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Specific and General Combining Abilities for Production and Reproduction among Lines of Holstein Cattle1, 2
Specific and General Combining Abilities for Production and Reproduction among Lines of Holstein Cattle 1 2 R. C. BECKETT, T. M. LUDWICK, E. R. RADER, H. C. HINES, and R. PEARSON Department of Dairy Science The Ohio Agricultural Research and Development Center and The Ohio State University Columbus 43210 INTRODUCTION
ABSTRACT
Many studies have reported effects of systems of mating on quantitative traits in dairy cattle. Generally inbreeding of a cattle population has depressed all aspects of performance (1, 2, 5, 6, 8, 10, 14, 15, 19, 21, 22, 24). Sizes of the effects have varied, and in several studies (5, 19) there was evidence for a difference in response between individual lines. Over the years, many animal breeders working with specific lines of cattle have claimed that inbreeding has been a useful tool for herd improvement. Others have placed considerable faith in the belief that certain lines have "nicked" well together while other lines have not. Crosses between breeds of cattle have revealed heterosis for milk production (4, 7, 18, 20, 23), but no single cross has been superior to the purebred Holstein. Performances of crosses between the Red Sindhi and Red Dane breeds in both Thailand (16) and India (17) suggest specific combining ability for yields of milk and fat. This inbreeding and linecrossing study involved the inbreeding and reciprocal crossing of several lines of Holstein cattle with no deliberate selection of females. Inbreds and linecrosses were compared under comparable environmental conditions. Analyses of earlier data on size and body weight have been reported by Brum et al. (3). This paper reports effects of mating system on productive and reproductive traits.
Six inbred lines of Holstein cattle were developed and reciprocally crossed to assess the importance of heterotic effects for yield and reproductive traits. Overall both yield and reproductive performance declined with inbreeding, but effects varied with different lines. In two of the lines milk yield increased during inbreeding. Regression coefficients for each percent of inbreeding ranged from +39 to - 7 3 kg of milk. Production for estimates of general combining abilities for the different lines ranged from 5799 to 7075 kg of milk indicating the genetic variability available for selection. Some evidence was found for specific combining ability for reproductive performance but none for yield traits. Reciprocal differences were observed only for reproductive performance involving two of the line combinations. Heterosis was present for milk fat percentage, persistency of lactation, and reproductive performance. Effects of dominant genes appeared to be of minor importance in determining yield traits, and the possibility of nicking between lines for production traits, while not excluded, was of low likelihood. While mild inbreeding sometimes may produce genetic improvement, a breeding program based on additive genetic theory offers the best opportunities for raising productive performance.
MATERIALS AND METHODS
Received July 31, 1978. 1A Contribution to the NC-2 Dairy Cattle Breeding Project - Improvement in Dairy Cattle Breeding with Emphasis on Selection. 2Journal Article No. 109-78 Ohio Agricultural Research and Development Center, Wooster 44691. 1979 J Dairy Sci 62:613-620
The experiment began in 1948 as a cooperative study between The Ohio State University, The Ohio Department of Mental Hygiene and Mental Retardation, and the United States Department of Agriculture. Six inbred lines of Holstein cattle were developed on state institutional farms in Ohio.
613
614
BECKETT ET AL.
Three of the lines were in separate herds; one large herd was divided into two lines, and one line was developed between two smaller herds. Two or three closely related .bulls were introduced as the basic foundation sires for each line. Sires were selected primarily on production of their dams and paternal half-sisters. Pedigrees of sires in each line were completely distinctive through seven generations. A system of mating was devised to develop uniformly a gradual increase in inbreeding. The average inbreeding within each line varied from 0 to 5% prior to the initiation of the project, and the herds were closed when the breeding scheme began. The objective of the mating system was to develop gradually a coefficient of relationship of 25 to 30% between all female members of a line. Young sires to continue the line development were chosen from the highest producing cows in each line. All heifer calves were retained, and no animals were voluntarily culled until they had made at least one normal or extendable production record. The rate of line development varied, and in 1961 four of the lines were well enough developed to allow linecrossing to begin with frozen semen. At this time the average inbreeding of the four earliest developed lines was approximately 12% and the average relationship among the females was about 28%. Sixty percent of the qualified animals in each line were selected at random within age groups for linecrossing, the remainder continued to be inbred to provide contemporaries. Linecrossing began in the remaining two herds in 1962 and in 1965. All possible reciprocal crosses were represented in the initial four lines in linecrossing, but some were missing when all six lines were considered. Contemporary linecrosses and linebreds were reared and milked in the same herd at the same time. Each sire represented in the study had both inbred and linecross progeny. Blood typing was routine for all animals, and this was used to resolve parentage queries. An analysis early in line development by Hines et al. (13) indicated that the degree of homozygosity of seven blood and milk polymorphic systems appeared to behave generally as predicted by inbreeding theory with little evidence for deviation from the expected linear relationship. In the present study, data analyzed included first lactation records for yields of milk, butterfat, solids not fat (SNF), protein, days open, Journal of Dairy Science Vol. 62, No. 4, 1979
age at calving, and lactation length. All production records were on a mature equivalent (ME) 305-day - 2× basis with appropriate Dairy Herd Improvement adjustment factors. The distribution of animals by lines and linecrosses is in Table 1 along with the n u m b e r of sires. Analysis of Inbreeding
Estimates were separate for the linebred animals belonging to each line by the following fixed model (Model I). Yijkl = ~/+ Si + YRj + SE k + by/Fx + eijkl where /~ is the mean, Yijkl is a measure of the performance of the lth daughter of the ith sire calving in the kth season of the jth year, eijki represents the random error associated with this lth individual and by/Fx represents the linear regression on inbreeding of the trait being studied. In line 1 sires were confounded with years, and regression coefficients for this line were estimated with a similar model in which sires were ignored. An additional analysis of line 1 fitting Year-Sire subclasses gave almost identical estimates of the regression coefficients and their standard deviations.
Estimation of General Combining Ability and Heterotic Effects
The procedure followed closely that described as analysis II by Gardner and Eberhart (9), and the following mixed model (Model I1)
TABLE 1. Distribution of linebred and linecross animals by line of sire and line of dam. Line of sire
No. of sires
1
Line of dam 3 4
2
5
6
1
7a
85 a
17
2 3 4
7 5 7
18 19 17
102 14 17
11 9 77 13
11 4 6 112
21 8 0 12
14 1 I1
5 6
6 7
15 0
3 38
0 0
0 0
65 10
2 85
0
aonly 6 sires with 79 linebred progeny were included in the 4 line analysis-one sire did not have linecross progeny in lines 2 to 4.
COMBINING ABILITIES FOR PRODUCTION AND REPRODUCTION initially was e m p l o y e d : Y i j k l m n o = bt Li + Sij + Tk + HI + Y R m + SEn (LT)ik + (ST)ij k + ( H R Y ) I m + (HSE)In + * (YRSE)mn + eijklmn o w h e r e Y i j k l m n o is a m e a s u r e o f t h e p e r f o r m a n c e o f t h e 0th d a u g h t e r o f t h e j t h sire w i t h i n t h e ith sire line b o r n t o t h e lth d a m line ( o r h e r d ) a n d b e g i n n i n g p r o d u c t i o n in t h e m t h y e a r a n d n t h season, /l is t h e m e a n , a n d T k refers t o t h e t y p e o f b r e e d i n g involved, l i n e b r e d or linecross. I n t e r a c t i o n s o f various t e r m s in t h e m o d e l also were f i t t e d as i n d i c a t e d . T h e analysis was b y M i x e d Model Least Squares A n a l y s i s P r o g r a m as described b y Harvey u n d e r M o d e l T y p e 07 (12). Sires w i t h i n lines were r a n d o m ; all o t h e r effects were fixed. Interactions (ST)ijk, (HSE)In, a n d ( Y R S E ) m n were n o t significant. T h e y were d e l e t e d f r o m t h e m o d e l , a n d t h e analysis was r e p e a t e d as M o d e l T y p e 03, as d e s c r i b e d b y Harvey. T h e s a m e m o d e l a n d p r o c e d u r e l a t e r i n c l u d e d linear regression o n i n b r e e d i n g as a c o n t i n u o u s i n d e p e n d e n t variable. T h e m e a n s q u a r e a n d c o n s t a n t e s t i m a t e s for lines L i were e q u i v a l e n t to t h e general c o m b i n ing ability ( G C A ) o f t h e s e lines e s t i m a t e d o n t h e basis o f b o t h t h e l i n e b r e d a n d linecross
615
p r o g e n y o f t h e sires o f each line. T h e m e a n s q u a r e a n d c o n s t a n t e s t i m a t e s for T--the t y p e o f breeding--measured the importance of heterosis c o m p u t e d as an average e f f e c t over all lines ( A V Het). T h e line × t y p e o f b r e e d i n g i n t e r a c t i o n c o m p o n e n t s (LT)ik were an i n d i c a t i o n o f t h e individual d i f f e r e n c e s b e t w e e n lines in t h e i r h e t e r o t i c effects. T h e sire w i t h i n line × t y p e o f b r e e d i n g i n t e r a c t i o n (ST)ij k c o m p o n e n t s indic a t e d w h e t h e r sires w i t h i n lines t e n d e d t o r a n k d i f f e r e n t l y d e p e n d i n g o n w h e t h e r t h e y were e v a l u a t e d o n t h e basis o f t h e i r l i n e b r e d or linecross p r o g e n y a n d was an i n d i c a t i o n o f t h e i m p o r t a n c e o f i n d i v i d u a l d i f f e r e n c e s in h e t e r o t i c effects b e t w e e n sires w i t h i n t h e s a m e line. Estimation of Specific Combining Ability and Residual Recriprocal Effects
D a t a f r o m t h e f o u r line crosses w h i c h h a d all 16 subclasses filled were used t o o b t a i n estim a t e s o f specific c o m b i n i n g ability ( S C A ) a n d residual reciprocal effects ( R R ) . T h e s e effects were e s t i m a t e d a c c o r d i n g t o t h e m e t h o d o f Harvey (11) b y t h e f o l l o w i n g m i x e d m o d e l (Model III). Yijklmn = bt +LDij + Sijk + YI + SEre + eijklmn w h e r e Yijklmn is a m e a s u r e o f t h e n th individual b r e d f r o m t h e kth sire in t h e ijth sire l i n e / d a m
TABLE 2. Regression coefficients and standard errors for effects of inbreeding on individual lines.
Variable
1
2
3
No. of animals Mean Fx
85 11.47 3.22 39.00 39.37 1.55 1.46 3.47 3.46 1.40 1.39 .02 .10 1.99 1.25 6.06 2.66
102 14.00 4.50 - 17.41 23.45 .51 .87 1.28 1.93 .35 .77 .02 .03 .41 1.18 -- 1.01 1.31
77 10.52 3.86 - 4.99 37.37 .42 1.19 .29 3.03 .32 1.13 .02 .10 1.81 .97 2.46 3.37
Milk (kg) Fat (kg) SNF (kg) Protein (kg) Age at calving Days in milk Days open
Sire line 4 112 11.40 3.78 25.22 46.39 1.45 1.51 .84 3.72 .25 1.46 .17 .11 .07 .83 -- 3.90 3.35
All lines
5
6
65 10.78 4.16 -72.61 38.82 - 2.73 1.33 - 5.46 3.45 - 1.71 1.40 .01 .09 - 1.37 1.62 1.58 2.65
85 16.21 5.11 -11.02 27.21 .33 1.00 .38 2.22 .09 .88 -
.04 1.24 1.39 .20 1.32
526 12.49 2.04 -3.19 11.98 .13 .43 - .20 1.01 .12 .40 - .05 .03 .28 .41 .74 .84
Journal of Dairy Science Vol. 62, No. 4, 1979
616
BECKETT ET AL.
TABLE 3. Estimates of average heterosis. Trait
Heterosis X 327.90 14.95 28.65 11.76 -.54 3.16 - 20.60
Milk, kg Fat, kg SNF, kg Protein, kg Age at calving, mo Days in milk Days open
--SD-117.8 3.82 9.63 3.52 .24 3.15 6.44
line subclass freshening in the lth year and mth season--/~ is the mean, and eijklmn is the random error associated with this ruth individual. Sires were random with all other effects fixed. The mean square for sire line/dam line subclasses was tested by the mean square for sires. All other effects were tested by the error term remaining after absorbing sires and sire line/dam line subclasses into all other effects in the model. Maternal effects could not be estimated as they were confounded completely with herd environmental effects. R ESU LTS
The effects of inbreeding were estimated only on linebred animals and were explained partially by a linear regression. Regression coefficients for each trait for the individual lines are in Table 2. While the standard errors of regression coefficients were large, the differences
TABLE 4. Test of average heterosis. Trait
F
F(a)
Milk yield Fat yield Protein yield SNF yield Age at calving Days in milk Days open
9.60*** 15.43"** 10.94"** 10.26"** 5.60** .76 7.66**
2.15 5.23** 4.40* * 2.68 .025 .46 .88
a
•
Linear regressmn on degree of inbreeding included in the model. **P<.05. ***P<.O01.
Journal of Dairy Science Vol. 62, No. 4, 1979
between estimates for several of the lines were different from 0 at .05 probability for yields of milk, fat, SNF, days open, and days in milk. In four of the lines, inbreeding had a depressing effect on milk production while in the other two lines the effects o f inbreeding were positive. There was no evidence for a marked change in milk composition associated with changes in production. The effects of inbreeding varied little among sires within lines, and mean squares for sires were generally n o t significant. Estimates of average heterosis measured as the difference in performance between linebreds and linecrosses of the six lines are in Table 3. The mean square for average heterosis was significant at .01 probability for all four yield traits and at .05 for age at calving and days open (Table 4). When the analysis was repeated with linear regression on inbreeding in the model, the mean squares for yields of fat and protein, though considerably reduced, were still significant at .05 probability. Using the model excluding the adjustment for inbreeding revealed that the linebreds were open 21 days longer than the linecrosses. Adjusting for inbreeding caused this difference to be reduced to 12 days, which, while not significant, did indicate the possible presence o f some small heterotic effects for reproductive performance. Mean squares for average heterosis for days in milk were not significant. The average yield o f the linecrosses exceeded that of the linebreds by 328, 15, 29, and 12 kg of milk, fat, SNF, and protein. Linecrosses also calved .5 mo younger, were open for 21 days less, and milked for 3 days longer in first lactation. Mean squares for line heterosis were significant at .05 for yields of milk and fat and at the .10 for yields of SNF and protein. No evidence was found for line heterosis for the three other traits. In all of the lines except line 1 linecrosses exceeded the linebreds in production of milk, SNF, and protein (Table 5). In line 4 yields of fat by linebreds and linecrosses were almost equal. Reproductive performance of the linecrosses was superior to that o f the linebreds in all six lines. Differences between linecrosses and linebreds in days open during lactation ranged from 6 to 51 days. Patterns o f differences between linecrosses and linebreds were not uniform for age at first calving or days in milk during lactation.
(3 O TABLE 5. Average performance and SD of linebreds (Lbd) and linecrosses (LX). Z Line 1 Lbd No. of Animals Milk, kg
o
85 7285 27 Fat, kg 251 8.9 SNF, kg 630 22.1 Protein, kg 248 8.3 Age at calving 28.42 .55 Days in milk 285.0 7.7 Days open 140.7 15.9
LX
Line 2 Lbd
LX
Line 3 Lbd
LX
Line 4 Lbd
LX
Line 5 Lbd
LX
Line 6 Lbd
LX
All Lines Lbd
~3 >
LX
.q r~ 60 6794 19 241 6.2 592 15.4 236 5.8 26.68 .38 295.8 5.4 134.6 11.0
102 6218 22 223 7.3 547 18.2 223 6.7 27.06 .45 279.6 6.1 153.6 12.6
53 6507 21 237 7.1 569 17.6 229 6.5 26.70 .43 286.1 6.0 132.8 12.2
77 6727 29 233 9.5 579 23.6 226 8.8 26.41 .58 291.6 8.2 164.5 16.8
40 7422 24 264 8.0 638 19.7 245 7.4 26.84 .49 290.0 6.9 128.2 14.0
112 6877 30 253 9.8 590 24.4 234 9.1 26.88 .60 295.0 8.4 179.6 17.2
70 7053 19 251 6.4 607 15.8 244 5.9 27.02 .39 292.5 5.5 128.7 11.2
65 5933 27 212 9.1 519 22.6 207 8.4 27.94 .56 290.1 7.8 118.1 16.0
20 6576 34 236 11.5 579 28.4 230 10.6 26.89 .70 279.5 9.8 112.5 20.1
85 5472 21 185 7.1 474 17.4 184 6.6 27.19 .43 276.8 6.2 152.3 12.7
48 6126 24 217 8.0 525 19.7 2O8 7.4 26.50 .49 293.2 7.0 148.6 14.4
526 6419 10 226 3.3 556 8.4 202.2 3.0 27.31 .20 286.4 2.5 151.5 5.1
291 6746 13 241 4.4 585 10.9 232 4.1 26.77 .27 289.5 3.8 130.9 7.7
© © c
Z > Z = © E; c~
< o
Z
Ox t~
Z
O
Ox -q
BECKETT ET AL.
618
TABLE 6. General combining ability and SD of six lines of Holsteins.
No. of animals Milk yield (kg) Fat yield (kg) SNF yield (kg) Protein yield (kg) Age of calving Days in milk Days open
Line 1
Line 2
Line 3
145 7039 175 246 5.6 611 14.3 242 5.2 27.55 .34 290.4 4.5 137.7 9.2
155 6363 194 230 6.1 558 15.7 226 5.6 26.88 .37 282.9 4,6 143.2 9.5
117 7075 204 248 6.5 608 15.7 235 6.0 26.62 .40 290.8 5.1 146.3 10.5
The general c o m b i n i n g ability of a line is a measure o f its additive genetic merit. Estimates in Table 6 based on b o t h linebred and linecross progeny indicated significant differences between lines for m a n y o f the traits. This d e m o n strated the wide genetic variability on which selection can be e x e r t e d within t h e Holstein breed. Estimates o f specific c o m b i n i n g ability c o m p a r e d the observed p e r f o r m a n c e o f specific reciprocal linecrosses with their e x p e c t e d p e r f o r m a n c e based on the G C A ' s of the lines f r o m which t h e y were derived. No evidence was f o u n d for specific c o m b i n i n g effects for pro-
TABLE 7. Specific combining effects for age at calving and days open. Line of dam
Line of sire 1
2
3
4
Age at calving 1
2 3
4
-
+
-
29
.29
+
-
.65
-
.36
.36
+
.65
.65
-
.36
+ -
-
.36 ,65 ,29
.29
Days open 1 2 3 4
-- 1.22 -- 1.22 +17.36 --16.14
-16.14 +17.36
+17.36 --16.14 -- 1.22
Journal of Dairy Science Vol. 62, No. 4, 1979
-16,14 +17,36 -- 1,22
Line 4
Line 5
182
85 6254 233 224 7.4
6965
186 252 5.9 598 15.1 239 5.41 26.95
.36 293.8 4.6 154.1 9.5
Line 6 133 5799
206 201 6.7
549
500
18.9 219 6.8 27.41 .45 284.8 5.8 115.3 11.9
16.9 196 6.t 26.84 .41 285.0 5.4 150.4 11.1
duction traits for the f o u r lines. However, there was definite evidence to suggest nicking for reproductive p e r f o r m a n c e for f o u r o f the linecross groups. Estimates of SCA for age at calving and days open during lactation are in Table 7. Effects of SCA for days open were significant for crosses b e t w e e n line 1 and line 3, line 1 and line 4, line 2 and line 3, and line 2 and line 4. The pattern of ages at first calving s u p p o r t e d the observations on o t h e r traits o f reproductive p e r f o r m a n c e during first lactation. Reciprocal differences for specific linecrosses were observed only for r e p r o d u c t i v e performance involving two of the line combinations. Females from line I m a t e d to line 3 sires were open for 368 days longer t h a n their reciprocal crosses. This difference was significant at .10. Females from line 1 m a t e d to line 4 sires conceived 47 days earlier (P<.05) than their reciprocal crosses. In all lines inbreeding n o t i c e a b l y decreased the vigor and vitality of s t o c k and increased calf m o r t a l i t y rates. The incidence of genetic abnormalities also was increased. DISCUSSION
The large differences in the effects of inbreeding on p r o d u c t i o n traits in d i f f e r e n t lines mean that the effects o f an inbreeding program are difficult to anticipate. For the m o s t part, such a system o f mating is likely to lead to a decline in p r o d u c t i o n , but this o u t c o m e is n o t inevitable with the inbreeding in this
COMBINING ABILITIES FOR PRODUCTION AND REPRODUCTION experiment. In all of the lines the inbreds had a poorer reproductive performance than the /inecrosses, although in some cases the difference was not significant. This experiment provided evidence to support the claim that linebreeding and other mild forms of inbreeding sometimes can result in genetic improvement. For most of the traits, heterotic effects greater than the depressing effects of inbreeding did not exist. There was some evidence for overdominance for fat percentage where the linecrosses not only outyielded the linebreds in milk but also produced milk higher by .05% in fat percentage. Increased yields of milk were not accompanied by the expected inverse response for protein and SNF percentages. The greatest contribution from heterosis effects appeared to be for reproductive performance and milking persistency. Often linecrosses were open for 21 days less than their linebred contemporaries yet milked for 3 days longer. When lactation length is considered in the light of the inhibitory effect of pregnancy, heterosis for milking persistency appears substantial. The observation that inbreeding did not lead to a decline in milk yield or reproductive performance in all lines and that in certain lines the performance of the linebreds was equivalent to that of the linecrosses favors the hypothesis that inbreeding depression is due to the accumulation of undesirable recessives rather than to the loss of merit due to heterozygosis p e r se. It is reasonable to consider that undesirable recessives may affect physiological as well as anatomical structures and lead to reduced efficiency of hormone and enzyme systems. CONCLUSIONS
The production traits appear to be largely under the control of additive gene effects, and the performance of each line when inbred was mainly a reflection of its additive genetic potential. Dominance gene effects appear to have some importance in determining milk compositional quality, reproductive performance, and lactation length. The probability of specific lines nicking for production traits, while not completely excluded, was low. Some evidence was available to support the view that specific gene combinations and the way in which they are assembled can have an important influence on reproductive performance. While inbreeding may on some occasions result in
619
genetic improvement, it is not a recommended mating procedure in view of decreased reproductive performance and vitality and an increased incidence of genetic abnormalities. Conventional methods of selection on additive genetic theory provide the most reliable basis for dairy cattle improvement in the near future. REFERENCES 1 Allaire, F. R., and C. R. Henderson. 1965. Inbreeding within an artificially bred dairy cattle population. J. Dairy Sei. 48:1366. 2 Bruin, E. W., T. M. Ludwick, D. O. Richardson, E. R. Rader, H. C. Hines, A. K. Fowler, and D. Plowman. 1963. Some effects of low levels of inbreeding on production in Holstein Cattle. J. Dairy Sci. 46:619. 3 Brum, E. W., T. M. Ludwick, E. R. Rader, D. O. Richardson, D. R. Davis, W. L. Crist, and D. L. Long. 1970. Combining abilities for size of linecross and linebred Holstein heifers. J. Dairy Sci. 53:1779. 4 Castle, W. E. 1919. Inheritance of quantity and quality of milk production in dairy cattle. Nat. Acad. Sci. Proc. 5(10):428. 5 Davis, H. P., W. Reed, M. Plum, and A. Wintherthur. 1953. A study in breeding dairy cattle. Nebraska Agr. Exp. Sta., Misc. Publ. 2. 6 Dayton, A. D. 1967. The effects of inbreeding on heritable traits in a herd of Jersey cattle. Ph.D. Thesis, Michigan State University. 7 Fohrman, M. H., R. E. McDowell, C. A. Matthews, and R. A. Hilder. 1954, A cross-breeding experiment with dairy cattle. USDA Tech. Bull. 1074. B Gaalas, R. F., W. R. Harvey, and R. D. Plowman. 1962. Effect of inbreeding on production in different lactations. J. Dairy Sci. 45:671 (Abstr.) 9 Gardner, C. O., and S. A. Eberhart. 1966. Analysis and interpretation of the variety cross diallel and related populations. Biometrics 22:439. 10 Hansson, A., T. During, and J. Zolkowski. 1961. Effect of specific combining ability (nicking) and inbreeding on yield of milk in dairy cows. K Lantbr. Hogskol. Ann. 27:287, 11 Harvey, W. R. 1960. Least-squares analysis of data with unequal subclass numbers. ARS 20-8 USDA. 12 Harvey, W. R, 1972. General outline of computing procedures for six types of mixed model. Mimeo. 13 Hines, H. C., E. W. Bruin, and T. M. Ludwick. 1966. Changes in degree of homozygousity of bovine blood and milk polymorphisms with inbreeding. J. Dairy Sci. 49:735 (Abstr.) 14 Laben, R. C., P. T. Cupps, S. W. Mead, and M. V. Regan. 1955. Some effects of inbreeding and evidence of heterosis through outcrossing in a Holstein-Friesian herd. J. Dairy Sci. 38:525. 15 Laben, R. C,, and H. A. Herman. 1950. Genetic factors affecting milk production in a selected Holstein-Friesian herd. Missouri Agr. Exp. Sta. Res. Bull. 459. 16 Madsen, O., and K. Vinther. 1975. Performance of purebred and crossbred dairy cattle in Thailand. Anim. Prod. 21:209.
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17 Madsen, O. 1976. Red Danish cattle in the tropics. World Anim. Rev. 19:8. 18 McDowell, R. E., and 8. T. McDaniel. 1968. Interbreed matings in dairy cattle. I. Yield traits, feed efficiency, type, and rate of milking. J. Dairy Sci. 51:767. 19 Mi, M. P., A. B. Chapman, and W. J. Tyler. 1965. Effects of mating system on production traits in dairy cattle. J. Dairy Sci. 48:77. 20 Pearson, R. E., N. W. Hooven, Jr., R. D. Plowman, R. H. Miller, J. W. Smith, and M. E. Creegan. 1973. Comparison of three mating systems. III. First, second and third lactation yield and milk compositions. J. Dairy Sci. 56:660 (Abstr.)
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21 Robertson, A. 1954. Inbreeding end performance in British Friesian cattle. Proc. Brit. Soc. Anita. Prod. 1954:87. 22 Rollins, W. C., R. C. Laben, and S. W. Mead. 1956. Gestation length in an inbred Jersey herd. J. Dairy Sci. 39:1578. 23 Touchberry, R. W. 1970. A comparison of the general merits of purebred and crossbred dairy cattle resulting from 20 years (four generations) of crossbreeding. Proc. 19th Ann. Nat. Breeders' Roundteble. 1970. 24 Van Krosigk, C. M., and J. L. Lush. 1958. Effect of inbreeding on production in Holsteins. J. Dairy Sci. 41:105.
ABSTRACT
Many studies have reported effects of systems of mating on quantitative traits in dairy cattle. Generally inbreeding of a cattle population has depressed all aspects of performance (1, 2, 5, 6, 8, 10, 14, 15, 19, 21, 22, 24). Sizes of the effects have varied, and in several studies (5, 19) there was evidence for a difference in response between individual lines. Over the years, many animal breeders working with specific lines of cattle have claimed that inbreeding has been a useful tool for herd improvement. Others have placed considerable faith in the belief that certain lines have "nicked" well together while other lines have not. Crosses between breeds of cattle have revealed heterosis for milk production (4, 7, 18, 20, 23), but no single cross has been superior to the purebred Holstein. Performances of crosses between the Red Sindhi and Red Dane breeds in both Thailand (16) and India (17) suggest specific combining ability for yields of milk and fat. This inbreeding and linecrossing study involved the inbreeding and reciprocal crossing of several lines of Holstein cattle with no deliberate selection of females. Inbreds and linecrosses were compared under comparable environmental conditions. Analyses of earlier data on size and body weight have been reported by Brum et al. (3). This paper reports effects of mating system on productive and reproductive traits.
Six inbred lines of Holstein cattle were developed and reciprocally crossed to assess the importance of heterotic effects for yield and reproductive traits. Overall both yield and reproductive performance declined with inbreeding, but effects varied with different lines. In two of the lines milk yield increased during inbreeding. Regression coefficients for each percent of inbreeding ranged from +39 to - 7 3 kg of milk. Production for estimates of general combining abilities for the different lines ranged from 5799 to 7075 kg of milk indicating the genetic variability available for selection. Some evidence was found for specific combining ability for reproductive performance but none for yield traits. Reciprocal differences were observed only for reproductive performance involving two of the line combinations. Heterosis was present for milk fat percentage, persistency of lactation, and reproductive performance. Effects of dominant genes appeared to be of minor importance in determining yield traits, and the possibility of nicking between lines for production traits, while not excluded, was of low likelihood. While mild inbreeding sometimes may produce genetic improvement, a breeding program based on additive genetic theory offers the best opportunities for raising productive performance.
MATERIALS AND METHODS
Received July 31, 1978. 1A Contribution to the NC-2 Dairy Cattle Breeding Project - Improvement in Dairy Cattle Breeding with Emphasis on Selection. 2Journal Article No. 109-78 Ohio Agricultural Research and Development Center, Wooster 44691. 1979 J Dairy Sci 62:613-620
The experiment began in 1948 as a cooperative study between The Ohio State University, The Ohio Department of Mental Hygiene and Mental Retardation, and the United States Department of Agriculture. Six inbred lines of Holstein cattle were developed on state institutional farms in Ohio.
613
614
BECKETT ET AL.
Three of the lines were in separate herds; one large herd was divided into two lines, and one line was developed between two smaller herds. Two or three closely related .bulls were introduced as the basic foundation sires for each line. Sires were selected primarily on production of their dams and paternal half-sisters. Pedigrees of sires in each line were completely distinctive through seven generations. A system of mating was devised to develop uniformly a gradual increase in inbreeding. The average inbreeding within each line varied from 0 to 5% prior to the initiation of the project, and the herds were closed when the breeding scheme began. The objective of the mating system was to develop gradually a coefficient of relationship of 25 to 30% between all female members of a line. Young sires to continue the line development were chosen from the highest producing cows in each line. All heifer calves were retained, and no animals were voluntarily culled until they had made at least one normal or extendable production record. The rate of line development varied, and in 1961 four of the lines were well enough developed to allow linecrossing to begin with frozen semen. At this time the average inbreeding of the four earliest developed lines was approximately 12% and the average relationship among the females was about 28%. Sixty percent of the qualified animals in each line were selected at random within age groups for linecrossing, the remainder continued to be inbred to provide contemporaries. Linecrossing began in the remaining two herds in 1962 and in 1965. All possible reciprocal crosses were represented in the initial four lines in linecrossing, but some were missing when all six lines were considered. Contemporary linecrosses and linebreds were reared and milked in the same herd at the same time. Each sire represented in the study had both inbred and linecross progeny. Blood typing was routine for all animals, and this was used to resolve parentage queries. An analysis early in line development by Hines et al. (13) indicated that the degree of homozygosity of seven blood and milk polymorphic systems appeared to behave generally as predicted by inbreeding theory with little evidence for deviation from the expected linear relationship. In the present study, data analyzed included first lactation records for yields of milk, butterfat, solids not fat (SNF), protein, days open, Journal of Dairy Science Vol. 62, No. 4, 1979
age at calving, and lactation length. All production records were on a mature equivalent (ME) 305-day - 2× basis with appropriate Dairy Herd Improvement adjustment factors. The distribution of animals by lines and linecrosses is in Table 1 along with the n u m b e r of sires. Analysis of Inbreeding
Estimates were separate for the linebred animals belonging to each line by the following fixed model (Model I). Yijkl = ~/+ Si + YRj + SE k + by/Fx + eijkl where /~ is the mean, Yijkl is a measure of the performance of the lth daughter of the ith sire calving in the kth season of the jth year, eijki represents the random error associated with this lth individual and by/Fx represents the linear regression on inbreeding of the trait being studied. In line 1 sires were confounded with years, and regression coefficients for this line were estimated with a similar model in which sires were ignored. An additional analysis of line 1 fitting Year-Sire subclasses gave almost identical estimates of the regression coefficients and their standard deviations.
Estimation of General Combining Ability and Heterotic Effects
The procedure followed closely that described as analysis II by Gardner and Eberhart (9), and the following mixed model (Model I1)
TABLE 1. Distribution of linebred and linecross animals by line of sire and line of dam. Line of sire
No. of sires
1
Line of dam 3 4
2
5
6
1
7a
85 a
17
2 3 4
7 5 7
18 19 17
102 14 17
11 9 77 13
11 4 6 112
21 8 0 12
14 1 I1
5 6
6 7
15 0
3 38
0 0
0 0
65 10
2 85
0
aonly 6 sires with 79 linebred progeny were included in the 4 line analysis-one sire did not have linecross progeny in lines 2 to 4.
COMBINING ABILITIES FOR PRODUCTION AND REPRODUCTION initially was e m p l o y e d : Y i j k l m n o = bt Li + Sij + Tk + HI + Y R m + SEn (LT)ik + (ST)ij k + ( H R Y ) I m + (HSE)In + * (YRSE)mn + eijklmn o w h e r e Y i j k l m n o is a m e a s u r e o f t h e p e r f o r m a n c e o f t h e 0th d a u g h t e r o f t h e j t h sire w i t h i n t h e ith sire line b o r n t o t h e lth d a m line ( o r h e r d ) a n d b e g i n n i n g p r o d u c t i o n in t h e m t h y e a r a n d n t h season, /l is t h e m e a n , a n d T k refers t o t h e t y p e o f b r e e d i n g involved, l i n e b r e d or linecross. I n t e r a c t i o n s o f various t e r m s in t h e m o d e l also were f i t t e d as i n d i c a t e d . T h e analysis was b y M i x e d Model Least Squares A n a l y s i s P r o g r a m as described b y Harvey u n d e r M o d e l T y p e 07 (12). Sires w i t h i n lines were r a n d o m ; all o t h e r effects were fixed. Interactions (ST)ijk, (HSE)In, a n d ( Y R S E ) m n were n o t significant. T h e y were d e l e t e d f r o m t h e m o d e l , a n d t h e analysis was r e p e a t e d as M o d e l T y p e 03, as d e s c r i b e d b y Harvey. T h e s a m e m o d e l a n d p r o c e d u r e l a t e r i n c l u d e d linear regression o n i n b r e e d i n g as a c o n t i n u o u s i n d e p e n d e n t variable. T h e m e a n s q u a r e a n d c o n s t a n t e s t i m a t e s for lines L i were e q u i v a l e n t to t h e general c o m b i n ing ability ( G C A ) o f t h e s e lines e s t i m a t e d o n t h e basis o f b o t h t h e l i n e b r e d a n d linecross
615
p r o g e n y o f t h e sires o f each line. T h e m e a n s q u a r e a n d c o n s t a n t e s t i m a t e s for T--the t y p e o f breeding--measured the importance of heterosis c o m p u t e d as an average e f f e c t over all lines ( A V Het). T h e line × t y p e o f b r e e d i n g i n t e r a c t i o n c o m p o n e n t s (LT)ik were an i n d i c a t i o n o f t h e individual d i f f e r e n c e s b e t w e e n lines in t h e i r h e t e r o t i c effects. T h e sire w i t h i n line × t y p e o f b r e e d i n g i n t e r a c t i o n (ST)ij k c o m p o n e n t s indic a t e d w h e t h e r sires w i t h i n lines t e n d e d t o r a n k d i f f e r e n t l y d e p e n d i n g o n w h e t h e r t h e y were e v a l u a t e d o n t h e basis o f t h e i r l i n e b r e d or linecross p r o g e n y a n d was an i n d i c a t i o n o f t h e i m p o r t a n c e o f i n d i v i d u a l d i f f e r e n c e s in h e t e r o t i c effects b e t w e e n sires w i t h i n t h e s a m e line. Estimation of Specific Combining Ability and Residual Recriprocal Effects
D a t a f r o m t h e f o u r line crosses w h i c h h a d all 16 subclasses filled were used t o o b t a i n estim a t e s o f specific c o m b i n i n g ability ( S C A ) a n d residual reciprocal effects ( R R ) . T h e s e effects were e s t i m a t e d a c c o r d i n g t o t h e m e t h o d o f Harvey (11) b y t h e f o l l o w i n g m i x e d m o d e l (Model III). Yijklmn = bt +LDij + Sijk + YI + SEre + eijklmn w h e r e Yijklmn is a m e a s u r e o f t h e n th individual b r e d f r o m t h e kth sire in t h e ijth sire l i n e / d a m
TABLE 2. Regression coefficients and standard errors for effects of inbreeding on individual lines.
Variable
1
2
3
No. of animals Mean Fx
85 11.47 3.22 39.00 39.37 1.55 1.46 3.47 3.46 1.40 1.39 .02 .10 1.99 1.25 6.06 2.66
102 14.00 4.50 - 17.41 23.45 .51 .87 1.28 1.93 .35 .77 .02 .03 .41 1.18 -- 1.01 1.31
77 10.52 3.86 - 4.99 37.37 .42 1.19 .29 3.03 .32 1.13 .02 .10 1.81 .97 2.46 3.37
Milk (kg) Fat (kg) SNF (kg) Protein (kg) Age at calving Days in milk Days open
Sire line 4 112 11.40 3.78 25.22 46.39 1.45 1.51 .84 3.72 .25 1.46 .17 .11 .07 .83 -- 3.90 3.35
All lines
5
6
65 10.78 4.16 -72.61 38.82 - 2.73 1.33 - 5.46 3.45 - 1.71 1.40 .01 .09 - 1.37 1.62 1.58 2.65
85 16.21 5.11 -11.02 27.21 .33 1.00 .38 2.22 .09 .88 -
.04 1.24 1.39 .20 1.32
526 12.49 2.04 -3.19 11.98 .13 .43 - .20 1.01 .12 .40 - .05 .03 .28 .41 .74 .84
Journal of Dairy Science Vol. 62, No. 4, 1979
616
BECKETT ET AL.
TABLE 3. Estimates of average heterosis. Trait
Heterosis X 327.90 14.95 28.65 11.76 -.54 3.16 - 20.60
Milk, kg Fat, kg SNF, kg Protein, kg Age at calving, mo Days in milk Days open
--SD-117.8 3.82 9.63 3.52 .24 3.15 6.44
line subclass freshening in the lth year and mth season--/~ is the mean, and eijklmn is the random error associated with this ruth individual. Sires were random with all other effects fixed. The mean square for sire line/dam line subclasses was tested by the mean square for sires. All other effects were tested by the error term remaining after absorbing sires and sire line/dam line subclasses into all other effects in the model. Maternal effects could not be estimated as they were confounded completely with herd environmental effects. R ESU LTS
The effects of inbreeding were estimated only on linebred animals and were explained partially by a linear regression. Regression coefficients for each trait for the individual lines are in Table 2. While the standard errors of regression coefficients were large, the differences
TABLE 4. Test of average heterosis. Trait
F
F(a)
Milk yield Fat yield Protein yield SNF yield Age at calving Days in milk Days open
9.60*** 15.43"** 10.94"** 10.26"** 5.60** .76 7.66**
2.15 5.23** 4.40* * 2.68 .025 .46 .88
a
•
Linear regressmn on degree of inbreeding included in the model. **P<.05. ***P<.O01.
Journal of Dairy Science Vol. 62, No. 4, 1979
between estimates for several of the lines were different from 0 at .05 probability for yields of milk, fat, SNF, days open, and days in milk. In four of the lines, inbreeding had a depressing effect on milk production while in the other two lines the effects o f inbreeding were positive. There was no evidence for a marked change in milk composition associated with changes in production. The effects of inbreeding varied little among sires within lines, and mean squares for sires were generally n o t significant. Estimates of average heterosis measured as the difference in performance between linebreds and linecrosses of the six lines are in Table 3. The mean square for average heterosis was significant at .01 probability for all four yield traits and at .05 for age at calving and days open (Table 4). When the analysis was repeated with linear regression on inbreeding in the model, the mean squares for yields of fat and protein, though considerably reduced, were still significant at .05 probability. Using the model excluding the adjustment for inbreeding revealed that the linebreds were open 21 days longer than the linecrosses. Adjusting for inbreeding caused this difference to be reduced to 12 days, which, while not significant, did indicate the possible presence o f some small heterotic effects for reproductive performance. Mean squares for average heterosis for days in milk were not significant. The average yield o f the linecrosses exceeded that of the linebreds by 328, 15, 29, and 12 kg of milk, fat, SNF, and protein. Linecrosses also calved .5 mo younger, were open for 21 days less, and milked for 3 days longer in first lactation. Mean squares for line heterosis were significant at .05 for yields of milk and fat and at the .10 for yields of SNF and protein. No evidence was found for line heterosis for the three other traits. In all of the lines except line 1 linecrosses exceeded the linebreds in production of milk, SNF, and protein (Table 5). In line 4 yields of fat by linebreds and linecrosses were almost equal. Reproductive performance of the linecrosses was superior to that o f the linebreds in all six lines. Differences between linecrosses and linebreds in days open during lactation ranged from 6 to 51 days. Patterns o f differences between linecrosses and linebreds were not uniform for age at first calving or days in milk during lactation.
(3 O TABLE 5. Average performance and SD of linebreds (Lbd) and linecrosses (LX). Z Line 1 Lbd No. of Animals Milk, kg
o
85 7285 27 Fat, kg 251 8.9 SNF, kg 630 22.1 Protein, kg 248 8.3 Age at calving 28.42 .55 Days in milk 285.0 7.7 Days open 140.7 15.9
LX
Line 2 Lbd
LX
Line 3 Lbd
LX
Line 4 Lbd
LX
Line 5 Lbd
LX
Line 6 Lbd
LX
All Lines Lbd
~3 >
LX
.q r~ 60 6794 19 241 6.2 592 15.4 236 5.8 26.68 .38 295.8 5.4 134.6 11.0
102 6218 22 223 7.3 547 18.2 223 6.7 27.06 .45 279.6 6.1 153.6 12.6
53 6507 21 237 7.1 569 17.6 229 6.5 26.70 .43 286.1 6.0 132.8 12.2
77 6727 29 233 9.5 579 23.6 226 8.8 26.41 .58 291.6 8.2 164.5 16.8
40 7422 24 264 8.0 638 19.7 245 7.4 26.84 .49 290.0 6.9 128.2 14.0
112 6877 30 253 9.8 590 24.4 234 9.1 26.88 .60 295.0 8.4 179.6 17.2
70 7053 19 251 6.4 607 15.8 244 5.9 27.02 .39 292.5 5.5 128.7 11.2
65 5933 27 212 9.1 519 22.6 207 8.4 27.94 .56 290.1 7.8 118.1 16.0
20 6576 34 236 11.5 579 28.4 230 10.6 26.89 .70 279.5 9.8 112.5 20.1
85 5472 21 185 7.1 474 17.4 184 6.6 27.19 .43 276.8 6.2 152.3 12.7
48 6126 24 217 8.0 525 19.7 2O8 7.4 26.50 .49 293.2 7.0 148.6 14.4
526 6419 10 226 3.3 556 8.4 202.2 3.0 27.31 .20 286.4 2.5 151.5 5.1
291 6746 13 241 4.4 585 10.9 232 4.1 26.77 .27 289.5 3.8 130.9 7.7
© © c
Z > Z = © E; c~
< o
Z
Ox t~
Z
O
Ox -q
BECKETT ET AL.
618
TABLE 6. General combining ability and SD of six lines of Holsteins.
No. of animals Milk yield (kg) Fat yield (kg) SNF yield (kg) Protein yield (kg) Age of calving Days in milk Days open
Line 1
Line 2
Line 3
145 7039 175 246 5.6 611 14.3 242 5.2 27.55 .34 290.4 4.5 137.7 9.2
155 6363 194 230 6.1 558 15.7 226 5.6 26.88 .37 282.9 4,6 143.2 9.5
117 7075 204 248 6.5 608 15.7 235 6.0 26.62 .40 290.8 5.1 146.3 10.5
The general c o m b i n i n g ability of a line is a measure o f its additive genetic merit. Estimates in Table 6 based on b o t h linebred and linecross progeny indicated significant differences between lines for m a n y o f the traits. This d e m o n strated the wide genetic variability on which selection can be e x e r t e d within t h e Holstein breed. Estimates o f specific c o m b i n i n g ability c o m p a r e d the observed p e r f o r m a n c e o f specific reciprocal linecrosses with their e x p e c t e d p e r f o r m a n c e based on the G C A ' s of the lines f r o m which t h e y were derived. No evidence was f o u n d for specific c o m b i n i n g effects for pro-
TABLE 7. Specific combining effects for age at calving and days open. Line of dam
Line of sire 1
2
3
4
Age at calving 1
2 3
4
-
+
-
29
.29
+
-
.65
-
.36
.36
+
.65
.65
-
.36
+ -
-
.36 ,65 ,29
.29
Days open 1 2 3 4
-- 1.22 -- 1.22 +17.36 --16.14
-16.14 +17.36
+17.36 --16.14 -- 1.22
Journal of Dairy Science Vol. 62, No. 4, 1979
-16,14 +17,36 -- 1,22
Line 4
Line 5
182
85 6254 233 224 7.4
6965
186 252 5.9 598 15.1 239 5.41 26.95
.36 293.8 4.6 154.1 9.5
Line 6 133 5799
206 201 6.7
549
500
18.9 219 6.8 27.41 .45 284.8 5.8 115.3 11.9
16.9 196 6.t 26.84 .41 285.0 5.4 150.4 11.1
duction traits for the f o u r lines. However, there was definite evidence to suggest nicking for reproductive p e r f o r m a n c e for f o u r o f the linecross groups. Estimates of SCA for age at calving and days open during lactation are in Table 7. Effects of SCA for days open were significant for crosses b e t w e e n line 1 and line 3, line 1 and line 4, line 2 and line 3, and line 2 and line 4. The pattern of ages at first calving s u p p o r t e d the observations on o t h e r traits o f reproductive p e r f o r m a n c e during first lactation. Reciprocal differences for specific linecrosses were observed only for r e p r o d u c t i v e performance involving two of the line combinations. Females from line I m a t e d to line 3 sires were open for 368 days longer t h a n their reciprocal crosses. This difference was significant at .10. Females from line 1 m a t e d to line 4 sires conceived 47 days earlier (P<.05) than their reciprocal crosses. In all lines inbreeding n o t i c e a b l y decreased the vigor and vitality of s t o c k and increased calf m o r t a l i t y rates. The incidence of genetic abnormalities also was increased. DISCUSSION
The large differences in the effects of inbreeding on p r o d u c t i o n traits in d i f f e r e n t lines mean that the effects o f an inbreeding program are difficult to anticipate. For the m o s t part, such a system o f mating is likely to lead to a decline in p r o d u c t i o n , but this o u t c o m e is n o t inevitable with the inbreeding in this
COMBINING ABILITIES FOR PRODUCTION AND REPRODUCTION experiment. In all of the lines the inbreds had a poorer reproductive performance than the /inecrosses, although in some cases the difference was not significant. This experiment provided evidence to support the claim that linebreeding and other mild forms of inbreeding sometimes can result in genetic improvement. For most of the traits, heterotic effects greater than the depressing effects of inbreeding did not exist. There was some evidence for overdominance for fat percentage where the linecrosses not only outyielded the linebreds in milk but also produced milk higher by .05% in fat percentage. Increased yields of milk were not accompanied by the expected inverse response for protein and SNF percentages. The greatest contribution from heterosis effects appeared to be for reproductive performance and milking persistency. Often linecrosses were open for 21 days less than their linebred contemporaries yet milked for 3 days longer. When lactation length is considered in the light of the inhibitory effect of pregnancy, heterosis for milking persistency appears substantial. The observation that inbreeding did not lead to a decline in milk yield or reproductive performance in all lines and that in certain lines the performance of the linebreds was equivalent to that of the linecrosses favors the hypothesis that inbreeding depression is due to the accumulation of undesirable recessives rather than to the loss of merit due to heterozygosis p e r se. It is reasonable to consider that undesirable recessives may affect physiological as well as anatomical structures and lead to reduced efficiency of hormone and enzyme systems. CONCLUSIONS
The production traits appear to be largely under the control of additive gene effects, and the performance of each line when inbred was mainly a reflection of its additive genetic potential. Dominance gene effects appear to have some importance in determining milk compositional quality, reproductive performance, and lactation length. The probability of specific lines nicking for production traits, while not completely excluded, was low. Some evidence was available to support the view that specific gene combinations and the way in which they are assembled can have an important influence on reproductive performance. While inbreeding may on some occasions result in
619
genetic improvement, it is not a recommended mating procedure in view of decreased reproductive performance and vitality and an increased incidence of genetic abnormalities. Conventional methods of selection on additive genetic theory provide the most reliable basis for dairy cattle improvement in the near future. REFERENCES 1 Allaire, F. R., and C. R. Henderson. 1965. Inbreeding within an artificially bred dairy cattle population. J. Dairy Sei. 48:1366. 2 Bruin, E. W., T. M. Ludwick, D. O. Richardson, E. R. Rader, H. C. Hines, A. K. Fowler, and D. Plowman. 1963. Some effects of low levels of inbreeding on production in Holstein Cattle. J. Dairy Sci. 46:619. 3 Brum, E. W., T. M. Ludwick, E. R. Rader, D. O. Richardson, D. R. Davis, W. L. Crist, and D. L. Long. 1970. Combining abilities for size of linecross and linebred Holstein heifers. J. Dairy Sci. 53:1779. 4 Castle, W. E. 1919. Inheritance of quantity and quality of milk production in dairy cattle. Nat. Acad. Sci. Proc. 5(10):428. 5 Davis, H. P., W. Reed, M. Plum, and A. Wintherthur. 1953. A study in breeding dairy cattle. Nebraska Agr. Exp. Sta., Misc. Publ. 2. 6 Dayton, A. D. 1967. The effects of inbreeding on heritable traits in a herd of Jersey cattle. Ph.D. Thesis, Michigan State University. 7 Fohrman, M. H., R. E. McDowell, C. A. Matthews, and R. A. Hilder. 1954, A cross-breeding experiment with dairy cattle. USDA Tech. Bull. 1074. B Gaalas, R. F., W. R. Harvey, and R. D. Plowman. 1962. Effect of inbreeding on production in different lactations. J. Dairy Sci. 45:671 (Abstr.) 9 Gardner, C. O., and S. A. Eberhart. 1966. Analysis and interpretation of the variety cross diallel and related populations. Biometrics 22:439. 10 Hansson, A., T. During, and J. Zolkowski. 1961. Effect of specific combining ability (nicking) and inbreeding on yield of milk in dairy cows. K Lantbr. Hogskol. Ann. 27:287, 11 Harvey, W. R. 1960. Least-squares analysis of data with unequal subclass numbers. ARS 20-8 USDA. 12 Harvey, W. R, 1972. General outline of computing procedures for six types of mixed model. Mimeo. 13 Hines, H. C., E. W. Bruin, and T. M. Ludwick. 1966. Changes in degree of homozygousity of bovine blood and milk polymorphisms with inbreeding. J. Dairy Sci. 49:735 (Abstr.) 14 Laben, R. C., P. T. Cupps, S. W. Mead, and M. V. Regan. 1955. Some effects of inbreeding and evidence of heterosis through outcrossing in a Holstein-Friesian herd. J. Dairy Sci. 38:525. 15 Laben, R. C,, and H. A. Herman. 1950. Genetic factors affecting milk production in a selected Holstein-Friesian herd. Missouri Agr. Exp. Sta. Res. Bull. 459. 16 Madsen, O., and K. Vinther. 1975. Performance of purebred and crossbred dairy cattle in Thailand. Anim. Prod. 21:209.
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17 Madsen, O. 1976. Red Danish cattle in the tropics. World Anim. Rev. 19:8. 18 McDowell, R. E., and 8. T. McDaniel. 1968. Interbreed matings in dairy cattle. I. Yield traits, feed efficiency, type, and rate of milking. J. Dairy Sci. 51:767. 19 Mi, M. P., A. B. Chapman, and W. J. Tyler. 1965. Effects of mating system on production traits in dairy cattle. J. Dairy Sci. 48:77. 20 Pearson, R. E., N. W. Hooven, Jr., R. D. Plowman, R. H. Miller, J. W. Smith, and M. E. Creegan. 1973. Comparison of three mating systems. III. First, second and third lactation yield and milk compositions. J. Dairy Sci. 56:660 (Abstr.)
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21 Robertson, A. 1954. Inbreeding end performance in British Friesian cattle. Proc. Brit. Soc. Anita. Prod. 1954:87. 22 Rollins, W. C., R. C. Laben, and S. W. Mead. 1956. Gestation length in an inbred Jersey herd. J. Dairy Sci. 39:1578. 23 Touchberry, R. W. 1970. A comparison of the general merits of purebred and crossbred dairy cattle resulting from 20 years (four generations) of crossbreeding. Proc. 19th Ann. Nat. Breeders' Roundteble. 1970. 24 Van Krosigk, C. M., and J. L. Lush. 1958. Effect of inbreeding on production in Holsteins. J. Dairy Sci. 41:105.