FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Nature genetics2015; 48(2); 152-158; doi: 10.1038/ng.3475

Regulatory mutations in TBX3 disrupt asymmetric hair pigmentation that underlies Dun camouflage color in horses.

Abstract: Dun is a wild-type coat color in horses characterized by pigment dilution with a striking pattern of dark areas termed primitive markings. Here we show that pigment dilution in Dun horses is due to radially asymmetric deposition of pigment in the growing hair caused by localized expression of the T-box 3 (TBX3) transcription factor in hair follicles, which in turn determines the distribution of hair follicle melanocytes. Most domestic horses are non-dun, a more intensely pigmented phenotype caused by regulatory mutations impairing TBX3 expression in the hair follicle, resulting in a more circumferential distribution of melanocytes and pigment granules in individual hairs. We identified two different alleles (non-dun1 and non-dun2) causing non-dun color. non-dun2 is a recently derived allele, whereas the Dun and non-dun1 alleles are found in ancient horse DNA, demonstrating that this polymorphism predates horse domestication. These findings uncover a new developmental role for T-box genes and new aspects of hair follicle biology and pigmentation.
Get Full Text
Publication Date: 2015-12-21 PubMed ID: 26691985PubMed Central: PMC4731265DOI: 10.1038/ng.3475Google 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.
LinkedInCopy
  • Journal Article
  • Research Support
  • N.I.H.
  • Extramural
  • 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.

This study discovered that genetic mutations in TBX3, a transcription factor, disrupt the usual distribution of hair pigmentation in horses, causing a particular camouflage colour known as Dun. They also identified two different Dun-disrupting alleles (non-dun1 and non-dun2), one of which predates horse domestication.

Understanding the Dun Coat Color

  • Dun is a unique coat color seen in wild horses characterized by diluted pigmentation and a distinct pattern of dark areas called primitive markings.
  • The researchers found that the pigment dilution in Dun horses occurs due to radially asymmetric deposition of the pigment in the growing hair. This irregular distribution of pigment is triggered by the localized expression of a transcription factor known as T-box 3 (TBX3) in the hair follicles of the horse.
  • TBX3 determines the distribution of melanocytes, cells that produce and contain pigments, in the hair follicles.

The Impact of TBX3 Disruptions

  • However, most domestic horses exhibit a condition known as non-dun, characterized by a more intensely pigmented phenotype. This is due to mutations that disrupt TBX3 expression.
  • These mutations result in impaired TBX3 expression in the hair follicle and lead to a more uniform, or circumferential, distribution of melanocytes and pigment granules in each hair, causing intense color pigmentation.

Identifying Non-dun Alleles

  • The researchers identified two different alleles responsible for the non-dun color, termed non-dun1 and non-dun2.
  • The non-dun2 allele is a recent one, while both Dun and non-dun1 alleles have been identified in ancient horse DNA. This indicates that this particular genetic variance predates horse domestication.

Implications of the Research

  • This study reveals a new developmental role for T-box genes, which were previously unassociated with hair follicle biology and pigmentation.
  • Understanding the mechanisms of coat color regulation may have broader implications for scientific understanding of genetic regulation of pigmentation, and for the development of new strategies for color manipulation in breeding programs.

Cite This Article

APA
Imsland F, McGowan K, Rubin CJ, Henegar C, Sundström E, Berglund J, Schwochow D, Gustafson U, Imsland P, Lindblad-Toh K, Lindgren G, Mikko S, Millon L, Wade C, Schubert M, Orlando L, Penedo MC, Barsh GS, Andersson L. (2015). Regulatory mutations in TBX3 disrupt asymmetric hair pigmentation that underlies Dun camouflage color in horses. Nat Genet, 48(2), 152-158. https://doi.org/10.1038/ng.3475

Publication

Nature genetics
ISSN: 1546-1718
NlmUniqueID: 9216904
Country: United States
Language: English
Volume: 48
Issue: 2
Pages: 152-158

Researcher Affiliations

Imsland, Freyja
  • Science for Life Laboratory Uppsala, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.
McGowan, Kelly
  • HudsonAlpha Institute for Biotechnology, Huntsville, Alabama, USA.
  • Department of Genetics, Stanford University School of Medicine, Stanford, California, USA.
Rubin, Carl-Johan
  • Science for Life Laboratory Uppsala, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.
Henegar, Corneliu
  • Department of Genetics, Stanford University School of Medicine, Stanford, California, USA.
Sundström, Elisabeth
  • Science for Life Laboratory Uppsala, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.
Berglund, Jonas
  • Science for Life Laboratory Uppsala, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.
Schwochow, Doreen
  • Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Uppsala, Sweden.
  • Institut National de la Recherche Agronomique (INRA), AgroParisTech, Génetique Animale et Biologie Intégrative, Jouy-en-Josas, France.
Gustafson, Ulla
  • Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Uppsala, Sweden.
Imsland, Páll
  • Menntaskólinn við Hamrahlíð, Reykjavík, Iceland.
Lindblad-Toh, Kerstin
  • Science for Life Laboratory Uppsala, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.
  • Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA.
Lindgren, Gabriella
  • Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Uppsala, Sweden.
Mikko, Sofia
  • Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Uppsala, Sweden.
Millon, Lee
  • Veterinary Genetics Laboratory, School of Veterinary Medicine, University of California, Davis, Davis, California, USA.
Wade, Claire
  • Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA.
Schubert, Mikkel
  • Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.
Orlando, Ludovic
  • Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.
Penedo, Maria Cecilia T
  • Veterinary Genetics Laboratory, School of Veterinary Medicine, University of California, Davis, Davis, California, USA.
Barsh, Gregory S
  • HudsonAlpha Institute for Biotechnology, Huntsville, Alabama, USA.
  • Department of Genetics, Stanford University School of Medicine, Stanford, California, USA.
Andersson, Leif
  • Science for Life Laboratory Uppsala, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.
  • Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Uppsala, Sweden.
  • Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, USA.

MeSH Terms

  • Animals
  • Gene Expression Profiling
  • Hair Color / genetics
  • Hair Follicle / metabolism
  • Horses / genetics
  • Mutation
  • Skin / metabolism
  • T-Box Domain Proteins / genetics

Grant Funding

  • R01 AR067925 / NIAMS NIH HHS

Conflict of Interest Statement

. The authors declare no competing financial interests.

References

This article includes 32 references
  1. Wade CM, Giulotto E, Sigurdsson S, Zoli M, Gnerre S, Imsland F, Lear TL, Adelson DL, Bailey E, Bellone RR, Blöcker H, Distl O, Edgar RC, Garber M, Leeb T, Mauceli E, MacLeod JN, Penedo MC, Raison JM, Sharpe T, Vogel J, Andersson L, Antczak DF, Biagi T, Binns MM, Chowdhary BP, Coleman SJ, Della Valle G, Fryc S, Guérin G, Hasegawa T, Hill EW, Jurka J, Kiialainen A, Lindgren G, Liu J, Magnani E, Mickelson JR, Murray J, Nergadze SG, Onofrio R, Pedroni S, Piras MF, Raudsepp T, Rocchi M, Røed KH, Ryder OA, Searle S, Skow L, Swinburne JE, Syvänen AC, Tozaki T, Valberg SJ, Vaudin M, White JR, Zody MC, Lander ES, Lindblad-Toh K. Genome sequence, comparative analysis, and population genetics of the domestic horse.. Science 2009 Nov 6;326(5954):865-7.
    pmc: PMC3785132pubmed: 19892987doi: 10.1126/science.1178158google scholar: lookup
  2. Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M, Schubert M, Cappellini E, Petersen B, Moltke I, Johnson PL, Fumagalli M, Vilstrup JT, Raghavan M, Korneliussen T, Malaspinas AS, Vogt J, Szklarczyk D, Kelstrup CD, Vinther J, Dolocan A, Stenderup J, Velazquez AM, Cahill J, Rasmussen M, Wang X, Min J, Zazula GD, Seguin-Orlando A, Mortensen C, Magnussen K, Thompson JF, Weinstock J, Gregersen K, Røed KH, Eisenmann V, Rubin CJ, Miller DC, Antczak DF, Bertelsen MF, Brunak S, Al-Rasheid KA, Ryder O, Andersson L, Mundy J, Krogh A, Gilbert MT, Kjær K, Sicheritz-Ponten T, Jensen LJ, Olsen JV, Hofreiter M, Nielsen R, Shapiro B, Wang J, Willerslev E. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse.. Nature 2013 Jul 4;499(7456):74-8.
    pubmed: 23803765doi: 10.1038/nature12323google scholar: lookup
  3. Bowling AT, Ryder OA. Genetic studies of blood markers in Przewalski's horses.. J Hered 1987 Mar-Apr;78(2):75-80.
    pubmed: 3584938doi: 10.1093/oxfordjournals.jhered.a110340google scholar: lookup
  4. Adalsteinsson S. Inheritance of yellow dun and blue dun in the Icelandic toelter horse.. J Hered 1978 May-Jun;69(3):146-8.
    pubmed: 731005doi: 10.1093/oxfordjournals.jhered.a108913google scholar: lookup
  5. Bamshad M, Lin RC, Law DJ, Watkins WC, Krakowiak PA, Moore ME, Franceschini P, Lala R, Holmes LB, Gebuhr TC, Bruneau BG, Schinzel A, Seidman JG, Seidman CE, Jorde LB. Mutations in human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome.. Nat Genet 1997 Jul;16(3):311-5.
    pubmed: 9207801doi: 10.1038/ng0797-311google scholar: lookup
  6. Frank DU, Emechebe U, Thomas KR, Moon AM. Mouse TBX3 mutants suggest novel molecular mechanisms for Ulnar-mammary syndrome.. PLoS One 2013;8(7):e67841.
    pmc: PMC3699485pubmed: 23844108doi: 10.1371/journal.pone.0067841google scholar: lookup
  7. Kumar P P, Franklin S, Emechebe U, Hu H, Moore B, Lehman C, Yandell M, Moon AM. TBX3 regulates splicing in vivo: a novel molecular mechanism for Ulnar-mammary syndrome.. PLoS Genet 2014 Mar;10(3):e1004247.
    pmc: PMC3967948pubmed: 24675841doi: 10.1371/journal.pgen.1004247google scholar: lookup
  8. Gremmel F. Coat colors in horses. J Hered 1939;30:437–445.
  9. Andersson LS, Larhammar M, Memic F, Wootz H, Schwochow D, Rubin CJ, Patra K, Arnason T, Wellbring L, Hjälm G, Imsland F, Petersen JL, McCue ME, Mickelson JR, Cothran G, Ahituv N, Roepstorff L, Mikko S, Vallstedt A, Lindgren G, Andersson L, Kullander K. Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice.. Nature 2012 Aug 30;488(7413):642-6.
    pmc: PMC3523687pubmed: 22932389doi: 10.1038/nature11399google scholar: lookup
  10. Schubert M, Jónsson H, Chang D, Der Sarkissian C, Ermini L, Ginolhac A, Albrechtsen A, Dupanloup I, Foucal A, Petersen B, Fumagalli M, Raghavan M, Seguin-Orlando A, Korneliussen TS, Velazquez AM, Stenderup J, Hoover CA, Rubin CJ, Alfarhan AH, Alquraishi SA, Al-Rasheid KA, MacHugh DE, Kalbfleisch T, MacLeod JN, Rubin EM, Sicheritz-Ponten T, Andersson L, Hofreiter M, Marques-Bonet T, Gilbert MT, Nielsen R, Excoffier L, Willerslev E, Shapiro B, Orlando L. Prehistoric genomes reveal the genetic foundation and cost of horse domestication.. Proc Natl Acad Sci U S A 2014 Dec 30;111(52):E5661-9.
    pmc: PMC4284583pubmed: 25512547doi: 10.1073/pnas.1416991111google scholar: lookup
  11. Thomas-Chollier M, Hufton A, Heinig M, O'Keeffe S, Masri NE, Roider HG, Manke T, Vingron M. Transcription factor binding predictions using TRAP for the analysis of ChIP-seq data and regulatory SNPs.. Nat Protoc 2011 Nov 3;6(12):1860-9.
    pubmed: 22051799doi: 10.1038/nprot.2011.409google scholar: lookup
  12. Ma L, Liu J, Wu T, Plikus M, Jiang TX, Bi Q, Liu YH, Müller-Röver S, Peters H, Sundberg JP, Maxson R, Maas RL, Chuong CM. 'Cyclic alopecia' in Msx2 mutants: defects in hair cycling and hair shaft differentiation.. Development 2003 Jan;130(2):379-89.
    pmc: PMC4386654pubmed: 12466204doi: 10.1242/dev.00201google scholar: lookup
  13. Kayserili H, Uz E, Niessen C, Vargel I, Alanay Y, Tuncbilek G, Yigit G, Uyguner O, Candan S, Okur H, Kaygin S, Balci S, Mavili E, Alikasifoglu M, Haase I, Wollnik B, Akarsu NA. ALX4 dysfunction disrupts craniofacial and epidermal development.. Hum Mol Genet 2009 Nov 15;18(22):4357-66.
    pubmed: 19692347doi: 10.1093/hmg/ddp391google scholar: lookup
  14. Reginelli AD, Wang YQ, Sassoon D, Muneoka K. Digit tip regeneration correlates with regions of Msx1 (Hox 7) expression in fetal and newborn mice.. Development 1995 Apr;121(4):1065-76.
    pubmed: 7538067doi: 10.1242/dev.121.4.1065google scholar: lookup
  15. Satokata I, Ma L, Ohshima H, Bei M, Woo I, Nishizawa K, Maeda T, Takano Y, Uchiyama M, Heaney S, Peters H, Tang Z, Maxson R, Maas R. Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation.. Nat Genet 2000 Apr;24(4):391-5.
    pubmed: 10742104doi: 10.1038/74231google scholar: lookup
  16. Steingrímsson E, Copeland NG, Jenkins NA. Melanocytes and the microphthalmia transcription factor network.. Annu Rev Genet 2004;38:365-411.
    pubmed: 15568981doi: 10.1146/annurev.genet.38.072902.092717google scholar: lookup
  17. Kunisada T, Yoshida H, Yamazaki H, Miyamoto A, Hemmi H, Nishimura E, Shultz LD, Nishikawa S, Hayashi S. Transgene expression of steel factor in the basal layer of epidermis promotes survival, proliferation, differentiation and migration of melanocyte precursors.. Development 1998 Aug;125(15):2915-23.
    pubmed: 9655813doi: 10.1242/dev.125.15.2915google scholar: lookup
  18. Yoshida H, Kunisada T, Grimm T, Nishimura EK, Nishioka E, Nishikawa SI. Review: melanocyte migration and survival controlled by SCF/c-kit expression.. J Investig Dermatol Symp Proc 2001 Nov;6(1):1-5.
    pubmed: 11764276doi: 10.1046/j.0022-202x.2001.00006.xgoogle scholar: lookup
  19. St-Jacques B, Dassule HR, Karavanova I, Botchkarev VA, Li J, Danielian PS, McMahon JA, Lewis PM, Paus R, McMahon AP. Sonic hedgehog signaling is essential for hair development.. Curr Biol 1998 Sep 24;8(19):1058-68.
    pubmed: 9768360doi: 10.1016/s0960-9822(98)70443-9google scholar: lookup
  20. van den Boogaard M, Wong LY, Tessadori F, Bakker ML, Dreizehnter LK, Wakker V, Bezzina CR, 't Hoen PA, Bakkers J, Barnett P, Christoffels VM. Genetic variation in T-box binding element functionally affects SCN5A/SCN10A enhancer.. J Clin Invest 2012 Jul;122(7):2519-30.
    pmc: PMC3386824pubmed: 22706305doi: 10.1172/jci62613google scholar: lookup
  21. Fang M, Larson G, Ribeiro HS, Li N, Andersson L. Contrasting mode of evolution at a coat color locus in wild and domestic pigs.. PLoS Genet 2009 Jan;5(1):e1000341.
    pmc: PMC2613536pubmed: 19148282doi: 10.1371/journal.pgen.1000341google scholar: lookup
  22. Pruvost M, Bellone R, Benecke N, Sandoval-Castellanos E, Cieslak M, Kuznetsova T, Morales-Muñiz A, O'Connor T, Reissmann M, Hofreiter M, Ludwig A. Genotypes of predomestic horses match phenotypes painted in Paleolithic works of cave art.. Proc Natl Acad Sci U S A 2011 Nov 15;108(46):18626-30.
    pmc: PMC3219153pubmed: 22065780doi: 10.1073/pnas.1108982108google scholar: lookup
  23. Gabriel SB, Schaffner SF, Nguyen H, Moore JM, Roy J, Blumenstiel B, Higgins J, DeFelice M, Lochner A, Faggart M, Liu-Cordero SN, Rotimi C, Adeyemo A, Cooper R, Ward R, Lander ES, Daly MJ, Altshuler D. The structure of haplotype blocks in the human genome.. Science 2002 Jun 21;296(5576):2225-9.
    pubmed: 12029063doi: 10.1126/science.1069424google scholar: lookup
  24. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps.. Bioinformatics 2005 Jan 15;21(2):263-5.
    pubmed: 15297300doi: 10.1093/bioinformatics/bth457google scholar: lookup
  25. Sundström E, Imsland F, Mikko S, Wade C, Sigurdsson S, Pielberg GR, Golovko A, Curik I, Seltenhammer MH, Sölkner J, Lindblad-Toh K, Andersson L. Copy number expansion of the STX17 duplication in melanoma tissue from Grey horses.. BMC Genomics 2012 Aug 2;13:365.
    pmc: PMC3443021pubmed: 22857264doi: 10.1186/1471-2164-13-365google scholar: lookup
  26. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform.. Bioinformatics 2009 Jul 15;25(14):1754-60.
    pmc: PMC2705234pubmed: 19451168doi: 10.1093/bioinformatics/btp324google scholar: lookup
  27. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ. A framework for variation discovery and genotyping using next-generation DNA sequencing data.. Nat Genet 2011 May;43(5):491-8.
    pmc: PMC3083463pubmed: 21478889doi: 10.1038/ng.806google scholar: lookup
  28. Schubert M, Ermini L, Der Sarkissian C, Jónsson H, Ginolhac A, Schaefer R, Martin MD, Fernández R, Kircher M, McCue M, Willerslev E, Orlando L. Characterization of ancient and modern genomes by SNP detection and phylogenomic and metagenomic analysis using PALEOMIX.. Nat Protoc 2014 May;9(5):1056-82.
    pubmed: 24722405doi: 10.1038/nprot.2014.063google scholar: lookup
  29. Lindgreen S. AdapterRemoval: easy cleaning of next-generation sequencing reads.. BMC Res Notes 2012 Jul 2;5:337.
    pmc: PMC3532080pubmed: 22748135doi: 10.1186/1756-0500-5-337google scholar: lookup
  30. Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data.. Nucleic Acids Res 2010 Sep;38(16):e164.
    pmc: PMC2938201pubmed: 20601685doi: 10.1093/nar/gkq603google scholar: lookup
  31. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC. PLINK: a tool set for whole-genome association and population-based linkage analyses.. Am J Hum Genet 2007 Sep;81(3):559-75.
    pmc: PMC1950838pubmed: 17701901doi: 10.1086/519795google scholar: lookup
  32. Delaneau O, Marchini J, Zagury JF. A linear complexity phasing method for thousands of genomes.. Nat Methods 2011 Dec 4;9(2):179-81.
    pubmed: 22138821doi: 10.1038/nmeth.1785google scholar: lookup

Citations

This article has been cited 39 times.
  1. Musiał AD, Ropka-Molik K, Stefaniuk-Szmukier M, Myćka G, Bieniek A, Yasynetska N. Characteristic of Przewalski horses population from Askania-Nova reserve based on genetic markers. Mol Biol Rep 2023 Aug;50(8):7121-7126.
    doi: 10.1007/s11033-023-08581-4pubmed: 37365410google scholar: lookup
  2. Berns HM, Watkins-Chow DE, Lu S, Louphrasitthiphol P, Zhang T, Brown KM, Moura-Alves P, Goding CR, Pavan WJ. Loss of MC1R signaling implicates TBX3 in pheomelanogenesis and melanoma predisposition. bioRxiv 2023 Mar 13;.
    doi: 10.1101/2023.03.10.532018pubmed: 37090624google scholar: lookup
  3. Sun D, Qi X, Wen H, Li C, Li J, Chen J, Tao Z, Zhu M, Zhang X, Li Y. The genetic basis and potential molecular mechanism of yellow-albino northern snakehead (Channa argus). Open Biol 2023 Feb;13(2):220235.
    doi: 10.1098/rsob.220235pubmed: 36789536google scholar: lookup
  4. Roldan-Kalil J, Zueva L, Alves J, Tsytsarev V, Sanabria P, Inyushin M. Amount of Melanin Granules in Human Hair Defines the Absorption and Conversion to Heat of Light Energy in the Visible Spectrum. Photochem Photobiol 2023 Jul-Aug;99(4):1092-1096.
    doi: 10.1111/php.13744pubmed: 36403200google scholar: lookup
  5. Avila F, Hughes SS, Magdesian KG, Penedo MCT, Bellone RR. Breed Distribution and Allele Frequencies of Base Coat Color, Dilution, and White Patterning Variants across 28 Horse Breeds. Genes (Basel) 2022 Sep 13;13(9).
    doi: 10.3390/genes13091641pubmed: 36140807google scholar: lookup
  6. Andersson L, Purugganan M. Molecular genetic variation of animals and plants under domestication. Proc Natl Acad Sci U S A 2022 Jul 26;119(30):e2122150119.
    doi: 10.1073/pnas.2122150119pubmed: 35858409google scholar: lookup
  7. Enbody ED, Sin SYW, Boersma J, Edwards SV, Ketaloya S, Schwabl H, Webster MS, Karubian J. The evolutionary history and mechanistic basis of female ornamentation in a tropical songbird. Evolution 2022 Aug;76(8):1720-1736.
    doi: 10.1111/evo.14545pubmed: 35748580google scholar: lookup
  8. Brandon AA, Almeida D, Powder KE. Neural crest cells as a source of microevolutionary variation. Semin Cell Dev Biol 2023 Aug;145:42-51.
    doi: 10.1016/j.semcdb.2022.06.001pubmed: 35718684google scholar: lookup
  9. Ng CS, Lai CK, Ke HM, Lee HH, Chen CF, Tang PC, Cheng HC, Lu MJ, Li WH, Tsai IJ. Genome Assembly and Evolutionary Analysis of the Mandarin Duck Aix galericulata Reveal Strong Genome Conservation among Ducks. Genome Biol Evol 2022 May 31;14(6).
    doi: 10.1093/gbe/evac083pubmed: 35640266google scholar: lookup
  10. Esdaile E, Kallenberg A, Avila F, Bellone RR. Identification of W13 in the American Miniature Horse and Shetland Pony Populations. Genes (Basel) 2021 Dec 14;12(12).
    doi: 10.3390/genes12121985pubmed: 34946933google scholar: lookup
  11. Liu X, Zhang Y, Liu W, Li Y, Pan J, Pu Y, Han J, Orlando L, Ma Y, Jiang L. A single-nucleotide mutation within the TBX3 enhancer increased body size in Chinese horses. Curr Biol 2022 Jan 24;32(2):480-487.e6.
    doi: 10.1016/j.cub.2021.11.052pubmed: 34906355google scholar: lookup
  12. Si S, Xu X, Zhuang Y, Gao X, Zhang H, Zou Z, Luo SJ. The genetics and evolution of eye color in domestic pigeons (Columba livia). PLoS Genet 2021 Aug;17(8):e1009770.
    doi: 10.1371/journal.pgen.1009770pubmed: 34460822google scholar: lookup
  13. Silva ILS, Junqueira GSB, Oliveira CAA, Costa RB, DE Camargo GMF. Inconsistencies in horse coat color registration: A case study. J Equine Sci 2020 Oct;31(3):57-60.
    doi: 10.1294/jes.31.57pubmed: 33061785google scholar: lookup
  14. Zhao R, Yihan W, Zhao Y, Li B, Han H, Mongke T, Bao T, Wang W, Dugarjaviin M, Bai D. Hair follicle regional specificity in different parts of bay Mongolian horse by histology and transcriptional profiling. BMC Genomics 2020 Sep 22;21(1):651.
    doi: 10.1186/s12864-020-07064-1pubmed: 32962644google scholar: lookup
  15. Inaba M, Chuong CM. Avian Pigment Pattern Formation: Developmental Control of Macro- (Across the Body) and Micro- (Within a Feather) Level of Pigment Patterns. Front Cell Dev Biol 2020;8:620.
    doi: 10.3389/fcell.2020.00620pubmed: 32754601google scholar: lookup
  16. Pacheco G, van Grouw H, Shapiro MD, Gilbert MTP, Vieira FG. Darwin's Fancy Revised: An Updated Understanding of the Genomic Constitution of Pigeon Breeds. Genome Biol Evol 2020 Mar 1;12(3):136-150.
    doi: 10.1093/gbe/evaa027pubmed: 32053199google scholar: lookup
  17. Solé M, Ablondi M, Binzer-Panchal A, Velie BD, Hollfelder N, Buys N, Ducro BJ, François L, Janssens S, Schurink A, Viklund Å, Eriksson S, Isaksson A, Kultima H, Mikko S, Lindgren G. Inter- and intra-breed genome-wide copy number diversity in a large cohort of European equine breeds. BMC Genomics 2019 Oct 22;20(1):759.
    doi: 10.1186/s12864-019-6141-zpubmed: 31640551google scholar: lookup
  18. Tanaka J, Leeb T, Rushton J, Famula TR, Mack M, Jagannathan V, Flury C, Bachmann I, Eberth J, McDonnell SM, Penedo MCT, Bellone RR. Frameshift Variant in MFSD12 Explains the Mushroom Coat Color Dilution in Shetland Ponies. Genes (Basel) 2019 Oct 19;10(10).
    doi: 10.3390/genes10100826pubmed: 31635058google scholar: lookup
  19. 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
  20. Inaba M, Jiang TX, Liang YC, Tsai S, Lai YC, Widelitz RB, Chuong CM. Instructive role of melanocytes during pigment pattern formation of the avian skin. Proc Natl Acad Sci U S A 2019 Apr 2;116(14):6884-6890.
    doi: 10.1073/pnas.1816107116pubmed: 30886106google scholar: lookup
  21. Gurgul A, Jasielczuk I, Semik-Gurgul E, Pawlina-Tyszko K, Stefaniuk-Szmukier M, Szmatoła T, Polak G, Tomczyk-Wrona I, Bugno-Poniewierska M. A genome-wide scan for diversifying selection signatures in selected horse breeds. PLoS One 2019;14(1):e0210751.
    doi: 10.1371/journal.pone.0210751pubmed: 30699152google scholar: lookup
  22. Qiu W, Chuong CM, Lei M. Regulation of melanocyte stem cells in the pigmentation of skin and its appendages: Biological patterning and therapeutic potentials. Exp Dermatol 2019 Apr;28(4):395-405.
    doi: 10.1111/exd.13856pubmed: 30537004google scholar: lookup
  23. Naval-Sanchez M, Nguyen Q, McWilliam S, Porto-Neto LR, Tellam R, Vuocolo T, Reverter A, Perez-Enciso M, Brauning R, Clarke S, McCulloch A, Zamani W, Naderi S, Rezaei HR, Pompanon F, Taberlet P, Worley KC, Gibbs RA, Muzny DM, Jhangiani SN, Cockett N, Daetwyler H, Kijas J. Sheep genome functional annotation reveals proximal regulatory elements contributed to the evolution of modern breeds. Nat Commun 2018 Feb 28;9(1):859.
    doi: 10.1038/s41467-017-02809-1pubmed: 29491421google scholar: lookup
  24. Wang Q, Pi J, Pan A, Shen J, Qu L. A novel sex-linked mutant affecting tail formation in Hongshan chicken. Sci Rep 2017 Aug 30;7(1):10079.
    doi: 10.1038/s41598-017-10943-5pubmed: 28855651google scholar: lookup
  25. Ma Q, Liu X, Pan J, Ma L, Ma Y, He X, Zhao Q, Pu Y, Li Y, Jiang L. Genome-wide detection of copy number variation in Chinese indigenous sheep using an ovine high-density 600 K SNP array. Sci Rep 2017 Apr 19;7(1):912.
    doi: 10.1038/s41598-017-00847-9pubmed: 28424525google scholar: lookup
  26. Librado P, Fages A, Gaunitz C, Leonardi M, Wagner S, Khan N, Hanghøj K, Alquraishi SA, Alfarhan AH, Al-Rasheid KA, Der Sarkissian C, Schubert M, Orlando L. The Evolutionary Origin and Genetic Makeup of Domestic Horses. Genetics 2016 Oct;204(2):423-434.
    doi: 10.1534/genetics.116.194860pubmed: 27729493google scholar: lookup
  27. Chen Y, Pan L, Su Z, Wang J, Li H, Ma X, Liu Y, Lu F, Qu J, Hou L. The transcription factor TBX2 regulates melanogenesis in melanocytes by repressing Oca2. Mol Cell Biochem 2016 Apr;415(1-2):103-9.
    doi: 10.1007/s11010-016-2680-7pubmed: 26971330google scholar: lookup
  28. McGowan KA, Barsh GS. Evolution: How the zebrafish got its stripes. Elife 2016 Feb 15;5.
    doi: 10.7554/eLife.14239pubmed: 26880558google scholar: lookup
  29. An T, Dugarjaviin M. Differential Expression and Analysis of TBX3 Gene in Skin Tissues of Dun Mongolian Horses with and Without Bider Markings. Animals (Basel) 2026 Jan 18;16(2).
    doi: 10.3390/ani16020297pubmed: 41594486google scholar: lookup
  30. Sharma M, Singh A, Kumar V, Olla N, Arora R, Sharma R, Mohan NH, Ahlawat S. Advances in Equine Genomics: Decoding the Genetic Architecture of Morphology, Performance, Behavior, and Adaptation. Mol Biotechnol 2025 Dec 19;.
    doi: 10.1007/s12033-025-01544-zpubmed: 41417456google scholar: lookup
  31. 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
  32. Wang G, Zhang X, Zhao X, Ren X, Chen A, Dai W, Zhang L, Lu Y, Jiang Z, Wang H, Liu Y, Zhao X, Wen J, Cheng X, Zhang Y, Ning Z, Ban L, Qu L. Genomic evidence for hybridization and introgression between blue peafowl and endangered green peafowl and molecular foundation of leucistic plumage of blue peafowl. Gigascience 2025 Jan 6;14.
    doi: 10.1093/gigascience/giae124pubmed: 39965774google scholar: lookup
  33. An T, Dugarjaviin M, Han H. Expression and Analysis of TBX3 Gene in the Skin from Three Locations on Dun Mongolian Bider Horse. Genes (Basel) 2024 Dec 11;15(12).
    doi: 10.3390/genes15121589pubmed: 39766856google scholar: lookup
  34. Parsad R, Bagiyal M, Ahlawat S, Arora R, Gera R, Chhabra P, Sharma U. Unraveling the genetic and physiological potential of donkeys: insights from genomics, proteomics, and metabolomics approaches. Mamm Genome 2025 Mar;36(1):10-24.
    doi: 10.1007/s00335-024-10083-ypubmed: 39510983google scholar: lookup
  35. Herbert AL, Allard CAH, McCoy MJ, Wucherpfennig JI, Krueger SP, Chen HI, Gourlay AN, Jackson KD, Abbo LA, Bennett SH, Sears JD, Rhyne AL, Bellono NW, Kingsley DM. Ancient developmental genes underlie evolutionary novelties in walking fish. Curr Biol 2024 Oct 7;34(19):4339-4348.e6.
    doi: 10.1016/j.cub.2024.08.042pubmed: 39332403google scholar: lookup
  36. Sigurðardóttir H, Ablondi M, Kristjansson T, Lindgren G, Eriksson S. Genetic diversity and signatures of selection in Icelandic horses and Exmoor ponies. BMC Genomics 2024 Aug 8;25(1):772.
    doi: 10.1186/s12864-024-10682-8pubmed: 39118059google scholar: lookup
  37. Liu X, Peng Y, Zhang X, Wang X, Chen W, Kou X, Liang H, Ren W, Khan MZ, Wang C. Coloration in Equine: Overview of Candidate Genes Associated with Coat Color Phenotypes. Animals (Basel) 2024 Jun 17;14(12).
    doi: 10.3390/ani14121802pubmed: 38929421google scholar: lookup
  38. Herbert AL, Allard CA, McCoy MJ, Wucherpfennig JI, Krueger SP, Chen HI, Gourlay AN, Jackson KD, Abbo LA, Bennett SH, Sears JD, Rhyne AL, Bellono NW, Kingsley DM. The genetic basis of novel trait gain in walking fish. bioRxiv 2023 Oct 14;.
    doi: 10.1101/2023.10.14.562356pubmed: 37873105google scholar: lookup
  39. Caro T, Mallarino R. Coloration in Mammals. Trends Ecol Evol 2020 Apr;35(4):357-366.
    doi: 10.1016/j.tree.2019.12.008pubmed: 31980234google scholar: lookup
Subscribe to our newsletter
Join 100,113 horse owners like you who receive our email updates on horse health and nutrition.