Potential role of maternal lineage in the thoroughbred breeding strategy
Xiang Lin A , Shi Zhou B , Li Wen A D , Allan Davie B , Xinkui Yao C D , Wujun Liu C and Yong Zhang AA Tianjin Key Laboratory of Exercise Physiology and Sports Medicine, Tianjin University of Sports, Tianjin, 300381, China.
B School of Health and Human Sciences, Southern Cross University, Lismore, NSW 2480, Australia.
C College of Animal Sciences, Xinjiang Agricultural University, Urumuqi, 830052, China.
D Corresponding authors. Emails: yxk61@126.com; wenli34@hotmail.com
Reproduction, Fertility and Development 28(11) 1704-1711 https://doi.org/10.1071/RD15063
Submitted: 29 May 2014 Accepted: 1 April 2015 Published: 5 May 2015
Abstract
Many studies have focused on identifying the genes or single nucleotide polymorphisms associated with the athletic ability of thoroughbreds, but few have considered differences in maternal and paternal heritability of athletic ability. Herein, we report on our association study of career race performances of 675 Australian thoroughbreds with their pedigrees. Racing performance data (prize money per start) were collected from the Bloodhound database. The performance of all horses was categorised as either poor or elite athletic achievement. Then, 675 foals were divided by their parents’ performance (elite or poor) into four groups: (1) elite dams and elite sires; (2) elite dams and poor sires; (3) poor dams and elite sires; and (4) poor dams and poor sires. The performance of foals was then compared between the four groups. The results show that the heritability of race performance between dams and foals (r = 0.141, P < 0.001) is much higher than that between sires and foals (r = 0.035, P = 0.366), and that this difference is statistically significant (P < 0.05). We also examined the effect of the child-bearing age of dams and sires on the ratio of elite foals. We found a strong correlation between the number of elite foals and dams’ child-bearing age (r = –0.105, P < 0.001), with the ratio of elite offspring reaching a high level between a child-bearing age of 8 and 11 years (χ2 = 14.31, d.f. = 1, P < 0.001). These findings suggest that the maternal line may play an important role in the selective breeding of athletic performance in thoroughbreds.
Additional keywords: athletic performance, birth age, horse breeding, mitochondrial DNA.
References
Allen, W. R., Wilsher, S., Turnbull, C., Stewart, F., Ousey, J., Rossdale, P. D., and Fowden, A. L. (2002). Influence of maternal size on placental, fetal and postnatal growth in the horse. I. Development in utero. Reproduction 123, 445–453.| Influence of maternal size on placental, fetal and postnatal growth in the horse. I. Development in utero.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Cls70%3D&md5=f3fa485a4384f926cbb34ade391d9760CAS | 11882022PubMed |
Australian Racing Board. (2011). ‘Australian Pattern Committee Procedure Manual.’ Available at: http://www.australianracingboard.com.au/uploadimg/AusPCProcedureManual.pdf [verified 20 February 2013].
Baumer, A., Zhang, C., Linnane, A. W., and Nagley, P. (1994). Age-related human mtDNA deletions: a heterogeneous set of deletions arising at a single pair of directly repeated sequences. Am. J. Hum. Genet. 54, 618–630.
| 1:CAS:528:DyaK2MXhtFWrtg%3D%3D&md5=01cbd0f6a4ba904ecfd53546b0ed2a55CAS | 8128959PubMed |
Brooks, A. A., Johnson, M. R., Steer, P. J., Pawson, M. E., and Abdalla, H. I. (1995). Birth weight: nature or nurture? Early Hum. Dev. 42, 29–35.
| Birth weight: nature or nurture?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2MvgtFyqug%3D%3D&md5=12ce50d15c7c77f9c0d769d387469edfCAS | 7671843PubMed |
Corral-Debrinski, M., Horton, T., Lott, M. T., Shoffner, J. M., Beal, M. F., and Wallace, D. C. (1992). Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nat. Genet. 2, 324–329.
| Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXnvVGntQ%3D%3D&md5=b19a5e3667f4a652995d2e7da1531cf6CAS | 1303288PubMed |
Cortopassi, G., and Wang, E. (1995). Modelling the effects of age-related mtDNA mutation accumulation; complex I deficiency, superoxide and cell death. Biochim. Biophys. Acta 1271, 171–176.
| Modelling the effects of age-related mtDNA mutation accumulation; complex I deficiency, superoxide and cell death.Crossref | GoogleScholarGoogle Scholar | 7599205PubMed |
Cunningham, E. P., Dooley, J. J., Splan, R. K., and Bradley, D. G. (2001). Microsatellite diversity, pedigree relatedness and the contributions of founder lineages to thoroughbred horses. Anim. Genet. 32, 360–364.
| Microsatellite diversity, pedigree relatedness and the contributions of founder lineages to thoroughbred horses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1yhsw%3D%3D&md5=de58702a6a058c2cff4d4a72de4138f0CAS | 11736806PubMed |
Das, J. (2006). The role of mitochondrial respiration in physiological and evolutionary adaptation. BioEssays 28, 890–901.
| The role of mitochondrial respiration in physiological and evolutionary adaptation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVKqsrvF&md5=e63ba8c65b664829d680677e7958d5f8CAS | 16937356PubMed |
Essén-Gustavsson, B., and Lindholm, A. (1985). Muscle fibre characteristics of active and inactive standardbred horses. Equine Vet. J. 17, 434–438.
| Muscle fibre characteristics of active and inactive standardbred horses.Crossref | GoogleScholarGoogle Scholar | 4076157PubMed |
Gallagher, J. R., and McMeniman, N. P. (1988). The nutritional status of pregnant and non-pregnant mares grazing south east Queensland pastures. Equine Vet. J. 20, 414–416.
| The nutritional status of pregnant and non-pregnant mares grazing south east Queensland pastures.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7gslWntA%3D%3D&md5=1390bb4d1dc31e28e87aee94a4812317CAS | 3215165PubMed |
Godfray, H. C., and Johnstone, R. A. (2000). Begging and bleating: the evolution of parent-offspring signalling. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 1581–1591.
| Begging and bleating: the evolution of parent-offspring signalling.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7ksVKmsw%3D%3D&md5=46af9b1eebe7178ea7eed1c5b3b82540CAS | 11127903PubMed |
Hattori, K., Tanaka, M., Sugiyama, S., Obayashi, T., Ito, T., Satake, T., Hanaki, Y., Asai, J., Nagano, M., and Ozawa, T. (1991). Age-dependent increase in deleted mitochondrial DNA in the human heart: possible contributory factor to presbycardia. Am. Heart J. 121, 1735–1742.
| Age-dependent increase in deleted mitochondrial DNA in the human heart: possible contributory factor to presbycardia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3ktV2nsQ%3D%3D&md5=846663e0c3b8bb2518c3004117ee103cCAS | 2035386PubMed |
Jackson, M., Vizard, A., Anderson, G., Clarke, A., and Whitton, R. (2011). Association between the purchase price of thoroughbred yearlings and their performance during the 2- and 3-year-old racing seasons. Aust. Vet. J. 89, 388–393.
| Association between the purchase price of thoroughbred yearlings and their performance during the 2- and 3-year-old racing seasons.Crossref | GoogleScholarGoogle Scholar | 21933166PubMed |
Kenneth, W. H., Baymond, J. G., and Andris, J. K. (2008). ‘Equine Exercise Physiology: The Science of Exercise in the Athletic Horse.’ (Saunders: Philadelphia.)
Kim, K. C., Cho, H. I., and Kim, W. (2012). MtDNA haplogroups and elite Korean athlete status. Int. J. Sports Med. 33, 76–80.
| MtDNA haplogroups and elite Korean athlete status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjvVSlu7g%3D&md5=41149b46916a28138b85577ff271de03CAS | 22134884PubMed |
Maegawa, S., Hinkal, G., Kim, H. S., Shen, L., Zhang, L., Zhang, J., Zhang, N., Liang, S., Donehower, L. A., and Issa, J. P. (2010). Widespread and tissue specific age-related DNA methylation changes in mice. Genome Res. 20, 332–340.
| Widespread and tissue specific age-related DNA methylation changes in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtlCktbs%3D&md5=3b20eff6459364fc8310c16cd3cd5f9fCAS | 20107151PubMed |
Martínez-Redondo, D., Marcuello, A., Casajús, J. A., Ara, I., Dahmani, Y., Montoya, J., Ruiz-Pesini, E., López-Pérez, M. J., and Díez-Sánchez, C. (2010). Human mitochondrial haplogroup H: the highest Vo2max consumer: is it a paradox? Mitochondrion 10, 102–107.
| Human mitochondrial haplogroup H: the highest Vo2max consumer: is it a paradox?Crossref | GoogleScholarGoogle Scholar | 19900587PubMed |
McBane, S. (1997). ‘The Illustrated Encyclopedia of Horse Breeds.’ (Wellfleet Press: New York.)
McGreevy, P. (2004). ‘Equine Behaviour: A Guide for Veterinarians and Equine Scientists.’ (Saunders: Edinburgh.)
Mikami, E., Fuku, N., Takahashi, H., Ohiwa, N., Scott, R. A., Pitsiladis, Y. P., Higuchi, M., Kawahara, T., and Tanaka, M. (2011). Mitochondrial haplogroups associated with elite Japanese athlete status. Br. J. Sports Med. 45, 1179–1183.
| Mitochondrial haplogroups associated with elite Japanese athlete status.Crossref | GoogleScholarGoogle Scholar | 20551160PubMed |
Moore, T. (2012). Review: Parent–offspring conflict and the control of placental function. Placenta 33, S33–S36.
| Review: Parent–offspring conflict and the control of placental function.Crossref | GoogleScholarGoogle Scholar | 22153682PubMed |
Moore, T., and Haig, D. (1991). Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 7, 45–49.
| Genomic imprinting in mammalian development: a parental tug-of-war.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3ktVGmug%3D%3D&md5=2b173257d00b174e80a9b6b007eabfeaCAS | 2035190PubMed |
Nogales-Gadea, G., Pinos, T., Ruiz, J. R., Marzo, P. F., Fiuza-Luces, C., Lopez-Gallardo, E., Ruiz-Pesini, E., Martin, M. A., Arenas, J., Moran, M., Andreu, A. L., and Lucia, A. (2011). Are mitochondrial haplogroups associated with elite athletic status? A study on a Spanish cohort. Mitochondrion 11, 905–908.
| Are mitochondrial haplogroups associated with elite athletic status? A study on a Spanish cohort.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtl2qs7fJ&md5=1f0d3cb1d31e3efa5233454aa6cc54c8CAS | 21856449PubMed |
Parker, R. (2007). ‘Equine Science.’ (Delmar Cengage Learning: Clifton Park, NY)
Parker, G. A., and MacNair, M. R. (1978). Models of parent–offspring conflict. I. Monogamy. Anim. Behav. 26, 97–110.
| Models of parent–offspring conflict. I. Monogamy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c7kt1yhtQ%3D%3D&md5=bbac01d45cdbac72884342fe67e878a6CAS | 637373PubMed |
Pösö, A. R., Essen-Gustavsson, B., and Persson, S. G. (1993). Metabolic response to standardised exercise test in standardbred trotters with red cell hypervolaemia. Equine Vet. J. 25, 527–531.
| Metabolic response to standardised exercise test in standardbred trotters with red cell hypervolaemia.Crossref | GoogleScholarGoogle Scholar | 8276001PubMed |
Ronéus, M., Lindholm, A., and Asheim, A. (1991). Muscle characteristics in thoroughbreds of different ages and sexes. Equine Vet. J. 23, 207–210.
| Muscle characteristics in thoroughbreds of different ages and sexes.Crossref | GoogleScholarGoogle Scholar | 1884703PubMed |
Ronéus, N., Essén-Gustavsson, B., Lindholm, A., and Eriksson, Y. (1994). Plasma lactate response to submaximal and maximal exercise tests with training, and its relationship to performance and muscle characteristics in standardbred trotters. Equine Vet. J. 26, 117–121.
| Plasma lactate response to submaximal and maximal exercise tests with training, and its relationship to performance and muscle characteristics in standardbred trotters.Crossref | GoogleScholarGoogle Scholar | 8575372PubMed |
Rönn, T., Poulsen, P., Hansson, O., Holmkvist, J., Almgren, P., Nilsson, P., Tuomi, T., Isomaa, B., Groop, L., Vaag, A., and Ling, C. (2008). Age influences DNA methylation and gene expression of COX7A1 in human skeletal muscle. Diabetologia 51, 1159–1168.
| Age influences DNA methylation and gene expression of COX7A1 in human skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 18488190PubMed |
Scott, R. A., Wilson, R. H., Goodwin, W. H., Moran, C. N., Georgiades, E., Wolde, B., and Pitsiladis, Y. P. (2005). Mitochondrial DNA lineages of elite Ethiopian athletes. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 140, 497–503.
| Mitochondrial DNA lineages of elite Ethiopian athletes.Crossref | GoogleScholarGoogle Scholar | 15694598PubMed |
Scott, R. A., Fuku, N., Onywera, V. O., Boit, M., Wilson, R. H., Tanaka, M., Goodwin, W., and Pitsiladis, Y. P. (2009). Mitochondrial haplogroups associated with elite Kenyan athlete status. Med. Sci. Sports Exerc. 41, 123–128.
| Mitochondrial haplogroups associated with elite Kenyan athlete status.Crossref | GoogleScholarGoogle Scholar | 19092698PubMed |
Shen, Y. Y., Liang, L., Zhu, Z. H., Zhou, W. P., Irwin, D. M., and Zhang, Y. P. (2010). Adaptive evolution of energy metabolism genes and the origin of flight in bats. Proc. Natl Acad. Sci. USA 107, 8666–8671.
| Adaptive evolution of energy metabolism genes and the origin of flight in bats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsFWmtLY%3D&md5=4d8d3dd75ea62e35d51bc951db556facCAS | 20421465PubMed |
Spence, N. J. (2008). The long-term consequences of childbearing: physical and psychological well-being of mothers in later life. Res. Aging 30, 722–751.
| The long-term consequences of childbearing: physical and psychological well-being of mothers in later life.Crossref | GoogleScholarGoogle Scholar | 19122886PubMed |
Trivers, R. L., and Willard, D. E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science 179, 90–92.
| Natural selection of parental ability to vary the sex ratio of offspring.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3s%2Fls1Wqsg%3D%3D&md5=6c0628b71b5bf9c09e3733a122492b17CAS | 4682135PubMed |
Trombetta, B., Cruciani, F., Underhill, P. A., Sellitto, D., and Scozzari, R. (2010). Footprints of X-to-Y gene conversion in recent human evolution. Mol. Biol. Evol. 27, 714–725.
| Footprints of X-to-Y gene conversion in recent human evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitlartL4%3D&md5=eecf9a12682feeea9ebcbbf61d1b9cb9CAS | 19812029PubMed |
Tyler-Smith, C., and Xue, Y. (2012). Sibling rivalry among paralogs promotes evolution of the human brain. Cell 149, 737–739.
| Sibling rivalry among paralogs promotes evolution of the human brain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntFantrc%3D&md5=c01df107ecd141becaf85c5bc5b7bfb4CAS | 22579279PubMed |
United States Agency for International Development (2008). ‘Healthy Timing and Spacing of Pregnancy.’ Available at: http://www.basics.org/reports/FinalReport/HTSP-Final-Report_BASICS.pdf [verified 10 June 2013.]
Velie, B. D., Wade, C. M., and Hamilton, N. A. (2013). Profiling the careers of thoroughbred horses racing in Australia between 2000 and 2010. Equine Vet. J. 45, 182–186.
| Profiling the careers of thoroughbred horses racing in Australia between 2000 and 2010.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38fkslKnsQ%3D%3D&md5=dc690faddcaa8606a7dd03993575c3dfCAS | 22853620PubMed |
Vilà, C., Leonard, J. A., Götherström, A., Marklund, S., Sandberg, K., Lidén, K., Wayne, R. K., and Ellegren, H. (2001). Widespread origins of domestic horse lineages. Science 291, 474–477.
| Widespread origins of domestic horse lineages.Crossref | GoogleScholarGoogle Scholar | 11161199PubMed |
Wallace, D. C. (2010). Mitochondrial DNA mutations in disease and aging. Environ. Mol. Mutagen. 51, 440–450.
| 1:CAS:528:DC%2BC3cXnsVWgtL8%3D&md5=62adbec3694ac3cdf80286395258d37eCAS | 20544884PubMed |
Wallner, B., Vogl, C., Shukla, P., Burgstaller, J. P., Druml, T., and Brem, G. (2013). Identification of genetic variation on the horse Y chromosome and the tracing of male founder lineages in modern breeds. PLoS One 8, e60015.
| Identification of genetic variation on the horse Y chromosome and the tracing of male founder lineages in modern breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtFWrurY%3D&md5=57447e20b1f3c274b6eda64c87903916CAS | 23573227PubMed |
Wilson, A. J., and Rambaut, A. (2008). Breeding racehorses: what price good genes? Biol. Lett. 4, 173–175.
| Breeding racehorses: what price good genes?Crossref | GoogleScholarGoogle Scholar | 18089517PubMed |