Dante J. Hernández-Rubio, María Del Carmen Navarro-Maldonado, Sergio S. González-Muñoz, Martha Hernández-Rodríguez, Miguel P. Conde-Hinojosa, César Cortez-Romero


Background: Genetic improvement in the sheep species focuses on increasing the number of offspring per sheep. Heritable characteristics such as ovulation rate, fertility, and prolificacy are desirable. Objective: To evaluate the influence of estrus pre-synchronization with PGF2α on the manifestation of estrus, onset and return to estrus (1st and 2nd), pregnancy, lambing, prolificacy, and fertility in Katahdin ewes carrying exon 2 of the gene Factor Growth and Differentiation 9 (GDF9). Methodology: Seventy-two ewes were randomized into four treatments (T): T1 (n = 18), ewes without GDF9 gene and without estrus pre-synchronization; T2 (n = 17), ewes without GDF9 gene and with estrus pre-synchronization; T3 (n = 19) ewes with the GDF9 gene and without estrus pre-synchronization, and T4 (n = 18), ewes with the GDF9 gene and with estrus pre-synchronization. Results: The presence of estrus, the onset of estrus, and returns to estrus, pregnancy, and lambing percentages were not different between treatments (p>0.05). The average pregnancy and lambing in both cases were 86.2% and the average general prolificacy was 1.4 lambs per ewe for all four treatments. There were also no significant differences for the prolificacy or fertility rate (p>0.05). Implications: The present study contributes to the understanding of the use of presynchronization with PGF2α and the effect of the presence of exon 2 of the GDF9 gene on reproductive variables. Conclusions: The presynchronization of estrus with PGF2α and the presence of exon 2 of the GDF9 gene in ewes of the Katahdin breed did not have a significant effect on the reproductive variables evaluated.


fecundity gene; synchronization; estrus; prolificacy; ewe.

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Aké-López, J., Aké-Villanueva, J., Villanueva, N., Yerves, J. and Cuicas, R., 2015. Fertilidad y prolificidad de ovejas Pelibuey sincronizadas con esponjas intravaginales o implantes subcutáneos reciclados. Bioagrociencias, 8, pp. 44–49.

Aké-Villanueva, J.R., Aké-López, J.R., Segura-Correa, J. C., Magaña-Monforte, J. G. and Aké-Villanueva, N. Y., 2017. Factors affecting conception rate of hair ewes after laparoscopic insemination with chilled semen under tropical conditions. Small Ruminant Research, 153, pp. 114–117.

Alavez Ramírez, A., Arroyo Ledezma, J., Montes Pérez, R., Zamora Bustillos, R., Navarrete Sierra, L. F. and Magaña Sevilla, H., 2014. Short communication: Estrus synchronization using progestogens or cloprostenol in tropical hair sheep. Tropical Animal Health and Production, 46(8), pp. 1515–1518.

Arroyo, J., Torre-Barrera, J. D. L. and Ávila-Serrano, N. Y., 2013. Reproductive response in hair sheep synchronized with progesterone or prostaglandins. Agrociencia, 47, pp. 661–670.

Bartlewski, P. M., Sohal, J., Paravinja, V., Baby, T., Oliveira, M. E. F., Murawski, M., Schwarz, T., Zieba, D. A. and Keisler, D. H., 2017. Is progesterone the key regulatory factor behind ovulation rate in sheep? Domestic Animal Endocrinology, 58, pp. 30–38.

Besufkad, S., Betsha, S., Demis, C., Zewude, T., Rouatbi, M., Getachew, T., Haile, A., Rischkowsky, B. and Rekik, M., 2020. Field synchronization of Ethiopian Highland sheep for fixed time artificial insemination: Improvement of conception rate with a double injection of prostaglandin at 11 days. Journal of Applied Animal Research, 48(1), pp. 413–418.

Bodensteiner, K. J., Clay, C. M., Moeller, C. L. and Sawyer, H. R., 1999. Molecular Cloning of the Ovine Growth/Differentiation Factor-9 Gene and Expression of Growth/Differentiation Factor-9 in Ovine and Bovine Ovaries1. Biology of Reproduction, 60(2), pp. 381–386.

Chay-Canul, A. J., 2019. Productividad de ovejas Pelibuey y Katahdin en el trópico húmedo. Ecosistemas y Recursos Agropecuarios, 6(16), pp. 159–165.

COLPOS (Colegio de Postgraduados). Reglamento para el uso y cuidado de animales destinados a la investigación en el Colegio de Postgraduados. Dirección de Investigación: Colegio de Posgraduados, México, 2019.

Dash, H. R., Shrivastava, P. and Das, S., 2020. Principles and practices of DNA analysis: A laboratory manual for forensic DNA typing. Humana Press.

De, K., Kumar, D., Sethi, D., Gulyani, R. and Naqvi, S. M. K., 2015. Estrus synchronization and fixed-time artificial insemination in sheep under field conditions of a semi-arid tropical region. Tropical Animal Health and Production, 47(2), pp. 469–472.

Fierro, S., Gil, J., Viñoles, C. and Olivera-Muzante, J., 2013. The use of prostaglandins in controlling estrous cycle of the ewe: A review. Theriogenology, 79(3), pp. 399–408.

García, E., 2004. Modificaciones al sistema de clasificación climática de Köppen: Para adaptarlo a las condiciones de la República Mexicana (Quinta, Vol. 1–cinco). Universidad Autonoma de Mexico.

Godfrey, R. W., Collins, J. R., Hensley, E. L. and Wheaton, J. E., 1999. Estrus synchronization and artificial insemination of hair sheep ewes in the tropics. Theriogenology, 51(5), pp. 985–997.

Gonzalez-Bulnes, A., Menchaca, A., Martin, G. B., and Martinez-Ros, P., 2020. Seventy years of progestagen treatments for management of the sheep oestrous cycle: Where we are and where we should go. Reproduction, Fertility and Development, 32(5), pp. 441.

González-Godínez, A., Urrutia-Morales, J., and Gámez-Vázquez, H. G., 2014. Comportamiento reproductivo de ovejas Dorper y Katahdin empadradas en primavera en el norte de México. pp. 123–127.

Gündo?an, M., Baki, D. and Yeni, D., 2003. Reproductive Seasonality in Sheep. Acta Agriculturae Scandinavica, Section A - Animal Science, 53(4), pp. 175–179.

Habeeb, H. M. H. and Anne Kutzler, M., 2021. Estrus Synchronization in the Sheep and Goat. Veterinary Clinics of North America: Food Animal Practice, 37(1), 125–137.

Hanrahan, J. P., Gregan, S. M., Mulsant, P., Mullen, M., Davis, G. H., Powell, R. and Galloway, S. M., 2004. Mutations in the Genes for Oocyte-Derived Growth Factors GDF9 and BMP15 Are Associated with Both Increased Ovulation Rate and Sterility in Cambridge and Belclare Sheep (Ovis aries)1. Biology of Reproduction, 70(4), pp. 900–909.

Juengel, J. L., Davis, G. H. and McNatty, K. P., 2013. Using sheep lines with mutations in single genes to better understand ovarian function. Reproduction, 146(4), pp. R111–R123.

Kona, S. S. R., Praveen Chakravarthi, V., Siva Kumar, A. V. N., Srividya, D., Padmaja, K. and Rao, V. H., 2016. Quantitative expression patterns of GDF9 and BMP15 genes in sheep ovarian follicles grown in vivo or cultured in vitro. Theriogenology, 85(2), pp. 315–322.

Martínez-Ros, P., Rios-Abellan, A. and Gonzalez-Bulnes, A., 2018. Influence of Progesterone-Treatment Length and eCG Administration on Appearance of Estrus Behavior, Ovulatory Success and Fertility in Sheep. Animals, 9(1), pp. 9.

Masoumi, R., Badiei, A., Shahneh, A. Z., Kohram, H., Dirandeh, E. and Colazo, M. G., 2017. A Short Presynchronization with PGF2? and GnRH Improves Ovarian Response and Fertility in Lactating Holstein Cows Subjected to a Heatsynch Protocol. Annals of Animal Science, 17(1), pp. 169–177.

McKelvey, W. A. C., Robinson, J. J., Aitken, R. P. and Henderson, G., 1985. The evaluation of a laparoscopic insemination technique in ewes. Theriogenology, 24(5), pp. 519–535.

Mekuriaw, Z., Assefa, H., Tegegne, A. and Muluneh, D., 2016. Estrus response and fertility of Menz and crossbred ewes to single prostaglandin injection protocol. Tropical Animal Health and Production, 48(1), pp. 53–57.

Muñoz-García, C., Vaquera-Huerta, H., Gallegos-Sánchez, J., Becerril-Pérez, C. M., Tarango-Arámbula, L. A., Bravo-Vinaja, Á. and Cortez-Romero, C., 2021. Influence of FecGE mutation on the reproductive variables of Pelibuey ewes in the anestrus period. Tropical Animal Health and Production, 53(2), pp. 328.

Mullen, M. P. and Hanrahan, J. P., 2014. Direct evidence on the contribution of a missense mutation in GDF9 to variation in ovulation rate of Finnsheep. PLoS ONE, 9(4).

Nicol, L., Bishop, S. C., Pong-Wong, R., Bendixen, C., Holm, L.-E., Rhind, S. M. and McNeilly, A. S., 2009. Homozygosity for a single base-pair mutation in the oocyte-specific GDF9 gene results in sterility in Thoka sheep. Reproduction, 138(6), pp. 921–933.

Notter, D. R., 2000. Potential for Hair Sheep in the United States. Journal of Animal Science, 77(E-Suppl), pp. 1.

Olivera-Muzante, J., Gil, J., Fierro, S., Menchaca, A. and Rubianes, E., 2011. Alternatives to improve a prostaglandin-based protocol for timed artificial insemination in sheep. Theriogenology, 76(8), pp. 1501–1507.

Prontuario de Información Geográfica Municipal., 2005. 3, 9.$File/prontuario.pdf

Ramírez-Ordóñes, S., Domínguez-Díaz, D., Salmerón-Zamora, J. J. and Villalobos-Villalobos, G., 2013. Produccion y calidad del forraje de variedades de avena en función del sistema de siembra y de la etapa de madurez al corte. 36, 9.

Russel, A., 1984. Body condition scoring of sheep. In Practice, 6(3), pp. 91–93.

Sadighi, M., Bodensteiner, K. J., Beattie, A. E. and Galloway, S. M., 2002. Genetic mapping of ovine growth differentiation factor 9 (GDF9) to sheep chromosome 5. Animal Genetics, 33(3), pp. 244–245.

SAGARPA (Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca, y Alimentación,)., 2001. Norma oficial Mexicana NOM-062-ZOO-1999, Especificaciones técnicas para la producción, cuidado y uso de los animales de laboratorio. Diario Oficial de La Federación, 22 Agosto, pp. 107–165. Retrieved from

SAS Institute Inc., Cary, NC, U., 2013. SAS 9.4 Statements ®. (S. Institute, Ed.) (9.4 Statem).

Silva, B. D. M., Castro, E. A., Souza, C. J. H., Paiva, S. R., Sartori, R., Franco, M. M., Azevedo, H. C., Silva, T. A. S. N., Vieira, A. M. C., Neves, J. P. and Melo, E. O., 2011. A new polymorphism in the Growth and Differentiation Factor 9 (GDF9) gene is associated with increased ovulation rate and prolificacy in homozygous sheep: New polymorphism in GDF9 and prolificacy. Animal Genetics, 42(1), pp. 89–92.

Souza, C. J. H., McNeilly, A. S., Benavides, M. V., Melo, E. O. and Moraes, J. C. F., 2014. Mutation in the protease cleavage site of GDF9 increases ovulation rate and litter size in heterozygous ewes and causes infertility in homozygous ewes. Animal Genetics, 45(5), pp. 732–739.

Strauss, J. F. and Williams, C. J., 2019. Ovarian Life Cycle. En Yen and Jaffe’s Reproductive Endocrinology pp. 167-205.e9. Elsevier.

Swelum, A. A.-A., Saadeldin, I. M., Moumen, A. F., Ali, M. A. and Alowaimer, A. N., 2018. Efficacy of controlled internal drug release (CIDR) treatment durations on the reproductive performance, hormone profiles, and economic profit of Awassi ewes. Small Ruminant Research, 166, pp. 47–52.

Våge, D. I., Husdal, M., Kent, M. P., Klemetsdal, G. and Boman, I. A., 2013. A missense mutation in growth differentiation factor 9 (GDF9) is strongly associated with litter size in sheep. BMC Genetics, 14(1), pp. 1.

Vilariño, M., Cuadro, F., dos Santos-Neto, P. C., García-Pintos, C. and Menchaca, A., 2017. Time of ovulation and pregnancy outcomes obtained with the prostaglandin-based protocol Synchrovine for FTAI in sheep. Theriogenology, 90, pp. 163–168.

Yu, H., Wang, Y., Wang, M., Liu, Y., Cheng, J. and Zhang, Q., 2020. Growth differentiation factor 9 (gdf9) and bone morphogenetic protein 15 (bmp15) are potential intraovarian regulators of steroidogenesis in Japanese flounder (Paralichthys olivaceus). General and Comparative Endocrinology, 297, 113547.



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