Skip to main content Accessibility help
×
Home

Review: Genomics of bull fertility

  • Jeremy F. Taylor (a1), Robert D. Schnabel (a1) (a2) and Peter Sutovsky (a1) (a3)

Abstract

Fertility is one of the most economically important traits in both beef and dairy cattle production; however, only female fertility is typically subjected to selection. Male and female fertility have only a small positive genetic correlation which is likely due to the existence of a relatively small number of genetic variants within each breed that cause embryonic and developmental losses. Genomic tools have been developed that allow the identification of lethal recessive loci based upon marker haplotypes. Selection against haplotypes harbouring lethal alleles in conjunction with selection to improve female fertility will result in an improvement in male fertility. Genomic selection has resulted in a two to fourfold increase in the rate of genetic improvement of most dairy traits in US Holstein cattle, including female fertility. Considering the rapidly increasing rate of adoption of high-throughput single nucleotide polymorphism genotyping in both the US dairy and beef industries, genomic selection should be the most effective of all currently available approaches to improve male fertility. However, male fertility phenotypes are not routinely recorded in natural service mating systems and when artificial insemination is used, semen doses may be titrated to lower post-thaw progressively motile sperm numbers for high-merit and high-demand bulls. Standardization of sperm dosages across bull studs for semen distributed from young bulls would allow the capture of sire conception rate phenotypes for young bulls that could be used to generate predictions of genetic merit for male fertility in both males and females. These data would allow genomic selection to be implemented for male fertility in addition to female fertility within the US dairy industry. While the rate of use of artificial insemination is much lower within the US beef industry, the adoption of sexed semen in the dairy industry has allowed dairy herds to select cows from which heifer replacements are produced and cows that are used to produce terminal crossbred bull calves sired by beef breed bulls. Capture of sire conception rate phenotypes in dairy herds utilizing sexed semen will contribute data enabling genomic selection for male fertility in beef cattle breeds. As the commercial sector of the beef industry increasingly adopts fixed-time artificial insemination, sire conception rate phenotypes can be captured to facilitate the development of estimates of genetic merit for male fertility within US beef breeds.

Copyright

Corresponding author

References

Hide All
Abdollahi-Arpanahi, R, Morota, G and Peñagaricano, F 2017. Predicting bull fertility using genomic data and biological information. Journal of Dairy Science 100, 96569666.
Berry, DP, Wall, E and Pryce, JE 2014. Genetics and genomics of reproductive performance in dairy and beef cattle. Animal 8 (suppl. 1), 105121.
Capra, E, Turri, F, Lazzari, B, Cremonesi, P, Gliozzi, TM, Fojadelli, I, Stella, A and Pizzi, F 2017. Small RNA sequencing of cryopreserved semen from single bull revealed altered miRNAs and piRNAs expression between high- and low-motile sperm populations. BMC Genomics 18, 14.
Card, CJ, Krieger, KE, Kaproth, M and Sartini, BL 2017. Oligo-dT selected spermatozoal transcript profiles differ among higher and lower fertility dairy sires. Animal Reproduction Science 177, 105123.
Chang, TC, Yang, Y, Retzel, EF and Liu, WS 2013. Male-specific region of the bovine Y chromosome is gene rich with a high transcriptomic activity in testis development. Proceedings of the National Academy of Science USA 110, 1237312378.
Charlier, C, Li, W, Harland, C, Littlejohn, M, Coppieters, W, Creagh, F, Davis, S, Druet, T, Faux, P, Guillaume, F, Karim, L, Keehan, M, Kadri, NK, Tamma, N, Spelman, R and Georges, M 2016. NGS-based reverse genetic screen for common embryonic lethal mutations compromising fertility in livestock. Genome Research 26, 13331341.
Chen, W-H, Lu, G, Chen, X, Zhao, X-M and Bork, P 2017. OGEE v2: an update of the online gene essentiality database with special focus on differentially essential genes in human cancer cell lines. Nucleic Acids Research 45, D940D944.
Cole, JB 2015. A simple strategy for managing many recessive disorders in a dairy cattle breeding program. Genetics Selection Evolution 47, 94.
Cole, JB, Null, DJ and VanRaden, PM 2016. Phenotypic and genetic effects of recessive haplotypes on yield, longevity, and fertility. Journal of Dairy Science 99, 72747288.
Cole, JB, VanRaden, PM, Null, DJ, Hutchison, JL, Cooper, TA and Hubbard, SM 2017. Haplotype tests for recessive disorders that affect fertility and other traits. Retrieved on 30 November 2017 from https://aipl.arsusda.gov/reference/recessive_haplotypes_ARR-G3.html.
David, I, Bodin, L, Lagriffoul, G, Leymarie, C, Manfredi, E and Robert-Granié, C 2007. Genetic analysis of male and female fertility after artificial insemination in sheep: comparison of single-trait and joint models. Journal of Dairy Science 90, 39173923.
De Camargo, GM, Porto-Neto, LR, Kelly, MJ, Bunch, RJ, McWilliam, SM, Tonhati, H, Lehnert, SA, Fortes, MR and Moore, SS 2015. Non-synonymous mutations mapped to chromosome X associated with andrological and growth traits in beef cattle. BMC Genomics 16, 384.
DeJarnette, JM, Nebel, RL and Marshall, CE 2010. Understanding estimates of AI sire fertility. Retrieved on 18 December 2017 from http://www.selectsires.com/programs/docs/UnderstandingAISireFertility.pdf?version=20170404.
Druet, T, Fritz, S, Sellem, E, Basso, B, Gérard, O, Salas-Cortes, L, Humblot, P, Druart, X and Eggen, A 2009. Estimation of genetic parameters and genome scan for 15 semen characteristics traits of Holstein bulls. Journal of Animal Breeding and Genetics 126, 269277.
Feugang, JM, Kaya, A, Page, GP, Chen, L, Mehta, T, Hirani, K, Nazareth, L, Topper, E, Gibbs, R and Memili, E 2009. Two-stage genome-wide association study identifies integrin beta 5 as having potential role in bull fertility. BMC Genomics 10, 176.
Flisikowski, K, Venhoranta, H, Nowacka-Woszuk, J, McKay, SD, Flyckt, A, Taponen, J, Schnabel, R, Schwarzenbacher, H, Szczerbal, I, Lohi, H, Fries, R, Taylor, JF, Switonski, M and Andersson, M 2010. A novel mutation in the maternally imprinted PEG3 domain results in a loss of MIMT1 expression and causes abortions and stillbirths in cattle (Bos taurus). PLoS One 5, e15116.
Fortes, MRS, DeAtley, KL, Lehnert, SA, Burns, BM, Reverter, A, Hawken, RJ, Boe-Hansen, G, Moore, SS and Thomas, MG 2013a. Genomic regions associated with fertility traits in male and female cattle: advances from microsatellites to high-density chips and beyond. Animal Reproduction Science 141, 119.
Fortes, MR, Reverter, A, Kelly, M, McCulloch, R and Lehnert, SA 2013b. Genome-wide association study for inhibin, luteinizing hormone, insulin-like growth factor 1, testicular size and semen traits in bovine species. Andrology 1, 644650.
Fritz, S, Capitan, A, Djari, A, Rodriguez, SC, Barbat, A, Baur, A, Grohs, C, Weiss, B, Boussaha, M, Esquerre, D, Klopp, C, Rocha, D and Boichard, D 2013. Detection of haplotypes associated with prenatal death in dairy cattle and identification of deleterious mutations in GART, SHBG and SLC37A2. PLoS One 8, e65550.
García-Ruiz, A, Cole, JB, VanRaden, PM, Wiggans, GR, Ruiz-López, FJ and Van Tassell, CP 2016. Changes in genetic selection differentials and generation intervals in US Holstein dairy cattle as a result of genomic selection. Proceedings of the National Academy of Sciences USA 113, E3995E4004.
Han, Y and Peñagaricano, F 2016. Unravelling the genomic architecture of bull fertility in Holstein cattle. BMC Genetics 17, 143.
Hansen, M 1979. Genetic investigations on male and female fertility in cattle. Livestock Science 6, 325334.
Hickey, JM, Bruce, C, Whitelaw, A and Gorjanc, G 2016. Promotion of alleles by genome editing in livestock breeding programmes. Journal of Animal Breeding and Genetics 133, 8384.
Hoff, JL, Decker, JE, Schnabel, RD and Taylor, JF 2017. Candidate lethal haplotypes and causal mutations in Angus cattle. BMC Genomics 18, 799.
Kadri, NK, Sahana, G, Charlier, C, Iso-Touru, T, Guldbrandtsen, B, Karim, L, Nielsen, US, Panitz, F, Aamand, GP, Schulman, N, Georges, M, Vilkki, J, Lund, MS and Druet, T 2014. A 660-Kb deletion with antagonistic effects on fertility and milk production segregates at high frequency in Nordic Red cattle: additional evidence for the common occurrence of balancing selection in livestock. PLoS Genetics 10, e1004049.
Khatib, H, Monson, RL, Huang, W, Khatib, R, Schutzkus, V, Khateeb, H and Parrish, JJ 2010. Short communication: validation of in vitro fertility genes in a Holstein bull population. Journal of Dairy Science 93, 22442249.
Kropp, J, Carrillo, JA, Namous, H, Daniels, A, Salih, SM, Song, J and Khatib, H 2017. Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos. BMC Genomics 18, 280.
Lan, XY, Peñagaricano, F, DeJung, L, Weigel, KA and Khatib, H 2013. Short communication: a missense mutation in the PROP1 (prophet of Pit 1) gene affects male fertility and milk production traits in the US Holstein population. Journal of Dairy Science 96, 12551257.
Magee, DA, Sikora, KM, Berkowicz, EW, Berry, DP, Howard, DJ, Mullen, MP, Evans, RD, Spillane, C and MacHugh, DE 2010. DNA sequence polymorphisms in a panel of eight candidate bovine imprinted genes and their association with performance traits in Irish Holstein-Friesian cattle. BMC Genetics 11, 93.
Matukumalli, LK, Lawley, CT, Schnabel, RD, Taylor, JF, Allan, MF, Heaton, MP, O’Connell, J, Moore, SS, Smith, TPL, Sonstegard, TS and Van Tassell, CP 2009. Development and characterization of a high density SNP genotyping assay for cattle. PLoS One 4, e5350.
Mesbah-Uddin, M, Guldbrandtsen, B, Iso-Touru, T, Vilkki, J, De Koning, DJ, Boichard, D, Lund, MS and Sahana, G 2018. Genome-wide mapping of large deletions and their population-genetic properties in dairy cattle. DNA Research 25, 4959.
Meuwissen, TH, Hayes, BJ and Goddard, ME 2001. Prediction of total genetic value using genome-wide dense marker maps. Genetics 157, 18191829.
Meyer, K, Hammond, K, Mackinnon, MJ and Parnell, PF 1991. Estimates of covariances between reproduction and growth in Australian beef cattle. Journal of Animal Science 69, 35333543.
Nagamori, I, Kobayashi, H, Shiromoto, Y, Nishimura, T, Kuramochi-Miyagawa, S, Kono, T and Nakano, T 2015. Comprehensive DNA methylation analysis of retrotransposons in male germ cells. Cell Reports 12, 15411547.
Pausch, H, Schwarzenbacher, H, Burgstaller, J, Flisikowski, K, Wurmser, C, Jansen, S, Jung, S, Schnieke, A, Wittek, T and Fries, R 2015. Homozygous haplotype deficiency reveals deleterious mutations compromising reproductive and rearing success in cattle. BMC Genomics 16, 312325.
Peddinti, D, Nanduri, B, Kaya, A, Feugang, JM, Burgess, SC and Memili, E 2008. Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility. BMC Systems Biology 2, 19.
Peñagaricano, F, Weigel, KA and Khatib, H 2012. Genome-wide association study identifies candidate markers for bull fertility in Holstein dairy cattle. Animal Genetics 43 (suppl. 1), 6571.
Piles, M and Tusell, L 2012. Genetic correlation between growth and female and male contributions to fertility in rabbit. Journal of Animal Breeding and Genetics 129, 298305.
Sahana, G, Nielsen, US, Aamand, GP, Lund, MS and Guldbrandtsen, B 2013. Novel harmful recessive haplotypes identified for fertility traits in Nordic Holstein cattle. PLoS One 8, e82909.
Sahana, G, Iso-Touru, T, Wu, X, Nielsen, US, de Koning, DJ, Lund, MS, Vilkki, J and Guldbrandtsen, B 2016. A 0.5-Mbp deletion on bovine chromosome 23 is a strong candidate for stillbirth in Nordic Red cattle. Genetics Selection Evolution 48, 35.
Syrstad, O 1981. Selection for fertility on the basis of AI data. Livestock Production Science 8, 247252.
Taylor, JF 2014. Implementation and accuracy of genomic selection. Aquaculture 420-421, S8S14.
Taylor, JF, Schnabel, RD and Sutovsky, P 2018. Identification of genomic variants causing sperm abnormalities and reduced male fertility. Animal Reproduction Science, pii: S0378-4320(17)31072-2, https://doi.org/10.1016/j.anireprosci.2018.02.007, Published online 10 February 2018.
VanRaden, PM, Olson, KM, Null, DJ and Hutchison, JL 2011. Harmful recessive effects on fertility detected by absence of homozygous haplotypes. Journal of Dairy Science 94, 61536161.
Verma, A, Rajput, S, De, S, Kumar, R, Chakravarty, AK and Datta, TK 2014. Genome-wide profiling of sperm DNA methylation in relation to buffalo (Bubalus bubalis) bull fertility. Theriogenology 82, 750759.
Wolc, A, White, IM, Olori, VE and Hill, WG 2009. Inheritance of fertility in broiler chickens. Genetics Selection Evolution 41, 47.
Yang, Y, Chang, TC, Yasue, H, Bharti, AK, Retzel, EF and Liu, WS 2011. ZNF280BY and ZNF280AY: autosome derived Y-chromosome gene families in Bovidae. BMC Genomics 12, 13.
Yue, XP, Chang, TC, DeJarnette, JM, Marshall, CE, Lei, CZ and Liu, WS 2013. Copy number variation of PRAMEY across breeds and its association with male fertility in Holstein sires. Journal of Dairy Science 96, 80248034.
Yue, XP, Dechow, C, Chang, TC, DeJarnette, JM, Marshall, CE, Lei, CZ and Liu, WS 2014. Copy number variations of the extensively amplified Y-linked genes, HSFY and ZNF280BY, in cattle and their association with male reproductive traits in Holstein bulls. BMC Genomics 15, 113.

Keywords

Type Description Title
WORD
Supplementary materials

Taylor et al. supplementary material
Taylor et al. supplementary material

 Word (148 KB)
148 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed