Embryo development and survival in peripubertal ewe lambs
Jennifer L. Juengel
A * , Laurel D. Quirke A , Jacqui Peers-Adams A , Peter D. Johnstone B and Peter Smith A
+ Author Affiliations
- Author Affiliations
A Agricultural Systems and Reproduction, Animal Science, Invermay Agricultural Centre, AgResearch Ltd, Puddle Alley, Mosgiel 9092, New Zealand.
B Bioinformatics & Statistics, Invermay Agricultural Centre, AgResearch Ltd, Puddle Alley, Mosgiel 9092, New Zealand.
Animal Production Science 63(12) 1177-1187 https://doi.org/10.1071/AN22417
Submitted: 9 November 2022 Accepted: 18 March 2023 Published: 13 April 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Context: Mating of ewe lambs can increase farm profitability, although uptake is limited by low reproductive success. Reproductive loss to Day 35 of pregnancy in peripubertal ewe lambs is greater than in adult ewes; however, the precise timing of this loss is unknown.
Aim: We aimed to define more clearly early embryo development and key times of loss in peripubertal ewes.
Methods: Health and development of embryos from naturally cycling crossbred ewes ~8 months of age were recorded. Following mating across 2 years, ewes were assigned to three groups (n = 80–87 per group): assessed on Day 3 of pregnancy, on Day 14, or between Day 35 and birth. For Day 3 and Day 14 groups, ewes were humanely killed, and embryos were assessed by microscope following recovery from the reproductive tract. Ultrasonography at around Days 35 and 70, and lambing data, were used to assess loss in the third group.
Key results: By Day 3 of pregnancy, 22.9% of ova released were not present as healthy embryos (P < 0.05). Embryo survival on Day 14 tended (P < 0.10) to decrease further, with 34.0% (±4.5%) of ova released not present as healthy embryos. No decrease was detected between Days 14 and 35, whereas between Day 35 and birth, an additional 6.8% reproductive loss occurred (P < 0.05). Attainment of puberty prior to introduction of the fertile ram did not affect reproductive loss. Structures collected on Day 3 ranged from one cell to 12 cells: 11% (13/120) being one cell; 49% (59/120) two to four cells; and the remainder (48/120) at least five or six cells. Conceptus length at Day 14 ranged from 5.3 to 200.0 mm, with large variation between and within animals; within-ewe variation was 67% of between-ewe variation. Concentration of progesterone at time of collection was associated (P < 0.001) with developmental stage on Day 3, but not Day 14, of pregnancy.
Conclusions: Reproductive loss in peripubertal ewes primarily occurred prior to Day 14, with much of this loss before Day 3.
Implications: Improving oocyte and oviduct quality is important to supporting normal fertilisation and early embryo development in peripubertal ewe lambs, thus improving reproductive success.
Keywords: crossbred ewes, embryo development, embryo survival, ewe lambs, mating of ewe lambs, morphology of day 14 embryo, morphology of day 3 embryo, reproductive loss.
References
Balakier H, Sojecki A, Motamedi G, Bashar S, Mandel R, Librach C (2012) Is the zona pellucida thickness of human embryos influenced by women’s age and hormonal levels? Fertility and Sterility 98, 77–83.| Is the zona pellucida thickness of human embryos influenced by women’s age and hormonal levels?Crossref | GoogleScholarGoogle Scholar |
Clune T, Lockwood A, Hancock S, Thompson AN, Beetson S, Campbell AJD, Glanville E, Brookes D, Trengove C, O’Handley R, Kearney G, Jacobson C (2022) Abortion and lamb mortality between pregnancy scanning and lamb marking for maiden ewes in Southern Australia. Animals (Basel) 12, 10
| Abortion and lamb mortality between pregnancy scanning and lamb marking for maiden ewes in Southern Australia.Crossref | GoogleScholarGoogle Scholar |
Corner-Thomas RA, Ridler AL, Morris ST, Kenyon PR (2015) Ewe lamb live weight and body condition scores affect reproductive rates in commercial flocks. New Zealand Journal of Agricultural Research 58, 26–34.
| Ewe lamb live weight and body condition scores affect reproductive rates in commercial flocks.Crossref | GoogleScholarGoogle Scholar |
Dixon AB, Knights M, Winkler JL, Marsh DJ, Pate JL, Wilson ME, Dailey RA, Seidel G, Inskeep EK (2007) Patterns of late embryonic and fetal mortality and association with several factors in sheep. Journal of Animal Science 85, 1274–1284.
| Patterns of late embryonic and fetal mortality and association with several factors in sheep.Crossref | GoogleScholarGoogle Scholar |
Edwards SJ, Juengel JL (2017) Limits on hogget lambing: the fertility of the young ewe. New Zealand Journal of Agricultural Research 60, 1–22.
| Limits on hogget lambing: the fertility of the young ewe.Crossref | GoogleScholarGoogle Scholar |
Edwards SJ, Juengel JL, O’Connell AR, Johnstone PD, Farquhar PA, Davis GH (2015) Attainment of puberty by ewes in the first year of life is associated with improved reproductive performance at 2 years of age. Small Ruminant Research 123, 118–123.
| Attainment of puberty by ewes in the first year of life is associated with improved reproductive performance at 2 years of age.Crossref | GoogleScholarGoogle Scholar |
Edwards SJ, Smaill B, O’Connell AR, Johnstone PD, Stevens DR, Quirke LD, Farquhar PA, Juengel JL (2016) Reduced ovulation rate, failure to be mated and fertilization failure/embryo loss are the underlying causes of poor reproductive performance in juvenile ewes. Animal Reproduction Science 167, 125–132.
| Reduced ovulation rate, failure to be mated and fertilization failure/embryo loss are the underlying causes of poor reproductive performance in juvenile ewes.Crossref | GoogleScholarGoogle Scholar |
El Shourbagy SH, Spikings EC, Freitas M, St John JC (2006) Mitochondria directly influence fertilisation outcome in the pig. Reproduction 131, 233–245.
| Mitochondria directly influence fertilisation outcome in the pig.Crossref | GoogleScholarGoogle Scholar |
Farrell LJ, Kenyon PR, Morris ST, Tozer PR (2020) The impact of hogget and mature flock reproductive success on sheep farm productivity. Agriculture 10, 566
| The impact of hogget and mature flock reproductive success on sheep farm productivity.Crossref | GoogleScholarGoogle Scholar |
Fermin LM, Pain SJ, Gedye KR, Morel PCH, Kenyon PR, Blair HT (2018a) Timing of exogenous progesterone administration is critical for embryo development and uterine gene expression in an ovine model of maternal constraint. Reproduction, Fertility and Development 1699–1712.
| Timing of exogenous progesterone administration is critical for embryo development and uterine gene expression in an ovine model of maternal constraint.Crossref | GoogleScholarGoogle Scholar |
Fermin LM, Pain SJ, Morel PCH, Gedye KR, Kenyon PR, Blair HT (2018b) Effect of exogenous progesterone on embryo size and ewe uterine gene expression in an ovine ‘dam size’ model of maternal constraint. Reproduction, Fertility and Development 30, 766–778.
| Effect of exogenous progesterone on embryo size and ewe uterine gene expression in an ovine ‘dam size’ model of maternal constraint.Crossref | GoogleScholarGoogle Scholar |
Ferreira-Silva JC, Freitas Neto LM, Moura MT, Filho FT, Oliveira LRS, Bartolomeu CC, Oliveira MAL (2018) Conceptus loss in Santa Inês ewes carrying twin pregnancies by natural mating or embryo transfer. Theriogenology 115, 94–98.
| Conceptus loss in Santa Inês ewes carrying twin pregnancies by natural mating or embryo transfer.Crossref | GoogleScholarGoogle Scholar |
Gandolfi F, Milanesi E, Pocar P, Luciano AM, Brevini TAL, Acocella F, Lauria A, Armstrong DT (1998) Comparative analysis of calf and cow oocytes during in vitro maturation. Molecular Reproduction and Development 49, 168–175.
| Comparative analysis of calf and cow oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar |
Gaskins CT, Snowder GD, Westman MK, Evans M (2005) Influence of body weight, age, and weight gain on fertility and prolificacy in four breeds of ewe lambs. Journal of Animal Science 83, 1680–1689.
| Influence of body weight, age, and weight gain on fertility and prolificacy in four breeds of ewe lambs.Crossref | GoogleScholarGoogle Scholar |
Hare L, Bryant MJ (1985) Ovulation rate and embryo survival in young ewes mated either at puberty or at the second or third oestrus. Animal Reproduction Science 8, 41–52.
| Ovulation rate and embryo survival in young ewes mated either at puberty or at the second or third oestrus.Crossref | GoogleScholarGoogle Scholar |
Kenyon PR, Thompson AN, Morris ST (2014) Breeding ewe lambs successfully to improve lifetime performance. Small Ruminant Research 118, 2–15.
| Breeding ewe lambs successfully to improve lifetime performance.Crossref | GoogleScholarGoogle Scholar |
Kleemann DO, Walker SK, Seamark RF (1994) Enhanced fetal growth in sheep administered progesterone during the first three days of pregnancy. Journal of Reproduction and Fertility 102, 411–417.
| Enhanced fetal growth in sheep administered progesterone during the first three days of pregnancy.Crossref | GoogleScholarGoogle Scholar |
Mann GE, Fray MD, Lamming GE (2006) Effects of time of progesterone supplementation on embryo development and interferon-τ production in the cow. The Veterinary Journal 171, 500–503.
| Effects of time of progesterone supplementation on embryo development and interferon-τ production in the cow.Crossref | GoogleScholarGoogle Scholar |
Marco-Jiménez F, Naturil-Alfonso C, Jiménez-Trigos E, Lavara R, Vicente JS (2012) Influence of zona pellucida thickness on fertilization, embryo implantation and birth. Animal Reproduction Science 132, 96–100.
| Influence of zona pellucida thickness on fertilization, embryo implantation and birth.Crossref | GoogleScholarGoogle Scholar |
Murakoshi Y, Sueoka K, Takahashi K, Sato S, Sakurai T, Tajima H, Yoshimura Y (2013) Embryo developmental capability and pregnancy outcome are related to the mitochondrial DNA copy number and ooplasmic volume. Journal of Assisted Reproduction and Genetics 30, 1367–1375.
| Embryo developmental capability and pregnancy outcome are related to the mitochondrial DNA copy number and ooplasmic volume.Crossref | GoogleScholarGoogle Scholar |
Nephew KP, McClure KE, Ott TL, Dubois DH, Bazer FW, Pope WF (1991) Relationship between variation in conceptus development and differences in estrous cycle duration in ewes. Biology of Reproduction 44, 536–539.
| Relationship between variation in conceptus development and differences in estrous cycle duration in ewes.Crossref | GoogleScholarGoogle Scholar |
Nephew KP, Cárdenas H, McClure KE, Ott TL, Bazer FW, Pope WF (1994) Effects of administration of human chorionic gonadotropin or progesterone before maternal recognition of pregnancy on blastocyst development and pregnancy in sheep. Journal of Animal Science 72, 453–458.
| Effects of administration of human chorionic gonadotropin or progesterone before maternal recognition of pregnancy on blastocyst development and pregnancy in sheep.Crossref | GoogleScholarGoogle Scholar |
O’Brien JK, Dwarte D, Ryan JP, Maxwell WM, Evans G (1996) Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep. Reproduction, Fertility and Development 8, 1029–1037.
| Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep.Crossref | GoogleScholarGoogle Scholar |
O’Brien JK, Dwarte D, Ryan JP, Maxwell WMC, Evans G (2000) Comparison of in vitro maturation, in vitro fertilization, metabolism and ultrastructure of oocytes from prepubertal and adult pigs. Reproduction in Domestic Animals 35, 101–107.
| Comparison of in vitro maturation, in vitro fertilization, metabolism and ultrastructure of oocytes from prepubertal and adult pigs.Crossref | GoogleScholarGoogle Scholar |
O’Connell AR, Hurst PR, Davis GH, McNatty KP, Taylor SL, Juengel JL (2013) An earlier rise in systemic progesterone and increased progesterone in the uterine vein during early pregnancy are associated with enhanced embryonic survival in the ewe. Theriogenology 80, 269–274.
| An earlier rise in systemic progesterone and increased progesterone in the uterine vein during early pregnancy are associated with enhanced embryonic survival in the ewe.Crossref | GoogleScholarGoogle Scholar |
O’Connell AR, Demmers KJ, Smaill B, Reader KL, Juengel JL (2016) Early embryo loss, morphology, and effect of previous immunization against androstenedione in the ewe. Theriogenology 86, 1285–1293.
| Early embryo loss, morphology, and effect of previous immunization against androstenedione in the ewe.Crossref | GoogleScholarGoogle Scholar |
Paganoni BL, Ferguson MB, Fierro S, Jones C, Kearney GA, Kenyon PR, Macleay C, Vinoles C, Thompson AN (2014) Early reproductive losses are a major factor contributing to the poor reproductive performance of Merino ewe lambs mated at 8-10 months of age. Animal Production Science 54, 762–772.
| Early reproductive losses are a major factor contributing to the poor reproductive performance of Merino ewe lambs mated at 8-10 months of age.Crossref | GoogleScholarGoogle Scholar |
Parr RA (1992) Nutrition-progesterone interactions during early pregnancy in sheep. Reproduction, Fertility and Development 4, 297–300.
| Nutrition-progesterone interactions during early pregnancy in sheep.Crossref | GoogleScholarGoogle Scholar |
Quinlivan TD, Martin CA, Taylor WB, Cairney IM (1966) Estimates of pre- and perinatal mortality in the New Zealand Romney Marsh ewe. I. Pre- and perinatal mortality in those ewes that conceived to one service. Journal of Reproduction and Fertility 11, 379–390.
| Estimates of pre- and perinatal mortality in the New Zealand Romney Marsh ewe. I. Pre- and perinatal mortality in those ewes that conceived to one service.Crossref | GoogleScholarGoogle Scholar |
Quirke JF, Hanrahan JP (1977) Comparison of the survival in the uteri of adult ewes of cleaved ova from adult ewes and ewe lambs. Journal of Reproduction and Fertility 51, 487–489.
| Comparison of the survival in the uteri of adult ewes of cleaved ova from adult ewes and ewe lambs.Crossref | GoogleScholarGoogle Scholar |
Quirke JF, Hanrahan JP (1983) Comparison of the survival of fertilized eggs from adult ewes in the uteri of adult ewes and ewe lambs. Journal of Reproduction and Fertility 68, 289–294.
| Comparison of the survival of fertilized eggs from adult ewes in the uteri of adult ewes and ewe lambs.Crossref | GoogleScholarGoogle Scholar |
Reader KL, Cox NR, Stanton J-AL, Juengel JL (2015) Mitochondria and vesicles differ between adult and prepubertal sheep oocytes during IVM. Reproduction, Fertility and Development 27, 513–522.
| Mitochondria and vesicles differ between adult and prepubertal sheep oocytes during IVM.Crossref | GoogleScholarGoogle Scholar |
Rees E, Phillips K (2016) Breeding from ewe lambs. Available at https://projectblue.blob.core.windows.net/media/Default/Research%20Papers/Beef%20&%20Lamb/ewelambblueprint_210710-final-report.pdf [Verified 4 November 2022]
Rosales Nieto CA, Ferguson MB, Macleay CA, Briegel JR, Martin GB, Thompson AN (2013) Selection for superior growth advances the onset of puberty and increases reproductive performance in ewe lambs. Animal 7, 990–997.
| Selection for superior growth advances the onset of puberty and increases reproductive performance in ewe lambs.Crossref | GoogleScholarGoogle Scholar |
Rosales Nieto CA, Thompson AN, Martin GB (2018) A new perspective on managing the onset of puberty and early reproductive performance in ewe lambs: a review. Animal Production Science 58, 1967–1975.
| A new perspective on managing the onset of puberty and early reproductive performance in ewe lambs: a review.Crossref | GoogleScholarGoogle Scholar |
Rowson LE, Moor RM (1966) Development of the sheep conceptus during the first fourteen days. Journal of Anatomy 100, 777–785.
Satterfield MC, Bazer FW, Spencer TE (2006) Progesterone regulation of preimplantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus. Biology of Reproduction 75, 289–296.
| Progesterone regulation of preimplantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus.Crossref | GoogleScholarGoogle Scholar |
Sharma RK, Parkinson TJ, Kenyon PR, Jenkinson CMC, Blair HT (2013) Uterine environment and early embryonic development in sheep. Small Ruminant Research 115, 67–70.
| Uterine environment and early embryonic development in sheep.Crossref | GoogleScholarGoogle Scholar |
Shorten PR, Ledgard AM, Donnison M, Pfeffer PL, McDonald RM, Berg DK (2018a) A mathematical model of the interaction between bovine blastocyst developmental stage and progesterone-stimulated uterine factors on differential embryonic development observed on Day 15 of gestation. Journal of Dairy Science 101, 736–751.
| A mathematical model of the interaction between bovine blastocyst developmental stage and progesterone-stimulated uterine factors on differential embryonic development observed on Day 15 of gestation.Crossref | GoogleScholarGoogle Scholar |
Shorten PR, Donnison M, McDonald RM, Meier S, Ledgard AM, Berg D (2018b) A mathematical model of in vivo bovine blastocyst developmental to gestational Day 15. Journal of Dairy Science 101, 8401–8416.
| A mathematical model of in vivo bovine blastocyst developmental to gestational Day 15.Crossref | GoogleScholarGoogle Scholar |
Smith P, Stanton J-AL, Quirke L, Juengel JL (2019) Gestational nutrition 1: alterations to gestational nutrition can increase indicators of fertility in sheep. Reproduction 157, 199–213.
| Gestational nutrition 1: alterations to gestational nutrition can increase indicators of fertility in sheep.Crossref | GoogleScholarGoogle Scholar |
VSN International (2014) ‘GenStat for windows.’ 17th edn. (VSN International: Hemel Hempstead, UK) Available at GenStat.co.uk
Whyman D, Johnson DL, Knight TW, Moore RW (1979) Intervals between multiple ovulations in PMSG-treated and untreated ewes and the relationship between ovulation and oestrus. Journal of Reproduction and Fertility 55, 481–488.
| Intervals between multiple ovulations in PMSG-treated and untreated ewes and the relationship between ovulation and oestrus.Crossref | GoogleScholarGoogle Scholar |
