Oocyte developmental competence is reduced in sows during the seasonal infertility period
M. Bertoldo A C , P. K. Holyoake B , G. Evans A and C. G. Grupen AA Faculty of Veterinary Science, The University of Sydney, Camden, NSW 2570, Australia.
B Wagga Wagga Agricultural Institute, Industry and Investment NSW, Wagga Wagga, NSW 2650, Australia.
C Corresponding author. Email: m.bertoldo@usyd.edu.au
Reproduction, Fertility and Development 22(8) 1222-1229 https://doi.org/10.1071/RD10093
Submitted: 4 May 2010 Accepted: 26 May 2010 Published: 1 October 2010
Abstract
The modern domestic sow exhibits a period of impaired reproductive performance during the late summer and early autumn months, known as ‘seasonal infertility’. A reduction in farrowing rate due to pregnancy loss is the most economically important manifestation of seasonal infertility. The aim of the present study was to determine whether there are changes in oocyte developmental competence associated with season. Ovaries were collected in pairs from sows sourced from commercial piggeries and slaughtered 4 days after weaning during winter and summer–autumn. Following oocyte IVM and parthenogenetic activation, the ability of oocytes from large follicles to form blastocysts was greater in winter (54.94 ± 6.11%) than in summer (21.09 ± 5.59%). During winter, the proportion of oocytes developing to the blastocyst stage from large follicles was significantly higher (54.94 ± 6.11%) than those oocytes from small follicles (23.17 ± 6.02%). There was no effect of season on the proportion of oocytes developing to the blastocyst stage from small follicles. There was no effect of follicle size on blastocyst formation from those oocytes recovered during summer. Blastocysts derived from small follicles during summer had the lowest number of cells (24.25 ± 1.48) compared with blastocysts derived from large follicles during winter (37.5 ± 1.3; P < 0.05). The mean progesterone concentration in follicular fluid collected from small follicles was greater in winter than summer (1235.55 ± 164.47 v. 701.3 ± 115.5 nmol L–1, respectively; P < 0.001). The mean progesterone concentration in the follicular fluid of large follicles was also greater in winter than in summer (2470.9 ± 169.1 v. 1469.2 ± 156.5 nmol L–1, respectively; P < 0.001). Regression analysis revealed a positive correlation between progesterone concentration and oocyte developmental competence. The results indicate that porcine oocytes fail to reach their full developmental potential during the period of seasonal infertility, suggesting that the pregnancy losses observed at this time of year may be due to reduced oocyte developmental competence.
Additional keywords: blastocyst, follicle, progesterone.
Acknowledgements
The authors are grateful to the Research Centre for Reproductive Health, University of Adelaide, Animal Reproduction Co. Pty Ltd and the Department of Zoology, University of Melbourne, for the use of their facilities. Peter Thomson is acknowledged for his statistical assistance. Bioniche Animal Health (A/Asia) is thanked for the donation of gonadotrophins. The authors also thank Big River Pork, Diamond Valley Pork and the farm groups that participated in the present study. This research was supported by the Australian Pork CRC. M.B. was supported by a postgraduate research scholarship from the Australian Pork CRC. The authors declare that there is no conflict of interest that would prejudice the impartiality of this scientific work.
Ainsworth, L. , Tsang, B. K. , Downey, B. R. , and Marcus, G. J. (1990). The synthesis and actions of steroids and prostaglandins during follicular maturation in the pig. J. Reprod. Fertil. Suppl. 40, 137–150.
| PubMed | CAS |
Mermillod, P. , Oussaid, B. , and Cognie, Y. (1999). Aspects of follicular and oocyte maturation that affect the developmental potential of embryos. J. Reprod. Fertil. Suppl. 54, 449–460.
| PubMed | CAS |
Peltoniemi, O. A. T. , Easton, B. G. , Love, R. J. , Klupiec, C. , and Evans, G. (1995). Effect of chronic treatment with a GnRH agonist (goserelin) on LH secretion and early pregnancy in gilts. Anim. Reprod. Sci. 40, 121–133.
| Crossref | GoogleScholarGoogle Scholar | CAS |
Peltoniemi, O. A. T. , Love, R. J. , Klupiec, C. , and Evans, G. (1997). Effect of feed restriction and season on LH and prolactin secretion, adrenal response, insulin and FFA in group housed pregnant gilts. Anim. Reprod. Sci. 49, 179–190.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Prunier, A. , Quesnel, H. , de Braganca, M. M. , and Kermabon, A. Y. (1996). Environmental and seasonal influences on the return-to-oestrus after weaning in primiparous sows: a review. Livest. Prod. Sci. 45, 103–110.
| Crossref | GoogleScholarGoogle Scholar |
Sato, C. , Shimada, M. , Mori, T. , Kumasako, Y. , Otsu, E. , Watanabe, H. , and Utsunomiya, T. (2007). Assessment of human oocyte developmental competence by cumulus cell morphology and circulating hormone profile. Reprod. Biomed. Online 14, 49–56.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Schoevers, E. J. , Colenbrander, B. , and Roelen, B. A. J. (2007). Developmental stage of the oocyte during antral follicle growth and cumulus investment determines in vitro embryo development of sow oocytes. Theriogenology 67, 1108–1122.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Silva, C. C. , Rosa, H. J. , and Knight, P. G. (2006). Seasonal variations in the developmental competence of bovine oocytes matured in vitro. Vet. Rec. 158, 473–475.
| PubMed | CAS |
Smith, C. A. , and Almond, G. W. (1991). Effects of season and stage of gestation on luteinizing hormone release in gilt. Can. J. Vet. Res. 55, 294–297.
| CAS | PubMed |
Somfai, T. , Kikuchi, K. , Onishi, A. , Iwamoto, M. , Fuchimoto, D. , Bali-Papp, A. , Sato, E. , and Nagai, T. (2004). Relationship between the morphological changes of somatic compartment and the kinetics of nuclear and cytoplasmic maturation of oocytes during in vitro maturation of porcine follicular oocytes. Mol. Reprod. Dev. 68, 484–491.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Tanghe, S. , Van Soom, A. , Nauwynck, H. , Coryn, M. , and de Kruif, A. (2002). Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol. Reprod. Dev. 61, 414–424.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Tast, A. , Peltoniemi, O. A. T. , Virolainen, J. V. , and Love, R. J. (2002). Early disruption of pregnancy as a manifestation of seasonal infertility in pigs. Anim. Reprod. Sci. 74, 75–86.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
van der Meulen, J. , Helmond, F. A. , and Oudenaarden, C. P. J. (1988). Effect of flushing of blastocysts on Days 10–13 on the life-span of the corpora lutea in the pig. J. Reprod. Fertil. 84, 157–162.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Vanderhyden, B. C. , Caron, P. J. , Buccione, R. , and Eppig, J. J. (1990). Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev. Biol. 140, 307–317.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Vázquez, M. I. , Forcada, F. , Casao, A. , Abecia, J. A. , Sosa, C. , and Palacín, I. (2010). Undernutrition and exogenous melatonin can affect the in vitro developmental competence of ovine oocytes on a seasonal basis. Reprod. Domest. Anim. ,
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Virolainen, J. V. , Love, R. J. , Tast, A. , and Peltoniemi, O. A. T. (2003). Effect of a gonadotrophin-releasing hormone antagonist on luteinising hormone secretion and early pregnancy in gilts. Reprod. Fertil. Dev. 15, 451–459.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wolfenson, D. , Sonego, H. , Bloch, A. , Shaham-Albalancy, A. , Kaim, M. , Folman, Y. , and Meidan, R. (2002). Seasonal differences in progesterone production by luteinized bovine thecal and granulosa cells. Domest. Anim. Endocrinol. 22, 81–90.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wrathall, A. E. , Wells, D. E. , Jones, P. C. , and Foulkes, J. A. (1986). Seasonal variations in serum progesterone levels in pregnant sows. Vet. Rec. 118, 685–687.
| PubMed | CAS |
Xue, J. L. , Dial, G. D. , Marsh, W. E. , and Davies, P. R. (1994). Multiple manifestations of season on reproductive performance of commercial swine. J. Am. Vet. Med. Assoc. 204, 1486–1489.
| PubMed | CAS |
Yoshioka, K. , Suzuki, C. , Tanaka, A. , Anas, I. M. , and Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–119.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Yoshizawa, M. , Watanabe, H. , and Fukui, Y. (2009). Effects of the presence and the numbers of corpora lutea in non-delivered and delivered pigs on in vitro oocyte maturation and embryonic development. J. Reprod. Dev. 55, 655–660.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zeron, Y. , Ocheretny, A. , Kedar, O. , Borochov, A. , Sklan, D. , and Arav, A. (2001). Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles. Reproduction 121, 447–454.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Zheng, P. , Si, W. , Wang, H. , Zou, R. , Bavister, B. D. , and Ji, W. (2001). Effect of age and breeding season on the developmental capacity of oocytes from unstimulated and follicle-stimulating hormone-stimulated rhesus monkeys. Biol. Reprod. 64, 1417–1421.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
