Sex of co-twin in utero environment does not alter reproductive fitness of Australian Merino sheep
David O. Kleemann
A * , Simon K. Walker A , Jennifer M. Kelly A and Raul W. Ponzoni B
A
B
Abstract
Reproductive efficiency in ewes can vary widely depending on their fertility (pregnancy rate) and fecundity (litter size) and on their ability to rear multiple litters. Litter size and sex are important factors that contribute to lamb mortality, and hence reproductive efficiency. However, little is known about their interaction when fetuses of either sex grow in utero as co-twins, nor the impact that this interaction has on subsequent performance in domestic flocks.
We examined the effect of type of birth (single, twin) and of sex of co-twin (F, F[F], F[M], M, M[M], M[F] where the symbol within brackets indicates sex of co-twin) on birth weight, survival to weaning, weaning and hogget liveweights and scrotal circumference. In addition, reproductive performance (fertility, fecundity, lamb survival, weaning rate) of female progeny was examined as well as the performance of their lambs (birth and weaning weight). This large-scale study (>13 000 lambing observations) was conducted with Australian Merino sheep from four studs, mated over nine annual cycles.
Sex of co-twin had no effect on birth weight and on later stages of growth. Sex of co-twin altered survival, with fewer of the M[M] class surviving to weaning compared with other co-twin classes (P < 0.05). Scrotal circumference did not vary between the male classes. Although reproductive performance (fecundity, lamb survival, weaning rate) was greater in ewes twin to a male (F[M]) than in single females (F) (P < 0.05), this difference could be due to greater genetic merit of twin versus single-born progeny.
Reproductive performance of females with a male co-twin exceeded that of single females; the difference could be due to greater genetic merit of twin-born ewes rather than a direct effect of in utero environment. There was no difference between females with a male co-twin and females with a co-twin of the same sex. Reproductive capacity of males was not affected by co-twin class or type of birth.
These results suggest that an increase in twinning rate by managerial or genetic means will not result in undesirable side effects due to sex of co-twin in utero.
Keywords: androgens, birth weight, co-twin, fecundity, fertility, fetal development, lamb survival, Merino sheep, reproduction, sex, scrotal size, type of birth.
References
Alexander G (1962) Temperature regulation in the new-born lamb. IV. The effect of wind and evaporation of water from the coat on metabolic rate and body temperature. Australian Journal of Agricultural Research 13, 82-99.
| Crossref | Google Scholar |
Atkins KD (1980) The comparative productivity of five ewe breeds. 3. Adult ewe performance. Australian Journal of Experimental Agriculture 20(104), 288-295.
| Crossref | Google Scholar |
Avdi M, Driancourt MA (1997) Influence of sex ratio during multiple pregnancies on productive and reproductive parameters of lambs and ewes. Reproduction Nutrition Development 37(1), 21-27.
| Crossref | Google Scholar | PubMed |
Baharin K, Beilharz RG (1977) A comparison of the performance of single and twin born Corriedale ewes and lambs. Australian Journal of Experimental Agriculture 17, 242-246.
| Crossref | Google Scholar |
Beatty RA (1956) Relation between genetic constitution of an offspring and weight of its litter-mates. Nature 178(4523), 48-49.
| Crossref | Google Scholar | PubMed |
Brien FD, Cloete SWP, Fogarty NM, Greeff JC, Hebart ML, Hiendleder S, Edwards JEH, Kelly JM, Kind KL, Kleemann DO, Plush KL, Miller DR (2014) A review of the genetic and epigenetic factors affecting lamb survival. Animal Production Science 54(6), 667-693.
| Crossref | Google Scholar |
Brown JA, Kirschten DP, Lewis GS, Taylor JB (2016) Sex of littermate twin affects lifetime ewe productivity. Sheep and Goat Research Journal 31, 1-8 Available at https://www.sheepusa.org/wp-content/uploads/2022/06/2016-Combined-SGRJ.pdf.
| Google Scholar |
Burfening PJ (1972) Prenatal and postnatal competition among twin lambs. Animal Science 15(1), 61-66.
| Crossref | Google Scholar |
Clark MM, Malenfant SA, Winter DA, Galef BG, Jr (1990) Fetal uterine position affects copulation and scent marking by adult male gerbils. Physiology & Behavior 47(2), 301-305.
| Crossref | Google Scholar | PubMed |
Clark MM, Tucker L, Galef BG, Jr (1992) Stud males and dud males: intra-uterine position effects on the reproductive success of male gerbils. Animal Behaviour 43(2), 215-221.
| Crossref | Google Scholar |
Clark MM, Vonk JM, Galef BG, Jr (1998) Intrauterine position, parenting, and nest-site attachment in male Mongolian gerbils. Developmental Psychobiology 32(3), 177-181.
| Crossref | Google Scholar | PubMed |
Cloete SWP, Heydenrych HJ (1986) Factors affecting reproduction in Merino ewes of the Tygerhoek flock. South African Journal of Animal Science 16(1), 36-42 Available at https://www.sasas.co.za/wp-content/uploads/2012/09/Cloete16Issue1_0.pdf.
| Google Scholar |
Cloete SWP, Heydenrych HJ, Du Plessis JJ (1984) The effect of two-tooth mating weight on the reproductive performance of single and twin born Merino ewes. In ‘Proceedings of the 2nd World Congress on Sheep and Beef Cattle Breeding’, Pretoria, South Africa. p. 725. (South African Stud Book and Livestock Improvement Association: Bloemfontein)
Donald HP, Purser AF (1956) Competition in utero between twin lambs. The Journal of Agricultural Science 48(2), 245-249.
| Crossref | Google Scholar |
Dwyer CM, Conington J, Corbiere F, Holmøy IH, Muri K, Nowak R, Rooke J, Vipond J, Gautier J-M (2016) Invited review: improving neonatal survival in small ruminants: science into practice. Animal 10(3), 449-459.
| Crossref | Google Scholar | PubMed |
Everett-Hincks JM, Mathias-Davis HC, Greer GJ, Auvray BA, Dodds KG (2014) Genetic parameters for lamb birth weight, survival and death risk traits. Journal of Animal Science 92, 2885-2895.
| Crossref | Google Scholar | PubMed |
Fitzgerald JA, Perkins A, Hemenway K (1993) Relationship of sex and number of siblings in utero with sexual behavior of mature rams. Applied Animal Behaviour Science 38(3–4), 283-290.
| Crossref | Google Scholar |
Foster R, Ladds P, Hoffmann D, Briggs G (1989) The relationship of scrotal circumference to testicular weight in rams. Australian Veterinary Journal 66(1), 20-22.
| Crossref | Google Scholar | PubMed |
Gifford DR, Ponzoni RW, Walkley JRW, Hynd PI, Ancell PMC (1992) A progress report on the estimation of phenotypic and genetic parameters for South Australian Merino sheep in the Turretfield resource flock. Wool Technology and Sheep Breeding 40, 114-116 Available at https://www.sheepjournal.net/index.php/WTSB/article/view/1232.
| Google Scholar |
Hatcher S, Atkins KD, Safari E (2009) Phenotypic aspects of lamb survival in Australian Merino sheep. Journal of Animal Science 87(9), 2781-2790.
| Crossref | Google Scholar | PubMed |
Kelly JM, Kleemann DO, McGrice H, Len JA, Kind KL, van Wettere WHEJ, Walker SK (2017) Sex of co-twin affects the in vitro developmental competence of oocytes derived from 6- to 8-week-old lambs. Reproduction, Fertility and Development 29(7), 1379-1383.
| Crossref | Google Scholar | PubMed |
Kleemann DO, Walker SK (2005a) Fertility in South Australian commercial Merino flocks: sources of reproductive wastage. Theriogenology 63(8), 2075-2088.
| Crossref | Google Scholar | PubMed |
Kleemann DO, Walker SK (2005b) Fertility in South Australian commercial Merino flocks: relationships between reproductive traits and environmental cues. Theriogenology 63(9), 2416-2433.
| Crossref | Google Scholar | PubMed |
Kleemann DO, Grosser TI, Walker SK (2006) Fertility in South Australian commercial Merino flocks: aspects of management. Theriogenology 65(8), 1649-1665.
| Crossref | Google Scholar | PubMed |
Korsten P, Clutton-Brock T, Pilkington JG, Pemberton JM, Kruuk LEB (2009) Sexual conflict in twins: male co-twins reduce fitness of female Soay sheep. Biology Letters 5(5), 663-666.
| Crossref | Google Scholar | PubMed |
Kritzinger NM, Stindt HW, van der Westhuysen JM (1984) Assessment of different selection criteria for reproduction rate in Dormer and SA Mutton Merino sheep. 1. Birth type and early reproductive-performance of the ewe. South African Journal of Animal Science 14(2), 79-83 Available at https://www.sasas.co.za/wp-content/uploads/2012/09/KritzingerA14Issue2_1.pdf.
| Google Scholar |
Manikkam M, Crespi EJ, Doop DD, Herkimer C, Lee JS, Yu S, Brown MB, Foster DL, Padmanabhan V (2004) Fetal programming: prenatal testosterone excess leads to fetal growth retardation and postnatal catch-up growth in sheep. Endocrinology 145(2), 790-798.
| Crossref | Google Scholar | PubMed |
Nel CL, Swan AA, Dzama K, Scholtz AJ, Cloete SWP (2021) Genetic parameters and trends for lamb survival following long-term divergent selection for number of lambs weaned in the Elsenburg Merino flock. Animal Production Science 61, 1965-1981.
| Crossref | Google Scholar |
Oldham CM, Thompson AN, Ferguson MB, Gordon DJ, Kearney GA, Paganoni BL (2011) The birthweight and survival of Merino lambs can be predicted from the profile of liveweight change of their mothers during pregnancy. Animal Production Science 51(9), 776-783.
| Crossref | Google Scholar |
Pettigrew EJ, Hickson RE, Morris ST, Lopez-Villalobos N, Pain SJ, Kenyon PR, Blair HT (2019) The effects of birth rank (single or twin) and dam age on the lifetime productive performance of female dual purpose sheep (Ovis aries) offspring in New Zealand. PLoS ONE 14(3), e0214021.
| Crossref | Google Scholar |
Ponzoni RW, Grimson RJ, Jaensch KS, Smith DH, Gifford DR, Ancell PMC, Walkley JRW, Hynd PI (1995) The Turretfield Sheep Breeding Project: messages on phenotypic and genetic parameters for South Australian Merino sheep. Proceedings of the Australian Association of Animal Breeding and Genetics 11, 303-313 Available at www.aaabg.org/livestocklibrary/1995/ab95064.pdf.
| Google Scholar |
Ponzoni RW, Grimson RJ, Jaensch KS, Smith DH, Hynd PI (1997) Birth coat: is it worth taking into consideration in Merino sheep genetic improvement programs? Wool Technology and Sheep Breeding 45(1), 12-26 Available at https://www.sheepjournal.net/index.php/WTSB/article/view/143.
| Google Scholar |
Price EO, Bench CJ, Borgwardt RE, Dally MR (2000) Sexual performance of twin ram lambs and the effect of number and sex of contemporary siblings. Applied Animal Behaviour Science 68(3), 199-205.
| Crossref | Google Scholar | PubMed |
Rohde Parfet KA, Lamberson WR, Rieke AR, Cantley TC, Ganjam VK, vom Saal FS, Day BN (1990) Intrauterine position effects in male and female swine: subsequent survivability, growth rate, morphology and semen characteristics. Journal of Animal Science 68(1), 179-185.
| Crossref | Google Scholar | PubMed |
Ryan BC, Vandenbergh JG (2002) Intrauterine position effects. Neuroscience & Biobehavioral Reviews 26(6), 665-678.
| Crossref | Google Scholar | PubMed |
Schinckel PG (1955) Inheritance of birthcoats in a strain of Merino sheep. Australian Journal of Agricultural Research 6, 595-607.
| Crossref | Google Scholar |
Skapetas B, Kalaitzidou M (2017) Current status and perspectives of sheep sector in the world. Livestock Research for Rural Development 29(2), paper 21 Available at www.lrrd.org/lrrd29/2/skap29021.html.
| Google Scholar |
Thrift FA, Dutt RH (1976) Relationship between birth type and preweaning productivity of southdown ewes. Journal of Animal Science 42(3), 560-564.
| Crossref | Google Scholar |
Turner HN (1969) Genetic improvement of reproduction rate in sheep. Animal Breeding Abstracts 37(4), 545-563.
| Google Scholar |
Turner HN, Young SSY (1969) ‘Quantitative genetics in sheep breeding.’ (Macmillan of Australia: Melbourne, Vic., Australia) Available at http://hdl.handle.net/102.100.100/320116?index=1
van der Hoeven T, Lefevre R, Mankes R (1992) Effects of intrauterine position on the hepatic microsomal polysubstrate monooxygenase and cytosolic glutathione S-transferase activity, plasma sex steroids and relative organ weights in adult male and female Long-Evans rats. The Journal of Pharmacology and Experimental Therapeutics 263(1), 32-39 Available at https://jpet-aspetjournals-org.eu1.proxy.openathens.net/content/jpet/263/1/32.full.pdf.
| Google Scholar | PubMed |
Vanderick S, Auvray B, Newman S-A, Dodds KG, Gengler N, Everett-Hincks JM (2015) Derivation of a new lamb survival trait for the New Zealand sheep industry. Journal of Animal Science 93, 3765-3772.
| Crossref | Google Scholar | PubMed |
van der Westhuysen JM (1973) The relationship of birth status and early reproductive performance with lifetime reproductive performance in Merino ewes. South African Journal of Animal Science 3(1), 29-31 Available at https://www.sasas.co.za/wp-content/uploads/2012/09/vdWesthuysenB3Issue1_1.pdf.
| Google Scholar |
vom Saal FS (1989) Sexual differentiation in litter-bearing mammals: influence of sex of adjacent fetuses in utero. Journal of Animal Science 67(7), 1824-1840.
| Crossref | Google Scholar | PubMed |
vom Saal FS, Bronson FH (1980) Sexual characteristics of adult female mice are correlated with their blood testosterone levels during prenatal development. Science 208(4444), 597-599.
| Crossref | Google Scholar | PubMed |
Vom Saal FS, Quadagno DM, Even MD, Keisler LW, Keisler DH, Khan S (1990) Paradoxical effects of maternal stress on fetal steroids and postnatal reproductive traits in female mice from different intrauterine positions. Biology of Reproduction 43(5), 751-761.
| Crossref | Google Scholar | PubMed |
