Heterozygous Inverdale ewes show increased ovulation rate sensitivity to pre-mating nutrition
K. J. Demmers A B , B. Smaill A , G. H. Davis A , K. G. Dodds A and J. L. Juengel A
+ Author Affiliations
- Author Affiliations
A Reproductive Biology, AgResearch Ltd, Invermay Agricultural Centre, Puddle Alley, Private Bag 50034, Mosgiel 9053, New Zealand.
B Corresponding author. Email: kristy.demmers@agresearch.co.nz
Reproduction, Fertility and Development 23(7) 866-875 https://doi.org/10.1071/RD10344
Submitted: 20 December 2010 Accepted: 29 March 2011 Published: 19 August 2011
Abstract
This study aimed to determine whether ewes heterozygous (I+) for the Inverdale mutation of the bone morphogenetic protein-15 (BMP15) gene with high natural ovulation rate (OR) show similar sensitivity to nutritional manipulation as non-carriers (++). Increasing pre-mating nutrition results in OR increases in sheep, but whether this effect occurs in ewes with naturally high OR is unknown. Over 2 years, I+ or ++ ewes were given high (ad libitum) or control (maintenance) pasture allowances for 6 weeks prior to mating at a synchronised oestrus, with OR measured 8 days later. The high group increased in weight compared with controls (+5.84 kg; P < 0.01), accompanied by increased OR (+19%; P < 0.01). As well as having higher OR (+45%; P < 0.01), I+ ewes responded to increased feed with a larger proportional increase in OR (+27%; P < 0.01) compared with the response in ++ ewes (+11%; P < 0.05), suggesting an interaction between BMP15 levels and nutritional signals in the follicle to control OR. Although litter size increases only tended to significance (+12%; P = 0.06), extra feed resulted in over 50% of I+ ewes giving birth to more than three lambs, compared with 20–31% of I+ ewes on maintenance rations. This information can guide feed management of prolific Inverdale ewes prior to breeding.
Additional keywords: BMP15, embryo survival, nutritional flushing, sex ratio.
References
Alink, F. M., Robinson, J. J., Mylne, M. J. A., Kenyon, R., Watt, R. G., Wood, M. J., and McEvoy, T. G. (2006). Number of ovulations in Texel × Scottish hill ewes carrying the Inverdale fecundity (FecX′) gene. Vet. Rec. 159, 154–156.| Number of ovulations in Texel × Scottish hill ewes carrying the Inverdale fecundity (FecX′) gene.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28vlsVKhsg%3D%3D&md5=23e254e6526441537c25faf8bcce9095CAS | 16877682PubMed |
Allen, D., and Lamming, G. (1961). Nutrition and reproduction in the ewe. J. Agric. Sci. 56, 69–79.
| Nutrition and reproduction in the ewe.Crossref | GoogleScholarGoogle Scholar |
Allison, A. J., and Kelly, R. W. (1979). Effects of differential nutrition on the incidence of oestrus and ovulation rate in Booroola × Romney and Romney ewes. Proc. N.Z. Soc. Anim. Prod. 39, 42–49.
Amer, P. R., McEwan, J. C., Dodds, K. G., and Davis, G. H. (1998). Cost benefit analysis of commercial use of the Inverdale prolificacy gene. Proc. N.Z. Soc. Anim. Prod. 58, 157–160.
Amer, P. R., McEwan, J. C., Dodds, K. G., and Davis, G. H. (1999). Economic values for ewe prolificacy and lamb survival in New Zealand sheep. Livest. Prod. Sci. 58, 75–90.
| Economic values for ewe prolificacy and lamb survival in New Zealand sheep.Crossref | GoogleScholarGoogle Scholar |
Bartlewski, P. M., Beard, A. P., Cook, S. J., and Rawlings, N. C. (1998). Ovarian follicular dynamics during anoestrus in ewes. Reproduction 113, 275–285.
| Ovarian follicular dynamics during anoestrus in ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFOmsr0%3D&md5=2fa3cbbd1a414b37a4a3a5b7138e684aCAS |
Clark, R. T. (1934). Studies on the physiology of reproduction in the sheep. I. The ovulation rate of the ewe as affected by the plane of nutrition. Anat. Rec. 60, 125–134.
| Studies on the physiology of reproduction in the sheep. I. The ovulation rate of the ewe as affected by the plane of nutrition.Crossref | GoogleScholarGoogle Scholar |
Coop, I. (1966). Effect of flushing on reproductive performance of ewes. J. Agric. Sci. 67, 305–323.
| Effect of flushing on reproductive performance of ewes.Crossref | GoogleScholarGoogle Scholar |
Davis, G. H. (2004). Fecundity genes in sheep. Anim. Reprod. Sci. 82–83, 247–253.
| Fecundity genes in sheep.Crossref | GoogleScholarGoogle Scholar | 15271457PubMed |
Davis, G. H. (2005). Major genes affecting ovulation rate in sheep. Genet. Sel. Evol. 37, (Suppl. 1), S11–S23.
| Major genes affecting ovulation rate in sheep.Crossref | GoogleScholarGoogle Scholar |
Davis, G. H., McEwan, J. C., Fennessy, P. F., Dodds, K. G., and Farquhar, P. A. (1991). Evidence for the presence of a major gene influencing ovulation rate on the X chromosome of sheep. Biol. Reprod. 44, 620–624.
| Evidence for the presence of a major gene influencing ovulation rate on the X chromosome of sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhsFygurs%3D&md5=e81adbd536a624db3a8d2fe0ffcde1b4CAS | 2043732PubMed |
Davis, G. H., McEwan, J. C., Fennessy, P. F., Dodds, K. G., McNatty, K. P., and O, W. S. (1992). Infertility due to bilateral ovarian hypoplasia in sheep homozygous (FecXI FecXI) for the Inverdale prolificacy gene located on the X chromosome. Biol. Reprod. 46, 636–640.
| Infertility due to bilateral ovarian hypoplasia in sheep homozygous (FecXI FecXI) for the Inverdale prolificacy gene located on the X chromosome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383ksl2muw%3D%3D&md5=1be497067d2b76b17dc3f2ac6bcd4e98CAS | 1533540PubMed |
Davis, G. H., Morris, C., and Dodds, K. G. (1998). Genetic studies of prolificacy in New Zealand sheep. Anim. Sci. 67, 289–297.
| Genetic studies of prolificacy in New Zealand sheep.Crossref | GoogleScholarGoogle Scholar |
Davis, G. H., Dodds, K. G., and Bruce, G. D. (1999). Combined effect of the Inverdale and Booroola prolificacy genes on ovulation rate in sheep. In ‘Proceedings of the Association for the Advancement of Animal Breeding and Genetics, Mandurah, WA’. pp. 74–77. Australia.
Davis, G. H., Balakrishnan, L., Ross, I. K., Wilson, T., Galloway, S. M., Lumsden, B. M., Hanrahan, J. P., Mullen, M., Mao, X. Z., Wang, G. L., Zhao, Z. S., Zeng, Y. Q., Robinson, J. J., Mavrogenis, A. P., Papachristoforou, C., Peter, C., Baumung, R., Cardyn, P., Boujenane, I., Cockett, N. E., Eythorsdottir, E., Arranz, J. J., and Notter, D. R. (2006). Investigation of the Booroola (FecB) and Inverdale (FecXI) mutations in 21 prolific breeds and strains of sheep sampled in 13 countries. Anim. Reprod. Sci. 92, 87–96.
| Investigation of the Booroola (FecB) and Inverdale (FecXI) mutations in 21 prolific breeds and strains of sheep sampled in 13 countries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVGjuro%3D&md5=62318648318b67a4571b8fb0c790cb7aCAS | 15982834PubMed |
Ducker, M. J., and Boyd, J. S. (1977). The effect of body size and body condition on the ovulation rate of ewes. Anim. Sci. 24, 377–385.
Frutos, P., Mantecón, A. R., and Giráldez, F. J. (1997). Relationship of body condition score and live weight with body composition in mature Churra ewes. Anim. Sci. 64, 447–452.
| Relationship of body condition score and live weight with body composition in mature Churra ewes.Crossref | GoogleScholarGoogle Scholar |
Galloway, S. M., McNatty, K. P., Cambridge, L. M., Laitinen, M. P., Juengel, J. L., Jokiranta, T. S., McLaren, R. J., Luiro, K., Dodds, K. G., Montgomery, G. W., Beattie, A. E., Davis, G. H., and Ritvos, O. (2000). Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25, 279–283.
| Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkvFKltbs%3D&md5=9326bcd9237d2b181f1d11a104125965CAS | 10888873PubMed |
Green, M. P., Spate, L. D., Parks, T. E., Kimura, K., Murphy, C. N., Williams, J. E., Kerley, M. S., Green, J. A., Keisler, D. H., and Roberts, R. M. (2008). Nutritional skewing of conceptus sex in sheep: effects of a maternal diet enriched in rumen-protected polyunsaturated fatty acids (PUFA). Reprod. Biol. Endocrinol. 6, 21–32.
| Nutritional skewing of conceptus sex in sheep: effects of a maternal diet enriched in rumen-protected polyunsaturated fatty acids (PUFA).Crossref | GoogleScholarGoogle Scholar | 18541015PubMed |
Hanrahan, J. P. (1982). Selection for increased ovulation rate, litter size and embryo survival. In ‘Proceedings of the Second World Congress of Genetics Applied to Livestock Production, Madrid’. pp. 294–309.
Kelly, R., and Allison, A. J. (1976). Measurement of ovulation rates by laparoscopy and effects on reproductive performance. Proc. N.Z. Soc. Anim. Prod. 36, 240–246.
Kelly, R. W., Thompson, K. F., Hawker, H., Crosbie, S. F., and McEwan, J. C. (1983). Live weight, ovulation rate and wool growth responses of light and heavy ewes to differential feeding. N.Z. J. Exp. Agric. 11, 219–224.
Kleemann, D. O., Walker, S. K., Walkley, J. R. W., Ponzoni, R. W., Smith, D. H., Grimson, R. J., and Seamark, R. F. (1991). Effect of pre-mating nutrition on reproductive performance of Booroola Merino × South Australian Merino ewes. Anim. Reprod. Sci. 26, 269–279.
| Effect of pre-mating nutrition on reproductive performance of Booroola Merino × South Australian Merino ewes.Crossref | GoogleScholarGoogle Scholar |
Landau, S., Bor, A., Leibovich, H., Zoref, Z., Nitsan, Z., and Madar, Z. (1995). The effect of ruminal starch degradability in the diet of Booroola crossbred ewes on induced ovulation rate and prolificacy. Anim. Reprod. Sci. 38, 97–108.
| The effect of ruminal starch degradability in the diet of Booroola crossbred ewes on induced ovulation rate and prolificacy.Crossref | GoogleScholarGoogle Scholar |
Lassoued, N., Rekik, M., Mahouachi, M., and Ben Hamouda, M. (2004). The effect of nutrition prior to and during mating on ovulation rate, reproductive wastage, and lambing rate in three sheep breeds. Small Rumin. Res. 52, 117–125.
| The effect of nutrition prior to and during mating on ovulation rate, reproductive wastage, and lambing rate in three sheep breeds.Crossref | GoogleScholarGoogle Scholar |
Lile, J., Blackwell, N., Thomson, N., Penno, J., MacDonald, K., Nicholas, P., Lancaster, J., and Coulter, M. (2001). Practical use of the rising plate meter (RPM) on New Zealand dairy farms. In ‘Proceedings of the New Zealand Grassland Association, Waikato’. pp. 159–164. New Zealand Grassland Association.
McDonald, P., Edwards, R. A., and Greenhalgh, J. F. D. (1981). ‘Animal Nutrition.’ (Longman Group Ltd: London.)
McMillan, W. H. (1987). The timing of CIDR withdrawal and ram introduction on ewe fertility. Proc. N.Z. Soc. Anim. Prod. 47, 139–142.
McNatty, K. P., Galloway, S. M., Wilson, T., Smith, P., Hudson, N. L., O’Connell, A., Bibby, A. H., Heath, D. A., Davis, G. H., Hanrahan, J. P., and Juengel, J. L. (2005). Physiological effects of major genes affecting ovulation rate in sheep. Genet. Sel. Evol. 37, (Suppl. 1), S25–S38.
| Physiological effects of major genes affecting ovulation rate in sheep.Crossref | GoogleScholarGoogle Scholar |
McNatty, K. P., Heath, D. A., Hudson, N. L., Lun, S., Juengel, J. L., and Moore, L. G. (2009). Gonadotrophin-responsiveness of granulosa cells from bone morphogenetic protein 15 heterozygous mutant sheep. Reproduction 138, 545–551.
| Gonadotrophin-responsiveness of granulosa cells from bone morphogenetic protein 15 heterozygous mutant sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOgtrjN&md5=989b7e2017e9b2648d77eafa8f44226cCAS | 19535491PubMed |
Montgomery, G. W., Bray, A. R., and Kelly, R. W. (1983). Ovulation rates of first cross Booroola compared with local breed ewes following differential feeding. Anim. Reprod. Sci. 6, 209–215.
| Ovulation rates of first cross Booroola compared with local breed ewes following differential feeding.Crossref | GoogleScholarGoogle Scholar |
Morley, F. H. W., White, D. H., Kenney, P. A., and Davis, I. F. (1978). Predicting ovulation rate from liveweight in ewes. Agric. Syst. 3, 27–45.
| Predicting ovulation rate from liveweight in ewes.Crossref | GoogleScholarGoogle Scholar |
Mulsant, P., Lecerf, F., Fabre, S., Schibler, L., Monget, P., Lanneluc, I., Pisselet, C., Riquet, J., Monniaux, D., Callebaut, I., Cribiu, E., Thimonier, J., Teyssier, J., Bodin, L., Cognie, Y., Chitour, N., and Elsen, J. M. (2001). Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Merino ewes. Proc. Natl. Acad. Sci. USA 98, 5104–5109.
| Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Merino ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt1Ons74%3D&md5=0a41523a6b6ff652de247bdf276831b4CAS | 11320249PubMed |
Rattray, P., Jagusch, K., Smith, G. W., Winn, E., and Maclean, K. (1981). Effects of genotype, liveweight, pasture type and feeding level on ovulation responses in ewes. Proc. N.Z. Soc. Anim. Prod. 41, 174–182.
Rhind, S. M., and McNeilly, A. S. (1998). Effects of level of food intake on ovarian follicle number, size and steroidogenic capacity in the ewe. Anim. Reprod. Sci. 52, 131–138.
| Effects of level of food intake on ovarian follicle number, size and steroidogenic capacity in the ewe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXls1ynur0%3D&md5=d098688dfe0cb36a73aaf757ea22d8a8CAS | 9776486PubMed |
Robinson, J. J. (1990). Nutrition in the reproduction of farm animals. Nutr. Res. Rev. 3, 253–276.
| Nutrition in the reproduction of farm animals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2FktVSgsg%3D%3D&md5=9fc75461d1910d385e671340af205a24CAS | 19094341PubMed |
Roche, J. R., Lee, J. M., and Berry, D. P. (2006). Pre-conception energy balance and secondary sex ratio – partial support for the Trivers–Willard hypothesis in dairy cows. J. Dairy Sci. 89, 2119–2125.
| Pre-conception energy balance and secondary sex ratio – partial support for the Trivers–Willard hypothesis in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xlt1eqs7s%3D&md5=dc20e119bc61500d9389020c0121ba21CAS | 16702278PubMed |
Russel, A. (1984). Body condition scoring of sheep. In Pract. 6, 91–93.
| Body condition scoring of sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c3jvVChsg%3D%3D&md5=dfe36758e64d5d6f6befcd35eb197675CAS | 6735487PubMed |
Scaramuzzi, R., and Martin, G. (2008). The importance of interactions among nutrition, seasonality and socio-sexual factors in the development of hormone-free methods for controlling fertility. Reprod. Domest. Anim. 43, 129–136.
| The importance of interactions among nutrition, seasonality and socio-sexual factors in the development of hormone-free methods for controlling fertility.Crossref | GoogleScholarGoogle Scholar | 18638114PubMed |
Scaramuzzi, R. J., Campbell, B. K., Downing, J. A., Kendall, N. R., Khalid, M., Munoz-Gutierrez, M., and Somchit, A. (2006). A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate. Reprod. Nutr. Dev. 46, 339–354.
| A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOnsrzF&md5=9155c3712574418876097eba185cbdf6CAS | 16824444PubMed |
Smith, J. (1988). Influence of nutrition on ovulation rate in the ewe. Aust. J. Biol. Sci. 41, 27–36.
| 1:STN:280:DyaK3c%2FntlCgtA%3D%3D&md5=7df94778f300a31b45662c9fe213d523CAS | 3152023PubMed |
Smith, J., and Stewart, R. (1990). Effects of nutrition on the ovulation rate of ewes. In ‘Reproductive Physiology of Merino Sheep, Concepts and Consequences’. (Eds C. Oldham, G. Martin and I. Purvis.) pp. 85–101. (School of Agriculture: The University of Western Australia.)
Smith, J., Jagusch, K., and Farquhar, P. (1983). The effect of the duration and timing of flushing on the ovulation rate of ewes. Proc. N.Z. Soc. Anim. Prod. 43, 13–16.
Smith, J., Cruickshank, G., McGowan, L., Parr, J., and Mortimer, B. (1988). Seasonal changes in oestrus, ovulation and conception of Coopworth ewes treated with CIDRs and PMSG. Proc. N.Z. Soc. Anim. Prod. 48, 99–102.
Souza, C. J., MacDougall, C., Campbell, B. K., McNeilly, A. S., and Baird, D. T. (2001). The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1 B (BMPR1B) gene. J. Endocrinol. 169, R1–R6.
| The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1 B (BMPR1B) gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFarur8%3D&md5=622448128d64f129866a58bef63472e3CAS | 11312159PubMed |
Sugiura, K., and Eppig, J. J. (2005). Society for Reproductive Biology Founders’ Lecture 2005. Control of metabolic cooperativity between oocytes and their companion granulosa cells by mouse oocytes. Reprod. Fertil. Dev. 17, 667–674.
| Society for Reproductive Biology Founders’ Lecture 2005. Control of metabolic cooperativity between oocytes and their companion granulosa cells by mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFKkt7%2FK&md5=8cce4882bb3a1db03096957584c82c8dCAS | 16364219PubMed |
Taylor, C. S., Murray, J. I., and Thonney, M. L. (1989). Breed and sex differences among equally mature sheep and goats 4. Carcass muscle, fat and bone. Anim. Sci. 49, 385–409.
Vacca, G. M., Dhaouadi, A., Rekik, M., Carcangiu, V., Pazzola, M., and Dettori, M. L. (2010). Prolificacy genotypes at BMPR 1B, BMP15 and GDF9 genes in North African sheep breeds. Small Rumin. Res. 88, 67–71.
| Prolificacy genotypes at BMPR 1B, BMP15 and GDF9 genes in North African sheep breeds.Crossref | GoogleScholarGoogle Scholar |
West, K., Meyer, H., and Nawaz, M. (1991). Effects of differential ewe condition at mating and early postmating nutrition on embryo survival. J. Anim. Sci. 69, 3931–3938.
| 1:STN:280:DyaK387jvVersA%3D%3D&md5=106ecb1438ffbbf878a7389be48d3ae2CAS | 1778804PubMed |
Wilson, T., Wu, X. Y., Juengel, J. L., Ross, I. K., Lumsden, J. M., Lord, E. A., Dodds, K. G., Walling, G. A., McEwan, J. C., O’Connell, A. R., McNatty, K. P., and Montgomery, G. W. (2001). Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biol. Reprod. 64, 1225–1235.
| Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1aqsr8%3D&md5=bc02defc484bc6ac557b11369fea952cCAS | 11259271PubMed |
