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Sire effect on early and late embryonic death in French Holstein cattle

  • D. Ledoux (a1) (a2), C. Ponsart (a3), B. Grimard (a1) (a2), J. Gatien (a3), M. C. Deloche (a3), S. Fritz (a3), R. Lefebvre (a4) and P. Humblot (a3)...


We investigated the effect of maternal sire on early pregnancy failure (between D0, day of insemination and D90) in their progeny during the first and second lactations (n=3508) in the Holstein breed. The estimated breeding value (EBV) for cow fertility of 12 bulls (reliability⩾0.95) was used to create the following three groups: low, medium and high EBV (EBV from −0.7 to 1 expressed as genetic standard deviation relative to the mean of the breed). In their daughters (93 to 516 per bull), progesterone measurement was carried out on the day of artificial insemination (AI; D0) to check whether the cows were in the follicular phase and on D18 to 25 to assess non-fertilisation-early embryonic mortality (NF-EEM). Late embryonic mortality (LEM) and early foetal death (FD) were determined by ultrasonography on D45 and D90 and by the return to oestrus after the first AI. Frequencies of NF-EEM, LEM, FD and pregnancy were 33.3%, 11.7%, 1.4% and 48.5% and incidences were 35.1, 19.0, 2.7 and 51.1, respectively. Sire EBV was significantly related to the incidences of pregnancy failure between D0 and D90, fertilisation failure-early embryonic mortality (FF-EEM) and LEM but not to the incidence of FD between D45 and D90 of pregnancy. The relative risk (RR) of FF-EEM was significantly higher (RR=1.2; P<0.05) for the progeny group of low EBV bulls when compared with high EBV bulls. The same effect was observed when comparing LEM of the progeny groups from the low EBV bulls to those from moderate and high EBV bulls (RR, respectively, of 1.3 and 1.4; P<005). The incidence of FF-EEM was significantly higher when cows were inseminated before 80 days postpartum compared with later, and for the extreme values of the difference between milk fat and protein content measured during the first 3 months of lactation. FF-EEM was also significantly related to the year of observation. The incidence of LEM was higher for the highest producing cows and was influenced by interaction between milk yield×lactation rank and milk yield×milk protein content. In conclusion, this study showed large differences in early pregnancy failure between progeny groups and highlights the interest of accurate characterisation of embryonic death in order to identify potential candidate genes for female fertility.


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Barbat, A, Le Mézec, P, Ducrocq, V, Mattalia, S, Fritz, S, Boichard, D, Ponsart, C and Humblot, P 2010. Female fertility in French dairy breeds: current situation and strategies for improvement. Journal of Reproduction and Development 56, S15S21.
Beaudeau, F and Fourichon, C 1998. Estimating relative risk of disease from outputs of logistic regression when the disease is not rare. Preventive Veterinary Medicine 36, 243256.
Ben Jemaa, S, Fritz, S, Guillaume, F, Druet, T, Denis, C, Eggen, A and Gautier, M 2008. Detection of quantitative trait loci affecting non-return rate in French dairy cattle. Journal of Animal Breeding and Genetics 125, 280288.
Berglund, B 2008. Genetic improvement of dairy cow reproductive performance. Reproduction in Domestic Animal 43 (suppl. 2), 8995.
Berry, DP, Wall, E and Pryce, JE 2014. Genetics and genomics of reproductive performance in dairy and beef cattle. Animal 8 (suppl. 1), 115121.
Berry, DP, Bastiaansen, JW, Veerkamp, RF, Wijga, S, Wall, E, Berglund, B and Calus, MP 2012. Genome-wide associations for fertility traits in Holstein-Friesian dairy cows using data from experimental research herds in four European countries. Animal 6, 12061215.
Boichard, D, Barbat, A and Briend, M 1998. Evaluation génétique des caractères de fertilité chez les bovins laitiers. Rencontres Recherches Ruminants 5, 103106.
Buckley, F, O’Sullivan, K, Mee, JF, Evans, RD and Dillon, P 2003. Relationships among milk yield, body condition, cow weight, and reproduction in spring-calved Holstein-Friesians. Journal of Dairy Science 86, 23082319.
Charlier, C, Agerholm, JS, Coppieters, W, Karlskov-Mortensen, P, Li, W, de Jong, G, Fasquelle, C, Karim, L, Cirera, S, Cambisano, N, Ahariz, N, Mullaart, E, Georges, M and Fredholm, M 2012. A deletion in the bovine fanci gene compromises fertility by causing fetal death and brachyspina. PLoS One 7, e43085.
Chebel, RC, Santos, JE, Reynolds, JP, Cerri, RL, Juchem, SO and Overton, M 2004. Factors affecting conception rate after artificial insemination and pregnancy loss in lactating dairy cows. Animal Reproduction Science 84, 239255.
Cummins, SB, Lonergan, P, Evans, AC and Butler, ST 2012a. Genetic merit for fertility traits in Holstein cows: ii. ovarian follicular and corpus luteum dynamics, reproductive hormones, and estrus behavior. Journal of Dairy Science 95, 36983710.
Cummins, SB, Lonergan, P, Evans, AC, Berry, DP, Evans, RD and Butler, ST 2012b. Genetic merit for fertility traits in Holstein cows: i. production characteristics and reproductive efficiency in a pasture-based system. Journal of Dairy Science 95, 13101322.
Cutullic, E, Delaby, L, Gallard, Y and Disenhaus, C 2012. Towards a better understanding of the respective effects of milk yield and body condition dynamics on reproduction in Holstein dairy cows. Animal 6, 476487.
Diskin, MG and Morris, DG 2008. Embryonic and early foetal losses in cattle and other ruminants. Reproduction in Domestic Animals 43 (suppl. 2), 260267.
Druet, T, Fritz, S, Boussaha, M, Ben-Jemaa, S, Guillaume, F, Derbala, D, Zelenika, D, Lechner, D, Charon, C, Boichard, D, Gut, IG, Eggen, A and Gautier, M 2008. Fine mapping of quantitative trait loci affecting female fertility in dairy cattle on BTA03 using a dense single-nucleotide polymorphism map. Genetics 178, 22272235.
Fortes, MR, Deatley, KL, Lehnert, SA, Burns, BM, Reverter, A, Hawken, RJ, Boe-Hansen, G, Moore, SS and Thomas, MG 2013. 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.
Fourichon, C, Seegers, H and Malher, X 2000. Effect of disease on reproduction in the dairy cow: a meta-analysis. Theriogenology 53, 17291759.
Fournier, JL and Humblot, P 1989. Fréquence et facteurs de variations de la mortalité embryonnaire tardive chez la vache laitière. Elevage et Insémination 229, 310.
Freret, S, Ponsart, C, Rai, DB, Jeanguyot, N, Paccard, P and Humblot, P 2006. Facteurs de variation de la fertilite en premiere insemination et des taux de mortalites embryonnaires en elevages laitiers prim’holstein. Rencontres Recherches Ruminants 13, 281284.
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.
Fulkerson, WJ, Davison, TM, Garcia, SC, Hough, G, Goddard, ME, Dobos, R and Blockey, M 2008. Holstein–Friesian dairy cows under a predominantly grazing system: interaction between genotype and environment. Journal of Dairy Science 91, 826839.
Grimard, B, Freret, S, Chevallier, A, Pinto, A, Ponsart, C and Humblot, P 2006. Genetic and environmental factors influencing first service conception rate and late embryonic/foetal mortality in low fertility dairy herds. Animal Reproduction Science 91, 3144.
Grohn, YT and Rajala-Schultz, PJ 2000. Epidemiology of reproductive performance in dairy cows. Animal Reproduction Science 60–61, 605614.
Guillaume, F, Gautier, M, Ben Jemaa, S, Fritz, S, Eggen, A, Boichard, D and Druet, T 2007. Refinement of two female fertility QTL using alternative phenotypes in French Holstein dairy cattle. Animal Genetics 38, 7274.
Hayes, BJ, Bowman, PJ, Chamberlain, AJ and Goddard, ME 2009. Invited review: genomic selection in dairy cattle: progress and challenges. Journal of Dairy Science 92, 433443.
Heuer, C, Schukken, YH and Dobbelaar, P 1999. Postpartum body condition score and results from the first test day milk as predictors of disease, fertility, yield, and culling in commercial dairy herds. Journal of Dairy Science 82, 295304.
Holmberg, M and Andersson-Eklund, L 2006. Quantitative trait loci affecting fertility and calving traits in Swedish dairy cattle. Journal of Dairy Science 89, 36643671.
Homer, EM, Derecka, K, Webb, R and Garnsworthy, PC 2013. Mutations in genes involved in oestrous cycle associated expression of oestrus. Animal Reproduction Science 142, 106112.
Humblot, P 2001. Use of pregnancy specific proteins and progesterone assays to monitor pregnancy and determine the timing, frequencies and sources of embryonic mortality in ruminants. Theriogenology 56, 14171433.
Humblot, P and Denis, JB 1986. Sire effects on cow fertility and late embryonic mortality in the Montbeliard breed. Livestock Production Science 14, 139148.
Institut de l'Elevage 2013. Indexation bovine laitiere: evaluation internationale d'aout 2013. note d'information aux organisations genetiques des bovins laitiers. Institut de l’Elevage, Paris.
Kessel, S, Stroehl, M, Meyer, HH, Hiss, S, Sauerwein, H, Schwarz, FJ and Bruckmaier, RM 2008. Individual variability in physiological adaptation to metabolic stress during early lactation in dairy cows kept under equal conditions. Journal of Animal Science 86, 29032912.
Le Mezec, P 2010. Fertilite des principales races laitieres: bilan 1999-2008. Institut de l'élevage, Paris.
Liquet, B and Commenges, D 2001. Correction of the P-value after multiple coding of an explanatory variable in logistic regression. Statistics in Medicine 20, 28152826.
Lopez-Gatius, F 2003. Is fertility declining in dairy cattle? A retrospective study in Northeastern Spain. Theriogenology 60, 8999.
Lopez-Gatius, F 2012. Factors of a noninfectious nature affecting fertility after artificial insemination in lactating dairy cows: a review. Theriogenology 77, 10291041.
Lopez-Gatius, F, Santolaria, P, Yaniz, J, Rutllant, J and Lopez-Bejar, M 2002. Factors affecting pregnancy loss from gestation day 38 to 90 in lactating dairy cows from a single herd. Theriogenology 57, 12511261.
Lucy, MC 2001. Reproductive loss in high-producing dairy cattle: where will it end? Journal of Dairy Science 84, 12771293.
Michel, A, Ponsart, C, Freret, S and Humblot, P 2003. Influence de la conduite de la reproduction sur les resultats a l'insemination en periode de paturage. Rencontres Recherche Ruminants 10, 131134.
Miglior, F, Muir, BL and Van Doormaal, BJ 2005. Selection indices in Holstein cattle of various countries. Journal of Dairy Science 88, 12551263.
Moore, SG, Fair, T, Lonergan, P and Butler, ST 2014. Genetic merit for fertility traits in Holstein cows: iv. Transition period, uterine health, and resumption of cyclicity. Journal of Dairy Science 97, 27402752.
Nusinovici, S, Seegers, H, Joly, A, Beaudeau, F and Fourichon, C 2011. A side effect of decreased fertility associated with vaccination against bluetongue virus serotype 8 in Holstein dairy cows. Preventive Veterinary Medicine 101, 4250.
Nusinovici, S, Seegers, H, Joly, A, Beaudeau, F and Fourichon, C 2012. Quantification and at-risk period of decreased fertility associated with exposure to bluetongue virus serotype 8 in naive dairy herds. Journal of Dairy Science 95, 30083020.
Roelofs, J, Lopez-Gatius, F, Hunter, RH, van Eerdenburg, FJ and Hanzen, C 2010. When is a cow in estrus? Clinical and practical aspects. Theriogenology 74, 327344.
Royal, M, Mann, GE and Flint, AP 2000a. Strategies for reversing the trend towards subfertility in dairy cattle. Veterinary Journal 160, 5360.
Royal, MD, Darwash, AO, Flint, APE, Webb, R, Woolliams, J and Lamming, GE 2000b. Declining fertility in dairy cattle: changes in traditional and endocrine parameters of fertility. Animal Science 70, 487501.
Sahana, G, Guldbrandtsen, B, Bendixen, C and Lund, MS 2010. Genome-wide association mapping for female fertility traits in Danish and Swedish Holstein cattle. Animal Genetics 41, 579588.
Santos, JE, Rutigliano, HM and Sa Filho, MF 2009. Risk factors for resumption of postpartum estrous cycles and embryonic survival in lactating dairy cows. Animal Reproduction Science 110, 207221.
Santos, JE, Thatcher, WW, Chebel, RC, Cerri, RL and Galvao, KN 2004. The effect of embryonic death rates in cattle on the efficacy of estrus synchronization programs. Animal Reproduction Science 82–83, 513535.
Silke, V, Diskin, MG, Kenny, DA, Boland, MP, Dillon, P, Mee, JF and Sreenan, JM 2002. Extent, pattern and factors associated with late embryonic loss in dairy cows. Animal Reproduction Science 71, 112.
Syrstad, O 1981. Selection for fertility on the basis of AI data. Livestock Production Science 8, 247252.
Veerkamp, RF and Beerda, B 2007. Genetics and genomics to improve fertility in high producing dairy cows. Theriogenology 68 (suppl. 1), S266S273.
Walsh, RB, Walton, JS, Kelton, DF, LeBlanc, SJ, Leslie, KE and Duffield, TF 2007. The effect of subclinical ketosis in early lactation on reproductive performance of postpartum dairy cows. Journal of Dairy Science 90, 27882796.
Witte, JS, Greenland, S, Kim, LL and Arab, L 2000. Multilevel modeling in epidemiology with GLIMMIX. Epidemiology 11, 684688.
Zobel, R, Tkalcic, S, Pipal, I and Buic, V 2011. Incidence and factors associated with early pregnancy losses in simmental dairy cows. Animal Reproduction Science 127, 121125.


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Sire effect on early and late embryonic death in French Holstein cattle

  • D. Ledoux (a1) (a2), C. Ponsart (a3), B. Grimard (a1) (a2), J. Gatien (a3), M. C. Deloche (a3), S. Fritz (a3), R. Lefebvre (a4) and P. Humblot (a3)...


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