Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T19:47:03.351Z Has data issue: false hasContentIssue false
  • English
  • Français

Reproduction biotechnologies in germplasm banking of livestock species: a review

Published online by Cambridge University Press:  24 August 2017

J.M. Morrell  and
I. Mayer
J.M. Morrell*
Affiliation:
Division of Reproduction, Clinical Sciences, Swedish University of Agricultural Sciences (SLU), Box 7054, SE- 75007 Uppsala, Sweden.
I. Mayer
Affiliation:
Norwegian University of Life Sciences, Faculty of Veterinary Medicine and Biosciences, P.O. Box 8146 Dep, N-0033 Oslo, Norway.
*
All correspondence to: J.M. Morrell. Division of Reproduction, Clinical Sciences, Swedish University of Agricultural Sciences (SLU), Box 7054, SE- 75007 Uppsala, Sweden. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Many biotechnologies are currently used in livestock breeding with the aim of improving reproductive efficiency and increasing the rate of genetic progress in production animals. Semen cryopreservation is the most widely used cryobiotechnology, although vitrification techniques now allow embryos and oocytes to be banked in ever-increasing numbers. Cryopreservation of other types of germplasm (reproductive tissue in general) is also possible, although the techniques are still in the early stages of development for use in livestock species. Although still in their infancy, these techniques are increasingly being used in aquaculture. Germplasm conservation enables reproductive tissues from both animals and fish to be preserved to generate offspring in the future without having to maintain large numbers of living populations of these species. However, such measures need careful planning and coordination. This review explains why the preservation of genetic diversity is needed for livestock and fish, and describes some of the issues involved in germplasm banking. Furthermore, some recent developments in semen handling leading to improved semen cryopreservation and biosecurity measures are also discussed.

Keywords

BiodiversityEndangered breedsEpigeneticsFishLivestock
Type
Commentary
Information
Zygote , Volume 25 , Issue 5 , October 2017 , pp. 545 - 557
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abraham, M.C., Johannisson, A. & Morrell, J.M. (2016). Effect of sperm preparation on development of blastocyst in vitro . Zygote 24, 825–30.CrossRefGoogle ScholarPubMed
Agha-Rahimi, A., Khalili, M.A., Nabi, A. & Ashourzadeh, S. (2014). Vitrification is not superior to rapid freezing of normospermic spermatozoa: effects on sperm parameters, DNA fragmentation and hyaluronan binding. Reprod. Biomed. Online 28, 352–8.CrossRefGoogle ScholarPubMed
Alvarenga, M.A., Papa, F.O., Landim-Alvarenga, F.C. & Medeiros, A.S. (2005). Amides as cryoprotectants for freezing stallion semen: a review. Anim. Reprod. Sci. 89:105–13.CrossRefGoogle ScholarPubMed
Álvarez, C., Gil, L., González, N., Olaciregui, M. & Luño, V. (2014). Equine sperm post-thaw evaluation after the addition of different cryoprotectants added to INRA 96® extender. Cryobiology 69:144–8.CrossRefGoogle ScholarPubMed
Amorim, E.A., Graham, J.K., Spizziri, B., Meyers, M. & Torres, C.A. (2009). Effect of cholesterol or cholesteryl conjugates on the cryosurvival of bull sperm. Cryobiology 58, 210–4.CrossRefGoogle ScholarPubMed
Arav, A. (2014). Cryopreservation of oocytes and embryos. Theriogenology 81, 96–102.CrossRefGoogle ScholarPubMed
Avery, B. & Greve, T. (1995). Impact of Percoll on bovine spermatozoa used for in vitro insemination. Theriogenology 44, 871–8.CrossRefGoogle ScholarPubMed
Bielanski, A. & Vajta, G. (2009). Risk of contamination of germplasm during cryopreservation and cryobanking in IVF units. Hum. Reprod. 24, 2457–67.CrossRefGoogle ScholarPubMed
Blomqvist, G., Persson, M., Wallgren, M., Wallgren, P. & Morrell, J.M. (2011). Removal of virus from boar semen spiked with porcine circovirus type 2. Anim. Reprod. Sci. 126, 108–14.CrossRefGoogle ScholarPubMed
Bolton, V.N. & Braude, P.R. (1984). Preparation of human spermatozoa for in vitro fertilization by isopycnic centrifugation on self-generating density gradients. Arch. Androl 13, 167–76.CrossRefGoogle ScholarPubMed
Comizzoli, P. & Holt, W.V. (2014). Recent advances and prospects in germplasm preservation of rare and endangered species. In: Reproduction Sciences in Animal Conservation (eds Holt, W.V., Brown, J.L. & Comizzoli, P.), pp. 331–56. New York, USA: Springer Science.CrossRefGoogle Scholar
Critser, J.K., Riley, L.K., Prather, R.S. (2003). In Reproduction Science and Integrated Conservation (eds Holt, W.V., Pickard, A.R., Rodger, J.C. & Wildt, D.E.), pp. 195–208. Cambridge, UK: Cambridge University Press.Google Scholar
Dadras, H., Sampels, S., Golpour, A., Dzyuba, V., Cosson, J. & Dzyuba, B. (2017). Analysis of common carp Cyprinus carpio sperm motility and lipid composition using different in vitro temperatures. Anim. Reprod. Sci. 180, 37–43.CrossRefGoogle ScholarPubMed
de Vries, A.C. & Colenbrander, B. (1990). Isolation and characterization of boar spermatozoa with and without a cytoplasmic droplet. Int. J. Biochem. 22, 519–24.CrossRefGoogle ScholarPubMed
Edmond, A.J., Teague, A.R., Brinsko, S.P., Comerford, K.L., Waite, J.A., Mancill, S.S., Love, C.C. & Varner, D.D. (2008). Effect of density gradient centrifugation on quality and recovery of equine spermatozoa. Anim. Reprod. Sci. 107(Abst. 16), 318.CrossRefGoogle Scholar
Faezah, S.S., Zuraina, F.M., Farah, J.H., Khairul, O., Hilwani, N.I., Iswadi, M.I., Fang, C.N., Zawawi, I., Abas, O.M. & Fatimah, S.I. (2014). The effects of magnetic separation on cryopreserved bovine spermatozoa motility, viability and cryo-capacitation status. Zygote 22, 378–86.CrossRefGoogle ScholarPubMed
Forero-González, RA, Celeghini, EC, Raphael, CF, Andrade, AF, Bressan, FF & Arruda, RP. (2012). Effects of bovine sperm cryopreservation using different freezing techniques and cryoprotective agents on plasma, acrosomal and mitochondrial membranes. Andrologia 44, 154–9.CrossRefGoogle ScholarPubMed
Galli, C., Vassiliev, I, Lagutina, I., Galli, A. & Lazzari, G. (2003). Bovine embryo development following ICSI: effect of activation, sperm capacitation and pre-treatment with dithiothreitol. Theriogenology 60, 1467–80.CrossRefGoogle ScholarPubMed
Galli, C., Duchi, R., Colleoni, S., Lagutina, I. & Lazzari, G. (2014). Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice. Theriogenology 81, 138–51.CrossRefGoogle ScholarPubMed
Gil, M., Sar-Shalom, V. Sivira, Y.M., Carreras, R. & Checa, M.A. (2013). Sperm selection using magnetic activated cell sorting (MACS) in assisted reproduction: a systematic review and meta-analysis. J. Assist. Reprod. Genet. 30, 479–85.CrossRefGoogle ScholarPubMed
Gibb, Z, Butler, T.J., Morris, L.H.A., Maxwell, W.M.C., Grupen, C.G. (2013). Quercetin improves the postthaw characteristics of cryopreserved sex-sorted and nonsorted stallion sperm. Theriogenology 79, 1001–9.CrossRefGoogle ScholarPubMed
Gouk, S.S., Loh, Y.F., Kumar, S.D., Watson, P.F. & Kuleshova, L.L. (2011). Cryopreservation of mouse testicular tissue: prospect for harvesting spermatogonial stem cells for fertility preservation. Fertil. Steril. 95, 2399–403.CrossRefGoogle ScholarPubMed
Grupen, C.G. (2014). The evolution of porcine embryo in vitro production. Theriogenology 81, 24–37.CrossRefGoogle ScholarPubMed
Hallap, T., Håård, M., Jaakma, U., Larsson, B. & Rodriguez-Martínez, H. (2004). Does cleansing of frozen–thawed bull semen before assessment provide samples that relate better to potential fertility? Theriogenology 62, 702–13.CrossRefGoogle ScholarPubMed
Hernández, M., Roca, J., Calvete, J.J., Sanz, L., Muiño-Blanco, T., Cebrián-Pérez, J.A., Vázquez, J.M., Martínez, E.A. (2007). Cryosurvival and in vitro fertilizing capacity postthaw is improved when boar spermatozoa are frozen in the presence of seminal plasma from good freezer boars. J. Androl. 28, 689–97.CrossRefGoogle ScholarPubMed
Herrid, M. & McFarlane, J. (2013). Application of testis germ cell transplantation in breeding systems of food producing species: a review, Anim. Biotechnol. 24, 293–306.CrossRefGoogle ScholarPubMed
Herrid, M., Vignarajan, S., Davey, R., Dobrinski, I. & Hill, J.R. (2006). Successful transplantation of bovine testicular cells to heterologous recipients. Reproduction 132, 617–24.CrossRefGoogle ScholarPubMed
Holt, W.V. 2008. Cryobiology, wildlife conservation and reality. Cryolett. 29, 43–52.Google Scholar
Holt, W.V., Pickard, A.R. & Prather, R.S. (2004). Reproduction 127, 317–24.CrossRefGoogle Scholar
Hoogewijs, M., Morrell, J.M., Van Soom, A., Govaere, J., Johannisson, A., Piepers, P., De Schauwer, C., de Kruif, A. & De Vliegher, S. (2011). Sperm selection using single layer centrifugation prior to cryopreservation can increase post thaw sperm quality in stallions. Equine Vet. J., 43 (Suppl 40), 35–41.CrossRefGoogle Scholar
Humblot, P., Le Bourhis, D., Fritz, S., Colleau, J.J., González, C., Guyader Joly, C., Malafosse, A., Heyman, Y., Amigues, Y., Tissier, M. & Ponsart, C. (2010). Reproduction technologies and genomic selection in cattle. Vet. Med. Int. Article ID 192787, doi:10.4061/2010/192787 CrossRefGoogle ScholarPubMed
International Union for Conservation of Nature (IUCN) (2016). IUCN Red List of Threatened Species. Version 2016-1. http://www.iucnredlist.org. Accessed 30 June 2016.Google Scholar
Isachenko, E., Mallmann, P., Rahimi, G., Risopatròn, J., Schulz, M., Isachenko, V. & Sànchez, R. (2012). Vitrification technique – new possibilities for male gamete low-temperature storage. In Current Frontiers in Cryobiology (ed. Katkov, I.I.), InTechOpen. ISBN: 978-953-51-0191-8.Google Scholar
Jovanovic, J., Ronneberg, J.A., Tost, J. & Kistensen, V. (2010). The epigenetics of breast cancer. Mol. Oncol. 4, 242–54.CrossRefGoogle ScholarPubMed
Kobayashi, T., Takeuchi, Y., Takeuchi, T. & Yoshizaki, G. (2007). Generation of viable fish from cryopreserved primordial germ cells. Mol. Reprod. Dev. 74, 207–13.CrossRefGoogle ScholarPubMed
Leite, T.G., do Vale-Filho, V.R., de Arruda, R.P., de Andrade, A.F., Emerick, L.L., Zaffalon, F.G., Martins, J.A. & de Andrade, V.J, (2010). Effects of extender and equilibration time on post-thaw motility and membrane integrity of cryopreserved Gyr bull semen evaluated by CASA and flow cytometry. Anim. Reprod. Sci. 120, 31–8.CrossRefGoogle ScholarPubMed
Lindemann, C.B., O'Brien, J.A. & Giblin, F.J. (1988). An investigation of the effectiveness of certain antioxidants in preserving the motility of reactivated bull sperm models. Biol Reprod. 38, 114–20.CrossRefGoogle ScholarPubMed
Loomis, P.R. & Graham, J.K. (2008). Commercial semen freezing: Individual male variation in cryosurvival and the response of stallion sperm to customized freezing protocols. Anim. Reprod. Sci. 105, 119–28.CrossRefGoogle ScholarPubMed
Lunardi, F.O., Araújo, V.R., Bernuci, M.P., Lunardi, L.O., Gonçalves, R.F., Carvalho Ade, A., de Figueiredo, J.R. & Rodrigues, A.P. (2012). Restoring fertility after ovarian tissue cryopreservation: a half century of research. Zygote 21, 394–405.CrossRefGoogle ScholarPubMed
Luño, V., Gil, L., Olaciregui, M., González, N., Jerez, R.A. & de Blas, I. (2014). Rosmarinic acid improves function and in vitro fertilising ability of boar sperm after cryopreservation. Cryobiology 69, 157–62.CrossRefGoogle ScholarPubMed
Machado, G.M., Carvalho, J.O., Filho, E.S., Caixeta, E.S., Franco, M.M., Rumpf, R. & Dode, M.A. (2009). Effect of Percoll volume, duration and force of centrifugation, on in vitro production and sex ratio of bovine embryos. Theriogenology 71, 1289–97.CrossRefGoogle ScholarPubMed
Malcuit, C., Maserati, M., Takahashi, Y., Page, R. & Fissore, R.A. (2006). Intracytoplasmic sperm injection in the bovine induces abnormal Ca2+ responses and oocyte activation. Reprod. Fertil. Dev. 18, 39–51.CrossRefGoogle ScholarPubMed
Mari, G., Castagnetti, C., Rizzato, G., Mislei, B., Iacono, E. & Merlo, B. (2011). Density gradient centrifugation of sperm from a subfertile stallion and effect of seminal plasma addition on fertility. Anim. Reprod. Sci. 126, 96–100.CrossRefGoogle ScholarPubMed
Marrs, R.P., Serafini, P.C., Kerin, J.F., Batzofin, J., Stone, B.A., Brown, J., Wilson, L. & Quinn, P. (1988). Methods used to improve gamete efficiency. Ann. NY Acad. Sci. USA 541, 310–6.CrossRefGoogle ScholarPubMed
Martinez-Alborcia, M.J., Morrell, J.M., Barranco, I., Maside, C., Gil, M.A., Parrilla, I., Vazquez, J.M., Martinez, E.A. & Roca, J. (2013). Suitability and effectiveness of single layer centrifugation using Androcoll-P in the cryopreservation protocol for boar spermatozoa. Anim. Reprod. Sci. 140, 173–9.CrossRefGoogle ScholarPubMed
Martínez-Páramo, S., Horváth, A., Labbé, C., Zhang, T., Robles, V., Herráez, P., Suquet, M., Adams, S., Viveiros, A., Tiersch, T.R. & Cabrita, E. (2017). Cryobanking of aquatic species Aquaculture 472, 156–77.CrossRefGoogle ScholarPubMed
Moore, A.I., Squires, E.L. & Graham, J.K. (2005). Effect of seminal plasma on the cryopreservation of equine spermatozoa. Theriogenology 63, 2372–81.CrossRefGoogle ScholarPubMed
Morita, T., Kumakura, N., Morishima, K., Mitsuboshi, T., Ishida, M., Hara, T., Kudo, S., Miwa, M., Ihara, S., Higuchi, K., Takeuchi, Y. & Yoshizaki, G. (2012). Production of donor-derived offspring by allogenic transplantation of spermatogonia in the yellowtail (Seriola quinqueradiata). Biol. Reprod. 86, 1–11.CrossRefGoogle ScholarPubMed
Morrell, J.M., Dalin, A-M & Rodriguez-Martinez, H. (2008a). Prolongation of stallion sperm survival by centrifugation through coated silica colloids: a preliminary study. Anim. Reprod. 5, 121–6.Google Scholar
Morrell, J.M., Peña, F.J., Johannisson, A., Dalin, A.-M., Samper, J.C., Rodriguez-Martinez, H. (2008b). Techniques for sperm clean-up and selection of stallion spermatozoa. Anim. Reprod. Sci. 107, 333–4.CrossRefGoogle Scholar
Morrell, J.M. & Rodriguez-Martinez, H. (2009). Biomimetic techniques for improving sperm quality in animal breeding: a review. Open Androl. J. 1, 1–9.Google Scholar
Morrell, J.M., Johannisson, A., Dalin, A-M. & Rodriguez-Martinez, H. (2009). Single layer centrifugation with Androcoll™-E can be scaled-up to allow large volumes of stallion ejaculate to be processed easily. Theriogenology 72, 879–84.CrossRefGoogle ScholarPubMed
Morrell, J.M. & Rodriguez-Martinez, H. (2011). Practical applications of sperm selection techniques as a tool for improving reproductive efficiency. Vet. Med. Int. Article ID 894767. doi:10.4061/2011/894767.CrossRefGoogle Scholar
Morrell, J.M. & Wallgren, M. (2011). Colloid centrifugation of boar semen. Reprod. Domest. Anim. 46, 18–22.CrossRefGoogle ScholarPubMed
Morrell, J.M., Johannisson, A. & Rodriguez-Martinez, H. (2011). Effect of osmolarity and density of colloid formulations on the outcome of SLC-selection of stallion spermatozoa. ISRN Vet. Sci. 2011, Article ID 128984, 5 pp. doi:10.5402/2011/128984.CrossRefGoogle ScholarPubMed
Morrell, J.M., van Wienen, M. & Wallgren, M. (2011). Single layer centrifugation can be scaled-up further to process up to 150 mL semen. ISRN Vet. Sci. Article ID 183412, doi: 10.5402/2011/183412.CrossRefGoogle ScholarPubMed
Morrell, J.M. & Wallgren, M. (2011). Removal of bacteria from boar ejaculates by single layer centrifugation can reduce the use of antibiotics in semen extenders. Anim. Reprod. Sci. 123, 64–9.CrossRefGoogle ScholarPubMed
Morrell, J.M., Richter, J., Martinsson, G., Stuhtmann, G., Hoogewijs, M., Roels, K. & Dalin, A.-M. 2014. Pregnancy rates are higher after artificial insemination with cooled stallion spermatozoa selected by single layer centrifugation than with control semen doses. Theriogenology 82, 1102–5.CrossRefGoogle Scholar
Morrell, J.M. & Wallgren, M. (2014). Alternatives to antibiotics in semen extenders: a review. Pathogens 3, 934–46.CrossRefGoogle ScholarPubMed
Morrell, J.M. & Rodriguez-Martinez, H. (2016). Colloid centrifugation of semen: applications in assisted reproduction. Am. J. Anal. Chem. 7, 597–610.CrossRefGoogle Scholar
Mortimer, D. (2000). Sperm preparation methods. J. Androl. 21, 357–66CrossRefGoogle ScholarPubMed
Munro, S.K., Farquhar, C.M., Mitchell, M.D. & Ponampalam, A.P. (2010). Epigenetic regulation of endometrium during the menstrual cycle. Mol. Hum. Reprod. 16, 297–310.CrossRefGoogle ScholarPubMed
Nicholson, C.M., Abramsson, L., Holm, S.E. & Bjurulf, E.X. (2000). Bacterial contamination and sperm recovery after semen preparation by density gradient centrifugation using silane-coated silica particles at different g forces. Hum. Reprod. 15, 662–6.CrossRefGoogle ScholarPubMed
Okutsu, T., Suzuki, K., Takeuchi, Y. & Yoshizaki, G. (2006). Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. Proc. Natl. Acad. Sci. USA 103, 2725–9.CrossRefGoogle ScholarPubMed
Okutsu, T., Shikina, S., Kanno, M., Takeuchi, Y. & Yoshizaki, G. (2007). Production of trout offspring from triploid salmon parents. Science 317, 1517.CrossRefGoogle ScholarPubMed
Polge, C., Smith, A.U. & Parkes, A.S. (1949). Revival of spermatozoa after vitrification and revival at low temperature. Nature 164, 666.CrossRefGoogle Scholar
Rodriguez-Martinez, H., Hultgren, J., Båge, R., Bergqvist, A-S., Svensson, C., Bergsten, C., Lidfors, L., Gunnarsson, S., Algers, B., Emanuelson, U., Berglund, B., Andersson, G., Håård, M., Lindhé, B., Stålhammar, H. & Gustafsson, H. (2008). Reproductive performance in high-producing dairy cows: can we sustain it under current practice? In IVIS Reviews in Veterinary Medicine (ed.). International Veterinary Information Service, Ithaca NY (www.ivis.org), Last updated: 12 December 2008; R0108.1208 (Open Journal), 23 pp.Google Scholar
Röpke, T., Oldenhof, H., Leiding, C., Sieme, H., Bollwein, H. & Wolkers, W.F., (2011). Liposomes for cryopreservation of bovine sperm. Theriogenology 76, 1465–72.CrossRefGoogle ScholarPubMed
Ryder, O.A. & Benirschke, K. (1997). The potential use of ‘cloning’ in the conservation effort. Zoo Biol. 16, 295–300.3.0.CO;2-5>CrossRefGoogle Scholar
Saito, T., Goto-Kazeto, R., Fujimoto, T., Kawakami, Y., Arai, K. & Yamaha, E. (2010). Inter-species transplantation and migration of primordial germ cells in cyprinid fish. Int. J. Dev. Biol. 54, 1479–84.CrossRefGoogle ScholarPubMed
Sánchez, R., Risopatrón, J., Schulz, M., Villegas, J., Isachenko, V., Kreinberg, R. & Isachenko, E. (2011). Canine sperm vitrification with sucrose: effect on sperm function. Andrologia 43, 233–41.CrossRefGoogle ScholarPubMed
Saragusty, J. & Arav, A. (2011). Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction 141, 1–19.CrossRefGoogle ScholarPubMed
Schagdarsurengin, U. & Steger, K. (2016). Epigenetics in male reproduction: effect of paternal diet on sperm quality and offspring health. Nat. Rev. Urol. 13, 584–95.CrossRefGoogle ScholarPubMed
Seki, S., Kouya, T., Tsuchiya, R., Valdez, D.M., Jin, B., Koshimoto, C. Kasai, M. & Edashige, K. (2011). Cryobiological properties of immature zebrafish oocytes assessed by their ability to be fertilized and develop into hatching embryos. Cryobiology 62, 8–14.CrossRefGoogle ScholarPubMed
Serafini, P., Blank, W., Tran, C., Mansourian, M., Tan, T. & Batzofin, J. (1990). Enhanced penetration of zona-free hamster ova by sperm prepared by Nycodenz and Percoll gradient centrifugation. Fertil. Steril. 53, 551–5.CrossRefGoogle ScholarPubMed
Sharma, R.K., Seifarth, K. & Agarwal, A. (1997). Comparison of single- and two-layer Percoll separation for selection of motile spermatozoa. Int. J. Fertil. Womens Med. 42, 412–7.Google ScholarPubMed
Sławeta, R., Waşowicz, W. & Laskowska, T. (1988). Selenium content, glutathione peroxidase activity, and lipid peroxide level in fresh bull semen and its relationship to motility of spermatozoa after freezing-thawing. Zentralbl Veterinarmed. 35, 455–60.CrossRefGoogle ScholarPubMed
Sprícigo, J.F.W., Diógenes, M.N., Leme, L.O., Guimarães, A.L., Muterlle, C.V., Silva, B.D.M., Solà-Oriol, D., Pivato, I., Silva, L.P. & Dode, M.A.N. (2015). Effects of different maturation systems on bovine oocyte quality, plasma membrane phospholipid composition and resistance to vitrification and warming. PLoS One 10, e0130164.CrossRefGoogle ScholarPubMed
Stockwell, S., Hill, J.R., Davey, R., Herrid, M., Lehnert, S.A. (2013). Transplanted germ cells persist long-term in irradiated ram testes. Anim. Reprod. Sci. 142, 137–40.CrossRefGoogle ScholarPubMed
Suarez, S. (2007). Interactions of spermatozoa with the female reproductive tract: inspiration for assisted reproduction. Reprod. Fertil. Dev. 19, 103–10.CrossRefGoogle ScholarPubMed
Tarig, A.A., Wahid, H., Rosnina, Y., Yimer, N., Goh, Y.M., Baiee, F.H., Khumran, A.M., Salman, H. & Ebrahimi, M. (2017). Effect of different concentrations of egg yolk and virgin coconut oil in Tris-based extenders on chilled and frozen–thawed bull semen. Anim. Reprod. Sci. 182, 21–7.CrossRefGoogle ScholarPubMed
Tiersch, T.R., Yang, H., Jenkins, J.A. & Dong, Q. (2007). Sperm cryopreservation in fish and shellfish. Soc. Reprod. Fertil. Suppl. 65, 493–508.Google ScholarPubMed
Urrego, R., Rodriguez-Osorio, N. & Niemann, H. (2014). Epigenetic disorders and altered gene expression after use of assisted reproductive technologies in domestic cattle, Epigenetics 9, 803–15.CrossRefGoogle ScholarPubMed
Valcarce, D.G., Herráez, M.P., Chereguini, O., Rodríguez, C. & Robles, V. (2016). Selection of nonapoptotic sperm by magnetic-activated cell sorting in Senegalese sole (Solea senegalensis). Theriogenology 86, 1195–202CrossRefGoogle ScholarPubMed
Vasicek, J., Makarevich, A.V. & Chrenek, P. (2013). Impact of the MACS on elimination of apoptotic spermatozoa from rabbit ejaculates. Slovak J. Anim. Sci. 46, 87–92.Google Scholar
Veerkamp, R.F. & Beerda, B. (2007). Genetics and genomics to improve fertility in high producing dairy cow. Theriogenology 68 (Suppl 1), S266–73.CrossRefGoogle Scholar
Watson, P.F. (1995). Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function. Reprod. Fertil. Dev. 7, 871–91.CrossRefGoogle ScholarPubMed
Weber, G.M. & Lee, C.-S. (2014). Current and future assisted reproductive technologies for fish species. In Current and Future Reproduction Technologies and World Food Production (eds Lamb, G.C. & DiLorenzo, N.), pp. 33–76. New York USA: Springer Science.CrossRefGoogle Scholar
Woelders, H., Windig, J. & Hiemstra, S.J. (2012). How developments in cryobiology, reproduction technologies and conservation genomics could shape gene banking strategies for (farm) animals. Reprod. Domest. Anim. 47 (Suppl. 4), 264–73.CrossRefGoogle ScholarPubMed
Wu, J., Hu, T., Guo, B., Yue, Z., Yang, Z. & Zhang, X. (2011). Cryopreservation of adult bovine tissue for spermatogonia enrichment. CryoLetters 32, 402–9.Google ScholarPubMed
Yang, C.H., Wu, T.W., Cheng, F.P., Wang, J.H. & Wu, J.T. (2016). Effects of different cryoprotectants and freezing methods on post-thaw boar semen quality. Reprod. Biol. 16, 41–6.CrossRefGoogle ScholarPubMed
Ye, H., Li, C.J., Yue, H.M., Du, H., Yang, X.G., Yoshino, T., Hayashida, T., Takeuchi, Y. & Wei, Q.W. (2017). Establishment of intraperitoneal germ cell transplantation for critically endangered Chinese sturgeon Acipenser sinensis . Theriogenology 94, 37–47.CrossRefGoogle ScholarPubMed
Yoshizaki, G., Okutsu, T., Morita, T., Terasawa, M., Yazawa, R. & Takeuchi, Y. (2012). Biological characteristics of fish germ cells and their application to developmental biotechnology. Reprod. Domest. Anim. 47, 187–92.CrossRefGoogle ScholarPubMed