Y-chromosome multicopy genes. Genome Biol. 2:reorts0023.
    doi: 10.1186/gb-2001-google scholar: lookup
  39. Vilà C, Leonard JA, Gotherstrom A, Marklund S, Sandberg K, Liden K, Wayne RK, Ellegren H. Widespread origins of domestic horse lineages.. Science 2001 Jan 19;291(5503):474-7.
    doi: 10.1126/science.291.5503.474pubmed: 11161199google scholar: lookup
  40. Wallner B, Palmieri N, Vogl C, Rigler D, Bozlak E, Druml T, Jagannathan V, Leeb T, Fries R, Tetens J, Thaller G, Metzger J, Distl O, Lindgren G, Rubin CJ, Andersson L, Schaefer R, McCue M, Neuditschko M, Rieder S, Schlötterer C, Brem G. Y Chromosome Uncovers the Recent Oriental Origin of Modern Stallions.. Curr Biol 2017 Jul 10;27(13):2029-2035.e5.
    doi: 10.1016/j.cubpubmed: 28669755google scholar: lookup
  41. 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 Mar-Apr;95(2):158-64.
    doi: 10.1093/jhered/esh020pubmed: 15073232google scholar: lookup
  42. Wallner B, Vogl C, Shukla P, Burgstaller JP, Druml T, Brem G. Identification of genetic variation on the horse y chromosome and the tracing of male founder lineages in modern breeds.. PLoS One 2013;8(4):e60015.
  43. Warmuth V, Eriksson A, Bower MA, Barker G, Barrett E, Hanks BK, Li S, Lomitashvili D, Ochir-Goryaeva M, Sizonov GV, Soyonov V, Manica A. Reconstructing the origin and spread of horse domestication in the Eurasian steppe.. Proc Natl Acad Sci U S A 2012 May 22;109(21):8202-6.
    doi: 10.1073/pnas.1111122109pmc: PMC3361400pubmed: 22566639google scholar: lookup
  44. Xu LX, Yang SL, Lin RY, Yang HB, Li AP, Wan QS. Genetic diversity and population structure of Chinese pony breeds using microsatellite markers.. Genet Mol Res 2012 Aug 16;11(3):2629-40.
    doi: 10.4238/2012.June.25.4pubmed: 22782636google scholar: lookup
  45. Yuan J.. Studies of chinese prehistory. Archaeology 436–443.
  46. Yue XP, Qin F, Campana MG, Liu DH, Mao CC, Wang XB, Lan XY, Chen H, Lei CZ. Characterization of cytochrome b diversity in Chinese domestic horses.. Anim Genet 2012 Oct;43(5):624-6.
  47. Zhang H, Roe D, Kuang R. Detecting Population-Differentiation Copy Number Variants in Human Population Tree by Sparse Group Selection.. IEEE/ACM Trans Comput Biol Bioinform 2019 Mar-Apr;16(2):538-549.
    doi: 10.1109/TCBB.2017.2779481pubmed: 29990238google scholar: lookup
  48. Zhang Z.. The nationalities on horseback in ancient Yunnan province and their related issues. Yunnan Natl. U 2 13–20.

Citations

This article has been cited 6 times.
  1. 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
  2. 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
  3. 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
  4. 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
  5. 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
  6. 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