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

Uterine crowding in the sow affects litter sex ratio, placental development and embryonic myogenin expression in early gestation

W.-Y. Tse A , S. C. Town A , G. K. Murdoch B , S. Novak A , M. K. Dyck A , C. T. Putman C , G. R. Foxcroft A and W. T. Dixon A D
+ Author Affiliations
- Author Affiliations

A Swine Reproduction–Development Program, Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta T6G 2P5, Canada.

B Department of Animal and Veterinary Science, College of Agricultural and Life Sciences, University of Idaho, Moscow, ID 83843-2330, USA.

C Faculty of Physical Education and the Centre for Neuroscience, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta T6G 2H9, Canada.

D Corresponding author. Email: walter.dixon@ualberta.ca

Reproduction, Fertility and Development 20(4) 497-504 https://doi.org/10.1071/RD07200
Submitted: 31 October 2007  Accepted: 21 January 2008   Published: 11 April 2008

Abstract

Uterine crowding in the pig results in intrauterine growth restriction (IUGR), and permanently affects fetal muscle fibre development, representing production losses for the commercial pig herd. The present study sought to understand how different levels of uterine crowding in sows affects muscle fibre development in the early embryo at the time of muscle fibre differentiation and proliferation. Sows either underwent surgical, unilateral oviduct ligation (LIG; n = 10) to reduce the number of embryos in the uterus, or remained as intact, relatively-crowded controls (CTR; n = 10). Embryos and placentae were collected at Day 30 of gestation, and myogenic regulatory factor (MRF) transcript abundance was determined using real-time PCR for both myogenin (MYOG) and myoblast differentiation 1 (MYOD1). Unilateral tubal ligation resulted in lower numbers of embryos in utero, higher placental weights and a higher male : female sex ratio (P < 0.05). Relative MYOD1 expression was not different, but MYOG expression was higher (P < 0.05) in the LIG group embryos; predominantly due to effects on the male embryos. Relatively modest uterine crowding therefore affects MRF expression, even at very early stages of embryonic development, and could contribute to reported differences in fetal muscle fibre development, birthweight and thus post-natal growth performance in swine.


Acknowledgements

The authors wish to thank the staff at the Swine Research and Technology Centre and the University of Alberta Metabolic Unit for the care of the animals, Jennifer Patterson for research project support, Rose O’Donoghue for help with necropsies and Joan Turchinsky for her valuable assistance in the laboratory. Funding for this project was received from Natural Sciences and Engineering Research Council of Canada, Alberta Agricultural Research Institute, Alberta Pork and the Genex Swine Group.


References

Arnold, H. H. , and Braun, T. (2000). Genetics of muscle determination and development. Curr. Top. Dev. Biol. 48, 129–164.
PubMed |

Chen, Z. Y. , and Dziuk, P. J. (1993). Influence of initial length of uterus per embryo and gestation stage on prenatal survival, development, and sex ratio in the pig. J. Anim. Sci. 71, 1895–1901.
PubMed |

Dwyer, C. M. , and Stickland, N. C. (1991). Sources of variation in myofibre number within and between litters of pigs. Anim. Prod. 52, 527–533.


Dwyer, C. M. , Stickland, N. C. , and Fletcher, J. M. (1994). The influence of maternal nutrition on muscle fiber number development in the porcine fetus and on subsequent postnatal growth. J. Anim. Sci. 72, 911–917.
PubMed |

Dwyer, C. M. , Madgwick, A. J. , Ward, S. S. , and Stickland, N. C. (1995). Effect of maternal undernutrition in early gestation on the development of fetal myofibres in the guinea-pig. Reprod. Fertil. Dev. 7, 1285–1292.
CrossRef | PubMed |

Edom-Vovard, F. , Mouly, V. , Barbet, J. P. , and Butler-Browne, G. S. (1999). The four populations of myoblasts involved in human limb muscle formation are present from the onset of primary myotube formation. J. Cell Sci. 112((Pt 2)), 191–199.
PubMed |

Fahey, A. J. , Brameld, J. M. , Parr, T. , and Buttery, P. J. (2005). The effect of maternal undernutrition before muscle differentiation on the muscle fiber development of the newborn lamb. J. Anim. Sci. 83, 2564–2571.
PubMed |

Foxcroft G., Bee G., Dixon W. T., Hahn M., Harding J., Patterson J., Putman T., Sarmento S., Smit M., Tse W.-Y., and Town S. (2007). Consequences of selection for litter size on piglet development. In ‘Paradigms in Pig Science’. (Eds J. Wiseman, M. A. Varley, S. McOrist and B. Kemp.) pp. 207–229. (Nottingham University Press: Thrumpton, Nottingham.)

Handel, S. E. , and Stickland, N. C. (1987). Muscle cellularity and birth weight. Anim. Prod. 44, 311–317.


Hegarty, P. V. , and Allen, C. E. (1978). Effect of pre-natal runting on the post-natal development of skeletal muscles in swine and rats. J. Anim. Sci. 46, 1634–1640.
PubMed |

Kassar-Duchossoy, L. , Gayraud-Morel, B. , Gomes, D. , Rocancourt, D. , Buckingham, M. , Shinin, V. , and Tajbakhsh, S. (2004). Mrf4 determines skeletal muscle identity in Myf5:Myod1 double-mutant mice. Nature 431, 466–471.
CrossRef | PubMed |

Koch, I. , Slotta-Huspenina, J. , Hollweck, R. , Anastasov, N. , Hofler, H. , Quintanilla-Martinez, L. , and Fend, F. (2006). Real-time quantitative RT–PCR shows variable, assay-dependent sensitivity to formalin fixation: implications for direct comparison of transcript levels in paraffin-embedded tissues. Diagn. Mol. Pathol. 15, 149–156.
CrossRef | PubMed |

Kochhar, H. P. , Peippo, J. , and King, W. A. (2001). Sex-related embryo development. Theriogenology 55, 3–14.
CrossRef | PubMed |

Livak, K. J. , and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods 25, 402–408.
CrossRef | PubMed |

Masuda, N. , Ohnishi, T. , Kawamoto, S. , Monden, M. , and Okubo, K. (1999). Analysis of chemical modification of RNA from formalin-fixed samples and optimization of molecular biology applications for such samples. Nucleic Acids Res. 27, 4436–4443.
CrossRef | PubMed |

Maxfield, E. K. , Sinclair, K. D. , Dunne, L. D. , Broadbent, P. J. , Robinson, J. J. , Stewart, E. , Kyle, D. G. , and Maltin, C. A. (1998). Temporary exposure of ovine embryos to an advanced uterine environment does not affect fetal weight but alters fetal muscle development. Biol. Reprod. 59, 321–325.
CrossRef | PubMed |

Pomp, D. , Good, B. A. , Geisert, R. D. , Corbin, C. J. , and Conley, A. J. (1995). Sex identification in mammals with polymerase chain reaction and its use to examine sex effects on diameter of Day 10 or 11 pig embryos. J. Anim. Sci. 73, 1408–1415.
PubMed |

Quigley, S. P. , Kleemann, D. O. , Kakar, M. A. , Owens, J. A. , Nattrass, G. S. , Maddocks, S. , and Walker, S. K. (2005). Myogenesis in sheep is altered by maternal feed intake during the peri-conception period. Anim. Reprod. Sci. 87, 241–251.
CrossRef | PubMed |

Rehfeldt, C. , Fiedler, I. , Weikard, R. , Kanitz, E. , and Ender, K. (1993). It is possible to increase skeletal muscle fibre number in utero. Biosci. Rep. 13, 213–220.
CrossRef | PubMed |

Stockdale, F. E. (1992). Myogenic cell lineages. Dev. Biol. 154, 284–298.
CrossRef | PubMed |

Tilley, R. E. , McNeil, C. J. , Ashworth, C. J. , Page, K. R. , and McArdle, H. J. (2007). Altered muscle development and expression of the insulin-like growth factor system in growth-retarded fetal pigs. Domest. Anim. Endocrinol. 32, 167–177.
CrossRef | PubMed |

Town, S. C. , Putman, C. T. , Turchinsky, N. J. , Dixon, W. T. , and Foxcroft, G. R. (2004). Number of conceptuses in utero affects porcine fetal muscle development. Reproduction 128, 443–454.
CrossRef | PubMed |

Town, S. C. , Patterson, J. L. , Pereira, C. Z. , Gourley, G. , and Foxcroft, G. R. (2005). Embryonic and fetal development in a commercial dam-line genotype. Anim. Reprod. Sci. 85, 301–316.
PubMed |

van der Lende, T. , and de Jager, D. (1991). Death risk and preweaning growth rate of piglets in relation to the within-litter weight distribution at birth. Livest. Prod. Sci. 28, 73–84.
CrossRef |

Venuti, J. M. , Morris, J. H. , Vivian, J. L. , Olson, E. N. , and Klein, W. H. (1995). Myogenin is required for late but not early aspects of myogenesis during mouse development. J. Cell Biol. 128, 563–576.
CrossRef | PubMed |

Vinsky, M. D. , Novak, S. , Dixon, W. T. , Dyck, M. K. , and Foxcroft, G. R. (2006). Nutritional restriction in lactating primiparous sows selectively affects female embryo survival and overall litter development. Reprod. Fertil. Dev. 18, 347–355.
CrossRef | PubMed |

Wigmore, P. M. , and Stickland, N. C. (1983). Muscle development in large and small pig fetuses. J. Anat. 137((Pt 2)), 235–245.
PubMed |

Wise, T. H. , and Christenson, R. K. (1992). Relationship of fetal position within the uterus to fetal weight, placental weight, testosterone, estrogens, and thymosin beta 4 concentrations at 70 and 104 days of gestation in swine. J. Anim. Sci. 70, 2787–2793.
PubMed |

Yuan, J. S. , Reed, A. , Chen, F. , and Stewart, C. N. (2006). Statistical analysis of real-time PCR data. BMC Bioinformatics 7, 85.
CrossRef | PubMed |



Rent Article (via Deepdyve) Export Citation Cited By (5)