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Animals : an open access journal from MDPI2021; 11(2); 393; doi: 10.3390/ani11020393

Impaired Reproductive Function in Equines: From Genetics to Genomics.

Abstract: Fertility is one of the key factors in the economic and productive success of the equine industry. Despite this, studies on the genetic causes affecting reproductive performance are scarce, especially in mares, where the genetic architecture of the reproductive traits is extremely complex. Today, with the increasing availability of new genomic methodologies for this species, we are presented with an interesting opportunity to understand the genetic basis of equine reproductive disorders. These include, among others, novel techniques for detecting chromosomal abnormalities, whose association with infertility in horses was established over 50 years ago; new sequencing technologies permitting an accurate detection of point mutations influencing fertility, as well as the study of inbreeding and molecular homozygosity, which has been widely suggested as one of the main causes of low reproductive performance in horses. Finally, over the last few years, reproductive performance has also been associated with copy number variants and candidate genes detected by genome-wide association studies on fertility traits. However, such studies are still scarce, probably because they depend on the existence of large and accurate phenotypic datasets of reproductive and/or fertility traits, which are still difficult to obtain in equines.
Publication Date: 2021-02-03 PubMed ID: 33546520PubMed Central: PMC7913728DOI: 10.3390/ani11020393Google Scholar: Lookup
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Summary

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This research article investigates the role of genetic factors in the reproductive performance of horses. With the enhanced genomic methodologies available today, the article emphasizes the potential to further understand the genetic basis of equine reproductive disorders including chromosomal abnormalities, point mutations, the impact of inbreeding and the role of copy number variants.

Understanding Equine Reproductive Disorders

  • The researchers in this paper explore how genomic methodologies can be used to understand the genetic underpinnings of reproductive function in horses.
  • Despite the economic and productive importance of horse fertility, the genetic dynamics that affect equine reproductive performance are poorly understood – an issue that is particularly acute in mares, where the genetic architecture of reproductive traits is incredibly complex.
  • The research calls attention to several reproductive disorders in horses that can be investigated using genomic methodologies, including chromosomal abnormalities, the presence of point mutations, and patterns of inbreeding and molecular homozygosity.

Genomic Methodologies at the Forefront

  • The article discusses an interesting opportunity presented by the increased availability of new genomic methodologies for horses.
  • These novel techniques allow for the detection of chromosomal abnormalities, which have been linked to infertility in horses for over 50 years.
  • Moreover, new sequencing technologies also allow for precise detection of point mutations that affect fertility.

Evidence of Genetic Influence on Horse Fertility

  • The review also mentions the study of inbreeding and molecular homozygosity, which has been suggested as one of the main causes of low reproductive performance in horses.
  • The researchers also noted that reproductive performance has been linked with variabilities in gene copy numbers. These variabilities, known as copy number variants, and candidate genes have been discovered by genome-wide association studies focusing on fertility traits.
  • However, these types of studies are still few and far between, in large part because they rely on the availability of large, accurate datasets of reproductive and fertility traits, which are difficult to collect in the case of horses.

Cite This Article

APA
Laseca N, Anaya G, Peña Z, Pirosanto Y, Molina A, Demyda Peyrás S. (2021). Impaired Reproductive Function in Equines: From Genetics to Genomics. Animals (Basel), 11(2), 393. https://doi.org/10.3390/ani11020393

Publication

ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 11
Issue: 2
PII: 393

Researcher Affiliations

Laseca, Nora
  • Departamento de genética, Universidad de Córdoba, Campus de Rabanales Ctra, Madrid-Cádiz, km 396, 14071 Córdoba, Spain.
Anaya, Gabriel
  • Departamento de genética, Universidad de Córdoba, Campus de Rabanales Ctra, Madrid-Cádiz, km 396, 14071 Córdoba, Spain.
Peña, Zahira
  • Departamento de genética, Universidad de Córdoba, Campus de Rabanales Ctra, Madrid-Cádiz, km 396, 14071 Córdoba, Spain.
Pirosanto, Yamila
  • Departamento de Producción Animal, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, La Plata 1900, Argentina.
  • Consejo Superior de Investigaciones Científicas y Tecnológicas (CONICET), CCT-La Plata, La Plata 1900, Argentina.
Molina, Antonio
  • Departamento de genética, Universidad de Córdoba, Campus de Rabanales Ctra, Madrid-Cádiz, km 396, 14071 Córdoba, Spain.
Demyda Peyrás, Sebastián
  • Departamento de Producción Animal, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, La Plata 1900, Argentina.
  • Consejo Superior de Investigaciones Científicas y Tecnológicas (CONICET), CCT-La Plata, La Plata 1900, Argentina.

Grant Funding

  • PICT2016-0359 / Agencia Nacional de Promociu00f3n Cientu00edfica y Tecnolu00f3gica
  • PICT2018-0227 / Agencia Nacional de Promociu00f3n Cientu00edfica y Tecnolu00f3gica
  • AGL-2017-84217-P / Ministerio de Economu00eda, Industria y Competitividad, Gobierno de Espau00f1a
  • PRE 2018-083492 / Ministerio de Economu00eda, Industria y Competitividad, Gobierno de Espau00f1a

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 96 references
  1. Mahon GAT, Cunningham EP. Inbreeding and the inheritance of fertility in the thoroughbred mare.. Livest. Prod. Sci. 1982;9:743–754.
  2. Valera M, Blesa F, Dos Santos R, Molina A. Genetic study of gestation length in Andalusian and Arabian mares.. Anim Reprod Sci 2006 Sep;95(1-2):75-96.
  3. Kuhl J, Stock KF, Wulf M, Aurich C. Maternal Lineage of Warmblood Mares Contributes to Variation of Gestation Length and Bias of Foal Sex Ratio.. PLoS One 2015;10(10):e0139358.
  4. Rodrigues JA, Gonçalves AR, Antunes L, Bettencourt EV, Gama LT. Genetic and Environmental Factors Influencing Gestation Length in Lusitano Horses.. J Equine Vet Sci 2020 Jan;84:102850.
    doi: 10.1016/j.jevs.2019.102850pubmed: 31864463google scholar: lookup
  5. Gómez MD, Sánchez MJ, Bartolomé E, Cervantes I, Poyato-Bonilla J, Demyda-Peyrás S, Valera M. Phenotypic and genetic analysis of reproductive traits in horse populations with different breeding purposes.. Animal 2020 Jul;14(7):1351-1361.
    doi: 10.1017/S1751731120000087pubmed: 32026801google scholar: lookup
  6. Gottschalk M, Sieme H, Martinsson G, Distl O. Analysis of breed effects on semen traits in light horse, warmblood, and draught horse breeds.. Theriogenology 2016 May;85(8):1375-81.
  7. Gottschalk M, Sieme H, Martinsson G, Distl O. Heritability of semen traits in German Warmblood stallions.. Anim Reprod Sci 2016 Jul;170:10-4.
  8. Greiser T, Sieme H, Martinsson G, Distl O. Genetic parameters and estimated breeding values for traits of raw and frozen-thawed semen in German Warmblood stallions.. Anim Reprod Sci 2019 Nov;210:106194.
  9. Pirosanto Y, Valera M, Molina A, Dorado J, Demyda-Peyrás S. Sperm quality of Pure Spanish stallions is affected by inbreeding coefficient and age.. Reprod. Fertil. Dev. 2020;32:137-137.
    doi: 10.1071/RDv32n2Ab23google scholar: lookup
  10. Dini P, Bartels T, Revah I, Claes AN, Stout TAE, Daels P. A retrospective study on semen quality parameters from four different Dutch horse breeds with different levels of inbreeding.. Theriogenology 2020 Nov;157:18-23.
  11. Freeman JL, Perry GH, Feuk L, Redon R, McCarroll SA, Altshuler DM, Aburatani H, Jones KW, Tyler-Smith C, Hurles ME, Carter NP, Scherer SW, Lee C. Copy number variation: new insights in genome diversity.. Genome Res 2006 Aug;16(8):949-61.
    doi: 10.1101/gr.3677206pubmed: 16809666google scholar: lookup
  12. McQuillan R, Leutenegger AL, Abdel-Rahman R, Franklin CS, Pericic M, Barac-Lauc L, Smolej-Narancic N, Janicijevic B, Polasek O, Tenesa A, Macleod AK, Farrington SM, Rudan P, Hayward C, Vitart V, Rudan I, Wild SH, Dunlop MG, Wright AF, Campbell H, Wilson JF. Runs of homozygosity in European populations.. Am J Hum Genet 2008 Sep;83(3):359-72.
    doi: 10.1016/j.ajhg.2008.08.007pmc: PMC2556426pubmed: 18760389google scholar: lookup
  13. Visscher PM, Brown MA, McCarthy MI, Yang J. Five years of GWAS discovery.. Am J Hum Genet 2012 Jan 13;90(1):7-24.
    doi: 10.1016/j.ajhg.2011.11.029pmc: PMC3257326pubmed: 22243964google scholar: lookup
  14. 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.12857pmc: PMC6825885pubmed: 31568563google scholar: lookup
  15. Pailhoux E, Cribiu EP, Parma P, Cotinot C. Molecular analysis of an XY mare with gonadal dysgenesis.. Hereditas 1995;122(2):109-12.
  16. Kent J, Wheatley SC, Andrews JE, Sinclair AH, Koopman P. A male-specific role for SOX9 in vertebrate sex determination.. Development 1996 Sep;122(9):2813-22.
    pubmed: 8787755doi: 10.1242/dev.122.9.2813google scholar: lookup
  17. Raudsepp T, Durkin K, Lear TL, Das PJ, Avila F, Kachroo P, Chowdhary BP. Molecular heterogeneity of XY sex reversal in horses.. Anim Genet 2010 Dec;41 Suppl 2:41-52.
  18. Villagómez DA, Lear TL, Chenier T, Lee S, McGee RB, Cahill J, Foster RA, Reyes E, St John E, King WA. Equine disorders of sexual development in 17 mares including XX, SRY-negative, XY, SRY-negative and XY, SRY-positive genotypes.. Sex Dev 2011;5(1):16-25.
    doi: 10.1159/000322811pubmed: 21196712google scholar: lookup
  19. Anaya G, Moreno-Millán M, Bugno-Poniewierska M, Pawlina K, Membrillo A, Molina A, Demyda-Peyrás S. Sex reversal syndrome in the horse: four new cases of feminization in individuals carrying a 64,XY SRY negative chromosomal complement.. Anim Reprod Sci 2014 Dec 10;151(1-2):22-7.
  20. Ghosh S, Qu Z, Das PJ, Fang E, Juras R, Cothran EG, McDonell S, Kenney DG, Lear TL, Adelson DL, Chowdhary BP, Raudsepp T. Copy number variation in the horse genome.. PLoS Genet 2014 Oct;10(10):e1004712.
  21. Villagomez DAF, Welsford EG, King WA, Revay T. Androgen Receptor Gene Variants in New Cases of Equine Androgen Insensitivity Syndrome.. Genes (Basel) 2020 Jan 10;11(1).
    doi: 10.3390/genes11010078pmc: PMC7017088pubmed: 31936796google scholar: lookup
  22. Revay T, Quach AT, Maignel L, Sullivan B, King WA. Copy number variations in high and low fertility breeding boars.. BMC Genomics 2015 Apr 10;16(1):280.
    doi: 10.1186/s12864-015-1473-9pmc: PMC4404230pubmed: 25888238google scholar: lookup
  23. Ghosh S, Carden CF, Juras R, Mendoza MN, Jevit MJ, Castaneda C, Phelps O, Dube J, Kelley DE, Varner DD, Love CC, Raudsepp T. Two Novel Cases of Autosomal Translocations in the Horse: Warmblood Family Segregating t(4;30) and a Cloned Arabian with a de novo t(12;25).. Cytogenet Genome Res 2020;160(11-12):688-697.
    doi: 10.1159/000512206pubmed: 33326979google scholar: lookup
  24. Révay T, Villagómez DA, Brewer D, Chenier T, King WA. GTG mutation in the start codon of the androgen receptor gene in a family of horses with 64,XY disorder of sex development.. Sex Dev 2012;6(1-3):108-16.
    doi: 10.1159/000334049pubmed: 22095250google scholar: lookup
  25. Bolzon C, Joonè CJ, Schulman ML, Harper CK, Villagómez DA, King WA, Révay T. Missense Mutation in the Ligand-Binding Domain of the Horse Androgen Receptor Gene in a Thoroughbred Family with Inherited 64,XY (SRY+) Disorder of Sex Development.. Sex Dev 2016;10(1):37-44.
    doi: 10.1159/000444991pubmed: 27073903google scholar: lookup
  26. Rižner TL, Penning TM. Role of aldo-keto reductase family 1 (AKR1) enzymes in human steroid metabolism.. Steroids 2014 Jan;79:49-63.
  27. Lear TL, Lundquist J, Zent WW, Fishback WD Jr, Clark A. Three autosomal chromosome translocations associated with repeated early embryonic loss (REEL) in the domestic horse (Equus caballus).. Cytogenet Genome Res 2008;120(1-2):117-22.
    doi: 10.1159/000118749pubmed: 18467834google scholar: lookup
  28. Lear TL, Raudsepp T, Lundquist JM, Brown SE. Repeated Early Embryonic Loss in a Thoroughbred Mare with a Chromosomal Translocation 64,XX,t(2;13). J. Equine Vet. Sci. 2014;34:805–809.
  29. Lear TL, Layton G. Use of zoo-FISH to characterise a reciprocal translocation in a thoroughbred mare: t(1;1 6)(q16;q21.3).. Equine Vet J 2002 Mar;34(2):207-9.
    doi: 10.2746/042516402776767295pubmed: 11902765google scholar: lookup
  30. Alkan C, Coe BP, Eichler EE. Genome structural variation discovery and genotyping.. Nat Rev Genet 2011 May;12(5):363-76.
    doi: 10.1038/nrg2958pmc: PMC4108431pubmed: 21358748google scholar: lookup
  31. Bugno M, Słota E, Kościelny M. Karyotype evaluation among young horse populations in Poland.. Schweiz Arch Tierheilkd 2007 May;149(5):227-32.
    doi: 10.1024/0036-7281.149.5.227pubmed: 17557614google scholar: lookup
  32. Chandley AC, Fletcher J, Rossdale PD, Peace CK, Ricketts SW, McEnery RJ, Thorne JP, Short RV, Allen WR. Chromosome abnormalities as a cause of infertility in mares.. J Reprod Fertil Suppl 1975 Oct;(23):377-83.
    pubmed: 1060811
  33. Hughes JP, Trommershausen-Smith A. Infertility in the horse associated with chromosomal abnormalities.. Aust Vet J 1977 Jun;53(6):253-7.
  34. Power M.M. Domestic Animal Cytogenetics. Volume 34. Academic Press, Inc.; San Diego, CA, USA: 1990. Chromosomes of the horse; pp. 131–167.
  35. Gamo S, Tozaki T, Kakoi H, Hirota KI, Nakamura K, Nishii N, Alumunia J, Takasu M. X monosomy in the endangered Kiso horse breed detected by a parentage test using sex chromosome linked genes and microsatellites.. J Vet Med Sci 2019 Jan 8;81(1):91-94.
    doi: 10.1292/jvms.18-0253pmc: PMC6361659pubmed: 30473577google scholar: lookup
  36. Kjöllerström HJ, Collares-Pereira MJ, Oom MM. First evidence of sex chromosome mosaicism in the endangered Sorraia Horse breed.. Livest. Sci. 2011;136:273–276.
  37. Lear TL, McGee RB. Disorders of sexual development in the domestic horse, Equus caballus.. Sex Dev 2012;6(1-3):61-71.
    doi: 10.1159/000334048pubmed: 22095202google scholar: lookup
  38. Bannasch D, Rinaldo C, Millon L, Latson K, Spangler T, Hubberty S, Galuppo L, Lowenstine L. SRY negative 64,XX intersex phenotype in an American saddlebred horse.. Vet J 2007 Mar;173(2):437-9.
    doi: 10.1016/j.tvjl.2005.11.008pubmed: 16386440google scholar: lookup
  39. Demyda-Peyrás S, Membrillo A, Bugno-Poniewierska M, Pawlina K, Anaya G, Moreno-Millán M. The use of molecular and cytogenetic methods as a valuable tool in the detection of chromosomal abnormalities in horses: a case of sex chromosome chimerism in a Spanish purebred colt.. Cytogenet Genome Res 2013;141(4):277-83.
    doi: 10.1159/000351225pubmed: 23735586google scholar: lookup
  40. Dunn HO, Smiley D, Duncan JR, McEntee K. Two equine true hermaphrodites with 64,XX/64,XY and 63,XO/64,XY chimerism.. Cornell Vet 1981 Apr;71(2):123-35.
    pubmed: 7194168
  41. Bugno M, Zabek T, Golonka P, Pieńkowska-Schelling A, Schelling C, Słota E. A case of an intersex horse with 63,X/64,XX/65,XX,del(Y)(q?) karyotype.. Cytogenet Genome Res 2008;120(1-2):123-6.
    doi: 10.1159/000118750pubmed: 18467835google scholar: lookup
  42. Lear TL, Bailey E. Equine clinical cytogenetics: the past and future.. Cytogenet Genome Res 2008;120(1-2):42-9.
    doi: 10.1159/000118739pubmed: 18467824google scholar: lookup
  43. Anaya G, Molina A, Valera M, Moreno-Millán M, Azor P, Peral-García P, Demyda-Peyrás S. Sex chromosomal abnormalities associated with equine infertility: validation of a simple molecular screening tool in the Purebred Spanish Horse.. Anim Genet 2017 Aug;48(4):412-419.
    doi: 10.1111/age.12543pubmed: 28224649google scholar: lookup
  44. Szczerbal I, Nowacka-Woszuk J, Kopp-Kuhlman C, Mackowski M, Switonski M. Application of droplet digital PCR in diagnosing of X monosomy in mares.. Equine Vet J 2020 Jul;52(4):627-631.
    doi: 10.1111/evj.13214pubmed: 31793061google scholar: lookup
  45. Pirosanto Y, Laseca N, Valera M, Molina A, Bugno Poniewierska M, Ross P, Azor P, Demyda Peyrás S. Screening and detection of chromosomal copy number alterations (CNA) in the domestic horse by SNP-array genotyping data.. Anim. Genet. 2021 acepted in press.
  46. 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
  47. Carrell DT, Aston KI. The search for SNPs, CNVs, and epigenetic variants associated with the complex disease of male infertility.. Syst Biol Reprod Med 2011 Feb;57(1-2):17-26.
    doi: 10.3109/19396368.2010.521615pubmed: 21208142google scholar: lookup
  48. Doan R, Cohen N, Harrington J, Veazey K, Juras R, Cothran G, McCue ME, Skow L, Dindot SV. Identification of copy number variants in horses.. Genome Res 2012 May;22(5):899-907.
    doi: 10.1101/gr.128991.111pmc: PMC3337435pubmed: 22383489google scholar: lookup
  49. 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-zpmc: PMC6805398pubmed: 31640551google scholar: lookup
  50. Gottschalk M, Metzger J, Martinsson G, Sieme H, Distl O. Genome-wide association study for semen quality traits in German Warmblood stallions.. Anim Reprod Sci 2016 Aug;171:81-6.
  51. Schrimpf R, Dierks C, Martinsson G, Sieme H, Distl O. Genome-wide association study identifies phospholipase C zeta 1 (PLCz1) as a stallion fertility locus in Hanoverian warmblood horses.. PLoS One 2014;9(10):e109675.
  52. Raudsepp T, McCue ME, Das PJ, Dobson L, Vishnoi M, Fritz KL, Schaefer R, Rendahl AK, Derr JN, Love CC, Varner DD, Chowdhary BP. Genome-wide association study implicates testis-sperm specific FKBP6 as a susceptibility locus for impaired acrosome reaction in stallions.. PLoS Genet 2012;8(12):e1003139.
  53. Schrimpf R, Gottschalk M, Metzger J, Martinsson G, Sieme H, Distl O. Screening of whole genome sequences identified high-impact variants for stallion fertility.. BMC Genomics 2016 Apr 14;17:288.
    doi: 10.1186/s12864-016-2608-3pmc: PMC4832559pubmed: 27079378google scholar: lookup
  54. 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.
  55. Metzger J, Karwath M, Tonda R, Beltran S, Águeda L, Gut M, Gut IG, Distl O. Runs of homozygosity reveal signatures of positive selection for reproduction traits in breed and non-breed horses.. BMC Genomics 2015 Oct 9;16:764.
    doi: 10.1186/s12864-015-1977-3pmc: PMC4600213pubmed: 26452642google scholar: lookup
  56. Ablondi M, Viklund Å, Lindgren G, Eriksson S, Mikko S. Signatures of selection in the genome of Swedish warmblood horses selected for sport performance.. BMC Genomics 2019 Sep 18;20(1):717.
    doi: 10.1186/s12864-019-6079-1pmc: PMC6751828pubmed: 31533613google scholar: lookup
  57. Todd ET, Thomson PC, Hamilton NA, Ang RA, Lindgren G, Viklund Å, Eriksson S, Mikko S, Strand E, Velie BD. A genome-wide scan for candidate lethal variants in Thoroughbred horses.. Sci Rep 2020 Aug 4;10(1):13153.
    doi: 10.1038/s41598-020-68946-8pmc: PMC7403398pubmed: 32753654google scholar: lookup
  58. Mau C, Poncet PA, Bucher B, Stranzinger G, Rieder S. Genetic mapping of dominant white (W), a homozygous lethal condition in the horse (Equus caballus). J. Anim. Breed. Genet. 2004;121:374–383.
  59. Schrimpf R, Metzger J, Martinsson G, Sieme H, Distl O. Implication of FKBP6 for male fertility in horses.. Reprod Domest Anim 2015 Apr;50(2):195-199.
    doi: 10.1111/rda.12467pubmed: 25495881google scholar: lookup
  60. Giese A, Jude R, Kuiper H, Piumi F, Schambony A, Guérin G, Distl O, Töpfer-Petersen E, Leeb T. Molecular characterization of the equine AEG1 locus.. Gene 2002 Jun 12;292(1-2):65-72.
    doi: 10.1016/S0378-1119(02)00673-Xpubmed: 12119100google scholar: lookup
  61. Hamann H, Jude R, Sieme H, Mertens U, Töpfer-Petersen E, Distl O, Leeb T. A polymorphism within the equine CRISP3 gene is associated with stallion fertility in Hanoverian warmblood horses.. Anim Genet 2007 Jun;38(3):259-64.
  62. Liu M, Fang L, Liu S, Pan MG, Seroussi E, Cole JB, Ma L, Chen H, Liu GE. Array CGH-based detection of CNV regions and their potential association with reproduction and other economic traits in Holsteins.. BMC Genomics 2019 Mar 7;20(1):181.
    doi: 10.1186/s12864-019-5552-1pmc: PMC6407259pubmed: 30845913google scholar: lookup
  63. Charlesworth D, Willis JH. The genetics of inbreeding depression.. Nat Rev Genet 2009 Nov;10(11):783-96.
    doi: 10.1038/nrg2664pubmed: 19834483google scholar: lookup
  64. Keller LF, Waller DM. Inbreeding effects in wild populations.. Trends Ecol. Evol. 2002;17:230–241.
  65. González-Recio O, López de Maturana E, Gutiérrez JP. Inbreeding depression on female fertility and calving ease in Spanish dairy cattle.. J Dairy Sci 2007 Dec;90(12):5744-52.
    doi: 10.3168/jds.2007-0203pubmed: 18024768google scholar: lookup
  66. Curik I, Ferenčaković M, Sölkner J. Modeling perspectives in the estimation of inbreeding depression based on genomic information: Lessons from the bull fertility. Proceedings of the 6th Conference of the Genetic Society of Slovenia; Maribor, Slovenia. 26–29 September 2012.
  67. Avdi M, Banos G. Genetic diversity and inbreeding in the Greek Skyros horse.. Livest. Sci. 2008;114:362–365.
  68. Gamboa S, Machado-Faria M, Ramalho-Santos J. Seminal traits, suitability for semen preservation and fertility in the native Portuguese horse breeds Puro Sangue Lusitano and Sorraia: Implications for stallion classification and assisted reproduction.. Anim Reprod Sci 2009 Jul;113(1-4):102-13.
  69. Perdomo-González DI, Sánchez-Guerrero MJ, Molina A, Valera M. Genetic Structure Analysis of the Pura Raza Español Horse Population through Partial Inbreeding Coefficient Estimation.. Animals (Basel) 2020 Aug 6;10(8).
    doi: 10.3390/ani10081360pmc: PMC7459874pubmed: 32781594google scholar: lookup
  70. Azcona F, Valera M, Molina A, Trigo P, García PP, Solé M, Demyda-Peyrás S. Impact of reproductive biotechnologies on genetic variability of Argentine Polo horses.. Livest. Sci. 2019.
  71. Todd ET, Ho SYW, Thomson PC, Ang RA, Velie BD, Hamilton NA. Founder-specific inbreeding depression affects racing performance in Thoroughbred horses.. Sci Rep 2018 Apr 18;8(1):6167.
    doi: 10.1038/s41598-018-24663-xpmc: PMC5906619pubmed: 29670190google scholar: lookup
  72. Gómez MD, Valera M, Molina A, Gutiérrez JP, Goyache F. Assessment of inbreeding depression for body measurements in Spanish Purebred (Andalusian) horses.. Livest. Sci. 2009;122:149–155.
  73. Lencz T, Lambert C, DeRosse P, Burdick KE, Morgan TV, Kane JM, Kucherlapati R, Malhotra AK. Runs of homozygosity reveal highly penetrant recessive loci in schizophrenia.. Proc Natl Acad Sci U S A 2007 Dec 11;104(50):19942-7.
    doi: 10.1073/pnas.0710021104pmc: PMC2148402pubmed: 18077426google scholar: lookup
  74. Kardos M, Luikart G, Allendorf FW. Measuring individual inbreeding in the age of genomics: marker-based measures are better than pedigrees.. Heredity (Edinb) 2015 Jul;115(1):63-72.
    doi: 10.1038/hdy.2015.17pmc: PMC4815495pubmed: 26059970google scholar: lookup
  75. Curik I, Ferenčaković M, Sölkner J. Inbreeding and runs of homozygosity: A possible solution to an old problem.. Livest. Sci. 2014;166:26–34.
  76. Ceballos FC, Joshi PK, Clark DW, Ramsay M, Wilson JF. Runs of homozygosity: windows into population history and trait architecture.. Nat Rev Genet 2018 Apr;19(4):220-234.
    doi: 10.1038/nrg.2017.109pubmed: 29335644google scholar: lookup
  77. Aurich C, Achmann R, Aurich JE. Semen parameters and level of microsatellite heterozygosity in Noriker draught horse stallions.. Theriogenology 2003 Jul;60(2):371-8.
    doi: 10.1016/S0093-691X(03)00005-0pubmed: 12749950google scholar: lookup
  78. Velie BD, Solé M, Fegraeus KJ, Rosengren MK, Røed KH, Ihler CF, Strand E, Lindgren G. Genomic measures of inbreeding in the Norwegian-Swedish Coldblooded Trotter and their associations with known QTL for reproduction and health traits.. Genet Sel Evol 2019 May 27;51(1):22.
    doi: 10.1186/s12711-019-0465-7pmc: PMC6537210pubmed: 31132983google scholar: lookup
  79. Laseca N, Perdomo-González DI, Valera M, Molina A, Sanchez-Guerrero MJ, Azcona F, Pirosanto Y, Demyda-Peyrás S. Foaling number are highly affected by the genomic homozygosity in the Pura Raza Spanish mares.. J. Equine Vet. Sci. 2020;89:103098.
  80. Orlando L, Librado P. Origin and Evolution of Deleterious Mutations in Horses.. Genes (Basel) 2019 Aug 28;10(9).
    doi: 10.3390/genes10090649pmc: PMC6769756pubmed: 31466279google scholar: lookup
  81. Davenport CB. DEGENERATION, ALBINISM AND INBREEDING.. Science 1908 Oct 2;28(718):454-5.
    doi: 10.1126/science.28.718.454-bpubmed: 17771943google scholar: lookup
  82. Azcona F, Alcala AM, Valera M, Dorado J, Peyras SD. Impact of the use of large-scale embryo transfer programs in the increase of inbreeding and relativeness in the Argentinean Polo horse.. Reprod. Domest. Anim. 2018;53:107-107.
  83. Gao Y, Li S, Lai Z, Zhou Z, Wu F, Huang Y, Lan X, Lei C, Chen H, Dang R. Analysis of Long Non-Coding RNA and mRNA Expression Profiling in Immature and Mature Bovine (Bos taurus) Testes.. Front Genet 2019;10:646.
    doi: 10.3389/fgene.2019.00646pmc: PMC6624472pubmed: 31333723google scholar: lookup
  84. Sharma A, Lee JS, Dang CG, Sudrajad P, Kim HC, Yeon SH, Kang HS, Lee SH. Stories and Challenges of Genome Wide Association Studies in Livestock - A Review.. Asian-Australas J Anim Sci 2015 Oct;28(10):1371-9.
    doi: 10.5713/ajas.14.0715pmc: PMC4554843pubmed: 26194229google scholar: lookup
  85. Ma L, Cole JB, Da Y, VanRaden PM. Symposium review: Genetics, genome-wide association study, and genetic improvement of dairy fertility traits.. J Dairy Sci 2019 Apr;102(4):3735-3743.
    doi: 10.3168/jds.2018-15269pubmed: 30268602google scholar: lookup
  86. Demars J, Fabre S, Sarry J, Rossetti R, Gilbert H, Persani L, Tosser-Klopp G, Mulsant P, Nowak Z, Drobik W, Martyniuk E, Bodin L. Genome-wide association studies identify two novel BMP15 mutations responsible for an atypical hyperprolificacy phenotype in sheep.. PLoS Genet 2013 Apr;9(4):e1003482.
  87. Giesecke K, Hamann H, Stock KF, Woehlke A, Sieme H, Distl O. Evaluation of SPATA1-associated markers for stallion fertility.. Anim Genet 2009 Aug;40(4):359-65.
  88. Giesecke K, Hamann H, Stock KF, Klewitz J, Martinsson G, Distl O, Sieme H. Evaluation of ACE, SP17, and FSHB as candidates for stallion fertility in Hanoverian warmblood horses.. Anim Reprod Sci 2011 Jul;126(3-4):200-6.
  89. Giesecke K, Hamann H, Sieme H, Distl O. Evaluation of prolactin receptor (PRLR) as candidate gene for male fertility in Hanoverian warmblood horses.. Reprod Domest Anim 2010 Oct;45(5):e124-30.
  90. Giesecke K, Hamann H, Sieme H, Distl O. INHBA-associated markers as candidates for stallion fertility.. Reprod Domest Anim 2010 Apr;45(2):342-7.
  91. El-Sheikh Ali H, Boakari YL, Loux SC, Dini P, Scoggin KE, Esteller-Vico A, Kalbfleisch T, Ball BA. Transcriptomic analysis reveals the key regulators and molecular mechanisms underlying myometrial activation during equine placentitis†.. Biol Reprod 2020 May 26;102(6):1306-1325.
    doi: 10.1093/biolre/ioaa020pubmed: 32065222google scholar: lookup
  92. Leon PM, Campos VF, Thurow HS, Hartwig FP, Selau LP, Dellagostin OA, Neto JB, Deschamps JC, Seixas FK, Collares T. Association between single nucleotide polymorphisms in p53 and abortion in Thoroughbred mares.. Vet J 2012 Aug;193(2):573-5.
    doi: 10.1016/j.tvjl.2012.02.003pubmed: 22414890google scholar: lookup
  93. Kalbfleisch TS, Rice ES, DePriest MS Jr, Walenz BP, Hestand MS, Vermeesch JR, O Connell BL, Fiddes IT, Vershinina AO, Saremi NF, Petersen JL, Finno CJ, Bellone RR, McCue ME, Brooks SA, Bailey E, Orlando L, Green RE, Miller DC, Antczak DF, MacLeod JN. Improved reference genome for the domestic horse increases assembly contiguity and composition.. Commun Biol 2018;1:197.
    doi: 10.1038/s42003-018-0199-zpmc: PMC6240028pubmed: 30456315google scholar: lookup
  94. McGivney BA, Han H, Corduff LR, Katz LM, Tozaki T, MacHugh DE, Hill EW. Genomic inbreeding trends, influential sire lines and selection in the global Thoroughbred horse population.. Sci Rep 2020 Jan 16;10(1):466.
    doi: 10.1038/s41598-019-57389-5pmc: PMC6965197pubmed: 31949252google scholar: lookup
  95. Demir Eksi D, Shen Y, Erman M, Chorich LP, Sullivan ME, Bilekdemir M, Yılmaz E, Luleci G, Kim HG, Alper OM, Layman LC. Copy number variation and regions of homozygosity analysis in patients with MÜLLERIAN aplasia.. Mol Cytogenet 2018;11:13.
    doi: 10.1186/s13039-018-0359-3pmc: PMC5797403pubmed: 29434669google scholar: lookup
  96. Nandolo W, Utsunomiya YT, Mészáros G, Wurzinger M, Khayadzadeh N, Torrecilha RBP, Mulindwa HA, Gondwe TN, Waldmann P, Ferenčaković M, Garcia JF, Rosen BD, Bickhart D, van Tassell CP, Curik I, Sölkner J. Misidentification of runs of homozygosity islands in cattle caused by interference with copy number variation or large intermarker distances.. Genet Sel Evol 2018 Aug 22;50(1):43.
    doi: 10.1186/s12711-018-0414-xpmc: PMC6106898pubmed: 30134820google scholar: lookup

Citations

This article has been cited 9 times.
  1. Nocera FP, Maurizi L, Masullo A, Nicoletti M, Conte AL, Brunetti F, De Martino L, Zagaglia C, Longhi C. Genotypic and Phenotypic Characterization of Escherichia coli Isolates Recovered from the Uterus of Mares with Fertility Problems. Animals (Basel) 2023 May 14;13(10).
    doi: 10.3390/ani13101639pubmed: 37238068google scholar: lookup
  2. Demyda-Peyrás S, Laseca N, Anaya G, Kij-Mitka B, Molina A, Karlau A, Valera M. Prevalence of Sex-Related Chromosomal Abnormalities in a Large Cohort of Spanish Purebred Horses. Animals (Basel) 2023 Feb 3;13(3).
    doi: 10.3390/ani13030539pubmed: 36766428google 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. Laseca N, Molina A, Ramón M, Valera M, Azcona F, Encina A, Demyda-Peyrás S. Fine-Scale Analysis of Runs of Homozygosity Islands Affecting Fertility in Mares. Front Vet Sci 2022;9:754028.
    doi: 10.3389/fvets.2022.754028pubmed: 35252415google scholar: lookup
  5. Ullah A, Chen W, Shi L, Wang M, Geng M, Na J, Akhtar MF, Khan MZ, Wang C. Challenges and Enhancing Strategies of Equine Semen Preservation: Nutritional and Genetic Perspectives. Vet Sci 2025 Aug 25;12(9).
    doi: 10.3390/vetsci12090807pubmed: 41012733google scholar: lookup
  6. Khan MZ, Chen W, Naz S, Liu X, Liang H, Chen Y, Kou X, Liu Y, Ashraf I, Han Y, Peng Y, Wang C, Zahoor M. Determinant genetic markers of semen quality in livestock. Front Endocrinol (Lausanne) 2024;15:1456305.
    doi: 10.3389/fendo.2024.1456305pubmed: 39429738google scholar: lookup
  7. Lovász L, Sommer-Trembo C, Barth JMI, Scasta JD, Grancharova-Hill R, Lemoine RT, Kerekes V, Merckling L, Bouskila A, Svenning JC, Fages A. Rewilded horses in European nature conservation - a genetics, ethics, and welfare perspective. Biol Rev Camb Philos Soc 2025 Feb;100(1):407-427.
    doi: 10.1111/brv.13146pubmed: 39279124google scholar: lookup
  8. Valera M, Karlau A, Anaya G, Bugno-Poniewierska M, Molina A, Encina A, Azor PJ, Demyda-Peyrás S. The Use of Genomic Screening for the Detection of Chromosomal Abnormalities in the Domestic Horse: Five New Cases of 65,XXY Syndrome in the Pura Raza Español Breed. Animals (Basel) 2024 Sep 3;14(17).
    doi: 10.3390/ani14172560pubmed: 39272345google scholar: lookup
  9. Santiviparat S, Swangchan-Uthai T, Stout TAE, Buranapraditkun S, Setthawong P, Taephatthanasagon T, Rodprasert W, Sawangmake C, Tharasanit T. De novo reconstruction of a functional in vivo-like equine endometrium using collagen-based tissue engineering. Sci Rep 2024 Apr 19;14(1):9012.
    doi: 10.1038/s41598-024-59471-zpubmed: 38641671google scholar: lookup