Effects of maternal nutrition during pregnancy on fetal growth and maternal constraint in sheep
C. M. C. Jenkinson A , A. K. Earl A , P. R. Kenyon A B and H. T. Blair AA Institute of Veterinary, Animal and Biomedical Sciences, Sheep Research Centre and National Research Centre for Growth and Development, Massey University, Palmerston North, New Zealand.
B Corresponding author. Email: p.r.Kenyon@massey.ac.nz
Animal Production Science 52(7) 524-532 https://doi.org/10.1071/AN11245
Submitted: 26 October 2011 Accepted: 2 March 2012 Published: 10 April 2012
Abstract
This study set out to determine the stage of gestation at which maternal constraint on fetal growth occurs and whether pregnancy nutritional level could alleviate that constraint. One-hundred and thirty-eight Cheviot (C) and 114 Suffolk (S) ewes were split into two groups and bred with either 12 S or 12 C rams to generate four ewe/fetal groups CC (C dam and C sire), CSinC (crossbred fetus in C ewe), CSinS, and SS. At Day 21 of pregnancy (P21), half of the ewes in each of the four groups were randomly allocated to either a maintenance (M) or ad libitum (A) nutritional treatment, under pastoral grazing conditions. At P100, a subgroup of singleton-bearing ewes including ewes from all four groups (n = 55 in total) were euthanised (Study 1). Maternal, placental and fetal weights and sizes were recorded. The remaining ewes were fed to appetite from P140 and were allowed to lamb (n = 114 in total, Study 2) and lamb liveweights were recorded within 12 h of birth and at average days 30 and 100 (L30, L100) of lactation.
In both studies, M ewes were lighter (P < 0.05) than A ewes, and CC and CSinC ewes were lighter (P < 0.05) than CSinS and SS ewes. In Study 1, maternal nutritional treatment had no effect (P > 0.05) on fetal bodyweight although fetuses from A ewes had heavier (P < 0.05) livers, spleens and thyroids than fetuses from M ewes. CC and CSinC fetuses were lighter (P < 0.01) than both CSinS and SS fetuses.
In Study 2, lambs born to M ewes were lighter (P < 0.05) at birth and at L100 than lambs born to A ewes. CC lambs were lighter (P < 0.01) than CSinC, CSinS and SS lambs at birth. At L30 and L100, CC lambs were lighter (P < 0.05) than CSinC lambs, which, in turn, were lighter (P < 0.05) than both CSinS and SS lambs, which did not differ (P > 0.05). Combined, these studies indicate that maternal nutrition may have little impact on singleton-offspring development until late gestation while, in contrast, dam size affected fetal size by the end of the second trimester. These data suggest that the C ewe constrains the growth of the crossbred fetus well before a ‘physical’ constraint would be expected.
References
Allen WR, Wilsher S, Turnbull C, Stewart F, Ousey J, Rossdale PD, Fowden AL (2002) Influence of maternal size on placental, fetal and postnatal growth in the horse. I. Development in utero. Reproduction (Cambridge, England) 123, 445–453.| Influence of maternal size on placental, fetal and postnatal growth in the horse. I. Development in utero.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Cls70%3D&md5=68bed6091c7a3fb51f5e6135427d7a35CAS |
Blair HT, van der Linden DS, Jenkinson CMC, Morris ST, Mackenzie DDS, Peterson SW, Firth EC, Kenyon PR (2011) Do ewe size and nutrition during pregnancy affect foetus and foetal organ weight in twins? Livestock Science 142, 99–107.
| Do ewe size and nutrition during pregnancy affect foetus and foetal organ weight in twins?Crossref | GoogleScholarGoogle Scholar |
Cafe LM, Hennessy DW, Hearnshaw H, Morris SG, Greenwood PL (2006) Influences of nutrition during pregnancy and lactation on birth weights and growth to weaning of calves sired by Piedmontese or Wagyu bulls. Australian Journal of Experimental Agriculture 46, 245–255.
| Influences of nutrition during pregnancy and lactation on birth weights and growth to weaning of calves sired by Piedmontese or Wagyu bulls.Crossref | GoogleScholarGoogle Scholar |
Clarke L, Heasman L, Juniper DT, Symonds ME (1998) Maternal nutrition in early-mid gestation and placental size in sheep. The British Journal of Nutrition 79, 359–364.
| Maternal nutrition in early-mid gestation and placental size in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivFOjsLs%3D&md5=c3a709153f35a238948d6b6d63645999CAS |
Dickinson AG, Hancock JL, Hovell GJR, Taylor SCS, Wiener G (1962) The size of lambs at birth – a study involving egg transfer. Animal Production 4, 64–79.
| The size of lambs at birth – a study involving egg transfer.Crossref | GoogleScholarGoogle Scholar |
Dyrmundsson OR (1991) Shearing time of sheep with special reference to conditions in northern Europe: a review. Icelandic Agricultural Sciences 5, 39–46.
Fox SI (1999) ‘Human physiology.’ (The McGraw-Hill Companies, Inc.: New York)
Gao F, Liu YC, Hou XZ (2009) Effect of maternal undernutrition during late pregnancy on growth and development of ovine fetal visceral organs. Asian-Australasian Journal of Animal Sciences 22, 1633–1639.
Gluckman PD, Pinal CS (2002) Maternal-placental-fetal interactions in the endocrine regulation of fetal growth. Endocrine 19, 81–90.
| Maternal-placental-fetal interactions in the endocrine regulation of fetal growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFKiur8%3D&md5=af5361c73218271708ac6a29ccf40377CAS |
Greenwood PL, Thompson AN, Ford SP (2010) Postnatal consequences of the maternal environment and of growth during prenatal life for productivity of ruminants. In ‘Management of the prenatal environment to enhance livestock productivity’. (Eds PL Greenwood, AW Bell, PE Vercoe, GJ Viljoen) pp. 3–36. (Springer Dordrecht: Heidelberg, London)
Harding JE (2001) The nutritional basis of the fetal origins of adult disease. International Journal of Epidemiology 30, 15–23.
| The nutritional basis of the fetal origins of adult disease.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvgvVGhug%3D%3D&md5=08e4120261559ddd835569264f70673bCAS |
Harding JE, Evans PC, Gluckman PD (1997) Maternal growth hormone treatment increases placental diffusion capacity but not fetal or placental growth in sheep. Endocrinology 138, 5352–5358.
| Maternal growth hormone treatment increases placental diffusion capacity but not fetal or placental growth in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnsFOqsLY%3D&md5=dc93a61b130fc6289c8933ef77a2c99bCAS |
Heasman L, Clarke L, Stephenson TJ, Symonds ME (1999) The influence of maternal nutrient restriction in early to mid-pregnancy on placental and fetal development in sheep. The Proceedings of the Nutrition Society 58, 283–288.
| The influence of maternal nutrient restriction in early to mid-pregnancy on placental and fetal development in sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MzpsFKlsA%3D%3D&md5=ae54652c0229515ef76c4fb5c5c9a3f1CAS |
Hodgson J, Matthews PNP, Matthew C, Lucas RJ (1999) Pasture measurement. In ‘New Zealand pasture and crop science’. (Eds J White, J Hodgson) pp. 59–66. (Oxford University Press: Auckland, New Zealand)
Hunter GL (1956) The maternal influence on size in sheep. The Journal of Agricultural Science 48, 36–60.
| The maternal influence on size in sheep.Crossref | GoogleScholarGoogle Scholar |
Hyatt MA, Gopalakrishnan GS, Bispham J, Gentili A, McMillen IC, Rhind SM, Rae MT, Kyle CE, Brooks AN, Jones C, Budge H, Walker D, Stephenson T, Symonds ME (2007) Maternal nutrient restriction in early pregnancy programs hepatic mRNA expression of growth-related genes and liver size in adult male sheep. The Journal of Endocrinology 192, 87–97.
| Maternal nutrient restriction in early pregnancy programs hepatic mRNA expression of growth-related genes and liver size in adult male sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktlKqtb4%3D&md5=2e2b5b44ac147806fd82f7c08b408661CAS |
Jenkinson CMC, Kenyon PR, Blair HT, Breier BH, Gluckman PD (2007) Maternal constraint in sheep breeds with diverse birth weight. Proceedings of the New Zealand Society of Animal Production 67, 187–191.
Joubert DM, Hammond J (1958) A crossbreeding experiment with cattle, with special reference to the maternal effect in South Devon – Dexter crosses. The Journal of Agricultural Science 51, 325–341.
| A crossbreeding experiment with cattle, with special reference to the maternal effect in South Devon – Dexter crosses.Crossref | GoogleScholarGoogle Scholar |
Kenyon PR (2008) A review of in-utero environmental effects on sheep production. Proceedings of the New Zealand Society of Animal Production 68, 142–155.
Kenyon PR, Morris ST, Revell DK, McCutcheon SN (2003) Shearing during pregnancy – review of a policy to increase birthweight and survival of lambs in New Zealand pastoral farming systems. New Zealand Veterinary Journal 51, 200–207.
| Shearing during pregnancy – review of a policy to increase birthweight and survival of lambs in New Zealand pastoral farming systems.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MznsVantA%3D%3D&md5=35940e22fc406c73e53a8f3458e6facfCAS |
Kenyon PR, Blair HT, Jenkinson CMC, Morris ST, Mackenzie DDS, Peterson SW, Firth EC, Johnston PL (2009) The effect of ewe size and nutritional regimen beginning in early pregnancy on ewe and lamb performance to weaning. New Zealand Journal of Agricultural Research 52, 203–212.
| The effect of ewe size and nutritional regimen beginning in early pregnancy on ewe and lamb performance to weaning.Crossref | GoogleScholarGoogle Scholar |
Kenyon PR, van der Linden DS, Jenkinson CMC, Morris ST, Mackenzie DDS, Peterson SW, Firth EC, Blair HT (2011) The effect of ewe size and nutritional regimen beginning in early pregnancy on development of singleton foetuses in late pregnancy. Livestock Science 142, 92–98.
| The effect of ewe size and nutritional regimen beginning in early pregnancy on development of singleton foetuses in late pregnancy.Crossref | GoogleScholarGoogle Scholar |
Kenyon PR, Blair HT, Jenkinson CMC (2011a) Does the lamb birth weight response to mid pregnancy shearing differ in two breeds of disparate size? Proceedings of the Association for the Advancement of Animal Breeding and Genetics 19, 351–354.
Kenyon PR, Pain SJ, Hutton PG, Jenkinson CMC, Morris ST, Peterson SW, Blair HT (2011b) Effects of twin-bearing ewe nutritional treatments on ewes and lamb performance to weaning. Animal Production Science 51, 406–415.
| Effects of twin-bearing ewe nutritional treatments on ewes and lamb performance to weaning.Crossref | GoogleScholarGoogle Scholar |
McMullen S, Osgerby JC, Milne JS, Wallace JM, Wathes DC (2005) The effects of acute nutrient restriction in the mid-gestational ewe on maternal and fetal nutrient status, the expression of placental growth factors and fetal growth. Placenta 26, 25–33.
| The effects of acute nutrient restriction in the mid-gestational ewe on maternal and fetal nutrient status, the expression of placental growth factors and fetal growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms1Grug%3D%3D&md5=f8f891338ae3ec121e645fd4ed03c812CAS |
Mellor DJ (1983) Nutritional and placental determinants of foetal growth rate in sheep and consequences for the newborn lamb. The British Veterinary Journal 139, 307–324.
Morel PCH, Blair HT, Ormsby JE, Breier BH, McCutcheon SN, Gluckman PD (1994) Influence of fetal and maternal genotype for circulating insulin like growth factor I on fetal growth in mice. Journal of Reproduction and Fertility 101, 9–14.
| Influence of fetal and maternal genotype for circulating insulin like growth factor I on fetal growth in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXkslCmtbY%3D&md5=9b91fe34c90369fd30bfbaff5858608aCAS |
Morris ST, Kenyon PR (2004) The effect of litter size and sward height on ewe and lamb performance. New Zealand Journal of Agricultural Research 47, 275–286.
| The effect of litter size and sward height on ewe and lamb performance.Crossref | GoogleScholarGoogle Scholar |
Munoz C, Carson AF, McCoy MA, Dawson LER, O’Connell NE, Gordon AW (2008) Nutritional status of adult ewes during early and mid-pregnancy. 1. Effects of plane of nutrition on ewe reproduction and offspring performance to weaning. Animal 2, 52–63.
Osgerby JC, Wathes DC, Howard D, Gadd TS (2002) The effect of maternal undernutrition on ovine fetal growth. The Journal of Endocrinology 173, 131–141.
| The effect of maternal undernutrition on ovine fetal growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1ejtr4%3D&md5=472e5efd4b2e3bddcd78a0bf5ffef87dCAS |
Rae MT, Rhind SM, Kyle CE, Miller DW, Brooks AN (2002) Maternal undernutrition alters triiodothyronine concentrations and pituitary response to GnRH in fetal sheep. The Journal of Endocrinology 173, 449–455.
| Maternal undernutrition alters triiodothyronine concentrations and pituitary response to GnRH in fetal sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1ehtb8%3D&md5=42d4ed281ac8179acb88d24438f50d97CAS |
Rattray PV, Garrett WN, East NE, Hinman N (1974) Growth, development and composition of the ovine conceptus and mammary gland during pregnancy. Journal of Animal Science 38, 613–626.
Rattray PV, Brookes IM, Nicol AM (Eds) (2007) ‘Pasture and supplements for grazing animals.’ (New Zealand Society of Animal Production, Inc.: Hamilton)
Redmer DA, Wallace JM, Reynolds LP (2004) Effect of nutrient uptake during pregnancy on fetal and placental growth and vascular development. Domestic Animal Endocrinology 27, 199–217.
| Effect of nutrient uptake during pregnancy on fetal and placental growth and vascular development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2cvot1KksQ%3D%3D&md5=ea0c8729b8dc2a9693344baddad37778CAS |
Robinson JJ, Sinclair KD, McEvoy TG (1999) Nutritional effects on foetal growth. Animal Science (Penicuik, Scotland) 68, 315–331.
Sharma RK, Jenkinson CMC, Blair HT, Kenyon PR, Parkinson TJ (2009) Maternal environment as a regulator of birth weight and body dimensions of newborn lambs. Proceedings of the New Zealand Society of Animal Production 69, 10–14.
Symonds ME (1995) Pregnancy, parturition and neonatal development – interactions between nutrition and thyroid-hormones. The Proceedings of the Nutrition Society 54, 329–343.
| Pregnancy, parturition and neonatal development – interactions between nutrition and thyroid-hormones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXptlaltro%3D&md5=dece88277a4803ffb34edab85a3de9b4CAS |
Symonds ME, Stephenson T, Gardner DS, Budge H (2007) Long-term effects of nutritional programming of the embryo and fetus: mechanisms and critical windows. Reproduction, Fertility and Development 19, 53–63.
| Long-term effects of nutritional programming of the embryo and fetus: mechanisms and critical windows.Crossref | GoogleScholarGoogle Scholar |
Vonnahme KA, Hess BW, Nijland MJ, Nathanielsz PW, Ford SP (2006) Placentomal differentiation may compensate for maternal nutrient restriction in ewes adapted to harsh range conditions. Journal of Animal Science 84, 3451–3459.
| Placentomal differentiation may compensate for maternal nutrient restriction in ewes adapted to harsh range conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1CnurfO&md5=c96089477c5102aab16d47045e746a72CAS |
Walton A, Hammond J (1938) The maternal effects on growth and conformation in Shire horse-Shetland pony crosses. Proceedings of the Royal Society of London. Series B. Biological Sciences 125, 311–335.
| The maternal effects on growth and conformation in Shire horse-Shetland pony crosses.Crossref | GoogleScholarGoogle Scholar |