Abstract
Colombian Paso horses have been classified into four categories based on gait performance: Colombian Paso Fino, Colombian Trocha, Colombian Trocha and Gallop, and Colombian Trot and Gallop. Selective breeding has led to the emergence of the Colombian Paso Fino as a distinct population. We describe the split of the Colombian Paso Horse breed into two genetic and phenotypic differentiated groups using 220,000 pedigree records, 132,637 microsatellites genotypes, 198 mtDNA d-loop haplotypes, and several conformation measurements from 178 horses. The first category, the Colombian Paso Fino subgroup was recognized as a new breed by the Colombian breeders and government since 2017 and the second category consists of the other three subgroups of Colombian Paso horses that perform different gaits and have different conformation traits. The breed splitting has been carried out through increased genetic differentiation between these two populations, mainly by intensive artificial selection on gaits and some anatomical conformation traits related to performance and is revealed by analysis of 30 years of traced genetic data, 60 years of pedigree records, and phenotypic differences. In addition, our phylogenetic reconstruction showed that the Colombian Paso horses have shared an evolutionary history that led to a complex breed origin. Some haplotypes represent an old Iberian haplogroup, even older than the domestication of horses. Finally, this study shows support for the designation of a distinct breed based on the use of genetic information as scientific support to breeding associations and governments for decision making about breeding management, genetic conservation, and genetic improvement.
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Data availability
We have deposited the primary data underlying these analyses as follows: (1) Conformation data is available from the figshare database (accession number 10.6084/m9.figshare.7040066). (2) Mitochondrial d-loop DNA sequences: Genbank accessions MH318582-MH318607. (3) STR and pedigree data not publically available.
References
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 MCT, Verini-Supplizi A, Houshmand M, Woodward SR, Semino O, Silvestrelli M, Giulotto E, Pereira L, Bandelt H-J, Torroni A (2012) Mitochondrial genomes from modern horses reveal the major haplogroups that underwent domestication. Proc Natl Acad Sci USA 109:2449–2454. https://doi.org/10.1073/pnas.1111637109
Andersson LS, Larhammar M, Memic F, Wootz H, Schwochow D, Rubin C-J, 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 (2012) Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice. Nature 488:642–646. https://doi.org/10.1038/nature11399
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Bowling AT, Clark RS (2009) Blood group and protein polymorphism gene frequencies for seven breeds of horses in the United States. Anim Blood Groups Biochem Genet 16:93–108. https://doi.org/10.1111/j.1365-2052.1985.tb01458.x
Clayton HM, Bradbury JW (1995) Temporal characteristics of the fox trot, a symmetrical equine gait. Appl Anim Behav Sci 42:153–159. https://doi.org/10.1016/0168-1591(94)00539-Q
Cortés O, Dunner S, Gama LT, Martínez AM, Delgado JV, Ginja C, Jiménez LM, Jordana J, Luis C, Oom MM, Sponenberg DP, Zaragoza P, Vega-Pla JL (2017) The legacy of Columbus in American horse populations assessed by microsatellite markers. J Anim Breed Genet 134:340–350. https://doi.org/10.1111/jbg.12255
Cothran EG, Canelon JL, Luis C, Conant E, Juras R (2011) Genetic analysis of the Venezuelan Criollo horse. funpecrp.com.br Genet. Mol Res Genet Mol Res 10:2394–2403. https://doi.org/10.4238/2011.October.7.1
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
Excoffier L, Lischer H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, New York
FAO (1999) The global strategy for the management of farm animal genetic resources: executive brief. Food and Agriculture Organization of the United Nations, Rome, p 43
Fedequinas (2006) El caballo colombiano. Cinco siglos de historia, 1era edn. Imprelibros S.A, Bogotá
Fox J, Weisberg S, Adler D, Bates D, Baud-Bovy G, Ellison S, Firth D, Friendly M, Gorjanc G, Graves S, Heiberger R, Laboissiere R, Monette G, Murdoch D, Nilsson H, Ogle D, Ripley B, Venables W, Zeileis A (2014) Companion to applied regression. R package version 2.0–20. Available at: http://CRAN.R-project.org/package=car
Friendly M (2007) HE plots for multivariate linear models. J Comput Graph Stat 16:421–444
Friendly M, Fox J (2013) Visualizing generalized canonical discriminant and canonical correlation analysis. R package version 0.6–5. http://CRAN.R-project.org/package=candisc
Gastwirth JL, Gel YR, Hui WLW, Lyubchich V, Miao W, Noguchi K (2013) An R package for biostatistics, public policy, and law. R package version 2.4.1. Available at: http://CRAN.Rproject.org/package=lawstat
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. https://doi.org/10.1080/10635150390235520
Guisande C, Vaamonde A, Barreiro A (2014) RWizard software. v 1.0. Available: http://www.ipez.es/RWizard
Hendricks BL (2007) International encyclopedia of horse breeds. University of Oklahoma Press, Oklahoma
Hinkle DE, Wiersma W, Jurs SG (2003) Applied statistics for the behavioral sciences, vol 663, 5th edn. Houghton Mifflin
Hothorn T, Bretz F, Westfall P, Heiberger R, Schuetzenmeister A (2014) Simultaneous inference in general parametric models. R package version 1.3–3. Available at: http://CRAN.Rproject.org/package=multcomp
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254. https://doi.org/10.1093/molbev/msj030
Ishida N, Hasegawa T, Takeda K, Sakagami M, Onishi A, Inumaru S, Komatsu M, Mukoyama H (1994) Polymorphic sequence in the D-loop region of equine mitochondrial DNA. Anim Genet 25:215–221
Jäderkvist K, Andersson LS, Johansson AM, Árnason T, Mikko S, Eriksson S, Andersson L, Lindgren G (2014) The DMRT3 ‘Gait keeper’ mutation affects performance of Nordic and Standardbred trotters. J Anim Sci 92:4279–4286. https://doi.org/10.2527/jas2014-7803
Jansen T, Forster P, Levine MA, Oelke H, Hurles M, Renfrew C, Weber J, Olek K (2002) Mitochondrial DNA and the origins of the domestic horse. Proc Natl Acad Sci USA 99:10905–10910. https://doi.org/10.1073/pnas.152330099
Jimenez LM, Mendez S, Dunner S, Cañón J, Cortés O (2012) Colombian Creole horse breeds: same origin but different diversity. Genet Mol Biol 35:790–796. https://doi.org/10.1590/S1415-47572012005000064
Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071. https://doi.org/10.1093/bioinformatics/btr521
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94
Kristjansson T, Bjornsdottir S, Sigurdsson A, Andersson LS, Lindgren G, Helyar SJ, Klonowski AM, Arnason T (2014) The effect of the “Gait keeper” mutation in the DMRT3 gene on gaiting ability in Icelandic horses. J Anim Breed Genet 131:415–425. https://doi.org/10.1111/jbg.12112
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 (2016) The evolutionary origin and genetic makeup of domestic horses. Genetics 204:423–434. https://doi.org/10.1534/genetics.116.194860
Lira J, Linderholm A, Olaria C, Brandström Durling M, Gilbert MTP, Ellegren H, Willerslev E, Lidén K, Arsuaga JL, Götherström A (2010) Ancient DNA reveals traces of Iberian Neolithic and Bronze Age lineages in modern Iberian horses. Mol Ecol 19:64–78. https://doi.org/10.1111/j.1365-294X.2009.04430.x
Lopes MS, Mendonça D, Cymbron T, Valera M, da Costa-Ferreira J, Machado ADC (2005) The Lusitano horse maternal lineage based on mitochondrial D-loop sequence variation. Anim Genet 36:196–202. https://doi.org/10.1111/j.1365-2052.2005.01279.x
Luis C, Bastos-Silveira C, Cothran EG, Oom MDMDM, Luís C (2006) Iberian origins of new world horse breeds. J Hered 97:107–113. https://doi.org/10.1093/jhered/esj020
Maccluer JW, Boyce AJ, Dyke B, Weitkamp LR, Pfenning DW, Parsons CJ (1983) Inbreeding and pedigree structure in standardbred horses. J Hered 74:394–399. https://doi.org/10.1093/oxfordjournals.jhered.a109824
Mirol PM, Peral García P, Vega-Pla JL, Dulout FN (2002) Phylogenetic relationships of Argentinean Creole horses and other South American and Spanish breeds inferred from mitochondrial DNA sequences. Anim Genet 33:356–363
Nicodemus MC, Clayton HM (2003) Temporal variables of four-beat, stepping gaits of gaited horses. Appl Anim Behav Sci 80:133–142. https://doi.org/10.1016/S0168-1591(02)00219-8
Novoa-Bravo M, Jäderkvist K, Rhodin M, Strand E, García LF, Lindgren G (2018) Selection on the Colombian paso horse’s gaits has produced kinematic differences partly explained by the DMRT3 gene. PLoS ONE 13:e0202584
Patterson L, Staiger EA, Brooks SA (2015) DMRT3 is associated with gait type in Mangalarga Marchador horses, but does not control gait ability. Anim Genet 46:213–215. https://doi.org/10.1111/age.12273
Petersen JL, Mickelson JR, Rendahl AK, Valberg SJ, Andersson LS, Axelsson J, Bailey E, Bannasch D, Binns MM, Borges AS, Brama P, da Câmara Machado A, Capomaccio S, Cappelli K, Cothran EG, Distl O, Fox-Clipsham L, Graves KT, Guérin G, Haase B, Hasegawa T, Hemmann K, Hill EW, Leeb T, Lindgren G, Lohi H, Lopes MS, McGivney BA, Mikko S, Orr N, Penedo MCT, Piercy RJ, Raekallio M, Rieder S, Røed KH, Swinburne J, Tozaki T, Vaudin M, Wade CM, McCue ME (2013) Genome-wide analysis reveals selection for important traits in domestic horse breeds. PLoS Genet 9:e1003211. https://doi.org/10.1371/journal.pgen.1003211
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Promerová M, Andersson LS, Juras R, Penedo MCT, Reissmann M, Tozaki T, Bellone R, Dunner S, Hořín P, Imsland F, Imsland P, Mikko S, Modrý D, Roed KH, Schwochow D, Vega-Pla JL, Mehrabani-Yeganeh H, Yousefi-Mashouf N, Cothran GE, Lindgren G, Andersson L (2014) Worldwide frequency distribution of the “Gait keeper” mutation in the DMRT3 gene. Anim Genet 45:274–282. https://doi.org/10.1111/age.12120
R Core team, 2016, 2016. R: A language and environment for statistical computing. R Found. Stat. Comput. Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org. https://doi.org/citeulike-article-id:2400517
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Ripley B, Venables B, Bates D, Hornik K, Ripley M (2014) Support functions and datasets for venables and ripley’s MASS. R package version 7.3–33. Available at: http://CRAN.R-project.org/package=MASS
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
van de Goor LHP, Panneman H, van Haeringen WA (2010) A proposal for standardization in forensic equine DNA typing: allele nomenclature for 17 equine-specific STR loci. Anim Genet 41:122–127. https://doi.org/10.1111/j.1365-2052.2009.01975.x
Venables W, Ripley B (2002) Modern applied statistics with S, 4th edn. Springer, Berlin
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution (NY). 38:1358–1370
Xu X, Arnason U (1994) The complete mitochondrial DNA sequence of the horse, Equus caballus: extensive heteroplasmy of the control region. Gene 148:357–362
Acknowledgements
We thank the Federación Nacional de Asociaciones Equinas—Fedequinas for providing the pedigree, conformation, hair samples and microsatellite data, and their support during the last years, especially to Beatriz Salgado, Eliana Serrano, Yovanny Avendaño, Enrique Neira, Fabio Jaramillo, Héctor Vergara, Eliseo Cárdenas, Mónica Jimenez and all the members of the Board of Directors who supported this project. In addition, we thank Felipe Jaramillo for obtaining conformation measurements by Fedequinas. Finally, we acknowledge Dr. Gabriella Lindgren, Dr. Cristina Luis, and Dr. Jaime Lira, Mr. Héctor Barriga, and anonymous reviewers for their valuable comments.
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This research was supported by Colfuturo-Colciencias, National PhD program (Grant 6172).
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MN-B, LFG, and EB designed research; MN-B performed research; MN-B and EB contributed with reagents or analytical tools. MN-B analyzed data. MN-B wrote the paper. LFG and EB reviewed the paper.
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Novoa-Bravo, M., Bernal-Pinilla, E. & García, L.F. Microevolution operating in domestic animals: evidence from the Colombian Paso horses. Mamm Biol 101, 181–192 (2021). https://doi.org/10.1007/s42991-021-00103-8
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DOI: https://doi.org/10.1007/s42991-021-00103-8