Abstract
The study aimed to verify the influence of the FecGE mutation in superovulated ewes and to evaluate the probability of logistic models to determine the response capacity of these ewes to superovulatory treatment. Santa Inês ewes (n = 29) were genotyped for the FecGE mutation and separated for their genotype group in carriers of the mutant E allele (FecGE/E, FecG+/E) and non-carrier (FecG+/+) alleles. The ewes underwent hormonal treatment for superovulation. Aside from the genotypes, variables included in the statistical model were reproductive status (empty, early lactation, or late lactation), age (> or < 6 years), and number of births (nulliparous, primiparous, multiparous). The carriers of the mutation could be discriminated from the non-carriers based on the number of corpora lutea, rate of frozen embryos, and fecundity. Recovery rate was significantly higher (P < 0.05) in FecGE/E (94.31%) compared to FecG+/E (63.15%) and FecG+/+ (61.90%) (P < 0.05), whereas fecundity rate of FecG+/+ ewes (50.76%) was significantly higher than FecG+/E (18.96%) and FecGE/E (32.53%) (P < 0.05). We determined in this study that the response to superovulation and embryo production can be discriminated between FecGE/E and FecG+/E ewes in relation to the FecG+/+ genotype. Logistic models that included reproductive status and mutation, or reproductive status and age, or reproductive status and number of births were effective in predicting the response to superovulatory treatment.
Similar content being viewed by others
Data availability
The authors declare that the raw data used to elaborating this paper will not be available to the readers of this research paper.
Code availability
Not applicable.
References
Abdoli, R., Zamani, P., Mirhoseini, S.Z., Ghavi, Hossein‐Zadeh, N. Nadri, S.A., 2016. Review on prolificacy genes in sheep. Reproduction in Domestic Animals, 51, 631-637.
Armstrong, D.T., Evans, G., 1983. Factors influencing success of embryo transfer in sheep and goats. Theriogenology,19, 31-42.
Bartlewski, P.M., Seaton, P., Oliveira, M.E.F., Kridli, R.T., Murawski, M., Schwarz, T., 2016. Intrinsic determinants and predictors of superovulatory yields in sheep: circulating concentrations of reproductive hormones, ovarian status, and antral follicular blood flow. Theriogenology, 86, 130-143.
Bindon, B.M., Piper, L.R., Cahill, L.P., Driancourt, M.A., O’Shea T., 1986. Genetic and hormonal factors affecting superovulation. Theriogenology, 25, 53-70.
Box, G.E., Cox, D.R., 1964. An analysis of transformations. Journal of the Royal Statistical Society: Series B, 26, 211-252.
Brasil, O.O., Moreira, N.H., Santos Júnior, G., Silva, B.D.M., Mariante, A.S., Ramos, A.F., 2016. Superovulatory and embryo yielding in sheep using increased exposure time to progesterone associated with a GnRH agonist. Small Ruminant Research, 136, 54-58.
Cavalcanti, A.S., Brandão, F.Z., Nogueira, L.A.G., Fonseca, J.F., 2012. Effects of GnRH administration on ovulation and fertility in ewes subjected to estrous synchronization. Revista Brasileira de Zootecnia, 41, 1412-1418.
Chaves, M.S., Luz, V.B., Ferreira-Silva, J.C., Melo, E.O., Paiva, S.R., Barros, I., Bartolomeu, C.C., Azevedo, H.C., Oliveira, M.A.L., 2019. Ovarian and follicular variables used to determine ewes with different FecGE genotypes. Animal Reproduction Science, 208, 106-117.
Chaves, M.S., Passos, H.S., Luz, V.B., Ferreira-Silva, J.C., Melo, E.O., Paiva, S.R., Bartolomeu, C.C., Oliveira, M.A.L., Azevedo, H.C., 2019. Evaluation of morphology, morphometry and follicular dynamics in FecGE genotyped ewes. Theriogenology, 136, 138-142.
Cognie, Y., Baril, G., Poulin, N., Mermillod, P., 2003. Current status of embryo technologies in sheep and goat. Theriogenology, 59, 171-188.
Driancourt, M.A., Fry, R.C., 1992. Effect of superovulation with pFSH or PMSG on growth and maturation of the ovulatory follicles in sheep. Animal Reproduction Science, 27, 279-292.
Dufour, J.J., Cognie, Y., Mermillod, P., Mariana, J.C., Romain, R.F., 2000. Effects of the Booroola Fec gene on ovarian follicular populations in superovulated Romanov ewes pretreated with a GnRH antagonist. Journal of Reproduction and Fertility, 118, 85-94.
Elvin, J.A., Yan, C., Wang, P., Nishimori, K., Matzuk, M.M., 1999. Molecular Characterization of the Follicle Defects in the Growth Differentiation Factor 9-Deficient Ovary. Molecular Endocrinology, 13, 1018-1034.
Gibbons, A., Cueto, M., 2011. Reproductive biotechnologies for genetic improvement in sheep. Revista Brasileira de Reprodução Animal, 35, 180-185.
Gode, F., Gulekli, B., Dogan, E., Korhan, P., Dogan, S., Bige, O., Cimrin, D., Atabey, N., 2011. Influence of follicular fluid GDF9 and BMP15 on embryo quality. Fertility and Sterility, 95, 2274-2278.
Gonzalez-Bulnes, A., Souza, C.J.H., Campbell, B.K., Baird, D.T., 2004. Effect of ageing on hormone secretion and follicular dynamics in sheep with and without the Booroola gene. Endocrinology, 145, 2858-2864.
Gootwine, E., Bor, A., Braw-Tal R., 1989. Plasma FSH levels and ovarian response to PMSG in ewe lambs of related genotypes that differ in their prolificacy. Animal Reproduction Science, 19, 09-116.
Gordon, K., Renfree, M.B., Short, R.V., Clarke, I.J., 1987. Hypothalamo-pituitary portal blood concentrations of ß-endorphin during suckling in the ewe. Journal of Reproduction and Fertility, 70, 397-408.
Henry, M., Neves, J.P., Jobim, M.I.M., 2013. Manual para exame andrológico e avaliação do sêmen animal. CBRA, Belo Horizonte, 3nd ed.
Kühholzer, B., Brem, G., 1999. In vivo development of microinjected embryos from superovulated prepuberal slaughter lambs. Theriogenology, 51, 1297-1302.
Lehloenya, K.C., Greyling, J.P.C., 2010. The effect of embryo donor age and parity on the superovulatory response in Boer goat does. South African Journal of Animal Science, 40, 65-69.
McNatty, K.P., Smith, P., Moore, L.G., Reader, K., Lun, S., Hanrahan, J.P., Groome, N.P., Laitinen, M., Ritvos, O., Juengel, J.L., 2005. Oocyte-expressed genes affecting ovulation rate. Molecular and Cellular Endocrinology, 29, 57-66.
Menchaca, A., Vilariño, M., Crispo, M., De Castro, T., Rubianes, E., 2009. New approaches to superovulation and embryo transfer in small ruminants. Reproduction, Fertility and Development, 22, 113-118.
Mitchell, L.M., King, M.E., Gebbie, F.E., Ranilla, M.J., Robinson, J.J., 1998. Resumption of oestrous and ovarian cyclicity during the post-partum period in autumn-lambing ewes is not influenced by age or dietary protein content. Animal Science, 67, 65-72.
Moraes, J.C.F., Souza, C.J.H., 2017. Ewes carrying the Booroola and Vacaria prolificacy alleles respond differently to ovulation induction with equine chorionic gonadotrophin. Genetics and Molecular Research, 16, 1-8.
Morales, G., Pro, A., Figueroa, B., Sánchez, C., Gallegos, J., 2004. Amamantamiento continuo o restringido y su relación con la duración del anestro postparto en ovejas Pelibuey. Agrociencia, 38, 165-171.
Pinto, P.H.N., Balaro, M.F.A., Arashiro, E.K.N., Batista, R.I.T.P., Oliveira, M.E.F., Bragança, G.M., Fonseca, J.F., Brandão, F.Z., 2017. Produção in vivo de embriões ovinos. Revista Brasileira de Reprodução Animal, 41, 208-216.
Pinto, P.H.N., Balaro, M.F.A., Souza-Fabjan, J.M.G., Ribeiro, L.D.S., Bragança, G.M., Leite, C.R., Arashiro E.K.N., Moraes, S.K., Da Fonseca, J.F., Brandão, F.Z.,2018. Anti-Müllerian hormone and antral follicle count are more effective for selecting ewes with good potential for in vivo embryo production than the presence of FecGE mutation or eCG pre-selection tests. Theriogenology, 113, 146-152.
Quirke, J.F., Meyer, H.H., Lahlou-Kassi, A., Hanrahan, J.P., Bradfords, G.E., Stabenfeldt, G.H., 1987. Natural and induced ovulation rate in prolific and non-prolific breeds of sheep in Ireland, Morocco and New Zealand. Journal of Reproduction and Fertility, 81, 309-316.
Santos, R.M., Vasconcelos, J.L.M., 2007. Efeito do intervalo entre recrutamentos foliculares na superovulação de vacas da raça Holandesa não-lactantes. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 59, 844-850.
Scaramuzzi, R.J., Radford, H.M.,1983. Factors regulating ovulation rate in the ewe. Journal of Reproduction and Fertility, 69, 353-367.
Scaramuzzi, R.J., Adams, N.R., Baird, D.T., Campbell, B.K., Downing, J.A., Findlay, J.K., Henderson, K.M., Martin, G.B., McNatty, K.P., McNeilly, A.S., Tsonis, C.G., 1993. A model for follicule selection and the determination of ovulation rate in the ewe. Reproduction, Fertility and Development, 5, 459-478.
Scaramuzzi, R.J., Baird, D.T., Campbell, B.K., Driancourt, M.A., Dupont, J., Fortune, J.E., Gilchrist, R.B., Martin, G.B., McNatty, K.P., McNeilly, A.S., Monget, P., Monniaux, D. (2011). Regulation of folliculogenesis and the determination of ovulation rate in ruminants. Reproduction, Fertility and Development, 23, 444-467.
Short, R.E., Adams, D.C., 1988. Nutritional and hormonal interrelationships in beef cattle reproduction. Canadian Journal of Animal Science, 68, 29-39.
Silva, B.D.M., Castro, E.A., Souza, C.J., Paiva, S.R., Sartori, R., Franco, M.M., Azevedo, H.C., Silva, T.A., Vieira, A.M., Neves, J.P., 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, 89-92.
Souza, C.J.H., Moraes, J.C.F., 1993. Biologia reprodutiva da linhagem merino booroola: um modelo experimental para estudos relativos à ovulação dos ovinos. Ciência Rural, 23, 391-398.
Spice, L.J., Aad, P.Y., Allen, D., Mazerbourg, S., Hsueh, A.J., 2006. Growth differentiation factor-9 has divergent effects on proliferation and steroidogenesis of bovine granulosa cells. Journal of Endocrinology, 189, 329-339.
Su, Y.Q., Sugiura, K., Eppig J.J., 2009. Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Seminars in Reproductive Medicine, 27, 32-42.
Sugiura, K., Eppig, J.J., 2005. Control of metabolic cooperativity between oocytes and their companion granulosa cells by mouse oocytes. Reproduction, Fertility and Development, 17, 667-674.
Sutton, M.L., Gilchrist, R.B., Thompson, J.G., 2003. Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity. Human Reproduction Update, 9, 35-48.
Torres, S., Cognie, Y., Colas, G., 1987. Transfer of superovulated sheep embryos obtained with different FSH-P. Theriogenology, 27, 407-419.
Viñoles, C., Forsberg, M., Martin, G.B., Cajarville, C., Repetto, J., Meikle, A., 2005. Short-term nutritional supplementation of ewes in low body condition affects follicle development due to an increase in glucose and metabolic hormones. Reproduction, 129, 299-309.
Yeo, C.X., Gilchrist, R.B., Thompson, J.G., Lane, M., 2007. Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Human Reproduction, 23, 67-73.
Funding
The study was financially supported, granted as a scholarship, by the Coordination for the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—CAPES) of Brazil, Finance Code 001.
Author information
Authors and Affiliations
Contributions
Maiana S. Chaves: conceptualization, methodology, investigation, and writing of the original draft; Alexandre F. Ramos and Nathalia H. M. Brasil: methodology and formal analysis; José C. Ferreira-Silva: support on writing; Samuel R. Paiva: ewe genotyping; Eduardo O. Melo: ewe genotyping; Inácio Barros: statistical analysis; Vicente José F. Freitas: support on the review and editing of the original draft; Valdir R. Junior: statistical analysis; Cláudio C. Bartolomeu: support on writing; Marcos A. L. Oliveira: support on the review and editing of the original draft editing of the original draft; Hymwrson C. Azevedo: supervision, support on the review, and editing of the original draft.
Corresponding author
Ethics declarations
Ethics approval
This research was conducted after evaluation and approval from the Committee of Ethics in Animal Use, Brazilian Agricultural Research Company—Embrapa, Tabuleiros Costeiros Unit, Aracaju-SE, Brazil (License: 13072016.006).
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chaves, M.S., Ramos, A.F., Brasil, N.H.M. et al. Use of logistic models to evaluate the response of superovulation treatment and embryo production in Santa Inês ewes. Trop Anim Health Prod 54, 276 (2022). https://doi.org/10.1007/s11250-022-03310-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11250-022-03310-8