James R. Clark, T. N. Edey, N. L. First, A. B. Chapman and L. E. Casida
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1 EFFECTS OF FOUR GENETIC GROUPS AND TWO LEVELS OF FEEDING ON OVULATION RATE AND FOLLICULAR DEVELOPMENT IN PUBERAL GILTS 1, 2 James R. Clark, T. N. Edey, N. L. First, A. B. Chapman and L. E. Casida University of Wisconsin, Madison Summary VULATION rate, follicular development, O anterior pituitary gland weight and corpora lutea weight were studied in a total of 74 puberal gilts of the Poland China and Yorkshire breeds and their reciprocal crosses. The effects of two levels of feeding also were studied for the first 16 days of the puberal estrous cycle in half of the gilts and for the puberal estrous cycle plus 3 days of the succeeding cycle in the other half of the gilts. The Yorkshire gilts exceeded the Poland China gilts in (1) ovulation rate (P~.01), (2) anterior pituitary gland weight (P<.01), (3) the number of small and medium follicles and the total number of follicles at day-16 (all P<.01) and (4) the number of small follicles and the total number of follicles at day-3 (both P<.01). At day-16 the Poland China gilts had heavier corpora lutea (P<.01) and more large follicles than the Yorkshire gilts (P<.01). Gilts on the high feeding level had a greater ovulation rate (P<.01) but had no significant difference in follicular development from those on the low feeding level. The act of mating had no significant effect on ovulation rate. There were more medium and total follicles at day-16 than at day-3 (both P~.01) with no significant difference in the number of small or large follicles. Introduction Breeds of swine differ in ovulation rate. Sows of the Yorkshire breed have been shown to have a greater ovulation rate than sows of the Poland China breed (Clark et al., 19). 1 This work was done under a cooperative agreement between the Research Division of the College of Agricultural and Life Sciences, University of Wisconsin, and the Animal Husbandry Research Division A.R.S., U.S.D.A. and supported in part by Cooperative U~S.D.A.-C.S.R.S., Grants No and It was also supported in part by the Ford Foundation, Grant No ; and by the Program Project in Genetics, Grant No. GM15422, from the National Institutes of Health. This is paper No from the Laboratory of Genetics and No. 621 from the Department of Meat and Animal Science. 2Address for reprint request: Department of Meat and Animal Science, University of Wisconsin, Madison Studies of these two breeds from birth to multiparity have shown several physiological characters to be associated with the above differences in ovulation rate (Bhalla et al., 1969; Dailey et al., 1969, 1970; Clark et al., 1970; Clark et al., 19). Studies on ovulation rate and its relation to follicular development and anterior pituitary gland weight have not been reported for puberal gilts or reciprocal crossbred gilts of these two breeds. When planning the present experiment there was little basis for deciding which stages of the estrous cycle would be of most value as far as critical studies of follicular development were concerned. It was assumed, however, that a new crop of follicles was formed each cycle with one or more waves of atresia of unknown length to adjust the follicle numbers to the ovulation rate. Two stages were chosen arbitrarily to characterize the differences in follicular development leading to differefices in ovulation rate. Follicular development was studied in half of the gilts on day-16 of the first post-puberal estrous cycle and on day-3 of the second estrous cycle in the other half of the gilts. Materials and Methods As they reached 170 days of age, 24 Poland China (PP), 39 Yorkshire (YY), 14 Yorkshire-sire x Poland China-dam (YP) and 33 Poland China-sire x Yorkshire-dam (PY) gilts, were placed on a pre-experimental feeding level in preparation for experimental treatments to be imposed on the day of onset of their first estrus (day-0). These animals were the available gilts from the experimental herd as described by Clark et al. (19). The preexperimental feeding level was 2.3 kg per day of the experimental ration a and estrus was checked once daily with a vasectomized boar. 8The composition of the experimental ration was: corn, 82.5%; soybean oil meal, 10.0%; meat scraps, 5.0%; trace mineralized salt,.5%, hi-mix,.5%; dicalcium phosphate,.5%; calcium carbonate,.5% ; vitamin premix,.2%; Aureofac,.2% ; and zinc,.05% JOURNAL OF ANIMAL SCIENCE, vol. 36, no. 6, 1973
2 OVULATION RATE AND FOLLICULAR DEVELOPMENT 1165 The experimental design is shown in table 1. Twenty-four PP, 24 YY, 12 YP and 24 PY gilts were assigned at 170 days of age to a 4 x 2 x 2 factorial experiment with genetic group, feeding level and day of the estrous cycle when slaughtered as the factors under study. Assignment to feeding level and day of the estrous cycle was random within genetic group. The feeding levels of the experimental ration, begun on the day of puberty, were i.4 kg per day (low feeding level) and ad libitum(high feeding level). 4 One-half of the gilts were slaughtered on day-16 of their first estrous cycle and the other half on day-3 of their second estrous cycle. In addition, half of the day-3 gilts within genetic group and feeding level were mated to a fertile boar at the onset of their second estrus (estrus checks were made every 12 hr.) to test for a possible effect of mating on ovulation rate. Cleavage of ova or presence of sperm in the zona pellucida was accepted as evidence that mating had involved cervical stimulation. The unassigned gilts were held as replacements for experimental animals under a predetermined set of conditions. A gilt removed from the experiment because of sickness or accident was replaced by the next "replacement" gilt to reach puberty. Six of these gilts were used, five in the YY genetic group and one in the PY genetic group. Previous information (Clark et al., 19.70) had shown that the YY gilts were approximately 20 to 30 days older at puberty than the other genetic groups Under study; therefore, it was stipulated in advance that YY gilts failing to reach puberty at the age of 316 days and that PP, YP and PY gilts at the age of 286 days would be disqualified and, if possible, replaced. Six gilts failed to reach puberty by the specified age and were discarded (4 YY, 1 PP and 1 PY). On the day of onset of her first estrus each gilt was weighed (average of all gilts used was 244 days of age and 106 kg in weight), transferred to an individual pen and placed on her assigned feeding level. Gilts were weighed before slaughter. 5 At slaughter the pituitary gland and reproductive tract were collected from each gilt. The anterior lobe of the pituitary gland was separated from the posterior lobe and weighed. The ovaries were trimmed free from the mesovaria and weighed. The a The average feed consumption per animal on the high feeding level was 3.1 kg per day. s The gilts on the low feeding level lost an average of,08 kg per day while those on the high feeding level gained an average of.46 kg per day. TABLE 1. EXPERIMENTAL DESIGN Stage of the estrous cycle when slaughtered Day- 16 Day-3 Genetic Feeding of the of the group" level first cycle second cycle PP (4) b~ 6 (6) (4) ~ 6 (6) yy (6) 6 (6) (5) a 6 (S) d yp 3 (3) 3 (3) 3 (3) 3 (3) py 6 (6) 6 (4) d 6 (6) 6 (4) ~ PP, Poland China; YY, Yorkshire; YP, Yorkshire sire- Poland China dam; PY, Poland China sire-yorkshire dam. b Figures represent number of animals assigned to each subclass. Those in parentheses are the numbers for which data were used in statistical analysis. e One animal in this group failed to show puberty by 286 days of age and was discarded. The other animal died. a Missing animal(s) in this group were those which failed to show a second estrus during the experiment and were discarded. macroscopically visible surface follicles were then measured by the use of calibrated wire loops. Each follicle was punctured as measuring was completed. The corpora lutea (CL) were dissected from the ovary, counted and weighed. The number of CL were used as a measurement of ovulation rate. The Ovarian residue was then sliced finely, blotted and weighed. The weight of the follicular fluid (FFW) was determined by taking the difference between the fresh ovarian weight and the combined weight of the CL and processed ovarian residue. All data were analyzed by the method of least-squares (Snedecor and Cochran, 1967). The data for the weight of the follicular fluid were transformed to loglo(x); the data for number of small, medium and large follicles and total number of follicles were transformed to loglo(x-~-l). The loglo of the total corpora lutea weight for each day-16 animal was adjusted by covariance for the loglo of its corpora lutea number. For the purpose of statistical analysis, the follicle-diameter frequencies were grouped arbitrarily as follows: small follicles (1 and 2 mm diameter), medium follicles (3 to 6 mm diameter) and large follicles (7 to 10 mm diameter). Sums of squares and cross-products were calculated within subgroups for the day-16 and day-3 animals separately, tested for heterogeneity and if not heterogenous, pooled for estimating the correlation coefficients for: anterior pituitary gland weight with follicular fluid weight, number of small follicles, num-
3 1166 CLARK ET AL. TABLE 2. LEAST-SQUARES MEANS FOR FOLLICULAR DEVELOPMENT IN PUBERAL GILTS a Day-16 Day-3 Number of follicles b Number of follicles b Genetic Feeding group level Small Medium Large Total FFW c Small Medium Large Total FFW ~ PP yy , yp py , , Genetic group means PP YY YP PY PB , XB 53, , Feeding level means , , , Standard deviation Degrees of freedom a Geometric means of the least-squares means. b The data were transformed to log(x+l) for analysis and the standard deviations are in logarithms. The geometric means need to be transformed to log(x+1) to be comparable to the standard deviation. e The data on follicular fluld weight (FFW) were transformed to log(x) for analysis and the standard deviations are in logarithms. The geometric means need to be transformed to log(x) to be comparable to the standard deviation. ber of medium follicles and total number of follicles; and ovulation rate with follicular fluid weight and anterior pituitary gland weight. The degrees of freedom for each main effect and their interactions were resolved into a set of orthogonal comparisons. 6 Results Ovulation Rate and Follicular Development Day-16 of the First Estrous Cycle. The ovulation rate at day-16 of the estrous cycle was from the pre-treatment ovulation. The overall mean and standard deviation for ovulation rate (not presented in tabular form) were 10.6 and 2.4, respectively (36 degrees of freedom). The Yorkshire gilts had a higher ovulation rate than the Poland China gilts (YY, 12.3 vs. PP, 8.4; P<.01). The YP gilts and the PY gilts, as well as the average of the two purebreeds (PB) and the average of the two crossbreeds (XB) did not differ sig- e The three degrees of freedom for genetic group were resolved into the following set of orthogonal comparisons: YY vs. PP, YP vs. PY and PB vs. XB. nificantly in ovulation rate (YP, 10.5 vs. PY, 11.1; PB, 10.4 vs. XB, 10.8). Follicular development was measured in two ways: (1) the number of follicles within each size class and (2) weight of the follicular fluid. The Yorkshire gilts had an average of 35.2 more small follicles (1 and 2 mm diameter), an average of 21.3 more medium follicles (3 to 6 mm diameter) and an average of 57.9 more total number of follicles than the Poland China gilts (all P~.01; table 2). The crossbred gilts averaged 17.6 more small follicles than the purebred gilts (P~.05). The Poland China had more large follicles (~7 mm diameter) than the Yorkshire and the average of the purebred gilts was more than the average of the crossbred gilts (both P<.01). No significant effects of feeding level or genetic group x feeding level interactions were found for the number of follicles within each size class. The weight of the follicular fluid (table 2) was not affected significantly by genetic group, feeding level or their interaction. Day-3 of the Second Estrous Cycle. The Yorkshire gilts exceeded the Poland China
4 Genetic group pp yy yp py OVULATION RATE AND FOLLICULAR DEVELOPMENT 1167 TABLE 3. LEAST-SQUARES MEANS FOR NUMBER OF CORPORA LUTEA, ANTERIOR PITUITARY GLAND WEIGHT AND ADJUSTED CORPORA LUTEA WEIGHT IN PUB ERAL GILTS Genetic group means PP YY YP PY PB XB Feeding level means Anterior pituitary Number of CL day-3" gland weight, mg b Adjusted Feeding CL weight level Mated Not rn~ted Day-16 Day-3 day-16, g*' d ~h I Standard deviation Degrees of freedom Means for mated and not mated were 10.5 and 11.5, respectively. b Means for dayol6 and day-3 were 196 and 197 rag, respectively. c Geometric means. a The data were transformed to log(x) for analysis and the standard deviation is a logarithm. The geometric means need to be transformed to log(x) to be comparable to the standard deviation. gilts by 5.0 ovulation (P<.O1; table 3). The differences in ovulation rate between the two reciprocal crosses and between the purebred and crossbred gilts were not significant. Gilts on the high feeding level had 2.6 more corpora lutea than those on the low feeding level (P<.01). The act of mating had no significant effect on ovulation rate (mated, 10.5; nonmated, 11.5). The Yorkshire gilts had more small follicles and a greater total number of follicles than the Poland China gilts (both P<.01; table 2). There was an interaction of YP vs. PY x low vs. high (P<.05) in the number of small follicles. The difference between low- and high-fed gilts for the YP was greater than that for the PY (YP-L, 14.0; YP-H, 54.9; PY-L 44.6; PY-H, 42.5). The difference in the number of small follicles between the low- and high-fed gilts was greater (P<.05) for the XB than for the PB (XB-L, 25.1; XB-H, 48.3; PB-L, 35.7; PB- H, 31.5). The same two interactions were significant (both P<.05) and in the same direction for the total number of follicles (YP-L, 17.2; YP-H, 56.3; PY-L, 49.4; PY-H, 45.4 and XB-L, 29.3; XB-H, 50.6; PB-L, 41.2; PB-H, 33.4). There were no significant effects of feeding level on the number of small, medium and large follicles and total number of follicles. Genetic group had no significant effect on the number of medium and large follicles. The weight of the follicular fluid was not affected significantly by genetic group, feeding level or their interactions (table 2). Day-16 of the First Estrous Cycle vs. Day-3 of the Second Estrous Cycle. Means for the number of follicles of the various sizes for day-16 and day-3 are shown in table 4. There were 25 times more medium follicles and 2.5 times more total follicles at day-16 than at day-3 of the estrous cycle (both P~.01). No significant difference was found between day- 16 and day-3 in the number of small or large follicles. Endocrine Gland Weights The means for the weight of the anterior pituitary glands are shown in table 3. The Yorkshire glands averaged 73 mg heavier than the Poland China glands (P~.01). The YP glands averaged 34 mg heavier than the PY glands
5 1168 TABLE 4. LEAST-SOUARES MEANS FOR THE NUMBER OF FOLLICLES AT DAY-16 AND DAY-3 OF THE ESTROUS CYCLE IN PUBERAL GILTS Day of the Number of follicles a estrous cycle when slaughtered Small Medium Large Total , Standard deviation ~ Degrees of freedom O. 26 O. 22 a Geometric means. b The d~ta were transformed, to log(x+l) for analysis and the standard deviations are in logarithms. The geometric means need to be transformed to log(x+1) to be comparable to the standard deviation. (P<.01). The 5 mg difference between the purebred and crossbred glands was not statistically significant. Feeding level and day of the estrous cycle had no significant effect on the gland weight. There was a significant difference between the Poland China and Yorkshire gilts in adjusted corpora lutea weights at day-16 of the estrous cycle (P~.01; table 3) with the Poland China's exceeding the Yorkshire's by an average of 1.4 grams. Feeding level or genetic group x feeding level had no significant effects on adjusted corpora weight. Estrous Cycle Length The overall mean and standard deviation for estrous cycle length in days were 19.7 and 1.2, respectively (26 degrees of freedom). There were no significant genetic group or feeding level effects; however, there was an interaction of PB vs. XB xlow vs. high (P<.05). The difference in estrous cycle length between the low- and high-fed gilts was greater in the purebred gilts than in the crossbred gilts (PB-L, 20.6; PB-H, 19.3; XB-L, 19.3; XB-H, 19.8). Correlations Between Traits The associations of anterior pituitary gland weight with follicular fluid weight, ovulation rate, number of small foilicies, number of medium follicles and total number of follicles and ovulation rate with follicular fluid weight were examined separately between individuals within subgroups at day-16 and day-3 of the estrous cycle. No significant heterogeneity between correlation coefficients was found. The only significant correiations were: (1) between ovulation rate and follicular fluid weight (r~.56, P~.01, 31 degrees of freedom) at day-16 CLARK ET AL. of the first estrous cycle, (2) between anterior pituitary gland weight and the number of small follicles (r , P<.05, 25 degrees of freedom) and (3) between anterior pituitary gland weight and the total number of follicles (r , P<.05, 25 degrees of freedora), the latter two being at day-3 of the second estrous cycle. Discussion The purpose of this study was to examine the association of certain characters with ovulation rate in puberal gilts within and between subgroups. These characters were the weight of the anterior pituitary glands, the weight of the follicular fluid and the number of follicles of different sizes. Genetic group differences existed in ovulation rate of puberal gilts (the Yorkshire's exceeded the Poland China's) just as was shown for nulliparous sows of the same genetic groups by Clark et al. (19). These genetic group differences in ovulation rate were accompanied by heavier anterior pituitary glands, more small (day-16 and day-3), medium (day-16) and total number of follicles (day-16 and day-3) with the Yorkshire exceeding the Poland China in all cases. In contrast, at day-16 of the first estrous cycle the Poland China gilts had more large follicles and heavier corpora lutea than the Yorkshire gilts. The difference between the reciprocal crossbred gilts for ovulation rate was not significant but there was a significant difference between the reciprocals in the weight of the anterior pituitary gland. Comparisons of the purebred females with the crossbred females showed no significant difference in ovulation rate but the crossbreds had more small follicles than the purebreds and the purebreds had more large follicles than the crossbreds, both at day-16 of the estrous cycle. The feeding of a high level of nutrition increased the ovulation rate in puberal gilts of the Poland China and Yorkshire breeds and their reciprocal crosses. Clark et al. (19) found the same relationship in nulliparous and multiparous sows of the same two breeds. This increase in ovulation rate by a high feeding level has been reported in various other breeds of swine (Kirkpatrick et al., 1967a, b; Rigor et al., 1963; Robertson et al., 1951; Zimmerman et al., 1960). The high level of nutrition had no significant effect on the weight of anterior pituitary glands. This is in agreement with other work in puberal gilts of other breeds (Rigor et al., 1963; Kirk-
6 OVULATION RATE AND FOLLICULAR DEVELOPMENT 1169 patrick et al., 1967b) but is in contrast to the work on nulliparous and multiparous swine (Clark et al., 19) and mature ewes (Darlow, 1942; Bellows et al., 1963; Howland et al., 1966; Memon et al., 1969). The number of follicles within each size class and the weight ~of the follicular fluid was not significantly affected by the level of feeding. A positive relationship was found between ovulation rate and weight of the follicular fluid at day-16. The higher the previous ovulation rate, the greater was the amount of follicular development. A negative relationship was found between anterior pituitary gland weight and the number of small follicles and the gland weight and the total number of follicles. If the assumption is made that anterior pituitary gland weight is indicative of levels of gonadotropins present in the gland, then the negative correlation between gland weight and number of follicles would be expected, that is, if gland weight decreases from release of hormone the number of follicles should increase. Literature Cited BeUows~ R. A., A. L. Pope, R. K. Meyer, A. B. Chapman and L. E. Casida Physiological mechanisms in nutritionally induced differences in ovarian activity of mature ewes. J. Anita. Sci. 22:93. Bhalla, R. C., N. L. First, A. B. Chapman and L. E. Casida Quantitative variation in ovarian and follicular development in four genetic groups of pigs at different ages. J. Anita. Sci. 28:780. Clark, J. R., R. A. D~iley, N. L. First, A. B. Chapman and L. E. C~sida. 19. Effect of feed level and parity on ovulation rate in three genetic groups of swine. J. Anita. Sci. 35:1216. Clark, J. R., N. L. First, A. B. Chapman and L. E. Casida Age at puberty in four genetic groups of swine. J. Anita. Sci. 31:1032. (Abstr.). Dailey, R. A., J. G. Cloud, N. L. First, A. B. Chapman and L. E. Casida Response of 170-dayold prepuberal Poland China, Yorkshire and crossbred gilts to unilateral ovariectomy. J. Anim. Sci. 31:937. Dailey, R. A., J. B. Peters, N. L. First, A. B. Chapman and L. E. Casida Effect of unilateral ovariectomy in the Yorkshire and Poland China prepuberai gilt. J. Anim. Sci. 28:775. Darlow, A. E Effect of plane of nutrition on reproductive processes in the ewe. Ph.D. Thesis, University of Wisconsin, Madison. Howland, B. E., R. L. Kirkpatrick, A. L. Pope and L. E. Casida Pituitary and ovarian function in ewes fed on two nutritional levels. J. Anita. Set. 25:716. Kirkpatrick, R. L., B. E. Howland, N. L. First and L. E. Casida. 1967a. Some characteristics associated with feed and breed differences in ovulation rate in the gilt. J. Anim. Sci. 26:188. Kirkpatrick, R. L., B. E. Howland, N. L. First and L. E. Casida. 1967b. Ovarian and pituitary gland changes in gilts on two nutrien.t energy levels. J. Anim. Sci. 26:358. Memon, G. N., R. J. Antoniewicz, N. J. Benevenga, A. L. Pope and L. E. Casida Some effects of differences in dietary energy and protein levels on the ovary and the anterior pituitary gland of the ewe. J. Anita. Sci. 28:57. Rigor, E. M., R. K. Meyer, N. L. First and L. E. Casida Endocrine differences associated with follicular development and ovulation rate in swine due to breed and energy intake. J. Anita. Sci. 22:43. Robertson, G. L., L. E. Casida, R. H. Grummer and A. B. Chapman Some feeding and management factors affecting age at puberty and related phenomena in Chester White and Poland China gilts. J. Anim. Sci. 10:841. Snedecor, G. W. and W. G. Cochran Statistical Methods (6th Ed.). Iowa State Press, Ames. Zimmerman, D. R., H. G. Spies, H. L. Self and L. E. Casida Ovulation rate in swine as affected by increased energy intake just prior to ovulation. J. Anim. Sci. 19:295.
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