Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effect of inbreeding depression on bull sperm quality and field fertility

Jesús Dorado A , Rosa Morales Cid B , Antonio Molina B , Manuel Hidalgo A , Julia Ariza C , Miguel Moreno-Millán B and Sebastián Demyda-Peyrás D E
+ Author Affiliations
- Author Affiliations

A Department of Animal Medicine and Surgery, University of Cordoba, CN IV KM 396 – Campus Rabanales, Fco. Santisteban building, CP 14071, Cordoba, Spain.

B Department of Genetics, University of Cordoba, CN IV KM 396 – Campus Rabanales, Gregor Mendel Building, CP 14071, Cordoba, Spain.

C Department of Cell Biology, Physiology and Immunology, University of Cordoba, CN IV KM 396 – Campus Rabanales. Gregor Mendel Building. CP 14071. Cordoba, Spain.

D Instituto de Genetica Veterinaria (IGEVET), CCT La Plata, CONICET – Facultad de Ciencias Veterinarias – Universidad de La Plata, Buenos Aires, Argentina.

E Corresponding author. Email: sebass@uco.es

Reproduction, Fertility and Development 29(4) 712-720 https://doi.org/10.1071/RD15324
Submitted: 7 August 2015  Accepted: 9 November 2015   Published: 18 December 2015

Abstract

The present study investigated the effect of inbreeding depression on sperm quality using automated and objective methods and subsequent effects on beef bull field fertility. Individual inbreeding coefficient (F) values and field fertility data were determined using a dataset of AI bulls belonging to the Spanish Retinta Breeders Association (Asociación Nacional de Criadores de Ganado Vacuno Selecto de Raza Retinta (ANCRE)). Animals were clustered in two groups according to the F values as follows: (1) a high inbreeding group (HI; F ≥ 13.5%, mean 16.3); and (2) a non-inbreeding group (NI; F = 0%). In total, 17 different assessments were performed in both experimental groups, including evaluation of sperm morphology, acrosomal and DNA status, sperm plasma membrane integrity and function (hypo-osmotic swelling test), 10 kinetic parameters and the structure of sperm subpopulations. Sperm morphology, acrosomal and DNA status and osmotic tolerance were similar in both groups. Three velocity parameters (curvilinear velocity, straight line velocity and average path velocity) and the amplitude of lateral head displacement were higher in HI (P < 0.05). Cluster analysis of kinematic parameters revealed three different sperm subpopulations (sP1, sP2 and sP3), with the proportion of the sP1 population (highly active but non-progressive spermatozoa) being significantly (P < 0.05) higher in the HI group. Field fertility was assessed using two calving record datasets. In a smaller database including only bulls evaluated in the present study, there was a significant increase in the calving interval of cows sired with HI bulls. Conversely, in an extended genetic analysis of the ANCRE database, inbreeding only explained a small part of the variation in calving interval, and the results of regression analysis were not significant among bulls. The findings of the present study suggest that high inbreeding levels have a moderate effect on bull semen quality, with an increased percentage of highly active but non-progressive spermatozoa, but only when F values reached a certain threshold. This motility pattern could explain, in part, the higher calving interval produced by inbred bulls under field conditions.

Additional keywords: calving interval, cattle, computer-aided sperm analysis (CASA), DNA fragmentation, genetic trait, sperm function, sperm morphology, sperm subpopulations.


References

Amann, R. P. (1989). Can the fertility potential of a seminal sample be predicted accurately? J. Androl. 10, 89–98.
| 1:STN:280:DyaL1M3jtl2ksA%3D%3D&md5=737cf88e57fc9d0419bfb38f84c85137CAS | 2715106PubMed |

Asa, C., Miller, P., Agnew, M., Rebolledo, J. A. R., Lindsey, S. L., Callahan, M., and Bauman, K. (2007). Relationship of inbreeding with sperm quality and reproductive success in Mexican gray wolves. Anim. Conserv. 10, 326–331.
Relationship of inbreeding with sperm quality and reproductive success in Mexican gray wolves.Crossref | GoogleScholarGoogle Scholar |

Brito, L. F., Silva, A. E., Rodrigues, L. H., Vieira, F. V., Deragon, L. A., and Kastelic, J. P. (2002). Effects of environmental factors, age and genotype on sperm production and semen quality in Bos indicus and Bos taurus AI bulls in Brazil. Anim. Reprod. Sci. 70, 181–190.
Effects of environmental factors, age and genotype on sperm production and semen quality in Bos indicus and Bos taurus AI bulls in Brazil.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD383gvFamtA%3D%3D&md5=f2bda3146fdac22ada3a913fd7cf6ea4CAS | 11943488PubMed |

Cancel, A. M. (2000). Objective evaluation of hyperactivated motility in rat spermatozoa using computer-assisted sperm analysis. Hum. Reprod. 15, 1322–1328.
Objective evaluation of hyperactivated motility in rat spermatozoa using computer-assisted sperm analysis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3ptlagsQ%3D%3D&md5=4d5180e0c51aeccb46c7bebeb6345a81CAS | 10831563PubMed |

Carey, J. E., and Olds-Clarke, P. (1980). Differences in sperm function in vitro but not in vivo between inbred and random-bred mice. Gamete Res. 3, 9–15.
Differences in sperm function in vitro but not in vivo between inbred and random-bred mice.Crossref | GoogleScholarGoogle Scholar |

Carvajal-Rodriguez, A., and de Uña-Alvarez, J. (2011). Assessing significance in high-throughput experiments by sequential goodness of fit and q-value estimation. PLoS One 6, e24700.
Assessing significance in high-throughput experiments by sequential goodness of fit and q-value estimation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Gju7nO&md5=63d176e84e0f707bc92b12fbda7aafedCAS | 21931819PubMed |

Cassinello, J., Abaigar, T., Gomendio, M., and Roldan, E. R. (1998). Characteristics of the semen of three endangered species of gazelles (Gazella dama mhorr, G. dorcas neglecta and G. cuvieri). J. Reprod. Fertil. 113, 35–45.
Characteristics of the semen of three endangered species of gazelles (Gazella dama mhorr, G. dorcas neglecta and G. cuvieri).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsVSgtbw%3D&md5=1fd2808d7029255b132527a950204810CAS | 9713374PubMed |

Charlesworth, D., and Willis, J. H. (2009). The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783–796.
The genetics of inbreeding depression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1KrtbrI&md5=feb39dcc9ceae7fde54496a49883e418CAS | 19834483PubMed |

Demyda-Peyras, S., Dorado, J., Hidalgo, M., De Luca, L., Muñoz-Serrano, A., and Moreno-Millan, M. (2012). In vitro induction of the acrosome reaction in spermatozoa from endangered spanish bulls: effect of breed, culture media and incubation time. Livest. Sci. 149, 275–281.
In vitro induction of the acrosome reaction in spermatozoa from endangered spanish bulls: effect of breed, culture media and incubation time.Crossref | GoogleScholarGoogle Scholar |

Dorado, J., Acha, D., Ortiz, I., Gálvez, M. J., Carrasco, J. J., Díaz, B., Gómez-Arrones, V., Calero-Carretero, R., and Hidalgo, M. (2013). Relationship between conventional semen characteristics, sperm motility patterns and fertility of andalusian donkeys (Equus asinus). Anim. Reprod. Sci. 143, 64–71.
Relationship between conventional semen characteristics, sperm motility patterns and fertility of andalusian donkeys (Equus asinus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c7ks1alsA%3D%3D&md5=a812ac9d66a9d7a6b09d983ea2c9f496CAS | 24210876PubMed |

Ducrocq, V., and Humblot, P. (1995). Genetic characteristics and evolution of semen production of young Normande bulls. Livest. Prod. Sci. 41, 1–10.
Genetic characteristics and evolution of semen production of young Normande bulls.Crossref | GoogleScholarGoogle Scholar |

Enciso, M., Cisale, H., Johnston, S. D., Sarasa, J., Fernandez, J. L., and Gosalvez, J. (2011a). Major morphological sperm abnormalities in the bull are related to sperm DNA damage. Theriogenology 76, 23–32.
Major morphological sperm abnormalities in the bull are related to sperm DNA damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntFKiur4%3D&md5=0a453bf605eb47a7c213fca67ef11411CAS | 21529921PubMed |

Enciso, M., Johnston, S. D., and Gosalvez, J. (2011b). Differential resistance of mammalian sperm chromatin to oxidative stress as assessed by a two-tailed comet assay. Reprod. Fertil. Dev. 23, 633–637.
Differential resistance of mammalian sperm chromatin to oxidative stress as assessed by a two-tailed comet assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvVWqur8%3D&md5=95cc4c7fe40e0bc70252a93711129827CAS | 21635811PubMed |

Evenson, D., and Jost, L. (2000). Sperm chromatin structure assay is useful for fertility assessment. Methods Cell Sci. 22, 169–189.
Sperm chromatin structure assay is useful for fertility assessment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXivVOhsbw%3D&md5=fcc3e04ca76159fa1136af8034b04b74CAS | 11264952PubMed |

Flade, D., and Zeller, K. (1992). Examination of the spermatozoa vitality and morphology on frozen semen from inbred bulls compared with noninbred half brothers. Arch. Tierz. 35, 327–333.

Gage, M. J. G., Surridge, A. K., Tomkins, J. L., Green, E., Wiskin, L., Bell, D. J., and Hewitt, G. M. (2006). Reduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus. Curr. Biol. 16, 612–617.
Reduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1ehtbw%3D&md5=e698b9612df11eb9f825f4164857d3a2CAS |

Gandini, G., Stella, A., Del Corvo, M., and Jansen, G. B. (2014). Selection with inbreeding control in simulated young bull schemes for local dairy cattle breeds. J. Dairy Sci. 97, 1790–1798.
Selection with inbreeding control in simulated young bull schemes for local dairy cattle breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXis1Cntbs%3D&md5=a913c311d8311d701b42dcfb4b50b98fCAS | 24440254PubMed |

Garde, J. J., Soler, A. J., Cassinello, J., Crespo, C., Malo, A. F., Espeso, G., Gomendio, M., and Roldan, E. R. (2003). Sperm cryopreservation in three species of endangered gazelles (Gazella cuvieri, G. dama mhorr, and G. dorcas neglecta). Biol. Reprod. 69, 602–611.
Sperm cryopreservation in three species of endangered gazelles (Gazella cuvieri, G. dama mhorr, and G. dorcas neglecta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVerurY%3D&md5=40eba5b04b2f03ed829066a577b0e6a5CAS | 12700201PubMed |

Gil, J., Januskauskas, A., Haard, M., Haard, M., Johanisson, A., Soderquist, L., and Rodriguez-Martinez, H. (2000). Functional sperm parameters and fertility of bull semen extended in Biociphos-plus® and triladyl®. Reprod. Domest. Anim. 35, 69–77.
Functional sperm parameters and fertility of bull semen extended in Biociphos-plus® and triladyl®.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlGlsb0%3D&md5=329ce63bd73dac08ca499b4e0558af5aCAS |

Godfrey, R. W., and Dodson, R. E. (2005). Breeding soundness evaluations of senepol bulls in the US virgin islands. Theriogenology 63, 831–840.
Breeding soundness evaluations of senepol bulls in the US virgin islands.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M%2FgsFSitw%3D%3D&md5=299eeb438cfde9408398e21d415dd8b5CAS | 15629801PubMed |

Gomendio, M., Cassinello, J., and Roldan, E. R. S. (2000). A comparative study of ejaculate traits in three endangered ungulates with different levels of inbreeding: fluctuating asymmetry as an indicator of reproductive and genetic stress. Proc. R. Soc. B Biol. Sci. 267, 875–882.
A comparative study of ejaculate traits in three endangered ungulates with different levels of inbreeding: fluctuating asymmetry as an indicator of reproductive and genetic stress.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvnsVCntA%3D%3D&md5=d21d6b84e0660c2232d4cfeebeff7ffbCAS |

González-Recio, O., López de Maturana, E., and Gutiérrez, J. P. (2007). Inbreeding depression on female fertility and calving ease in Spanish dairy cattle. J. Dairy Sci. 90, 5744–5752.
Inbreeding depression on female fertility and calving ease in Spanish dairy cattle.Crossref | GoogleScholarGoogle Scholar | 18024768PubMed |

Gutierrez, J. P., and Goyache, F. (2005). A note on endog: a computer program for analysing pedigree information. J. Anim. Breed. Genet. 122, 172–176.
A note on endog: a computer program for analysing pedigree information.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2Mvmtlajsg%3D%3D&md5=ae576f3f9258cafec93e3175c1169019CAS | 16130468PubMed |

Hansen, L. B. (2000). Consequences of selection for milk yield from a geneticist’s viewpoint. J. Dairy Sci. 83, 1145–1150.
Consequences of selection for milk yield from a geneticist’s viewpoint.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsVWksL8%3D&md5=42b4efa78f327ef8af34dab2c65353c3CAS | 10821591PubMed |

Hidalgo, M., and Dorado, J. (2009). Objective assessment of goat sperm head size by computer-assisted sperm morphometry analysis (ASMA). Small Rumin. Res. 87, 108–110.
Objective assessment of goat sperm head size by computer-assisted sperm morphometry analysis (ASMA).Crossref | GoogleScholarGoogle Scholar |

Karoui, S., Díaz, C., Serrano, M., Cue, R., Celorrio, I., and Carabaño, M. J. (2011). Time trends, environmental factors and genetic basis of semen traits collected in holstein bulls under commercial conditions. Anim. Reprod. Sci. 124, 28–38.
Time trends, environmental factors and genetic basis of semen traits collected in holstein bulls under commercial conditions.Crossref | GoogleScholarGoogle Scholar | 21377297PubMed |

Karoui, S., Díaz, C., González-Marín, C., Amenabar, M. E., Serrano, M., Ugarte, E., Gosálvez, J., Roy, R., López-Fernández, C., and Carabaño, M. J. (2012). Is sperm DNA fragmentation a good marker for field AI bull fertility? J. Anim. Sci. 90, 2437–2449.
Is sperm DNA fragmentation a good marker for field AI bull fertility?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlSgs77N&md5=690c616a00d36243fea3822d7b69da21CAS | 22367070PubMed |

Kathiravan, P., Kalatharan, J., Karthikeya, G., Rengarajan, K., and Kadirvel, G. (2011). Objective sperm motion analysis to assess dairy bull fertility using computer-aided system: a review. Reprod. Domest. Anim. 46, 165–172.
Objective sperm motion analysis to assess dairy bull fertility using computer-aided system: a review.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itlOgtQ%3D%3D&md5=11fee8c5ea489a8eb33bd50be436d3e8CAS | 20403134PubMed |

Keller, L. F., and Waller, D. M. (2002). Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230–241.
Inbreeding effects in wild populations.Crossref | GoogleScholarGoogle Scholar |

Kristensen, T. N., Pedersen, K. S., Vermeulen, C. J., and Loeschcke, V. (2010). Research on inbreeding in the ‘omic’ era. Trends Ecol. Evol. 25, 44–52.
Research on inbreeding in the ‘omic’ era.Crossref | GoogleScholarGoogle Scholar | 19733933PubMed |

Lacy, R. C. (1997). Importance of genetic variation to the viability of mammalian populations. J. Mammal. 78, 320–335.
Importance of genetic variation to the viability of mammalian populations.Crossref | GoogleScholarGoogle Scholar |

Leberg, P. L., and Firmin, B. D. (2008). Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol. Ecol. 17, 334–343.
Role of inbreeding depression and purging in captive breeding and restoration programmes.Crossref | GoogleScholarGoogle Scholar | 18173505PubMed |

Legarra, A., Varona, L., and López de Maturana, E. (2008). ‘TM & GS3 & BLUP_GEN & BLUP_SNP. Software for Threshold and Censored Models, and Genomic Selection.’ Available at http://snp.toulouse.inra.fr/~alegarra [verified 23 November 2015].

Leroy, G. (2014). Inbreeding depression in livestock species: review and meta-analysis. Anim. Genet. 45, 618–628.
Inbreeding depression in livestock species: review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cfns1Smuw%3D%3D&md5=6e0bbc6c9ca5d11625322daf1d10eeabCAS | 24975026PubMed |

Losdat, S., Chang, S. M., and Reid, J. M. (2014). Inbreeding depression in male gametic performance. J. Evol. Biol. 27, 992–1011.
Inbreeding depression in male gametic performance.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cjitVSlsw%3D%3D&md5=3df67a4c7d3de2719e47f84007338720CAS | 24820115PubMed |

Mackinnon, M. J., Taylor, J. F., and Hetzel, D. J. (1990). Genetic variation and covariation in beef cow and bull fertility. J. Anim. Sci. 68, 1208–1214.
| 1:STN:280:DyaK3czgslGksw%3D%3D&md5=311e5429d49fbab36ab7bcc584b9df7cCAS | 2365639PubMed |

Malo, A. F., Martinez-Pastor, F., Alaks, G., Dubach, J., and Lacy, R. C. (2010). Effects of genetic captive-breeding protocols on sperm quality and fertility in the white-footed mouse. Biol. Reprod. 83, 540–548.
Effects of genetic captive-breeding protocols on sperm quality and fertility in the white-footed mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1ahtr7O&md5=cf272d9aac51f22d7d324c94222ee644CAS | 20519695PubMed |

Martinez-Pastor, F., Garcia-Macias, V., Alvarez, M., Herraez, P., Anel, L., and De Paz, P. (2005). Sperm subpopulations in Iberian red deer epididymal sperm and their changes through the cryopreservation process. Biol. Reprod. 72, 316–327.
Sperm subpopulations in Iberian red deer epididymal sperm and their changes through the cryopreservation process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXptFGmtA%3D%3D&md5=c3b36ca238e664c8e6b0132cb4747359CAS | 15385419PubMed |

Martz, E. (1992–2001). ‘MFI: a Flow Cytometry List Mode Data Analysis Program Optimized for Batch Processing Under MS-DOS.’ Available at http://www.umass.edu/microbio/mfi [verified 23 November 2015].

Mathevon, M., Buhr, M. M., and Dekkers, J. C. (1998). Environmental, management, and genetic factors affecting semen production in holstein bulls. J. Dairy Sci. 81, 3321–3330.
Environmental, management, and genetic factors affecting semen production in holstein bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvVansw%3D%3D&md5=ac8a7005cce9b7672e838cb830955953CAS | 9891279PubMed |

Maximini, L., Fuerst-Waltl, B., Gredler, B., and Baumung, R. (2011). Inbreeding depression on semen quality in Austrian dual-purpose simmental bulls. Reprod. Domest. Anim. 46, e102–e104.
Inbreeding depression on semen quality in Austrian dual-purpose simmental bulls.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itl2ltw%3D%3D&md5=22e036cac8f33bc8583d579ac44344bdCAS | 20546181PubMed |

McParland, S., Kearney, F., and Berry, D. P. (2009). Purging of inbreeding depression within the Irish holstein–friesian population. Genet. Sel. Evol. 41, 16.
Purging of inbreeding depression within the Irish holstein–friesian population.Crossref | GoogleScholarGoogle Scholar |

Muiño, R., Tamargo, C., Hidalgo, C. O., and Peña, A. I. (2008). Identification of sperm subpopulations with defined motility characteristics in ejaculates from holstein bulls: effects of cryopreservation and between-bull variation. Anim. Reprod. Sci. 109, 27–39.
Identification of sperm subpopulations with defined motility characteristics in ejaculates from holstein bulls: effects of cryopreservation and between-bull variation.Crossref | GoogleScholarGoogle Scholar | 18036750PubMed |

Nishizono, H., Shioda, M., Takeo, T., Irie, T., and Nakagata, N. (2004). Decrease of fertilizing ability of mouse spermatozoa after freezing and thawing is related to cellular injury. Biol. Reprod. 71, 973–978.
Decrease of fertilizing ability of mouse spermatozoa after freezing and thawing is related to cellular injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFeju7k%3D&md5=70cec24da48a01afd4052ba4425e49acCAS | 15151925PubMed |

O’Grady, J. J., Brook, B. W., Reed, D. H., Ballou, J. D., Tonkyn, D. W., and Frankham, R. (2006). Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol. Conserv. 133, 42–51.
Realistic levels of inbreeding depression strongly affect extinction risk in wild populations.Crossref | GoogleScholarGoogle Scholar |

Olds-Clarke, P., and Wivell, W. (1992). Impaired transport and fertilization in vivo of calcium-treated spermatozoa from +/+ or congenic t(w32)/+ mice. Biol. Reprod. 47, 621–628.
Impaired transport and fertilization in vivo of calcium-treated spermatozoa from +/+ or congenic t(w32)/+ mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtlSqur4%3D&md5=40c4dd260f6b7e3f8cd22b07ca32c573CAS | 1391349PubMed |

Persson, Y., and Soderquist, L. (2005). The proportion of beef bulls in Sweden with mature spermiograms at 11–13 months of age. Reprod. Domest. Anim. 40, 131–135.
The proportion of beef bulls in Sweden with mature spermiograms at 11–13 months of age.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M7ovVGqsA%3D%3D&md5=ccbf6def3c3a524b09e0d3c11d1640b6CAS | 15819962PubMed |

Petrovic, V. C., Maksimovic, N., Petrovic, M. P., Petrovic, M. M., Ilic, Z. Z., Muslic, D. R., and Mikulec, D. P. (2013). Effect of inbreeding on body growth traits and sperm DNA fragmentation level in rams. Anim. Sci. Pap. Rep. 31, 27–33.
| 1:CAS:528:DC%2BC3sXms1Khtbs%3D&md5=f5fdfa40de0e039cd7a60661ca85ac8aCAS |

Pukazhenthi, B. S., Neubauer, K., Jewgenow, K., Howard, J., and Wildt, D. E. (2006). The impact and potential etiology of teratospermia in the domestic cat and its wild relatives. Theriogenology 66, 112–121.
The impact and potential etiology of teratospermia in the domestic cat and its wild relatives.Crossref | GoogleScholarGoogle Scholar | 16644003PubMed |

Revell, S. G., and Mrode, R. A. (1994). An osmotic resistance test for bovine semen. Anim. Reprod. Sci. 36, 77–86.
An osmotic resistance test for bovine semen.Crossref | GoogleScholarGoogle Scholar |

Rodero-Serrano, E., Demyda-Peyrás, S., González-Martinez, A., Rodero-Franganillo, A., and Moreno-Millán, M. (2013). The rob(1;29) chromosome translocation in endangered Andalusian cattle breeds. Livest. Sci. 158, 32–39.
The rob(1;29) chromosome translocation in endangered Andalusian cattle breeds.Crossref | GoogleScholarGoogle Scholar |

Rodriguez-Martinez, H., and Larsson, B. (1998). Assessment of sperm fertilizing ability in farm animals. Acta Agr. Scand. A Anim. Sci. 29, 12–18.

Ruiz-Lopez, M. J., Evenson, D. P., Espeso, G., Gomendio, M., and Roldan, E. R. (2010). High levels of DNA fragmentation in spermatozoa are associated with inbreeding and poor sperm quality in endangered ungulates. Biol. Reprod. 83, 332–338.
High levels of DNA fragmentation in spermatozoa are associated with inbreeding and poor sperm quality in endangered ungulates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyrsrrP&md5=d124a38464a76916c1e3fd8391ab7526CAS | 20505170PubMed |

Rybar, R., Faldikova, L., Faldyna, M., Machatkova, M., and Rubes, J. (2004). Bull and boar sperm DNA integrity evaluated by sperm chromatin structure assay in the Czech Republic. Vet. Med. Czech. 49, 1–8.
| 1:CAS:528:DC%2BD2cXjt1Sqt7o%3D&md5=32cbf131be59edaaf3d9ee8145466b67CAS |

Rybar, R., Kopecka, V., Prinosilova, P., Kubickova, S., Veznik, Z., and Rubes, J. (2010). Fertile bull sperm aneuploidy and chromatin integrity in relationship to fertility. Int. J. Androl. 33, 613–622.
| 1:STN:280:DC%2BC3cnosFajsQ%3D%3D&md5=a2fa8cef93e3d48b392032a8f2eca50aCAS | 19751362PubMed |

Sewalem, A., Kistemaker, G. J., Miglior, F., and Van Doormaal, B. J. (2006). Analysis of inbreeding and its relationship with functional longevity in Canadian dairy cattle. J. Dairy Sci. 89, 2210–2216.
Analysis of inbreeding and its relationship with functional longevity in Canadian dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xlt1eqsLo%3D&md5=0ebe4cc551d3fd92c6de62ce1df8016dCAS | 16702287PubMed |

Shivaji, S., Jayaprakash, D., and Patil, S. B. (1998). Assessment of inbreeding depression in big cats: testosterone levels and semen analysis. Curr. Sci. 75, 923–930.
| 1:CAS:528:DyaK1cXnvVCktbc%3D&md5=f18c38248ff2c27e2d5de6acbbccad58CAS |

Smith, L. A., Cassell, B. G., and Pearson, R. E. (1998). The effects of inbreeding on the lifetime performance of dairy cattle. J. Dairy Sci. 81, 2729–2737.
The effects of inbreeding on the lifetime performance of dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnt1Sms7Y%3D&md5=5fc8fbc09fbc719c029f4b17b04886e7CAS | 9812278PubMed |

Söderquist, L., Janson, L., Håård, M., and Einarsson, S. (1996). Influence of season, age, breed and some other factors on the variation in sperm morphological abnormalities in Swedish dairy A.I. bulls. Anim. Reprod. Sci. 44, 91–98.
Influence of season, age, breed and some other factors on the variation in sperm morphological abnormalities in Swedish dairy A.I. bulls.Crossref | GoogleScholarGoogle Scholar |

Songsasen, N., and Leibo, S. P. (1997). Cryopreservation of mouse spermatozoa II. Relationship between survival after cryopreservation and osmotic tolerance of spermatozoa from three strains of mice. Cryobiology 35, 255–269.
Cryopreservation of mouse spermatozoa II. Relationship between survival after cryopreservation and osmotic tolerance of spermatozoa from three strains of mice.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FjsFKqug%3D%3D&md5=ce4c30c02d88fb8cabaeb761e190bf42CAS | 9367613PubMed |

Sørensen, A. C., Sørensen, M. K., and Berg, P. (2005). Inbreeding in danish dairy cattle breeds. J. Dairy Sci. 88, 1865–1872.
Inbreeding in danish dairy cattle breeds.Crossref | GoogleScholarGoogle Scholar | 15829680PubMed |

Stachowicz, K., Sargolzaei, M., Miglior, F., and Schenkel, F. S. (2011). Rates of inbreeding and genetic diversity in Canadian holstein and jersey cattle. J. Dairy Sci. 94, 5160–5175.
Rates of inbreeding and genetic diversity in Canadian holstein and jersey cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eisb3O&md5=12594d5e3fbb84aa8df37807d7784277CAS | 21943766PubMed |

Thompson, J. R., Everett, R. W., and Hammerschmidt, N. L. (2000). Effects of inbreeding on production and survival in holsteins. J. Dairy Sci. 83, 1856–1864.
Effects of inbreeding on production and survival in holsteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvFersb4%3D&md5=3faa518cd45b689bd82eef59008d8225CAS | 10984163PubMed |

Tier, B. (1990). Computing inbreeding coefficients quickly. Genet. Sel. Evol. 22, 419–430.
Computing inbreeding coefficients quickly.Crossref | GoogleScholarGoogle Scholar |

van Eldik, P., van der Waaij, E. H., Ducro, B., Kooper, A. W., Stout, T. A., and Colenbrander, B. (2006). Possible negative effects of inbreeding on semen quality in Shetland pony stallions. Theriogenology 65, 1159–1170.
Possible negative effects of inbreeding on semen quality in Shetland pony stallions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD287jtFWhug%3D%3D&md5=9994aa3fa0a6f07d1347ea1cfb3ae270CAS | 16165199PubMed |

Verstegen, J. P., Onclin, K., and Iguer-Ouada, M. (2005). Long-term motility and fertility conservation of chilled canine semen using egg yolk added Tris-glucose extender: in vitro and in vivo studies. Theriogenology 64, 720–733.
Long-term motility and fertility conservation of chilled canine semen using egg yolk added Tris-glucose extender: in vitro and in vivo studies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MzmslKmuw%3D%3D&md5=06a88406b0e605dc3cb3c71c30c11cedCAS | 15970316PubMed |

Walters, E. M., Men, H., Agca, Y., Mullen, S. F., Critser, E. S., and Critser, J. K. (2005). Osmotic tolerance of mouse spermatozoa from various genetic backgrounds: acrosome integrity, membrane integrity, and maintenance of motility. Cryobiology 50, 193–205.
Osmotic tolerance of mouse spermatozoa from various genetic backgrounds: acrosome integrity, membrane integrity, and maintenance of motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsVGks7o%3D&md5=7a632146da4cd9499567afa5f038441eCAS | 15843009PubMed |

Wright, S. (1931). Evolution in Mendelian populations. Genetics 16, 97–159.
| 1:STN:280:DC%2BD2s%2FmsVGqsw%3D%3D&md5=2aba0f5fe6829fd32b5e637038e35966CAS | 17246615PubMed |