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The Relationship between Breed and Litter Size in Sheep and Maternal Serum Concentrations of Placental Lactogen, Estradiol

and Progesterone W. R. Butler, S. M. Fullenkamp, L. A. Cappiello and S. Handwerger J ANIM SCI 1981, 53:1077-1081.

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Duke Univ. 4. Circulating concentrations of placental lactogen were directly related to litter size in all breeds. Taylor between January 1 and April 15.. S. Michel ram of their own breed. Handwerger a Cornell University. with the greatest concentrations being observed in Finnish Landrace ewes bearing three lambs. parturition dates 2 Dept. A. in addition. (1972. The relationship between litter size and placental lactogen concentrations.T H E R E L A T I O N S H I P B E T W E E N B R E E D A N D L I T T E R S I Z E IN SHEEP A N D M A T E R N A L S E R U M C O N C E N T R A T I O N S OF PLACENTAL LACTOGEN. Hampshire and Corriedale ewe lambs were mated to Suffolk 1The authors express appreciation to Dr. Sheep. 1977. thus providing a mechanism by which the mammary gland is suitably prepared for future demands (Hayden et al. of Anita. PL production in goats is directly related to the number of young in utero. except for Corriedale ewes. Cappiello and S. Fullenkamp. like placental lactogen. Durham. 1964. but ewe lambs bearing crossbred fetuses had higher placental lactogen concentrations than ewes of the same breed carrying purebred offspring. No. within a breed-age group. 1975b). Davies. rams. Blood was collected biweekly beginning 6 to 8 weeks before expected parturition from ewe lambs and mature ewes of the Hampshire. hay and ground concentrate. 1077 JOURNAL OF ANIMAL SCIENCE. It is known that the number of offspring influences milk production in sheep (Alexander and Davies. Itbaca N Y 1 4 8 5 3 Summary Milk production in sheep is known to be affected by breed and litter size. Placental lactogen concentrations were similar in all animals bearing twins. ESTRADIOL AND PROGESTERONE 1 W. was related to litter size and. Progesterone.. Medical Center. together with the absence of difference in estradiol secretion. Sci.. 1967. breed differences in lactational ability have been reported (Gardner and Hogue. 1978. P. for assistance in typing this manuscript. Nicoll for technical assistance and to L. F. Butler 2. All lambings occurred and V. (Key Words: Placental Lactogen..) Introduction The identification and measurement of placental lactogen (PL) during gestation in domestic ruminants (see Blank et al. L. Gardner and Hogue. All animals were housed in adjacent pens and were fed a diet of grass silage. no significant breed differences were observed. Serum estradiol concentrations 2 to 5 weeks prepartum did not differ between ewes of different breeds or ewes with different litter sizes. To investigate a possible hormonal basis for such effects. 1976) and goats (Hayden et al. 53. which had the lowest concentrations. presumably placental mass. Materialsand Methods Blood samples were collected by jugular puncture biweekly from mating to parturition from nine Dorset ewe lambs. for review) has led to studies showing a high correlation between circulating levels of this hormone and postpartum milk production by c a t d e (Bolander et al. R. Each group of ewes was mated to a single ram. and. Vol. 1981 . A. Progesterone. Estradiol. we measured maternal serum concentrations of placental lactogen. Corriedale and Finnish Landrace (Finnsheep) breeds. Karaka. while other ewes were mated to a purebred Ohenacu for statistical analysis. Peart et al. 1959. NC 27710. 1979). suggests that differences in production of the lactogenic hormone may contribute to the superior lactational performance that has been reported for ewes which bear muhiple offspring. 1979). The purpose of the present study was to investigate the effect of breed and litter size on the secretion of PL and other mammogenic hormones in sheep. R. estradiol and progesterone during late gestation in sheep of several breeds and ages. Peart. 1966). 1963. ranged over no more than 3 weeks. Among monotocous animals. M. and. Furthermore.

Handwerger et al. PL concentrations were highest in Finnsheep bearing three lambs. 1978) and estradiol. Serum samples were stored at . Pooled serum samples were included in each hormone assay at three volumes for determination of intra. This serum correction was . (1978) but somewhat later than the period when peaks were detected by a radioreceptor assay technique (Kelly et al. 1977. Because our results for Dorset ewe lambs and all the reports cited above indicated that maximum PL concentrations occur during late gestation.5 to 1. Analysis of variance showed highly significant differences among breeds and among number of offspring. Maternal serum concentrations of placental lactogen (oPL) and progesterone (PROG) during gestation (weeks) in Dorset ewe lambs. Charcoaltreated serum from cows was used as the assay blank for the calculation of serum samples. The greatest differences in mean concentrations of PL were related to litter size. for PL.. estradiol and progesterone. 1977). 1974).17-3H) estradiol 4 was used as tracer after Sephadex LH-20 purification. and concentrations increased with increasing number of offspring. but no significant breed x litter size interaction. Serum samples (400 to 1. (1974).16. PL concentrations were maximal at week 19 which is in agreement with C h a n e t al.1078 B U T L E R ET AL.. 1974. the coefficients were 8 and 11% (n = 6). . Two of the animals bore twins. Comparison of serum PL concentrations in Finnsheep showed no differences due to age or previous parity in the secretion of this hormone.. Lambs in these two groups also had higher PL concentrations than the N-9 1. concentrations occurred simultaneously with the increase in PL concentrations (Kelly et al. in accordance with previous reports (Kelly et aL. This was true in all breed-age groups. The antiserum was diluted to an initial concentration of 1:50. Procedural losses were measured by the addition of 200 to 500 cpm (3H) estradiol before extraction (Chenault et al... This difference may have been due to the techniques used or to variation among animals. PL first became detectable in the peripheral circulation at about 60 days of gestation.. An increase in serum progesterone 2C0 8 I t 4 New England Nuclear. Hormone concentrations were compared among breed-age groups within litter size by Duncan's new multiple range test. Mean serum PL concentrations between 2 and 5 weeks prepartum for several breed-age groups are shown in table 1. 1976. progesterone (Gengenbach et al. Figure 1. 10 and 12% (n = 8) and 5 and 7% (n = 8). Robertson et al.000/J1) in duplicate were extracted with 5 ml freshly redistilled benzene: toluene (2/1 v/v).4. This was not the case for monotocous Corriedales and Hampshires.6. 1975). MA. Estradiol-173 was measured with antibody GDN-#244. Estradiol from serum extracts was isolated on Sephadex LH-20 columns (50 mg) eluted with chlorofbrm: methanol: heptane: water (500:225:1500:9). Hormones concentrations in two samples from each ewe collected between 2 and 5 weeks prepartum were averaged and subjected to least-squares analysis of variance.5 pg/ml.and interassay coefficients of variation.2~3 803 Results and Discussion The pattern of serum concentrations of PL and progesterone during gestation in Dorset ewe lambs is shown in figure 1. Boston.7. Blood samples were allowed to clot and then were refrigerated (4 C) for 24 hr before centrifugation. Mean recovery averaged 84%. 1980). A similar extraction efficiency (75 to 90%) was calculated from the recovery of estradiol added to serum..000 and (2. respectively. which is similar to that previously described by Korenman et al. the lambs of each breed had higher circulating concentrations of PL than did the adults. 1974.2 0 C until aliquots were removed for radioimmunoassay of PL (Handwerger et al. 1976). blood samples were collected during this period for evaluation of breed differences.

More direct tests of the effect of crossbreeding. but nursing a single lamb (Alexander and Davies. Thus.3(12) avalues listed are mean + standard errors.672 + 421(6) 1. Davies.8 8. n-. Gardner and Hogue. 1959. Estrogen and progesterone are important components in the mammogenic complex in a number of species (Anderson. The enhanced hormone production in the Corriedale and Hampshire lambs may have been an effect of crossbreeding. are needed.997 • 289(6) x 2. n = 20.260 + 163(10) b 939 • 137(8) 1.PLACENTAL LACTOGEN AND LITTER SIZE TABLE 1. 1972).271 • 153(9) c 790 +.6 • • • • • • 1079 .343 • 706(2) 3 2. 5 + .05).267 • 167(12) d 1. Peart e t a l . 2 kg. b'c'd~X'YMeanconcentrations within rows and columns with the same superscript are different (P<. Thimonier e t al. Serum estradiol concentrations were remarkably consistent within litter sizes. Although birth weights of lambs were not available in all groups.3 +.9 10. as they were mated to Suffolk rams.3(14) 1. (1977) have reported that total estrogen concentrations on day 102 of pregnancy are related to numbers of lambs born and total birth weight. 1963). When a study was conducted in which this nursing regimen was investigated. Peart.3 9. 1964) are the likely explanation for the observed differences in progesterone secretion.2 11. 1967. They were measured in the present study for an assessment of breed and litter size effects. Serum progesterone concentrations during late gestation increased as number of fetuses increased (table 2). 1977). Davies. 1974). numbers in parentheses are numbers of animals. 1959.205(7) 2 1. the only significant difference in PL concentrations was between Hampshire and Corriedale ewes (table 1). 1979) is directly related to the number of offspring.9. Among ewes bearing twins. respectively). THE RELATIONSHIP BETWEEN BREED AND NUMBER OF OFFSPRING ON SERUM PLACENTAL LACTOGEN (PL) AND ESTRADIOL (E) CONCENTRATIONS IN PREGNANT LAMBS AND MATURE EWESa PL in ewes with varying number of offspring. in suport of previous observations (Gadsby e t al. n = 54. Enhanced milk secretion following the birth of multiple young is apparent within the first week postpartum in both species.831 • 246(6) d 1. Unfortunately.. 1966). ng/ml Breed-age group Finnsheep ewes Finnsheep lambs Corriedale ewes Corriedale lambs Hampshire ewes Hampshire lambs Dorset lambs 1 1.4 12. and the data were pooled within breed-age groups (table 1). whereas all other animals were bearing purebred lambs. other lambs (Dorset and Finnsheep).150(4)Y 669 • 53(7) bc 1. 5972.5(19) . Progesterone concentrations were generally lower in Finnsheep than in Hampshire or Corriedale ewes. The effects of multiple births on milk yield have been attributed to increased suckling intensity (Alexander and Davies.8(14) 1.4.7(10) 1. Milk production in both sheep (Alexander and Davies. Milk production was 150% greater in ewes bearing and nursing twins than in ewes either bearing singles or ewes bearing twins. because this hormone derives primarily from the placenta during late gestation (Linzell and Heap. 1964.802 • 665(4)Y E.7 + ..584 • 186(16) 1. Finnsheep lambs weighed less than Hampshire or Corriedale lambs (2. 1975b) and goats (Hayden e t al. 1959).895 + 428(3) 1.1 kg. pg/ml 9. but this difference was not statistically significant.9(25) 1. although estradiol secretion may serve important functions such as inducing the onset of labor (Currie. total serum estrogens seem to have a better correlation with fetal-placental mass. 1963. The positive relationships between weight and number of lambs and placental mass (Alexander. a n d 4 . as well as more detaiJed information on the secretion of PL in the Suffolk breed.3 kg.197 + 559(3) x 727 +. a group of ewes that gave birth to a single lamb but nursed two lambs was not included. 1968). These results suggest that greater potential for milk yield in multiparous ewes is largely determined before parturition and that realization of such potential is modified . milk production was n o t increased by the greater suckling intensity (Moore.

R. and H. 10~720.. Chan and H.24(3) 2 8. Thimonier et al... However. C. 1974) and with the observation that ewes that gave birth to twins but were suckled by only one lamb produced more colostral milk than ewes bearing and suckling single lambs (Peart et aL. Friesen. R. 1966).10 • . TABLE 2.D. Australian J. Endocrinology 99:1273. 1974. Vol. 1966. numbers in parentheses are numbers of animals. In order to maximize milk production for increased efficiency of lamb production..O01).e. 1972). new developments.c P<. Circulating placental lactogen levels in dairy and beef cattle. of Wisconsin. Reprod. Alexander. 1977. A. Relationship of milk production to number of lambs born or suckled. R. SERUM PROGESTERONE CONCENTRATIONS(NANOGRAMS/M1LL1LITER) DURING LATE GESTATION IN MATURE EWESa No. 8:403.. P. 1975). Academic Press. 7:289. Fellows. L..54 -+. 1979) and goats (Currie et al. Peart et al. J.. 1979) provides an explanation for the previously observed relationship between milk yield and number of offspring in these species. 1959. M.44(12) de 4. . Lactational performance of Hampshire ewes was superior to that of Corriedale ewes (Gardner and Hogue.. 1977). Ulberg and R. Handwerger et al. J.f P<. Gluckman et al. 1977.45 • . Madison. Agr. Literature Cited Alexander. E. Although estradiol and PL may synergistically stimulate mammary development. 1979). Friesem 1977. further studies should be conducted to characterize genetic (breed or sire) effects on PL secretion and the relationship of PL to subsequent mammary function. Blank. Bolander. Res. Smith (Ed. and differences due to fetal number could be expressed at that time and would not be observed under the sampling schedule used in the present study. j. which may be partly related to genetic differences in PL secretion. G. J. New York. major changes in estradiol secretion occur just before parturition (Currie. Fertil. G. Placental lactogens.98(6) f 7. 1964.81 +-. which is consistent with the difference in PL levels between these breeds. I. 1975a). In Management of Reproduction in Sheep adn Goats Symposium.d'e'fMeans within rows and columns with the same superscript differ (b. 1977. Davies. F. Anderson. Jr. The milk production by ewes bearing crossbred lambs was greater within the first week of lactation than that by similar ewes bearing purebred lambs (Peart et al. Hayden et al.): Placental size. a finding consistent with enhanced PL concentrations in lambs bearing crossbred offspring. Larson and V. L. Genetic differences in milk production by ewes have been reported (Gardner and Hogue. Total estrogen concentrations on day 110 of pregnancy in ewes were positively correlated to milk production and growth of Iambs (Terqui and Delouis. Univ.S. Chan. Genetic differences in suckling activity are also involved (Moore. Control of the time of parturition of sheep and goat. the uniformity of estradiol concentrations in all breed-age groups studied suggests that differences in milk production with varying number of fetuses are more likely attributable to the differences in serum PL concentrations. 1976). L.. d. Steroid Biochem.. Endocrinological control. M. Robertson and H. 32(7)bd 4. b'c. J. 1976. Bosc. Studies on the placenta of the sheep (Ovis aries L.1080 BUTLER ET AL.05.75 • . This is consistent with the direct effect of multiple offspring on mammary growth during late pregnancy in ewes (Rattray et al.. which is consistent with the positive effects on lactation of estradiol given to induce parturition (Bosc et al. G. 1966). 1977). 1977. A synergistic relationship hetween PL and estrogen on mammary development might be expected from the accepted actions of these hormones. In light of the mammogenic activity of PL (Martal and Djiane. F. G. 94-147 In B.83(8) b 4. C.S. Terqui.46(6) c avalues listed are mean • standard errors. by the suckling activity of the lamb(s).23(16) cef 3 5.53 • . H. S. the positive association between PL concentration and number of fetuses in sheep (present data.06 -+.) Lactation: A Comprehensive Treatise.. Delouis and M... of offspring Breed Hampshire Corriedale Finnsheep 1 6.D.

Delouis. Sci. J. L. C. Gengenbach. Steroid Biochem. M. R. Hinman. Temporal pattern of placental lactogen and progesterone secretion in sheep. F. Donaldson.) 85:315. D.. (Camb. Hayden. Madison. 1975a. 1979. Fertil. milk composition. H. J. 1963. 58:709. S. 17:191. Vet. N. M. B. J. 1975b. J. J. 1977.) 79:303. Thorburn. Robb. and D. P. D. Robertson and H. Kalra. 41:433. A. Edwards and E. Djiane. Controlled superovulation in dairy heifers using prostaglandin F2a and pregnant mare serum gonadotropin. Robertson. P. Oltenacu and R.and late gestation in the fetal and maternal circulations. II. G. Fellows. En docrinol.PLACENTAL LACTOGEN AND LITTER SIZE 1978. E. Caprine placental lactogen: Levels o f prolactin-like and growth hormone-like activities in the circulation of pregnant goats determined by radioreceptor assays. Res. J. development and composition of the ovine conceptus and mammary gland during pregnancy. Kelly. Tsushima. W. Sci. E. (Camb. J. Endocrinol. E. Milk production.. 72:27. Edwards. Anita. Carpenter. J. Ewes and lambs maintained indoors. R. The yield and composition of the milk o f Finnish Landrace • Blackface ewes. L. Kelly. Mammotrophic and growth promoting activities of a placental hormone in sheep. Butendieck. J.. Clin. M.) 92:133. In Management of Reproduction in Sheep and Goats Symposium. Sci. Friesen. Sci. R. J. Martal. INRA. A. Gardner. Thomas and I. and D. and energetic efficiency of lactating ewes. R. Chan and H. R. A.) 68:365. Thimonier. 46:1293. Reprod. 1979. Bolander and R. J. Lactation pattern in Scottish Blackface and East Friesland • Scottish Blackface crossbred ewes. A. I.. Dairy Sci. 25:789. R. M. Linzell. J. M. In Management of Reproduction in Sheep and Goats Symposium. P. Estradiol radioimmunoassay without chromatography: Procedure.C. Gluckman. Heap. G. N. Maurer. Anim.. Shiu and H. Endocrinology of pregnancy and parturition in sheep and goats. 38:718. G. Hurley. Gadsby. Agr. R. F. Lactogenic and growth hormonelike activities in pregnancy determined by radioreceptor assays. Thatcher. D. W. S. 1974. A. J. Agr. R. as an indicator of pregnancy in sheep. W. P. G. The effect of different levels of nutrition during late pregnancy on the subsequent milk production of Blackface ewes and on the growth o f their lambs.P. J. chorionic somatomammotrophin. Cuttle. R.. B. and R.S. Kelly.. J. 1966. and C. . M. M. J. Peart. S. Rec. 1977. M. 1968. A. J. J. A. P. Les oestrogenes au cours de la gestation et de la parturition. Agr. 1974. B. Hormone ontogeny in the ovine fetus. A. M. Metab. D. Stevens. L. P. 1972. Transitory changes in plasma progestins. Heap. Powell and D. Waiters. Ovine chorionic somatomammotrophin in mid. Bosc. Endocrinology 99: 765. Studies on ovine placental lactogen secretion by homologous radioimmunoassay. 8:415. Growth. N. S. T. J. Peart. Hormonal diagnosis of pregnancy and number of fetuses in sheep and goats. J... W. E. Sci. 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