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In vitro competitive binding index using fluorochrome-labelled spermatozoa for predicting bull fertility

Published online by Cambridge University Press:  25 June 2010

R. Puglisi*
Affiliation:
Istituto Sperimentale Italiano ‘L. Spallanzani’, Loc. La Quercia, 26027 Rivolta d'Adda (CR), Italy.
L. Krvavac
Affiliation:
Istituto Sperimentale Italiano ‘L. Spallanzani’, Loc. La Quercia, 26027 Rivolta d'Adda (CR), Italy.
C. Bonacina
Affiliation:
Istituto Sperimentale Italiano ‘L. Spallanzani’, Loc. La Quercia, 26027 Rivolta d'Adda (CR), Italy.
A. Galli
Affiliation:
Istituto Sperimentale Italiano ‘L. Spallanzani’, Loc. La Quercia, 26027 Rivolta d'Adda (CR), Italy.
*
All correspondence to: Roberto Puglisi. Istituto Sperimentale Italiano ‘L. Spallanzani’, Loc. La Quercia, 26027 Rivolta d'Adda (CR), Italy. Tel: +39 03637888. Fax: +39 0363 371021. e-mail: [email protected]

Summary

This work evaluated if an in vitro test, with the combined power of the statistical evaluation of spermatozoa and zona pellucida (ZP) competitive binding ability and a rapid method for accessory sperm counts, could predict the bull fertility. Ten Holstein Friesian bulls of known field fertility (five of high and five of low fertility) were selected. An in vitro heterospermic insemination approach, based on differential staining, was tested on 45 possible pairs of bulls (two batches per bull). Motility and quality (abnormalities and membrane status) seminal characteristics and estimated relative conception rates (ERCR) highlighted only one association between membrane integrity and ERCR (p = 0.007). Differences in ZP binding allowed us to rank bulls into two categories based on low and high binding ability. For eight bulls, this classification reflected the ERCR. Differences between batches were reported for two bulls, in which the effect of heterospermic insemination (the number of sperm binding to ZP from different bulls not in a 1:1 ratio) showed a significant bull-related effect (p < 0.001) in the first batch and no effect (p > 0.05) in the second batch for both bulls. Reduction of the number of oocytes per assay from 25 to 5 had no effect (p > 0.5) on the bulls’ ranking. Our results suggest that in vitro competitive binding is a promising approach for estimating bull fertility and support concepts for further implementation, e.g. drastic reduction of oocyte number in a single pair assay and larger scale testing for batches.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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References

Amann, R. (1989). Can the fertility potential of a semen sample be predicted accurately? J. Androl. 10, 8998.CrossRefGoogle Scholar
Beatty, R.A., Bennett, G.H., Hall, J.G., Hancock, J.L. & Stewart, D.L. (1969). An experiment with heterospermic insemination in cattle. J. Reprod. Fertil. 19, 491502.CrossRefGoogle Scholar
Berger, T. (1995). Proportion of males with lower fertility spermatozoa estimated from heterospermic insemination. Theriogenology 43, 769–75.CrossRefGoogle ScholarPubMed
Berger, T. & Dally, M. (2001). Do sire-dam interactions contribute significantly to fertility comparisons in heterospermic insemination trials? Theriogenology 56, 535–43.CrossRefGoogle ScholarPubMed
Boichard, D., Barbat, A. & Briend, M. (2002). Evaluation génétique des caractères de fertilité femelle chez les bovins laitiers. In: Association Pour l’Étude de la Reproduction animale, Journée Reproduction, Génétique et Performances. Paris, France, pp. 59.Google Scholar
Bousquet, D., Bouchard, E. & Du Tremblay, D. (2004). Decreasing fertility in dairy cows: myth or realty? Med. Vet. Quebec 34, 5961.Google Scholar
Braundmeier, A.G., Demers, J.M., Shanks, R.D., Saacke, R.G. & Miller, D.J. (2002). Examination of the binding ability of bovine spermatozoa to the zona pellucida as an indicator of fertility. J. Androl. 23, 645–51.CrossRefGoogle Scholar
Butler, W.R. (1998). Effect of protein nutrition on ovarian and uterine physiology in dairy cattle. J. Dairy Sci. 81, 2533–39.CrossRefGoogle ScholarPubMed
Clay, J.S. & McDaniel, B.T. (2001). Computing mating bull fertility from DHI nonreturn data. J. Dairy Sci. 84, 1238–45.CrossRefGoogle ScholarPubMed
Crawley, M.J. (2007). The R Book. John Wiley, New York.CrossRefGoogle Scholar
Den Daas, J.H.G. (1992). Laboratory assessment of semen characteristics. Anim. Reprod. Sci. 28, 8794.CrossRefGoogle Scholar
Den Daas, J.H.G. (1997). Prediction of Bovine Male Fertility. Doctoral Thesis, Lantbouwuniversiteit te Wageningen, The Netherlands.Google Scholar
Evans, R.D., Dillon, P., Buckley, F., Berry, D.P., Wallace, M., Ducrocq, V. & Garrick, D.J. (2006). Trends in milk production, calving rate and survival of cows in 14 Irish dairy herds as a result of the introgression of Holstein-Friesian genes. Anim. Sci. 82, 423–33.CrossRefGoogle Scholar
Farrell, P.B., Presicce, G.A., Brockett, C.C. & Foote, R.H. (1998). Quantification of bull sperm characteristics measured by computer-assisted sperm analysis_CASA and the relationship to fertility. Theriogenology 49, 871–79.CrossRefGoogle Scholar
Fazeli, A.R., Zhang, B.R., Steenweg, W., Larsson, B., Bevers, M.M., Van Den Broek, J., Rodriguez-Martinez, H. & Colenbrander, B. (1997). Relationship between sperm–zona pellucida binding assays and the 56-day nonreturn rate of cattle inseminated with frozen–thawed bull semen. Theriogenology 48, 853–63.CrossRefGoogle ScholarPubMed
Flint, A.F., Chapman, P.L. & Seidel, G.E. (2003). Fertility assessment through heterospermic insemination of flow-sorted sperm in cattle. J. Anim. Sci. 81, 1814–22.CrossRefGoogle ScholarPubMed
Flint, A.P.F., Ahmad, S. & Derecka, K. (2009). Genetic selection for fertility. Cattle Practice 17, 14.Google Scholar
Franken, D.R., Lombard, C.J., Acosta, A.A., Oehninger, A., Kruger, T.F. & Hodgen, G.D. (1993). The hemizona assay: its role in identifying male factor infertility in assistant reproduction. Fertil. Steril. 59, 1075–80.CrossRefGoogle Scholar
Galli, A., Bornaghi, V., Basetti, M., Martignoni, M., Balduzzi, D. & Moretti, M. (1990). Maximizing frozen bovine semen production at an artificial insemination centre. Theriogenology 34, 1129–37.CrossRefGoogle Scholar
Galli, C., Crotti, G., Notari, C., Turini, P., Duchi, R. & Lazzari, G. (2001). Embryo production by ovum pick up from live donors. Theriogenology 55, 1341–57.CrossRefGoogle ScholarPubMed
Gillan, L., Kroetsch, T., Chis Maxwell, W.M. & Evans, G. (2008). Assessment of in vitro sperm characteristics in relation to fertility in dairy bulls, Anim. Reprod. Sci. 103 (3–4), 201–14.CrossRefGoogle ScholarPubMed
Giritharan, G., Ramakrishnappa, N., Balendran, A., Cheng, K.M. & Rajamahendran, R. (2005). Development of in vitro tests to predict fertility of bulls. Can. J. Anim. Sci. 85, 4752.CrossRefGoogle Scholar
Hallap, T., Nagy, S., Jaakma, U., Johannisson, A. & Rodriguez-Martinez, H. (2006). Usefulness of a triple fluorochrome combination merocyanine 540/Yo-Pro 1/Hoechst 33342 in assessing membrane stability of viable frozen–thawed spermatozoa from Estonian Holstein AI bulls. Theriogenology 65, 1122–36.CrossRefGoogle ScholarPubMed
Hammerstedt, R.H. (1996). Evaluation of sperm quality: identification of the subfertile male and courses of action. Anim. Reprod. Sci. 42, 7787.CrossRefGoogle Scholar
Harrison, R.O., Ford, S.P., Young, J.W., Conley, A.J. & Freeman, A.E. (1990). Increased milk production versus reproductive and energy status of high producing dairy cows. J. Dairy Sci. 73, 2749–58.CrossRefGoogle ScholarPubMed
Henault, M.A. & Killian, G.J. (1994). Effects of sperm preparation and bull fertility on in vitro penetration of zona-free bovine oocytes. Theriogenology 43, 739–49.CrossRefGoogle Scholar
Hermansson, U., Axnér, E. & Ström Holst, B. (2007). Application of a zona pellucida binding assay (ZBA) in the domestic cat benefits from the use of in vitro matured oocytes. Acta Vet. Scand. doi: 10.1186/1751–0147–49–28.CrossRefGoogle Scholar
Januskauskas, A., Johannisson, A. & Rodriguez-Martinez, H. (2003). Subtle membrane changes in cryopreserved bull semen in relation with sperm viability, chromatin structure, and field fertility. Theriogenology 60, 743–58.CrossRefGoogle ScholarPubMed
Kastelic, J.P. & Thundathil, J.C. (2008). Breeding soundness evaluation and semen analysis for predicting bull fertility. Reprod. Domest. Anim. 43, 368–73.CrossRefGoogle ScholarPubMed
Kerby, M., (2009). The reproductive performance of 42 commercial dairy herds in the southwest of England in 2006/2007 – observations, lessons learnt and thoughts for the future. Cattle Practice 17, 2632.Google Scholar
Lucas, X., Martìnez, E.A., Roca, J., Vàzquez, J.M., Gil, M.A., Pastor, L.M. & Alabart, J.L. (2003). Influence of follicle size on the penetrability of immature pig oocytes for homologous in vitro penetration assay. Theriogenology 60, 659–70.CrossRefGoogle ScholarPubMed
Lucy, M.C. (2001). Reproductive loss in high-producing dairy cattle: where will it end? J. Dairy Sci. 84, 1277–91.CrossRefGoogle ScholarPubMed
Maas, J.A., Garnsworthy, P.C. & Flint, A.P.F. (2009). Modelling responses to nutritional, endocrine and genetic strategies to increase fertility in the UK dairy herd. Vet. J. 180, 356–62.CrossRefGoogle ScholarPubMed
Magerkurth, C., Töpfer-Petersen, E., Schwartz, P. & Michelmann, H.W. (1999). Scanning electron microscopy analysis of the human zona pellucida: influence of maturity and fertilization on morphology and sperm binding pattern. Hum. Reprod. 14, 1057–66.CrossRefGoogle ScholarPubMed
Marco-Jiménez, F. & Vicente, J. (2004). Ability of frozen-thawed ram spermatozoa to bind to vitrified homologous oocytes. Span. J. Agric. Res. 2, 7377.CrossRefGoogle Scholar
Martin, P.A. & Dziuk, P.J. (1977). Assessment of relative fertility of males (cockerels and boars) by competitive mating. J. Reprod. Fertil. 49, 323–29.CrossRefGoogle ScholarPubMed
Mehmood, A., Anwar, M. & Naqvi, S.M.S. (2009). Motility, acrosome integrity, membrane integrity and oocyte cleavage rate of sperm separated by swim-up or Percoll gradient method from frozen–thawed buffalo semen. Anim. Reprod. Sci. 111, 141–48.CrossRefGoogle ScholarPubMed
Miller, D.J., Demers, J.M., Braundmeier, A.G., Behrens, M.L. (1998). The use of two fluorescent dyes to identify sperm in a competitive binding assay to oocytes. J. Androl. 19, 650–56.CrossRefGoogle Scholar
Niu, Y., Greube, A., Ji, W. & Jewgenow, K. (2006). The application of in vitro sperm competition test to evaluate the impact of ZP-derived peptides on fertilization capacity of cat sperm. Theriogenology 66, 989–95.CrossRefGoogle ScholarPubMed
Otoi, T., Tachikaw, S., Kondo, S. & Suzuki, T. (1993). Effects of different lots of semen from the same bull on in vitro development of bovine oocytes fertilized in vitro. Theriogenology 39, 713–18.CrossRefGoogle ScholarPubMed
Pace, M.M., Sullivan, J.J., Elliot, F.I., Graham, E.F. & Coulter, G.H. (1981). Effects of thawing temperature, number of spermatozoa and spermatozoal quality on fertility of bovine spermatozoa packaged in .5-ml french straws. J. Anim. Sci. 53, 693701.CrossRefGoogle Scholar
Parrish, J.J. & Foote, R.H. (1985). Fertility differences among male rabbits determined by heterospermic insemination of fluorochrome-labeled spermatozoa. Biol. Reprod. 33, 940–49.CrossRefGoogle ScholarPubMed
Phillips, N.J., Mcgowan, M.R., Johnston, S.D. & Mayer, D.G. (2004). Relationship between thirty post-thaw spermatozoal characteristics and the field fertility of 11 high-use Australian dairy AI sires. Anim. Reprod. Sci. 80, 4761.CrossRefGoogle Scholar
Pollott, G.E. & Coffey, M.P. (2008). The effect of genetic merit and production system on dairy cow fertility, measured using progesterone profiles and on-farm recording. J. Dairy Sci. 91, 3649–60.CrossRefGoogle ScholarPubMed
Rosenkrans, C.F. Jr, Zeng, G.Q., McNamara, G.T., Schoff, P.K. & First, N.L. (1993). Development of bovine embryos in vitro as affected by energy substrates. Biol. Reprod. 49, 459–62.CrossRefGoogle ScholarPubMed
Royal, M.D., Smith, R.F. & Friggens, N.C. (2008). Fertility in dairy cows: bridging the gaps. Animal 2, 1101–03.CrossRefGoogle ScholarPubMed
Saacke, R.G., Dalton, J.C., Nadir, S., Nebel, R.L. & Bame, J.H. (2000). Relationship of seminal traits and insemination time to fertilization rate and embryo quality. Anim. Reprod. Sci. 60–61, 663–77.CrossRefGoogle ScholarPubMed
Saacke, R.G., Nadir, S. & Nebel, R.L. (1994). Relationships of semen quality to sperm transport, fertilization and embryo quality in ruminants. Theriogenology 41, 4550.CrossRefGoogle Scholar
Seidel, G.E. Jr, Schenk, J.L., Herickhoff, L.A., Doyle, S.P., Brink, Z., Greenm, R.D. & Cran, D.G. (1999). Insemination of heifers with sexed sperm. Theriogenology 52, 1407–20.CrossRefGoogle ScholarPubMed
Stahlberg, R., Harhzius, B., Weitze, K.F. & Waberskila, D. (2000). Identification of embryo paternity using polymorphic DNA markers to assess fertilizing capacity of spermatozoa after heterospermic insemination in boars. Theriogenology 53, 1365–73.CrossRefGoogle ScholarPubMed
Ström Holst, B., Larsson, B., Linde-Forsberg, C. & Rodriguez-Martinez, H. (2000). Evaluation of chilled and frozen–thawed canine spermatozoa using a zona pellucida binding assay. J. Reprod. Fertil. 119, 201–06.CrossRefGoogle ScholarPubMed
Wall, E., Brotherstone, S., Kearney, J.F., Woolliams, J.A. & Coffey, M.P. (2005). Impact of nonadditive genetic effects in the estimation of breeding values for fertility and correlated traits. J. Dairy Sci. 88, 376–85.CrossRefGoogle ScholarPubMed
Wall, E., Brotherstone, S., Woolliams, J.A., Banos, G. & Coffey, M.P. (2003). Genetic evaluation of fertility using direct and correlated traits. J. Dairy Sci. 86, 4093–102.CrossRefGoogle ScholarPubMed
Winding, J.J., Calus, M.P.L., Beerda, B. & Veerkamp, R.F. (2006). Genetic correlations between milk production and health and fertility depending upon a herd environment. J. Dairy Sci. 89, 1765–75.CrossRefGoogle Scholar
Yániz, J., López-Gatius, F., Bech-Sàbat, G., García-Ispierto, I., Serrano, B. & Santolaria, P. (2008). Relationships between milk production, ovarian function and fertility in high-producing dairy herds in north-eastern Spain. Reprod. Domest. Anim. 43, 3843.CrossRefGoogle ScholarPubMed
Zhang, B.R., Larsson, B., Lundeheim, N., Håård, M.G.H. & Rodriguez-Martinez, H. (1999). Prediction of bull fertility by combined in vitro assessments of frozen–thawed semen from young dairy bulls entering an AI-programme. Int. J. Androl. 22, 253–60.CrossRefGoogle ScholarPubMed
Zhang, B.R., Larsson, B., Lundeheim, N. & Rodriguez-Martinez, H. (1997). Relationship between embryo development in vitro and 56-day nonreturn rates of cows inseminated with frozen–thawed semen from dairy bulls. Theriogenology 48, 221–31.CrossRefGoogle ScholarPubMed
Zhang, B.R., Larsson, B., Lundeheim, N. & Rodriguez-Martinez, H. (1998a). Sperm characteristics and zona pellucida binding in relation to field fertility of frozen–thawed semen from dairy AI bulls. Int. J. Androl. 21, 207–16.CrossRefGoogle ScholarPubMed
Zhang, B.R., Larsson, B. & Rodriguez-Martinez, H. (1995). Influence of batches of bovine oocytes on the outcome of an intact zona pellucida binding assay and in vitro fertilization. Int. J. Androl. 18, 213–20.CrossRefGoogle ScholarPubMed
Zhang, B.R., Larsson, B. & Rodriguez-Martinez, H. (1998b). The effect of ejaculates on the in vitro and in vivo fertility of young AI bulls. In Gametes: Development and Function. (eds Lauria, A., Gandolfi, F., Enne, G. & Gianaroli, L.) 623 pp. Rome: Serono Symposia.Google Scholar