Embryo survival and fertility differ in lines divergently selected for birth weight homogeneity in mice.


Journal

Journal of animal breeding and genetics = Zeitschrift fur Tierzuchtung und Zuchtungsbiologie
ISSN: 1439-0388
Titre abrégé: J Anim Breed Genet
Pays: Germany
ID NLM: 100955807

Informations de publication

Date de publication:
Sep 2023
Historique:
revised: 09 03 2023
received: 15 11 2022
accepted: 23 04 2023
medline: 15 8 2023
pubmed: 8 5 2023
entrez: 8 5 2023
Statut: ppublish

Résumé

The selection of animals for lower environment sensitivity around the optimum trait value can also provide benefits in productivity and welfare. A divergent selection experiment for birth weight environmental variability in mice was successfully conducted over 17 generations. Animals from low variability selected line (L-line) were more robust by having a higher litter size and survival at weaning in a common breeding environment, than those from high variability line (H-line). The objective of this study was to analyze the differences between those divergently selected lines for embryo and fetal survival and for fertility and prolificacy rate. To study embryo survival and ovulation rate, a total of 98 females (34 H-line and 50 L-line) were studied in four generations of the divergent experiment. To analyze fetal survival and fertility rate, 378 female mice (138 H-line and 240 L-line) in 10 generations or the divergent experiment were studied. Ultrasound scans were performed at day 14 of gestation to establish the number of total fetal and the embryo absorptions. Mortality was addressed as the difference between litter size at birth and the number of fetuses at 14 days of gestation. The number of pregnant females in the first 3 days after mating was used to measure fertility. A linear model was also fitted to analyze embryo mortality, litter size, and the number of embryos at 14 days of gestation. A categorical model was then used to study fertility, including line, generation, and its interaction as effects. Despite the fact that there were no significant differences in the ovulation rate, litter size at birth was significantly higher in the L-line than in the H-line (9.82 vs. 8.36 pups, p < 0.001). Moreover, embryo mortality was significantly lower in the L-line than in the H-line (1.39 vs. 2.87 fetuses, p < 0.001). L-line females were more fertile (53.49% vs. 23.26% for the H-line). According to these results, the line selected for low environmental variance would be preferable for robustness and animal welfare.

Identifiants

pubmed: 37150976
doi: 10.1111/jbg.12778
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

549-557

Subventions

Organisme : Ministerio de Ciencia, Innovación y Universidades
ID : PGC2018-096198-A-I00

Informations de copyright

© 2023 The Authors. Journal of Animal Breeding and Genetics published by John Wiley & Sons Ltd.

Références

Amdi, C., Krogh, U., Flummer, C., Oksbjerg, N., Hansen, C. F., & Theil, P. K. (2013). Intrauterine growth restricted piglets defined by their head shape ingest insufficient amounts of colostrum. Journal of Animal Science, 91, 5605-5613. https://doi.org/10.2527/jas.2013-6824
Andersen, I. L., Naevdal, E., & Boe, K. E. (2011). Maternal investment, sibling competition, and offspring survival with increasing litter size and parity in pigs (Sus scrofa). Behavioral Ecology and Sociobiology, 65, 1159-1167. https://doi.org/10.1007/s00265-010-1128-4
Argente, M. J., Calle, E. W., García, M. L., & Blasco, A. (2017). Correlated response in litter size components in rabbits selected for litter size variability. Journal of Animal Breeding and Genetics, 134, 505-511. https://doi.org/10.1111/jbg.12283
Argente, M. J., García, M. L., Muelas, R., & Blasco, A. (2014). Effect of selection for residual variance of litter size on components of litter size in rabbits. In Proceedings of the 10th World Congress on Genetics Applied to Livestock Production, 17-22 August 2014, Vancouver, Canada, Communication 149.
Argente, M. J., Santacreu, M. A., Climent, A., & Blasco, A. (2000). Genetic correlations between litter size and uterine capacity. In Proceeding of the 8th World Rabbit Congress. Valencia (Spain), 4-7 July 2000, 333-338.
Ashworth, C. J., Finch, A. M., Page, K. R., Nwagwu, M. O., & McArdle, H. J. (2001). Causes and consequences of fetal growth retardation in pigs. Reproduction, 58, 233-246.
Auvigne, V., Leneveu, P., Jehannin, C., Peltoniemi, O., & Sallé, E. (2010). Seasonal infertility in sows: A five year field study to analyze the relative roles of heat stress and photoperiod. Theriogenology, 74, 60-66. https://doi.org/10.1016/j.theriogenology.2009.12.019
Baxter, E. M., Rutherford, R. B., D'Eath, G., Arnott, S. P., Turner, P., Sandøe, V. A., Moustsen, T., Edwards, S. A., & Lawrence, A. B. (2013). The welfare implications of large litter size in the domestic pig II: Management factors. Animal Welfare, 22, 219-238. https://doi.org/10.7120/09627286.22.2.219
Behringer, R., Gertsenstein, M., Nagy, K. V., & Nagy, A. (2016). Selecting female mice in estrus and checking plugs. Cold Spring Harbor Protocols, 2016, 729-731. https://doi.org/10.1101/pdb.prot092387
Bertoldo, M. J., Holyoake, P. K., Evans, G., & Grupen, C. G. (2011). Seasonal effects on oocyte developmental competence in sows experiencing pregnancy loss. Animal Reproduction Science, 124, 104-111. https://doi.org/10.1016/j.anireprosci.2011.02.012
Biensen, N. J., Wilson, M. E., & Ford, S. P. (1998). The impact of either a Meishan or Yorkshire uterus on Meishan or Yorkshire fetal and placental development to days 70, 90, and 110 of gestation. Journal of Animal Science, 76, 2169-2176. https://doi.org/10.2527/1998.7682169x
Bolet, G., Gaffeau, H., Joly, T., Theau-Clement, M., Falieres, J., Hurtaud, J., & Bodin, L. (2007). Genetic homogenisation of birth weight in rabbits: Indirect selection response for uterine horn characteristics. Livestock Science, 111, 28-32. https://doi.org/10.1016/j.livsci.2006.11.012
Boletín Oficial del Estado (BOE). (2013). Real Decreto 53/2013, por el que seestablecen las normas básicas aplicables para la protección de losanimales utilizados en experimentación y otros fines científicos, incluyendo la docencia. B.O.E. 34, 11370-11421.
Broom, D. M. (2008). Welfare assessment and relevant ethical decisions: Key concepts. Annual Review of Biomedical Sciences, 20, 79-90. https://doi.org/10.5016/1806-8774.2008.v10pT79
Brown, S. D., Zurakowski, D., Rodriguez, D. P., Dunning, P. S., Hurley, R. J., & Taylor, G. A. (2006). Ultrasound diagnosis of mouse pregnancy and gestational staging. Comparative Medicine, 56, 262-271.
Burkus, J., Kacmarová, M., Kubandová, J., Kokosová, N., Fabianová, K., Fabian, D., Koppel, J., & Cikos, S. (2015). Stress exposure during the preimplantation period affects blastocyst lineages and offspring development. Journal of Reproduction and Development, 61(4), 325-331. https://doi.org/10.1262/jrd.2015-012
Damgaard, L. H., Rydhmer, L., Lovendahl, P., & Grandinson, K. (2003). Genetic parameters for within-litter variation in piglet birth weight and change in within-litter variation during suckling. Journal of Animal Science, 81, 604-610. https://doi.org/10.2527/2003.813604x
Dobrzanski, J., Mulder, H. A., Knol, E. F., Szwaczkowski, T., & Sell-Kubiak, E. (2020). Estimation of litter size variability phenotypes in Large White sows. Journal of Animal Breeding and Genetics, 137, 559-570. https://doi.org/10.1111/jbg.12465
Formoso-Rafferty, N., Arias-Álvarez, M., Gutiérrez, J. P., & Cervantes, I. (2018). Embryo mortality and fertility in divergently selected lines for birth weight homogeneity in mice. In Proceedings of the 69th Annual Meeting of European Association for Animal Production, 27-31 August 2018, Dubrovnik, Croatia, 580.
Formoso-Rafferty, N., Cervantes, I., Ibáñez-Escriche, N., & Gutiérrez, J. P. (2016a). Genetic control of the environmental variance for birth weight in seven generations of a divergent selection experiment in mice. Journal of Animal Breeding and Genetics, 113, 227-237. https://doi.org/10.1111/jbg.12174
Formoso-Rafferty, N., Cervantes, I., Ibáñez-Escriche, N., & Gutiérrez, J. P. (2016b). Correlated genetic trends for production and welfare traits in a mouse population divergently selected for birth weight environmental variability. Animal, 10, 1770-1777. https://doi.org/10.1017/S1751731116000860
Formoso-Rafferty, N., Cervantes, I., Ibáñez-Escriche, N., & Gutiérrez, J. P. (2017). Modulating birth weight heritability in mice. Journal of Animal Science, 95, 531-537. https://doi.org/10.2527/jas.2016.1169
Formoso-Rafferty, N., Cervantes, I., Sánchez, J. P., Gutiérrez, J. P., & Bodin, L. (2019). Effect of feed restriction on the environmental variability of birth weight in divergently selected lines of mice. Genetics Selection Evolution, 51, 27. https://doi.org/10.1186/s12711-019-0471-9
Formoso-Rafferty, N., Gutiérrez, J. P., García-Álvarez, A., Pérez, T., & Cervantes, I. (2022). Impact of selection for birth weight variability on reproductive longevity: A mice model. Journal of Animal Breeding and Genetics, 139, 370-379. https://doi.org/10.1111/jbg.12676
Foxcroft, G. R., Dixon, W. T., Dyck, M. K., Novak, S., Harding, J. C. S., & Almeida, F. C. R. L. (2009). Prenatal programming of postnatal development in the pig. Society of Reproduction and Fertility Supplement, 66, 213-231.
Foxcroft, G. R., Dixon, W. T., Novak, S., Putman, C. T., Town, S. C., & Vinsky, M. D. A. (2006). The biological basis for prenatal programming of postnatal performance in pigs. Journal of Animal Science, 84, E105-E112. https://doi.org/10.2527/2006.8413_supple105x
Freyer, G. (2018). Maximum number of total born piglets in a parity and individual ranges in litter size expressed as specific characteristics of sows. Journal of Animal Science and Technology, 60, 13. https://doi.org/10.1186/s40781-018-0172-x
Gagioti, S., Scavone, C., & Bevilacqua, E. (2000). Participation of the mouse implanting trophoblast in nitric oxide production during pregnancy. Biology of Reproduction, 62, 260-268. https://doi.org/10.1095/biolreprod62.2.260
Gouge, R. C., Marshburn, P., Gordon, B. E., Nunley, W., & Huet-Hudson, Y. M. (1998). Nitric oxide as a regulator of embryonic development. Biology of Reproduction, 58, 875-879.
Hales, J., Moustsen, V. A., Nielsen, M. B. F., & Hansen, C. F. (2013). Individual physical characteristics of neonatal piglets affect preweaning survival of piglets born in a noncrated system. Journal of Animal Science, 91, 4991-4903. https://doi.org/10.2527/jas.2012-5740
Hansen, C. F., Hales, J., Amdi, C., & Moustsen, V. A. (2018). Intrauterine growth restricted piglets defined by their head shape have impaired growth during the suckling period. Animal Production Science, 59, 1056-1062. https://doi.org/10.1071/AN17581
He, L. C., Li, P. H., Ma, X., Sui, S. P., Gao, S., Kim, S. W., Gu, Y. Q., Huang, Y., Ding, S., & Huang, R. H. (2016). Identification of new single nucleotide polymorphisms affecting total number born and candidate genes related to ovulation rate in Chinese Erhualian pigs. Animal Genetics, 48, 48-54. https://doi.org/10.1111/age.12492
Hefler, L. A., Reyes, C. A., O'Brien, W. E., & Gregg, A. R. (2001). Perinatal development of endothelial nitric oxide synthase-deficient mice. Biology of Reproduction, 64, 666-6673. https://doi.org/10.1095/biolreprod64.2.666
Hill, W. G., & Caballero, A. (2000). Artificial selection experiments. Annual Review of Ecology and Systematics, 23, 287-310.
Huting, A. M. S., Sakkas, P., Wellock, I., Almond, K., & Kyriazakis, I. (2018). Once small always small? To what extent morphometric characteristics and post-weaning starter regime affect pig lifetime growth performance. Porcine Health Management, 7, 1-14. https://doi.org/10.1186/s40813-018-0098-1
Ibáñez-Escriche, N., Sorensen, D., Waagepetersen, R., & Blasco, A. (2008). Selection for environmental variation: A statistical analysis and power calculations to detect response. Genetics, 180(4), 2209-2226. https://doi.org/10.1534/genetics.108.091678
Knox, R. V. (2016). Artificial insemination in pigs today. Theriogenology, 85, 83-93. https://doi.org/10.1016/j.theriogenology.2015.07.009
Lopes, T. P., Padilla, L., Bolarin, A., Rodriguez-Martinez, H., & Roca, J. (2000). Ovarian follicle growth during lactation determines the reproductive performance of weaned sows. Animals, 10, 1012. https://doi.org/10.3390/ani10061012
Lynegaard, J. C., Hansen, C. F., Kristensen, A. R., & Amdi, C. (2020). Body composition and organ development of intra-uterine growth restricted pigs at weaning. Animal, 14(2), 322-329. https://doi.org/10.1017/S175173111900171X
Mulder, H. A., Bijma, P., & Hill, W. (2008). Selection for uniformity in livestock by exploiting genetic heterogeneity of residual variance. Genetics Selection Evolution, 40, 37-59. https://doi.org/10.1051/gse:2007034
Pallares, P., & Gonzalez-Bulnes, A. (2010). The effect of embryo and maternal genotypes on prolificacy, intrauterine growth retardation and postnatal development of Nos3-knockout mice. Reproductive Biology, 10(3), 241-248.
Prunier, A., Heinonen, M., & Quesnel, H. (2010). High physiological demands in intensively raised pigs: Impact on health and welfare. Animal, 4, 886-888. https://doi.org/10.1017/S175173111000008X
Quiniou, N., Dagorn, J., & Gaudré, D. (2002). Variation of piglets' birth weight and consequences on subsequent performance. Livestock Science, 78, 63-70. https://doi.org/10.1016/S0301-6226(02)00181-1
Roca, J., Parrilla, I., Bolarin, A., Martinez, E. A., & Rodriguez-Martinez, H. (2016). Will AI in pigs become more efficient? Theriogenology, 86, 187-193. https://doi.org/10.1016/j.theriogenology.2015.11.026
Rutherford, K. M. D., Baxter, E. M., D'Eath, R. B., Turner, S. P., Arnott, G., Roehe, R., Ask, B., Sandøe, P., Moustsen, V. A., Thorup, F., Edwards, S. A., Berg, P., & Lawrence, A. B. (2013). The welfare implications of large litter size in the domestic pig I: Biological factors. Animal Welfare, 22, 199-218. https://doi.org/10.7120/09627286.22.2.199
SAS Institute. (1990). SAS/STAT® user's guide (release 8.2). SAS Institute Inc.
Schneider, J. F., Rempel, L. A., & Rohrer, G. A. (2012). Genome-wide association study of swine farrowing traits. Part I: Genetic and genomic parameter estimates. Journal of Animal Science, 90, 3353-3359. https://doi.org/10.2527/jas.2011-4729
Sell-Kubiak, E., Duijvesteijn, N., Lopes, M. S., Janss, L. L. G., Knol, E. F., Bijma, P., & Mulder, H. A. (2015). Genome-wide association study reveals novel loci for litter size and its variability in a Large White pig population. BMC Genomics, 16, 1049. https://doi.org/10.1186/s12864-015-2273-y
Spötter, A., & Distl, O. (2006). Genetic approaches to the improvement of fertility traits in the pig. The Veterinary Journal, 172, 234-247. https://doi.org/10.1016/j.tvjl.2005.11.013
Town, S. C., Putman, C. T., Turchinsky, N. J., Dixon, W. T., & Foxcroft, G. R. (2004). Number of conceptuses in utero affects porcine fetal muscle development. Reproduction, 28, 443-454. https://doi.org/10.1530/rep.1.00069
Tuchscherer, M., Puppe, B., Tuchscherer, A., & Tiemann, U. (2000). Early identification of neonates at risk: Traits of newborn piglets with respect to survival. Theriogenology, 54, 371-388. https://doi.org/10.1016/S0093-691X(00)00355-1
Van der Heijden, O. W., Essers, Y. P., Fazzi, G., Peeters, L. L., De Mey, J. G., & van Eys, G. J. (2005). Uterine artery remodeling and reproductive performance are impaired in endothelial nitric oxide synthase-deficient mice. Biology of Reproduction, 72, 1161-1168. https://doi.org/10.1095/biolreprod.104.033985
Varón-González, C., Pallares, L., Debat, V., & Navarro, N. (2019). Mouse skull mean shape and shape robustness rely on different genetic architectures and different loci. Frontiers in Genetics, 10, 64. https://doi.org/10.3389/fgene.2019.00064
Webb, A. J. (1998). Objectives and strategies in pig improvement: An applied perspective. Journal of Dairy Science, 81(2), 36-46. https://doi.org/10.3168/jds.S0022-0302(98)70152-3
Wilson, M. E., Biensen, N. J., & Ford, P. (1999). Novel insight into the control of litter size in pigs, using placental efficiency as a selection tool. Journal of Animal Science, 77, 1654-1658. https://doi.org/10.2527/1999.7771654x

Auteurs

Nora Formoso-Rafferty (N)

Departamento de Producción Agraria, E.T.S. Ingeniería Agronómica, Alimentaria y de Biosistemas, Universidad Politécnica de Madrid, Madrid, Spain.

Laila El-Ouazizi El-Kahia (L)

Departamento de Producción Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, Madrid, Spain.

María Arias-Álvarez (M)

Departamento de Producción Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, Madrid, Spain.

Juan Pablo Gutiérrez (JP)

Departamento de Producción Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, Madrid, Spain.

Isabel Cervantes (I)

Departamento de Producción Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, Madrid, Spain.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH