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1 PREPUBERTAL PLASMA LH CONCENTRATION, OVULATION RATE AND PROLIFICACY IN FINN, SUFFOLK AND FINN-SUFFOLK EWES J. CHIQUETTE', F. MINVIELLE', and J. J. DUFOUR, td partement de Zootechnie, FSAA, Universitt Laval, Ste-Foy, Qutbec GIK 7P4; and2research Station, Agriculture Canada, Lennoxville, Qutbec JIM IZ3. Contribution 147AC, received 4 May 1983, accepted I7 Nctvember CHtquerre, J., MrNvtslle, F. ano Dunoun, J. J Prepubertal plasma LH concentration, ovulation rate and prolificacy in Finn, Suffolk and Finn- Suffolk ewes. Can. J. Anim. Sci '72. Fifty-seven Finn, Suffolk or Finn-Suffolk ewe lambs were used to study the relationships between prepubertal LH levels, measured at intervals between 2 and 10 wk of age, ovulation rate and litter size, both within and between genetic types. The most prolific group of ewes (Finn) did not have consistently higher mean levels of LH than the two other genetic groups possibly because the relationship between LH and number of ovulations among breeds may be age-dependent. On the other hand, within each genetic group, mean LH levels were generally higher in more prolific ewe lambs: small differences were observed up to 6 wk of age. These results show that early mean prepubertal LH concentration alone is not a precise indicator of future reproductive performance. Key words: Prepubertal plasma LH, ovulation rate, prolificacy, breed differences, ewes [Concentration pr6pubertaire de LH plasmatique, taux d'ovulation et prolificit6 chez les brebis de races Finn, Suffolk et Finn-Suffolk.l Titre abr6g6: Concentration de LH, taux d'ovulation et prolifici16 chez les brebis. Cinquante-sept brebis de races Finn, Suffolk et Finn-suffolk ont servi ir une 6tude visant ir d6terminer la relation entre la concentration prdpubertaire de LH, mesur6 ir divers intervalles entre I'age de 2 et 10 semaines, le taux d'ovulation et la taille des port6es, ir I'int6rieur d'un mome type g6n6tique ainsi qu'entre des types diff6rents. Le groupe de brebis le plus prolifique (race Finn) n'a pas affich6 une concentration en LH plus 6lev6e que les deux autres groupes, et ce probablement en raison du fait que la relation entre ce facteur et le nombre d'ovulations chez les diverses races est fonction de l'. En revanche, on a constat6 qu'ir I'int6rieur d'un m6me groupe, la concentration moyenne de LH est g6n6ralement plus 6lev6e chez les brebis plus prolifiques: de faibles diff6rences ont 616 notdes jusqu'd I' de 6 semaines. A la lumibre de ces r6sultats, on peut conclure qu'i elle seule, la concentration pr6pubertaire moyenne de LH ne peut servir d'indicateur pr6cis des aptitudes de reproduction futures de l'animal. Mots cl6s: Concentration plasmatique de LH avant la pubert6, taux d'ovulation, prolificit6, diff6rences entre les races, brebis Selection of highly fecund replacement ewe lambs at an early age is of considerable importance. Ovulation rate is a good indicator of prolificacy (Hulet and Foote 1966; Packham and Triffitt 1966; Lindsay et al. 1975) but it is measured well after Can. J. Anirn. Sci, 64: (Mar. 1984) ewe lamb selection has taken place. However, the systemic concentration of LH measured as early as 30 days after birth appears to be a promising tool for selecting more prolific ewe lambs. Bindon and Turner (1914) detected a significant difference in LH concentration between sinsle 61
2 68 CANADIAN JOURNAL OF ANIMAL SCIENCE and twin-born lambs from selected Dorset ewes. Likewise, Hanrahan et al. (1911) reported higher plasma LH at 8 wk of age in ewe lambs from Elite Galway ewes than in lambs from control ewes of the same breed. On the other hand, Echternkamp and Laster (1916) found no correlation between ovulation rate and LH concentration within or among Finnish Landrace, Rambouillet, their crosses and Hampshire ewe lambs. But, the results of these previous studies were not directly comparable since the relationship between LH concentration and ovulation rate was not examined in the works of Bindon and Turner (1914) and Hanrahan et al. (1911) and age at collection was different in the work of Echternkamp and Laster (1916). The purpose of the present study was to determine the association between prepubertal plasma LH concentration between 2 and 10 wk of age and the subsequent ovulation rate and prolificacy of Finnish Landrace (F), Suffolk (S) and reciprocal crossbred (C) ewe lambs. MATERIAL AND METHODS Seventy-two ewe lambs born fiom January to March 1981 fiom planned matings of the Laval University flock at Saint-Augustin, Quebec, constituted the base population. Ewe lambs were raised by their dams until weaning at 3 mo of age. Eight lambs died at an early age and seven others were eliminated later for various reasons (absence of estrus, mortality, hermaphrodism) so that the whole experiment was carried out with the remaining fifty-seven ewe lambs: l4 Suffolk (S), l7 Finnish Landrace (F) and 26 crossbreds (C). The sheep were housed in a closed barn under natural lighting from November to May. The barn, situated at latitude 47'N, had a north-south orienta6ion. Lambs had free access to a medium quality hay and were given up to a mean of 0.4 kg per head per day of a commercial concentrate for growing lambs. Water and iodized salt were available at all tlmes. Two 1O-mL jugular vein blood samples were collected at l-h intervals from each ewe lamb at 2, 4,6, 8 and l0 wk of age. All blood samples were taken at the same time on each collection day. Plasma LH concentration was determined by using the double antibody radioimmunoassay of ovine LH of Lewis et al. (1974). Each series of assays was done on contemporaneous samples. Results were expressed as nanograms NIH-LH-S 21 per millilitre plasma. Interassay and intraassay coefficients of variation were 10.9Va and l1.6vc, respectively. The ewe lambs were checked for estrus when the oldest was 4 mo of age by exposure to vasectomized rams once daily. A lamb which stood to be mounted was recorded in estrus. Each ewe lamb in estrus was separated fiom its group immediately so that the rams would detect estrus in other lambs. Later the same day, these lambs were returned to their group after estrus checking had been completed. The ewe lambs were exposed to fertile Suffolk rams at the second recorded estrus and mated at least twice. The number of ovulations was determined by endoscopy days after the fertile mating, by using the technique of Oldham and Lindsay ( I 980). Raw LH data were log-transformed to normalize the distributions and eliminate the heterogeneity of variances. An overall analysis of LH variation showed that the effect of the sample accounted for less Ihan lvo of the totai variance. Consequently, results of the two samples taken at 1-h intervals were averaged and statistical analyses were performed on the mean and on the lower LH concentrations obtained at each age for each ewe lamb. The set of lower values was analyzed in an effort to minimize in the data the possible "noise" caused by the pulsatile nature of LH secretion (Leifer et al'. 1972l. Foster et al. 1975b). But, since the results with the two data sets were consistent, only those obtained with the mean values are presented. Since batch and age effects were confounded due to the stratification of LH determination by age at collection, it was not possible to compare LH concentrations across ages by analysis of regression. However, unbiased comparisons of LH mean values among the three genetlc groups were performed for each age class by using Duncan's multiple range test. To determine the relationships between LH and prolificacy and between LH and ovulation rate within each population, ewes of the same genetlc type were grouped into two classes after their prolificacy or their ovulation rate, and Student's /-tests were performed to compare these LH subgroup
3 CHIQUETTE ET AL. - LH, OVULATION RATE AND PROLIFICACY IN SHEEP means at each age. The possibility that the association between LH and number of ovulations depends on the age of the prepubertal lamb at blood collection was studied by using a twoway (genetic group, age) analysis of variance with interaction of the LH data. All statistical analyses were carried out with the procedures of the statistical analysis system (SAS 1979). Differences were considered to be significant at P<0.10. RESULTS Mean age of the ewe lambs at puberty was 250 days. The S ewes reached puberty 25 days earlier (P<0.05) than the F ewes (Table 1). Average date of puberty (with the range) was l0/21 (1012 to 11120), l0l 19 (10/1 to l116) and 10/13 (09ll2to lll l3), respectively, for the S, F and C ewes. Ovulation rate (OR) differed significantly (P<0.05) between the genetic groups (Table 1). The F ewe lambs had an average OR of 2.7 at the second estrus after puberty, 1.5 and 0.9 more than the S and the C groups, respectively. The F ewes had an average litter size of 1.9, 0.8 above the S ewes (P<0.05). The C females had an intermediate lambing rate of 1.6, still above (P<0.05) the mean litter size of the S ewes. In both genetic groups with high OR, mean body weight at puberty was significantly higher in ewes with higher OR. Finnish ewes which ovulated more than two eggs weighed 43.1 kg at puberty, 7.2 kg above ewes with two or less ovulations (Table 2). Likewise, C ewes with more than one ovulation weighed 5.0 kg more at puberty than ewes with only one egg shed. However, no such association was found between litter size and weight at puberty. Among the three genetic groups, significant differences (P<0.05) in LH concentration were observed in three of five age groups (Table 3). The F and S groups had higher mean plasma LH levels than the C group at 6 and 8 wk of age. However, at l0 wk of age the mean plasma LH level of the S group was higher than those of the F and C groups. When ewes within each genetic group were separated in terms of number of ovu- Table l. Mean reproductive performances offinnish Landrace (F), Suffolk (S) and Finn-Suffolk crossbred (C) ewes Genetic group F S C (SXF) (FXS) Number of ewes t5 lambing l6 t2 l0 ll at puberty (days) '+ SD Oa b ab 256+ l2a Ovulation rate +SD l.0a l, c O.5b l b a - c Means with a different letter within a column are sisnificantlv different at P < Prolificacy +SD a I + 0.3b a a Table 2. Relationship between the ovulation rate and the body weight at puberty of three groups of Finnish Landrace. Suffolk and Finn-Suffolk crossbred ewes Genetic group Finnish Landrace (F) Suffolk (s) Finn-Suffolk (c) Number of ovulations <2 I >l 1 >l Number of ewes 8 9 ll Weight at puberty (kg) + SD ** * * +*Mean weights within the same genetic group are significantly different at P < 0.05 and P < 0.01, resdectivelv.
4 70 CANADIAN JOURNAL OF ANIMAL SCIENCE Table 3. Means and standard deviations of log (plasma LH concentration) in Finnish Landrace, Suffolk and Finn-Suffblk crossbred prepubertal ewes Genetic group Finnish Landrace (F) Suffolk (S) Finn-Suffolk (C) Overall 2 wk wk wk a 8 wk r 0.65 ):0.27 a l0 wk Number of ovulations <2 >2 2 wk wk wk *+ 8 wk l0 wk Littersize I > 1 2 wk wk ** 6 wk wk I 0.56:! wk O.4la a b >l a - b Means with a different letter within a line are significantly different at P < I I o.64 + O :! ' i 0. 30b b O a 1 > : " :r I >t *x* * l **E*x*Subgroup means within the same genetic group and age are significantly different at P < 0.10, P < 0.05 and P < 0.01, respectively. lations or litter size, it was observed that the mean LH levels were generally higher among the more prolific ewes (Table 3). The mean LH level in F ewes was higher (P<0.05) at 6 wk of age in the class with more than two ovulations. When F ewes were grouped on the basis of litter size, the mean LH level was higher (P<0.05) at 4 wk of age in the class with a litter size of two or more lambs. The mean LH levels in S ewes grouped either by ovulation rate or by prolificacy were marginally to significantly higher (P<0.10 and P<0.01, Table 4. Analysis of variance of log (plasma LH Source df SS F Genetic group Genetic group x age Error *P < respectively) at 2 wk of age in more prolific ewes. However, less prolific C ewes had a marginally higher (P<0.10) mean LH level at 6 wk of age. The interaction between the effects of the age and of the genetic group on the mean LH level was marginally significant (Table 4), which indicates that the differences between the mean LH levels of the three genetic groups were dependent on the age at blood sampling DISCUSSION Puberty of the Finnish Landrace ewe lambs used in the present study was reached at a mean age of 259 days, relatively older than the age reported in the studies of Dyrmundsson (1973) and Dickerson and Laster (1915). These authors reported puberty in spring-born purebred and halfbred Finn ewe lambs was reached at 210 and 219 days of age, respectively. However, in the latter work, only ages of ewes which
5 CHIQUETTE ET AL LH. OVULATION RATE AND PROLIFICACY IN SHEEP 7I reached puberty by l0 November (72.47o of the Finn population) were recorded, so the calculated mean age at puberty was certainly underestimated. In the present study, it is possible that cumulative effects of inbreeding may have contributed to the later onset of puberty in the Finnsheep. Since the importation of the original flock from Finland in 1962, the flock has been kept closed. In any case, the ewe lambs used in this work reached puberty at dates well into the breeding season and had enough time to start cycling. Adult Suffolk ewes, known to have a short breeding season, have been shown to initiate their breeding season in mid-september in eastern Canada (Dufour t91 4). In the present work, the ovulation rates for purebred and halfured Finnsheep observed by endoscopy after the second estrus were 0.7 and 0.6 ovulations higher, respectively, than those observed in similar groups by Echternkamp and Laster (1976). While the mean weight at puberty of the Suffolk ewe lambs was comparable to previously reported data, the Finnish Landrace ewe lambs were 7 kg heavier on the average at puberty than those studied by Dyrmundsson (1973). This difference could be responsible for the higher ovulation rates of the Finnsheep in the present work, since we found that pure- and halfbred Finn ewe lambs with higher ovulation rates weighed, respectively, L2 and 5.0 kg more on the average than those with lower ovulation rates (Table 2). These observations are in agreement with a report of Foote et al. (1959) who demonstrated that ovulation rate was more influenced by the growth pattern of the lamb than by its nutritive state at breeding. Using LH concentrations across breeds to identify more prolific females among prepubertal ewe lambs does not appear to be possible since, at any given age between 2 and 10 wk, ewe lambs with a significantly higher level of LH were not necessarily from the genetic group with the highest ovulation rate. For examole. at 6 wk of age the Suffolk ewe lambs and the much more prolific Finn ewe lambs had about the same mean LH concentration (Table 3). A more complete examination of changes in plasma LH concentration during the prepubertal period by increasing the frequency of blood sampling might have discriminated between high and low fecundity ewe lambs (Foster et al. 1915b). However, it is possible that breed differences in prolificacy could be explained by differences in ovarian sensitivity or in responsiveness to gonadotropins. Also, different breeds may have different physiological ages at the same chronological age. Indeed, the interaction found in this work between genetic group and age (Table 4) indicates that the relation between LH and number of ovulations is age-dependent and supports the hypothesis developed by Land et al. (1919). The age-dependency could also be related to breed differences in the rates of sexual development. Within-breed comparisons of plasma LH levels between ewe lambs with a high and a low ovulation rate or prolificacy indicated that, at 2 and 4 wk of age, basic LH levels were consistentlv but marsinallv higher in more fecund ewe lambs jruul" 3). Foster et al. (1915a) have shown that during the first few weeks of postnatal life, plasma LH concentrations of female lambs were low and remained at baseline levels during periods of frequent sampling. Subsequently, pulsatile patterns of LH release were evident. These authors have suggested that the period of low secretion followed by the onset of pulsatile LH release could be related to maturational events occurring within the hypothalamo-hypophyseal system such as changes in gonadotropin-releasing hormone(s) or releasable pools of LH. If the timing of these events is different in high and low fecundity female lambs, it is possible that they might be reflected by differences in basal LH levels during early postnatal life or in the time of onset of pulsatile LH release. Alternat ively. it has been shown that the LH
6 '72 CANADIAN JOURNAL OF ANIMAL SCIENCE response to a single injection of gonadotropin-releasing hormone is highly repeatable (Land et al. 1979). The LH response of female lambs to a single injection of gonadotropin-releasing hormone could provide a more reliable and less time consuming method for discriminating between potential high and low fecundity ewes and could possibly amplify the differences in timing of maturational events associated with LH release. ACKNOWLEDGMENTS This study was supported by grants LA from CRSAQ and MAC 1018 from Agriculture Canada to F. M., and J. C. held a NRC postgraduate scholarship. Technical assistance provided by the staff at the St-Augustin experimental farm and by A. Bouchard is gratefully acknowledged. LH assays were performed in Dr. R. Tremblay's laboratory, CHUL Laval University. The assistance given by Dr. J. P. Lemay in establishing the research team is appreciated. BINDON, B. M. and TURNER, H. N Plasma LH of the prepuberal lamb: a possible early indicator of fecundity. J. Reprod. Fertil. 39: DICKERSON, G. E. and LASTER, D. B Breed. heterosis and environmental influences on growth and puberty in ewe lambs. J. Anim. Sci. 4l: 1-9. DUFOUR. I. I The duration of the breeding season of four breeds of sheep. Can. J. Anim. Sci. 54: DYRMUNDSSON, D. R Puberty and early reproductive performance in sheep. 1. Ewe lambs. Anim. Breed Abstr. 4l: 2' ECHTERNKAMP, S. E. and LASTER, D. B Plasma LH concentrations for prepubertal, postpubertal, anestrous and cyclic ewes of varying fecundity. J. Anim. Sci. 42: FOSTER. D. L.. JAFFE. R. B. and NISWEN- DER, G. D. l9'75a. Sequential patterns of circulating LH and FSH in female sheep during the early postnatal period: effect of gonadectomy. Endocrinology 96: FOSTER, D. L., LEMONS, J. A., JAFFE, R. B. and NISWENDER, G. D. 1975b. Sequential patterns of circulating luteinizing hormone and follicle stimulating hormone in female sheep from early postnatal life through the first estrous cycles. Endocrinology 97: FOOTE, W. C., POPE, A. L., CHAPMAN, A. B. and CASIDA, L. E Reproduction in the yearling ewes as affected by breed and sequence of feeding levels. 1. Effects on ovulation rate and embryo survival. J. Anim. Sci. 18: HANRAHAN, J. P., QUIRKE, J. F. and GOSLING, J. P Genetic and nongenetic effects on plasma LH concentrations in lambs at 4 and 8 weeks of age. J. Reprod. Fertil. 51: HULET, C. V. and FOOTE, W. C Relationship between ovulation rate and reproductive performance in sheep. J. Anim. Sci. 25: LAND, R. B., CARR, W. R. and LEE, G. J A consideration of physiological criteria of reproductive merit in sheep. Pages ln A. Robertson, ed. Selection experiments in laboratory and domestic animals. Commonwealth Agricultural Bureaux, Slough, U.K. LIEFER, R. W., FOSTER, D. L. and DZIUK, P. J Levels of LH in the sera and pituitaries of female lambs following ovariectomy and administration of estrogen. Endocrinology 90: LEWIS, P. E., BOLT, D. J. and INSKEEP, E. K Luteinizing hormone release and ovulation in anestrous ewes. J. Anim. Sci. 38: LINDSAY, D. R., KNIGHT, T. W., SMITH, J. F. and OLDHAM. C. M Studies in ovine fertility in agricultural regions of western Australia: ovulation rate, fertility and lambing performance. Aust. J. Agric. Res.26: OLDHAM, C. M. and LINDSAY, D. R Laparoscopy in the ewe: photographic record of the ovarian activity of ewes experiencing normal or abnormal oestrous cycles. Anim. Reprod. Sci. 3: l PACKHAM, A. and TRIFFITT, L. K Association of ovulation rate and twinning in Merino sheep. Aust. J. Agric. Res. l7: STATISTICAL ANALYSIS SYSTEM SAS user's guide. SAS, Cary, N.C.
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