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Heritability of Fertility in Dairy Cattle1
HERITABILITY
OF F E R T I L I T Y
IN DAIRY CATTLE ~
R. S. DUNBAR, J[~.,* .~ND C. R. HENDERSOG-D¢'p(~rt,~t,'~tt of Animal H~¢sba~dr~ Cor~,(ql UtHt'ersity, Ithaca, Ne.w York
Low reproductive effieieney of d a i r y cattle has long been recognized as a cause of serious economic loss to the d a i r y farmer, and it has seemed reasonable to assume that iml)rovement in reproductive efficiency eouhl be attained b y selecting for some measure of this trait. I f d a i r y cattle breeders are to select for high fertility measured in some p a r t i c u l a r m a n n e r - - i n addition to selecting for other traits of eeonomie i m p o r t a n c e - - i t is i m p o r t a n t to know how effective selection for t h a t p a r t i c u l a r measure of fertility can be, what the best selection procedure is, and what relative emphasis should be placed on fertility and other traits of eeonomie importance. I n order to answer such questions, it is necessary to have reliable estimates of the repeatability and heritability of the p a r t i c u l a r measure of reproductive ef~ciel~cv which is to be used. I n recent years a considerable amount of work has been done on this problem, and the measures of fertility most f r e q u e n t l y employed have been the n u m b e r of services required for conception, n o n r e t u r n s to first service--which is u n d o u b t e d l y highly eorrelated with the f o r m e r - - a n d in some instances, calving interval. Most of the earlier w o r k has been done within certain exp e r i m e n t station herds, but in the last few years several investigations have dealt with populations of d a i r y cattle being bred artificially by bulls belonging to artificial breeding cooperatives. One of the earlier reports of the work on the pt'oblem of infertility is t h a t of Spielman and Jones (5) in which they reported a correlation, r ~ q-0.546 ± 0.118, between the reproductive efficiency of the foundation cows in the Oregon State College herd and the mean reproductive efficiency of their female descendants. I t is not clear, however, whether or not this correlation is biased u p w a r d by the breed differences which they report. Although Tanabe and Casida (6) and T r i m b e r g e r and Davis (7) do not present estimates of repeatability of the n u m b e r of services required per conception, it is clear f r o m their data that repeatability is v e r y low. This is i n f e r r e d f r o m their finding t h a t the n u m b e r of services required for previous conceptions is of no practical value in predicting the n u m b e r of services required for later conceptions and of still less value for predicting the services required for Conception by their progeny. Olds et al. (3) have r e p o r t e d similar results f r o m a s t u d y of the K e n t u c k y A g r i c u l t u r a l E x p e r i m e n t Station herd, and recently Olds and Seath (4) have Received for publication AI'.ril 17, 1953. 1 The material herein reported was submitted in partial fulfillment of the requirements fGr the degree of Master of Science, Cornell University, Ithaca, ~. Y. "-Present address : Department of Dairy Husbandry, West Virginia University, Morgantown. 10(}3
1064
R. S. D U N B A R , JR., AND C. R. H E N D E R S O N
reported a correlation, r ~ 0.084-~-0.012, between the number of services required per conception by dair.y cattle bred artificially by the Kentucky Artificial Breeding Association in two consecutive years. Leonard (2) studied the services required per conception in a population of dairy cattle bred artificially in Maine, and from these data he estimated repeatability to be 0.075. SOURCE AND A N A L Y S I S OF DATA
Nonret~lr~ts to first service. The data utilized ill this s t u d y were obtained by checking a list of cows sired artificially by Holstein bulls in New York against the records of the New York Artificial Breeders' Cooperative, Inc., to determine which of these cows had been insenfinated artificially and what the outcome of the first service had been. Because the list of cows was obtained from the D a i r y Records' Office, this study included production tested cows only. As m a n y first services were observed for each animal as could be found in the records of the New York Artificial Breeders' Cooperative, Inc. I f a cow had not r e t u r n e d to first service within 180 days, the observation was assigned the value 1, and if the cow had returned, that observation was assigned the value 0. The particular value assigned to a r e t u r n and a n o n r e t u r n has no bearing on the estimates of repeatability and heritability, and the numbers 1 and 0 were chosen as a matter of convenience. To facilitate the analysis of these data, they were punched on I.B.M. cards, each card containing the following i n f o r m a t i o n : 1. 2. 3. 4. 5.
Identification of the cow. Identification of the sire of the cow. Identification of the herd in which the cow was located. The year-season 3 i n which the insemination was made. The coded value of a single first service of the cow, 0 or 1.
A total of 1,833 observations was made on 1,0].5 cows located in 297 different herds t h r o u g h o u t the state. These 1,015 cows were sired by 52 different Holstein bulls. The inseminations observed were made in a total of 33 different year-seasons. The analysis of these data consisted of estimating certain components of variance by an estimation procedure designated as Method 1 in a paper by Henderson (1). This estimation procedure results in unbiased estimates of variance components from nonorthogonal data under the assumption of uncorrelated random variables. The components of variance estimated from these data on nonreturns to first service were ~'s, a"h, a-~y, afc, qfsh, O'2hy, and O'fe . _ o is the variance due to sires. The difference among sires which would contribute to the variation among nonreturns of their daughters are additive a The year-season term includes differences associated with years and differences among seasons within years. The months of the year were grouped into four seasons with an attempt to group them such that seasonal variations would be maximized. The four seasons were Dee., Jan., Feb.; Mar., Apr., May; June, July, Aug.; and Sept., Oct., Nov.
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genetic differences plus a certain fraction of epistatic differences. This results f r o m the fact that each of the cows observed had received a sample one-half of the genotype of their respective sires. :Because each sire had d a u g h t e r s located in m a n y different herds and the herds contained daughters of one or more sires, it was possible to separate v a r i a t i o n due to genetic differences among sires f r o m variation due to genetic and environmental differences a m o n g herds. ,T'-'~,is the variance due to herds. Differences which m a y exist among herds include genetic differences, differences due to genetic and environmental interaction and differences in herd environments. Such things as the ability of herd owners to detect estrus and the skill of inseminating technicians, as well as other m a n a g e m e n t factors, are possible sources of enviromnental differences a m o n g herds whi~,h m a y contribute to v a r i a t i o n in n o n r e t u r n s to first service. 2 y is the variance due to year-seasons, and results front changes in the average environment of the poplflation f r o m one year-season to another. Environmental changes f r o m season to season within years and environmental changes associated with different years are included in this component. A n y effects of seasonal changes ]u light, t e m p e r a t u r e , and weather would be i n eluded, as well as a n y effects due to changes ill the techniques of semen processing and artificial insemination. a-~ is the variance among p a t e r n a l half-sisters located ill the same herd. I t is due to genetic differences which include deviations due to dominance and epistasis in addition to additive genetic differences, and what m a y be called p e r m a n e n t environmental effects. P e r m a n e n t enviromnental differences result f r o m those modifications of the cows' inherent fertilities b r o u g h t about b y the environments to which they have been subjected d u r i n g their lifetimes. Such things as p e r m a n e n t injuries due to accident or disease eonie to m i n d most readily. ¢-°~h is the variance due to sire-herd interaction. A n y interactions which m a y have occurred between the genotypes of the sires studied and the environm e n t of the herds in which their daughters were located a n d / o r the genetic constitution of these herds, as represented b y the mates of the sires, would be included in this component of variance. ¢2hy is the variance due to interaction between herds and year-seasons. A n y interactions between the genetic constitutions of individual herds and seasonal environmental effects would be included in this component of variance. The effect of changes in the environment of individual herds due to changes in m a n a g e m e n t practices would also be included in this component. ~-"~ is the variance due to all remaining, nonidentified sources of variation. The quality of the semen used for insemination and t e m p o r a r y infection of the individual at the time of Service are two such nonidentified sources of variation, There are p'erhaps m a n y such factors which are not known.
Calving interval. A f t e r completing the analysis of the data in which nonr e t u r n s to first service were utilized as the measure of fertility of cows sired artificially by Holstein bulls, another sample was studied with calving interval
R. S. D U N B A R ,
1066
J R . , ~IND C. It. H E N D E R S O N
as the measure of fertility. This second group of Holstein cows differed somewhat from those in which nonreturns to first service were used as the measure. of fertility because it was not necessary for the second group to have been inseminated artificially. However, it was necessary for each cow to have freshened at least twice. F r o m these data it was possible to make up a calving interval card for each cow having two or more production records by subtracting the first freshening date from the second. Only the first two freshening dates were considered for any cow or, in other words, there was but a single observation on each cow. Each of the cards nmde up for the s t u d y had the following information punched on it. 1. The identification of the cow. 2. The identification of the s{re of the cow. 3. The identification of the herd in which the cow was located. 4. The length of the calving interval measured in nlonths. These data included 1,636 cows sired artificially by 57 different bulls on 281 farms. The analysis of the data on calving interval was exactly the same as the analysis of the data on nonreturns to first service with the exception that fewer components of variance were estimated. As may be seen from an examination of Table 1, the data <)n n
1
C o m p o n e n t s o f varia~we and p e r c e n t o f total variance ( N o~r et~tr~s ) Compon(u~ts a2 s
ah
Estimated wdue 0.0002 --0.0015
Percent of total 0.1 0.0
a'-'
0.0002
0.1
a~
0.0063
2.6
f i s-~ h
0.0056
2.3
a ~
0.0092
3.7
a-"
0.2255
91.3
Y
c
hy
e
certain sources of variation were probably of 11o consequence. Also, because there was but a single calving interval observed for each individual, it was impossible to separate variation due to genetic and permanent cnvironnmntal differences from other sources of variation among paternal half-sisters within a herd. Consequently, the total variation among paternal half-sisters in the same herd is called ~r~ in the calving interval study. Other components of variance which were estimated from the data on calving interval were a'-'~, a-~h, and a2~u. The interpretation of these components of variance is essentially
~ERTILITY IN DAIRY CATTLE
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the same as described for the components estimated f r o m the data on n o n r e t u r n s to first service. RESULTS AND DISCUSSION
I n the data on n o n r e t u r n s to first service, the n u m b e r of daughters p e r sire ranged f r o m 1 to 212 with an average of 35.2. The mean n o n r e t u r n s per sire ranged f r o m 0 to 1, and the mean of all observations was 0.567 or 56.7% n o n r e t u r n s to first service. The estimates of the components of variance f r o m these data and the p e r cent of the total variance which each of them contributes are presented in Table 1. H a v i n g obtained estimates of the different components of variance, it was possible to use certain of them to estimate the repeatability and heritability of fertility as measured by n o n r e t u r n s to first service. Since a~¢ in Table 1 is an estimate of the variance among p a t e r n a l halfsisters within the same herd, an estimate of the repeatability of n o n r e t u r n s to first service in such a population of half-sisters m a y be computed f r o m the ratio a~¢f[cr-~ -+- a o] ~ 0.0063 / [0.0063 ~ 0.2255] ~ 0.027. All estimate of repeatability in a population of cows in the same herd, but each having a different sire, m a y be computed f r o m the ratio [~'-'~-~- ~ ~- ~ - j / [~2 ~_ 2 ~_ or-oh _~_ #-'~]. Repeatability of n o n r e t u r n s to first service for such a population as this is estimated to be 0.051. Since most herds are composed of p a t e r n a l half-sisters, a few more closely related pairs, and m a n y more less closely related pairs, the intra-herd repeatability of n o n r e t u r n s to first service would be estimated to be some value between 0.027 and 0.051. An estimate of the heritability m a y be computed also f r o m the estimates of the components of variance in Table 1. The ratio used to estimate heritability is ~-'J[~-~ ~ - ~ ] . Although a~-g is not estimated directly f r o m the data, it m a y be estimated indirectly f r o m the relationship ~-~ ~ 1~ a~g. This relationship is an a p p r o x i m a t i o n r a t h e r t h a n an equality because ~-~ contains some variation due to epistasis in addition to additive genetic differences while ~2g represents only additive effects. This computation yields a heritability estimate of 0.004. This is an estimate of the i n t r a h e r d heritability of n o n r e t u r n s to first service in a population with i n t r a h e r d additive genetic variance equal to the additive genetic variance among sires used in artificial breeding but with no nonadditive genetic variance, and no variance due to p e r m a n e n t environmental effects. Consequently, 0.004 is an overestimate of the heritability of n o n r e t u r n s to first service. T u r n i n g to the analysis of the data on calving intervals, it was f o u n d t h a t the u m n b e r of d a u g h t e r s per sire r a n g e d f r o m 1 to 110 with a mean of 18.2 The mean calving interval per sire ranged f r o m 11.00 to 17.25 with a population mean of 13.08 months. The estimates of the components of variance f r o m the calving interval d a t a a n d the per cent of the total variance which each component represents are presented in Table 2. The estimate of a2, in Table 2 is --0.10, but because a
R. S. DUNBAR, JR., AND C. R. HENDERSON
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TABLE 2
Compo~ents of varia~we and percent of total variance (Cah, i~g interval) Component ca
Estimated value
P e r c e n t of total
--0.10
0.0
--0.33
0.0
a~,
1.97
21.8
¢~
7.05
78.2
s
~
negative variance is impossible by definition, the most plausible interpretation of such an estimate is to attribute the negative sign to sampling error and consider it to be an estimate of zero variance. When the estimate of (r~ is interpreted in this way it immediately follows that the heritability of calving interval is estimated from these data to be zero. The most striking feature of Tables 1 and 2 is the large percentage of the total variation attributable to error. This reveals that in these analyses the factors which can be identified and measured are a p p a r e n t l y of little consequence as sources of variation among nonreturns to first service and calving intervals, whereas nonidentifiable and nonmeasurable factors grouped together as sources of error are the cause of a very large part of the total variation in these measures of fertility. There are certain characteristics of the data on nonreturns and calving interval which shouhl be noted. F i r s t of all, the data were limited to produetion tested cows. Perhaps the most significant consequence of this is that heifers which never conceived were not included in the sample. How much bias this introduces into the above estimates of heritability depends upon the extent to which this phenomenon is dependent upon genetic differences among sires. Perhaps estimates of heritability obtained from data which do not include heifers which never conceived are more desirable than estimates from data which do include such females since the measures of fertility usually employed are not applicable to the latter animals, and any selection practiced would be based on these measures. A f u r t h e r limitation of these data is that nonreturns to first service and calving interval, the nleasurcs of fertility used in this study, fail to evaluate the significance of the viability or nonviability of the calf resulting from service. This, however, is a matter of choosing the appropriate measure of reproductive efficiency. Another pertinent consideration concerns the limitations of the method of analysis. I f the assumptions concerning the distribution of the variables are valid, then it may be stated with certainty that the method results in unbiased estimates of the components of variance. To assnme that the effects of consecutive periods of time are independent and that seasonal effects are random variables is probably not entirely valid. I t is possible, however, that removal
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of the bias in the estimates resulting f r o m this invalid assumption would not j u s t i f y the increased complexity of the analysis which would be required if year-seasons had been considered as fixed effects. ~ A f u r t h e r unknown in the method of analysis utilized in this s t u d y concerns the sampling errors of the estimates of components of variance. Therefore, it is impossible to compute confidence limits. When the sample size is large, as in this instance, the sampling errors are probably quite snmll. I n addition to the limitations imposed by the nature of the data and the m a n n e r in which they were collected and analyzed, there is the question as to whether or not the genetic variance with respect to fertility is less in bulls selected for use in artificial breeding t h a n in the population as a whole. But, there are reasons for thinking t h a t the genetic variance for fertility among the bulls studied was not reduced a p p r e c i a b l y b y selection. W h e n bulls are selected for use in artificial breeding, considerably more emphasis is placed on t r a n s m i t t i n g ability for production t h a n on t r a n s m i t t i n g ability for fertility. Of course, the fertility of a bull's semen is given considerable emphasis. Although there is f r e q u e n t l y considerable i n f o r m a t i o n with which to appraise the fertility of the bull's semen, there is usually v e r y little i n f o r m a t i o n which m i g h t be used to appraise the bull's t r a n s m i t t i n g ability for fertility. These considerations, plus the evidence f r o m other studies t h a t repeatability and heritability for the more common measures of fertility are quite low, indicate that selection for inherent fertility of the bulls brought into artificial breeding is relatively ineffective. Consequently, it seems valid to assume t h a t the genetic variance among the sires studied with respect to fertility is essentially the same as t h a t which exists among individuals which m i g h t be included in a r a n d o m sample of Holstein bulls. I t seems certain f r o m this study, and f r o m those reviewed briefly, t h a t genetic variance with respect to fertility is essentially zero when fertility is measured by n o n r e t u r n s to first service, services required per conception, or by length of calving interval. This does not preclude the possibility t h a t there exists appreciable genetic variance of some other measures of reproductive efficiency. I f some measure of fertility such as the n u m b e r of viable calves produced per month of reproductive life were employed, the estimate of genetic variance m i g h t be considerably different f r o m t h a t for n o n r e t u r n s and calving interval. Certainly such a measure of fertility would evaluate the presence or absence of lethal and sublethal genes which result in nonviable calves. W h e t h e r or not these different deleterious genes present a serious problem depends considerably on what the frequencies of such genes are in the population. B y the v e r y n a t u r e of their action, it would be expected t h a t their frequencies would be v e r y low, but it would be i n f o r m a t i v e to have estimates of genetic variance of some measure which reflected the presence or absence of these kinds of genes. 4 The reader is referred to Henderson (1), Methods 2 and 3 for indications of the increased complexity of the analysis necessary if certain elements are regarded as fixed.
1070
R. S. D U N B A R ,
/YR., A N D C. R. H E N D E R S O N
SUMMARY AND CONCLUSIONS U t i l i z i n g d a t a o b t a i n e d f r o n l the D a i r y R e c o r d s ' Office in t h e A n i m a l H u s b a n d r y J ) e p a r t m e n t a t C o r n e l l U n i v e r s i t y a n d t h e New Y o r k A r t i f i c i a l B r e e d e r s ' C o o p e r a t i v e , Inc., i t h a s b e e n p o s s i b l e to s t u d y t h e r e l a t i v e r e p r o d u c t i v e efficiency of g r o u p s of a r t i f i c i a l l y s i r e d p a t e r n a l h a l f - s i b s l o c a t e d on d i f f e r e n t f a r m s t h r o u g h o u t N e w Y o r k state. B e c a u s e these sires h a d d a u g h t e r s on m a n y d i f f e r e n t f a r m s , it was p o s s i b l e to s e p a r a t e v a r i a t i o n d u e to differences a m o n g h e r d s f r o m v a r i a t i o n d u e to d i f f e r e n c e s a m o n g sires. The a n a l y t i c a l p r o c e d u r e cons i s t e d of e s t i m a t i n g tile v a r i a n c e d u e to sires, h e r d s , y e a r - s e a s o n s , cows, a n d certain interactions. B a s e d on t h e e s t i m a t e s o f the c o m p o n e n t s of v a r i a n c e , r e p e a t a b i l i t y of f e r t i l i t y m e a s u r e d b y n o n r e t u r n s to first service in a p o p u l a t i o n of h a l f - s i s t e r s w i t h i n the s a m e h e r d is e s t i m a t e d to be 0.027, a n d r e p e a t a b i l i t y of t h i s m e a s u r e in a p o p u l a t i o n of cows b y d i f f e r e n t sires w i t h i n the s a m e h e r d is e s t i m a t e d t o be 0.051. The a v e r a g e i n t r a h e r d r e p e a t a b i l i t y is e s t i m a t e d to be some v a l u e b e t w e e n 0.027 a n d 0.051. The h e r i t a b i l i t y of n o n r e t u r n s to first service is e s t i m a t e d to be 0.004. W h e n c a l v i n g i n t e r v a l is u s e d as t h e m e a s u r e of f e r t i l i t y , h e r i t a b i l i t y is e s t i m a t e d to be zero. On the basis of this w o r k a n d the w o r k of o t h e r s w h i c h h a s been r e v i e w e d briefly, i t seems c e r t a i n t h a t selection f o r f e r t i l i t y m e a s u r e d b y n o n r e t u r n s t o first service, services r e q u i r e d p e r c o n c e p t i o n , o r c a l v i n g i n t e r v a l c a n n o t b e v e r y effective a n d t h a t c o n s i d e r a t i o n g i v e n to f e r t i l i t y in s e l e c t i n g b r e e d i n g stock will b u t serve to d e c r e a s e t h e effectiveness of selection f o r such t r a i t s as b u t t e r f a t p r o d u c t i o n a n d t y p e c o n f o r m a t i o n . A f u r t h e r i m p l i c a t i o n o f these r e s u l t s is t h a t a n y m a r k e d i m p r o v e m e n t o b t a i n e d in t h e r e p r o d u c t i v e efficiency of t h e d a i r y c a t t l e p o p u l a t i o n n m s t be b r o u g h t a b o u t b y i m p r o v e m e n t of n u t r i t i o n a l , p a t h o l o g i c a l , a n d / ' o r o t h e r e n v i r o n m e n t a l f a c t o r s w h i c h e x e r t an influence on the p r o c e s s of r e p r o d u c t i o n . ACKNOWLEI)GMENTS The authors wish to exI)ress their "lppreciation to tile New York Artificial Breeders' Cooperative, Inc. and the Extension Division of the (!ornell University Department of Animal Husbandry for makh~g avnilal>lt the basic d',t-~ for this study. REFERENCES (1) ~-IENDERSOt¢,C. ]{. Estimation of Variance and Covariance Components. Biometrics. In Press. (2) LEONARD,H. A. All Analysis of Factors Affecting Artifiei-fl Breeding Efficiency of Dairy Cattle in Maine. UnI)utdished Research Problem. 1950. (3) OLDS, D., MORP~ISON,H. B., AND SEATIJ, D. M. Efficiency of Natural Breeding in Dairy Cattle. Kentucky Agr. Expt. Sta. Bull. 539. 1949. (4) OLDS, I)., AND SE.~T~.~,D. M. Predicting the Breeding Efficiency of Dairy Cattle. J. Dairy Sci., 32: 376. 1950. (Abs.)
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(5) SPIEL:~[AN, A. A., AND ,]-ONES, I. R. The Reproductive Efficiency of Dairy Cattle. J. Dairy Sci., 22: 329-334. 1939. (6) TANA~E, R., AN]) C_~SIDA, L. E. The Nature of Reproductive Failures in Cows of Low Fertility. J. Dairy Sci., 32: 237-246. 1949. (7) TRII~IBEI~GER,G. W., AND DAVIS, H. P. Predictability of Breeding Efficiency in Dairy Cattle from Their Previous Conception Rate and from Their Heredity. J. Dairy Sci., 28: 659-669. 1945.
OF F E R T I L I T Y
IN DAIRY CATTLE ~
R. S. DUNBAR, J[~.,* .~ND C. R. HENDERSOG-D¢'p(~rt,~t,'~tt of Animal H~¢sba~dr~ Cor~,(ql UtHt'ersity, Ithaca, Ne.w York
Low reproductive effieieney of d a i r y cattle has long been recognized as a cause of serious economic loss to the d a i r y farmer, and it has seemed reasonable to assume that iml)rovement in reproductive efficiency eouhl be attained b y selecting for some measure of this trait. I f d a i r y cattle breeders are to select for high fertility measured in some p a r t i c u l a r m a n n e r - - i n addition to selecting for other traits of eeonomie i m p o r t a n c e - - i t is i m p o r t a n t to know how effective selection for t h a t p a r t i c u l a r measure of fertility can be, what the best selection procedure is, and what relative emphasis should be placed on fertility and other traits of eeonomie importance. I n order to answer such questions, it is necessary to have reliable estimates of the repeatability and heritability of the p a r t i c u l a r measure of reproductive ef~ciel~cv which is to be used. I n recent years a considerable amount of work has been done on this problem, and the measures of fertility most f r e q u e n t l y employed have been the n u m b e r of services required for conception, n o n r e t u r n s to first service--which is u n d o u b t e d l y highly eorrelated with the f o r m e r - - a n d in some instances, calving interval. Most of the earlier w o r k has been done within certain exp e r i m e n t station herds, but in the last few years several investigations have dealt with populations of d a i r y cattle being bred artificially by bulls belonging to artificial breeding cooperatives. One of the earlier reports of the work on the pt'oblem of infertility is t h a t of Spielman and Jones (5) in which they reported a correlation, r ~ q-0.546 ± 0.118, between the reproductive efficiency of the foundation cows in the Oregon State College herd and the mean reproductive efficiency of their female descendants. I t is not clear, however, whether or not this correlation is biased u p w a r d by the breed differences which they report. Although Tanabe and Casida (6) and T r i m b e r g e r and Davis (7) do not present estimates of repeatability of the n u m b e r of services required per conception, it is clear f r o m their data that repeatability is v e r y low. This is i n f e r r e d f r o m their finding t h a t the n u m b e r of services required for previous conceptions is of no practical value in predicting the n u m b e r of services required for later conceptions and of still less value for predicting the services required for Conception by their progeny. Olds et al. (3) have r e p o r t e d similar results f r o m a s t u d y of the K e n t u c k y A g r i c u l t u r a l E x p e r i m e n t Station herd, and recently Olds and Seath (4) have Received for publication AI'.ril 17, 1953. 1 The material herein reported was submitted in partial fulfillment of the requirements fGr the degree of Master of Science, Cornell University, Ithaca, ~. Y. "-Present address : Department of Dairy Husbandry, West Virginia University, Morgantown. 10(}3
1064
R. S. D U N B A R , JR., AND C. R. H E N D E R S O N
reported a correlation, r ~ 0.084-~-0.012, between the number of services required per conception by dair.y cattle bred artificially by the Kentucky Artificial Breeding Association in two consecutive years. Leonard (2) studied the services required per conception in a population of dairy cattle bred artificially in Maine, and from these data he estimated repeatability to be 0.075. SOURCE AND A N A L Y S I S OF DATA
Nonret~lr~ts to first service. The data utilized ill this s t u d y were obtained by checking a list of cows sired artificially by Holstein bulls in New York against the records of the New York Artificial Breeders' Cooperative, Inc., to determine which of these cows had been insenfinated artificially and what the outcome of the first service had been. Because the list of cows was obtained from the D a i r y Records' Office, this study included production tested cows only. As m a n y first services were observed for each animal as could be found in the records of the New York Artificial Breeders' Cooperative, Inc. I f a cow had not r e t u r n e d to first service within 180 days, the observation was assigned the value 1, and if the cow had returned, that observation was assigned the value 0. The particular value assigned to a r e t u r n and a n o n r e t u r n has no bearing on the estimates of repeatability and heritability, and the numbers 1 and 0 were chosen as a matter of convenience. To facilitate the analysis of these data, they were punched on I.B.M. cards, each card containing the following i n f o r m a t i o n : 1. 2. 3. 4. 5.
Identification of the cow. Identification of the sire of the cow. Identification of the herd in which the cow was located. The year-season 3 i n which the insemination was made. The coded value of a single first service of the cow, 0 or 1.
A total of 1,833 observations was made on 1,0].5 cows located in 297 different herds t h r o u g h o u t the state. These 1,015 cows were sired by 52 different Holstein bulls. The inseminations observed were made in a total of 33 different year-seasons. The analysis of these data consisted of estimating certain components of variance by an estimation procedure designated as Method 1 in a paper by Henderson (1). This estimation procedure results in unbiased estimates of variance components from nonorthogonal data under the assumption of uncorrelated random variables. The components of variance estimated from these data on nonreturns to first service were ~'s, a"h, a-~y, afc, qfsh, O'2hy, and O'fe . _ o is the variance due to sires. The difference among sires which would contribute to the variation among nonreturns of their daughters are additive a The year-season term includes differences associated with years and differences among seasons within years. The months of the year were grouped into four seasons with an attempt to group them such that seasonal variations would be maximized. The four seasons were Dee., Jan., Feb.; Mar., Apr., May; June, July, Aug.; and Sept., Oct., Nov.
FERTILITY
IN DAIRY CATTLE
1065
genetic differences plus a certain fraction of epistatic differences. This results f r o m the fact that each of the cows observed had received a sample one-half of the genotype of their respective sires. :Because each sire had d a u g h t e r s located in m a n y different herds and the herds contained daughters of one or more sires, it was possible to separate v a r i a t i o n due to genetic differences among sires f r o m variation due to genetic and environmental differences a m o n g herds. ,T'-'~,is the variance due to herds. Differences which m a y exist among herds include genetic differences, differences due to genetic and environmental interaction and differences in herd environments. Such things as the ability of herd owners to detect estrus and the skill of inseminating technicians, as well as other m a n a g e m e n t factors, are possible sources of enviromnental differences a m o n g herds whi~,h m a y contribute to v a r i a t i o n in n o n r e t u r n s to first service. 2 y is the variance due to year-seasons, and results front changes in the average environment of the poplflation f r o m one year-season to another. Environmental changes f r o m season to season within years and environmental changes associated with different years are included in this component. A n y effects of seasonal changes ]u light, t e m p e r a t u r e , and weather would be i n eluded, as well as a n y effects due to changes ill the techniques of semen processing and artificial insemination. a-~ is the variance among p a t e r n a l half-sisters located ill the same herd. I t is due to genetic differences which include deviations due to dominance and epistasis in addition to additive genetic differences, and what m a y be called p e r m a n e n t environmental effects. P e r m a n e n t enviromnental differences result f r o m those modifications of the cows' inherent fertilities b r o u g h t about b y the environments to which they have been subjected d u r i n g their lifetimes. Such things as p e r m a n e n t injuries due to accident or disease eonie to m i n d most readily. ¢-°~h is the variance due to sire-herd interaction. A n y interactions which m a y have occurred between the genotypes of the sires studied and the environm e n t of the herds in which their daughters were located a n d / o r the genetic constitution of these herds, as represented b y the mates of the sires, would be included in this component of variance. ¢2hy is the variance due to interaction between herds and year-seasons. A n y interactions between the genetic constitutions of individual herds and seasonal environmental effects would be included in this component of variance. The effect of changes in the environment of individual herds due to changes in m a n a g e m e n t practices would also be included in this component. ~-"~ is the variance due to all remaining, nonidentified sources of variation. The quality of the semen used for insemination and t e m p o r a r y infection of the individual at the time of Service are two such nonidentified sources of variation, There are p'erhaps m a n y such factors which are not known.
Calving interval. A f t e r completing the analysis of the data in which nonr e t u r n s to first service were utilized as the measure of fertility of cows sired artificially by Holstein bulls, another sample was studied with calving interval
R. S. D U N B A R ,
1066
J R . , ~IND C. It. H E N D E R S O N
as the measure of fertility. This second group of Holstein cows differed somewhat from those in which nonreturns to first service were used as the measure. of fertility because it was not necessary for the second group to have been inseminated artificially. However, it was necessary for each cow to have freshened at least twice. F r o m these data it was possible to make up a calving interval card for each cow having two or more production records by subtracting the first freshening date from the second. Only the first two freshening dates were considered for any cow or, in other words, there was but a single observation on each cow. Each of the cards nmde up for the s t u d y had the following information punched on it. 1. The identification of the cow. 2. The identification of the s{re of the cow. 3. The identification of the herd in which the cow was located. 4. The length of the calving interval measured in nlonths. These data included 1,636 cows sired artificially by 57 different bulls on 281 farms. The analysis of the data on calving interval was exactly the same as the analysis of the data on nonreturns to first service with the exception that fewer components of variance were estimated. As may be seen from an examination of Table 1, the data <)n n
1
C o m p o n e n t s o f varia~we and p e r c e n t o f total variance ( N o~r et~tr~s ) Compon(u~ts a2 s
ah
Estimated wdue 0.0002 --0.0015
Percent of total 0.1 0.0
a'-'
0.0002
0.1
a~
0.0063
2.6
f i s-~ h
0.0056
2.3
a ~
0.0092
3.7
a-"
0.2255
91.3
Y
c
hy
e
certain sources of variation were probably of 11o consequence. Also, because there was but a single calving interval observed for each individual, it was impossible to separate variation due to genetic and permanent cnvironnmntal differences from other sources of variation among paternal half-sisters within a herd. Consequently, the total variation among paternal half-sisters in the same herd is called ~r~ in the calving interval study. Other components of variance which were estimated from the data on calving interval were a'-'~, a-~h, and a2~u. The interpretation of these components of variance is essentially
~ERTILITY IN DAIRY CATTLE
1067
the same as described for the components estimated f r o m the data on n o n r e t u r n s to first service. RESULTS AND DISCUSSION
I n the data on n o n r e t u r n s to first service, the n u m b e r of daughters p e r sire ranged f r o m 1 to 212 with an average of 35.2. The mean n o n r e t u r n s per sire ranged f r o m 0 to 1, and the mean of all observations was 0.567 or 56.7% n o n r e t u r n s to first service. The estimates of the components of variance f r o m these data and the p e r cent of the total variance which each of them contributes are presented in Table 1. H a v i n g obtained estimates of the different components of variance, it was possible to use certain of them to estimate the repeatability and heritability of fertility as measured by n o n r e t u r n s to first service. Since a~¢ in Table 1 is an estimate of the variance among p a t e r n a l halfsisters within the same herd, an estimate of the repeatability of n o n r e t u r n s to first service in such a population of half-sisters m a y be computed f r o m the ratio a~¢f[cr-~ -+- a o] ~ 0.0063 / [0.0063 ~ 0.2255] ~ 0.027. All estimate of repeatability in a population of cows in the same herd, but each having a different sire, m a y be computed f r o m the ratio [~'-'~-~- ~ ~- ~ - j / [~2 ~_ 2 ~_ or-oh _~_ #-'~]. Repeatability of n o n r e t u r n s to first service for such a population as this is estimated to be 0.051. Since most herds are composed of p a t e r n a l half-sisters, a few more closely related pairs, and m a n y more less closely related pairs, the intra-herd repeatability of n o n r e t u r n s to first service would be estimated to be some value between 0.027 and 0.051. An estimate of the heritability m a y be computed also f r o m the estimates of the components of variance in Table 1. The ratio used to estimate heritability is ~-'J[~-~ ~ - ~ ] . Although a~-g is not estimated directly f r o m the data, it m a y be estimated indirectly f r o m the relationship ~-~ ~ 1~ a~g. This relationship is an a p p r o x i m a t i o n r a t h e r t h a n an equality because ~-~ contains some variation due to epistasis in addition to additive genetic differences while ~2g represents only additive effects. This computation yields a heritability estimate of 0.004. This is an estimate of the i n t r a h e r d heritability of n o n r e t u r n s to first service in a population with i n t r a h e r d additive genetic variance equal to the additive genetic variance among sires used in artificial breeding but with no nonadditive genetic variance, and no variance due to p e r m a n e n t environmental effects. Consequently, 0.004 is an overestimate of the heritability of n o n r e t u r n s to first service. T u r n i n g to the analysis of the data on calving intervals, it was f o u n d t h a t the u m n b e r of d a u g h t e r s per sire r a n g e d f r o m 1 to 110 with a mean of 18.2 The mean calving interval per sire ranged f r o m 11.00 to 17.25 with a population mean of 13.08 months. The estimates of the components of variance f r o m the calving interval d a t a a n d the per cent of the total variance which each component represents are presented in Table 2. The estimate of a2, in Table 2 is --0.10, but because a
R. S. DUNBAR, JR., AND C. R. HENDERSON
1068
TABLE 2
Compo~ents of varia~we and percent of total variance (Cah, i~g interval) Component ca
Estimated value
P e r c e n t of total
--0.10
0.0
--0.33
0.0
a~,
1.97
21.8
¢~
7.05
78.2
s
~
negative variance is impossible by definition, the most plausible interpretation of such an estimate is to attribute the negative sign to sampling error and consider it to be an estimate of zero variance. When the estimate of (r~ is interpreted in this way it immediately follows that the heritability of calving interval is estimated from these data to be zero. The most striking feature of Tables 1 and 2 is the large percentage of the total variation attributable to error. This reveals that in these analyses the factors which can be identified and measured are a p p a r e n t l y of little consequence as sources of variation among nonreturns to first service and calving intervals, whereas nonidentifiable and nonmeasurable factors grouped together as sources of error are the cause of a very large part of the total variation in these measures of fertility. There are certain characteristics of the data on nonreturns and calving interval which shouhl be noted. F i r s t of all, the data were limited to produetion tested cows. Perhaps the most significant consequence of this is that heifers which never conceived were not included in the sample. How much bias this introduces into the above estimates of heritability depends upon the extent to which this phenomenon is dependent upon genetic differences among sires. Perhaps estimates of heritability obtained from data which do not include heifers which never conceived are more desirable than estimates from data which do include such females since the measures of fertility usually employed are not applicable to the latter animals, and any selection practiced would be based on these measures. A f u r t h e r limitation of these data is that nonreturns to first service and calving interval, the nleasurcs of fertility used in this study, fail to evaluate the significance of the viability or nonviability of the calf resulting from service. This, however, is a matter of choosing the appropriate measure of reproductive efficiency. Another pertinent consideration concerns the limitations of the method of analysis. I f the assumptions concerning the distribution of the variables are valid, then it may be stated with certainty that the method results in unbiased estimates of the components of variance. To assnme that the effects of consecutive periods of time are independent and that seasonal effects are random variables is probably not entirely valid. I t is possible, however, that removal
FERTILITY
IN DA[I~Y CATTLE
i0,6~)
of the bias in the estimates resulting f r o m this invalid assumption would not j u s t i f y the increased complexity of the analysis which would be required if year-seasons had been considered as fixed effects. ~ A f u r t h e r unknown in the method of analysis utilized in this s t u d y concerns the sampling errors of the estimates of components of variance. Therefore, it is impossible to compute confidence limits. When the sample size is large, as in this instance, the sampling errors are probably quite snmll. I n addition to the limitations imposed by the nature of the data and the m a n n e r in which they were collected and analyzed, there is the question as to whether or not the genetic variance with respect to fertility is less in bulls selected for use in artificial breeding t h a n in the population as a whole. But, there are reasons for thinking t h a t the genetic variance for fertility among the bulls studied was not reduced a p p r e c i a b l y b y selection. W h e n bulls are selected for use in artificial breeding, considerably more emphasis is placed on t r a n s m i t t i n g ability for production t h a n on t r a n s m i t t i n g ability for fertility. Of course, the fertility of a bull's semen is given considerable emphasis. Although there is f r e q u e n t l y considerable i n f o r m a t i o n with which to appraise the fertility of the bull's semen, there is usually v e r y little i n f o r m a t i o n which m i g h t be used to appraise the bull's t r a n s m i t t i n g ability for fertility. These considerations, plus the evidence f r o m other studies t h a t repeatability and heritability for the more common measures of fertility are quite low, indicate that selection for inherent fertility of the bulls brought into artificial breeding is relatively ineffective. Consequently, it seems valid to assume t h a t the genetic variance among the sires studied with respect to fertility is essentially the same as t h a t which exists among individuals which m i g h t be included in a r a n d o m sample of Holstein bulls. I t seems certain f r o m this study, and f r o m those reviewed briefly, t h a t genetic variance with respect to fertility is essentially zero when fertility is measured by n o n r e t u r n s to first service, services required per conception, or by length of calving interval. This does not preclude the possibility t h a t there exists appreciable genetic variance of some other measures of reproductive efficiency. I f some measure of fertility such as the n u m b e r of viable calves produced per month of reproductive life were employed, the estimate of genetic variance m i g h t be considerably different f r o m t h a t for n o n r e t u r n s and calving interval. Certainly such a measure of fertility would evaluate the presence or absence of lethal and sublethal genes which result in nonviable calves. W h e t h e r or not these different deleterious genes present a serious problem depends considerably on what the frequencies of such genes are in the population. B y the v e r y n a t u r e of their action, it would be expected t h a t their frequencies would be v e r y low, but it would be i n f o r m a t i v e to have estimates of genetic variance of some measure which reflected the presence or absence of these kinds of genes. 4 The reader is referred to Henderson (1), Methods 2 and 3 for indications of the increased complexity of the analysis necessary if certain elements are regarded as fixed.
1070
R. S. D U N B A R ,
/YR., A N D C. R. H E N D E R S O N
SUMMARY AND CONCLUSIONS U t i l i z i n g d a t a o b t a i n e d f r o n l the D a i r y R e c o r d s ' Office in t h e A n i m a l H u s b a n d r y J ) e p a r t m e n t a t C o r n e l l U n i v e r s i t y a n d t h e New Y o r k A r t i f i c i a l B r e e d e r s ' C o o p e r a t i v e , Inc., i t h a s b e e n p o s s i b l e to s t u d y t h e r e l a t i v e r e p r o d u c t i v e efficiency of g r o u p s of a r t i f i c i a l l y s i r e d p a t e r n a l h a l f - s i b s l o c a t e d on d i f f e r e n t f a r m s t h r o u g h o u t N e w Y o r k state. B e c a u s e these sires h a d d a u g h t e r s on m a n y d i f f e r e n t f a r m s , it was p o s s i b l e to s e p a r a t e v a r i a t i o n d u e to differences a m o n g h e r d s f r o m v a r i a t i o n d u e to d i f f e r e n c e s a m o n g sires. The a n a l y t i c a l p r o c e d u r e cons i s t e d of e s t i m a t i n g tile v a r i a n c e d u e to sires, h e r d s , y e a r - s e a s o n s , cows, a n d certain interactions. B a s e d on t h e e s t i m a t e s o f the c o m p o n e n t s of v a r i a n c e , r e p e a t a b i l i t y of f e r t i l i t y m e a s u r e d b y n o n r e t u r n s to first service in a p o p u l a t i o n of h a l f - s i s t e r s w i t h i n the s a m e h e r d is e s t i m a t e d to be 0.027, a n d r e p e a t a b i l i t y of t h i s m e a s u r e in a p o p u l a t i o n of cows b y d i f f e r e n t sires w i t h i n the s a m e h e r d is e s t i m a t e d t o be 0.051. The a v e r a g e i n t r a h e r d r e p e a t a b i l i t y is e s t i m a t e d to be some v a l u e b e t w e e n 0.027 a n d 0.051. The h e r i t a b i l i t y of n o n r e t u r n s to first service is e s t i m a t e d to be 0.004. W h e n c a l v i n g i n t e r v a l is u s e d as t h e m e a s u r e of f e r t i l i t y , h e r i t a b i l i t y is e s t i m a t e d to be zero. On the basis of this w o r k a n d the w o r k of o t h e r s w h i c h h a s been r e v i e w e d briefly, i t seems c e r t a i n t h a t selection f o r f e r t i l i t y m e a s u r e d b y n o n r e t u r n s t o first service, services r e q u i r e d p e r c o n c e p t i o n , o r c a l v i n g i n t e r v a l c a n n o t b e v e r y effective a n d t h a t c o n s i d e r a t i o n g i v e n to f e r t i l i t y in s e l e c t i n g b r e e d i n g stock will b u t serve to d e c r e a s e t h e effectiveness of selection f o r such t r a i t s as b u t t e r f a t p r o d u c t i o n a n d t y p e c o n f o r m a t i o n . A f u r t h e r i m p l i c a t i o n o f these r e s u l t s is t h a t a n y m a r k e d i m p r o v e m e n t o b t a i n e d in t h e r e p r o d u c t i v e efficiency of t h e d a i r y c a t t l e p o p u l a t i o n n m s t be b r o u g h t a b o u t b y i m p r o v e m e n t of n u t r i t i o n a l , p a t h o l o g i c a l , a n d / ' o r o t h e r e n v i r o n m e n t a l f a c t o r s w h i c h e x e r t an influence on the p r o c e s s of r e p r o d u c t i o n . ACKNOWLEI)GMENTS The authors wish to exI)ress their "lppreciation to tile New York Artificial Breeders' Cooperative, Inc. and the Extension Division of the (!ornell University Department of Animal Husbandry for makh~g avnilal>lt the basic d',t-~ for this study. REFERENCES (1) ~-IENDERSOt¢,C. ]{. Estimation of Variance and Covariance Components. Biometrics. In Press. (2) LEONARD,H. A. All Analysis of Factors Affecting Artifiei-fl Breeding Efficiency of Dairy Cattle in Maine. UnI)utdished Research Problem. 1950. (3) OLDS, D., MORP~ISON,H. B., AND SEATIJ, D. M. Efficiency of Natural Breeding in Dairy Cattle. Kentucky Agr. Expt. Sta. Bull. 539. 1949. (4) OLDS, I)., AND SE.~T~.~,D. M. Predicting the Breeding Efficiency of Dairy Cattle. J. Dairy Sci., 32: 376. 1950. (Abs.)
FERTILITY
IN
DAIRY
CATTLE
1071
(5) SPIEL:~[AN, A. A., AND ,]-ONES, I. R. The Reproductive Efficiency of Dairy Cattle. J. Dairy Sci., 22: 329-334. 1939. (6) TANA~E, R., AN]) C_~SIDA, L. E. The Nature of Reproductive Failures in Cows of Low Fertility. J. Dairy Sci., 32: 237-246. 1949. (7) TRII~IBEI~GER,G. W., AND DAVIS, H. P. Predictability of Breeding Efficiency in Dairy Cattle from Their Previous Conception Rate and from Their Heredity. J. Dairy Sci., 28: 659-669. 1945.