Maternal effects due to cytoplasmic inheritance in dairy cattle. Influence on milk production and reproduction traits

Livestock Production Science, 15 ( 1 9 8 6 ) 1 1 - - 2 6

11

Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands

MATERNAL EFFECTS DUE TO CYTOPLASMIC INHERITANCE IN D A I R Y CATTLE. INFLUENCE ON MILK PRODUCTION A N D REPRODUCTION TRAITS

H.A. HUIZINGA a, S. KORVER a, B.T. McDANIEL b and R.D. POLITIEK a

aDepartment of Animal Breeding, Agricultural University, P.O. Box 338, 6700 AH Wageningen (The Netherlands) b Department of Animal Science, North Carolina State University, Raleigh, NC 27695-7621 (U.S.A.) (Accepted 24 December 1985)

ABSTRACT Huizinga, H.A., Korver, S., McDaniel, B.T. and Politick, R.D., 1986. Maternal effects due to cytoplasmic inheritance in dairy cattle. Influence on milk production and reproduction traits. Livest. Prod. Sci., 15: 11--26. The objectives of this study were to determine the importance of effects of cytoplasmic origin on milk production and reproduction traits. Cow families at the experimental farm originated from randomly collected calves from 240 herds in two breeding districts. Cytoplasmic origin was defined as the first animal in the traced, maternal lineage. Milk production of 290 cows in first lactation from 1976 to 1982 was used. Reproduction records of the same cows as nulliparous and primiparous could be analysed in cow families. Cytoplasmic origin was a significant ( P < 0 . 0 1 ) source of variation in kg fat plus protein, and milk returns (Dfl.) after adjustment for district of origin of the cytoplasmic source, site's breed, calving year and season, breeding values of sires and material grandsires, and age at calving. Cytoplasmic origin accounted for maximal 10% and 13%, respectively, of the phenotypic variation in the two traits. Cytoplasmic origin was not a significant source of variation in nulliparous and primiparous reproduction traits after adjustment for effects of sire's breed, calving year and season. Although not significant, the cytoplasmic components accounted for 10 to 4% of the phenotypic variation in number of inseminations per first conception and for -0.04% to 13% of the phenotypic variation in age at first calving for the first and second generation, respectively. Some of these cytoplasmic components accounted for more phenotypic variation in reproductive traits of nulliparous heifers than most additive genetic components found in the literature. The effects of cytoplasmic inheritance on production and reproduction traits might have an impact on breeding policies in dairy cattle.

INTRODUCTION

In the past, any cytoplasmic c o m p o n e n t of maternal effects on production traits in dairy cattle was ignored. However, recent findings in molecular

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12 genetics have proven that cytoplasmic and extranuclear organelles, including mitochondria, which contain DNA (mtDNA), are maternally inherited in mammals (Laipis et al., 1982). Differences in m t D N A between cytoplasmic or maternal lines might contribute to different performances in dairy traits between these lines. Cytoplasmic inheritance could be the basis of differences between cow families. Bell et al. {1985} reported maternal effects on production traits of dairy cattle, which were ascribed to cytoplasmic or other forms of maternal inheritance. In the present study, results of Bell et al. {1985) were tested in another population and more recent developments in research on maternal inherited c o m p o n e n t s were taken into account. Our specific objectives were to determine if cytoplasmic sources were a significant source of variation in milk production and reproduction traits and to determine the relative importance of any such contribution. Similar results in a different population should confirm the existence of effects of cytoplasmic inheritance in dairy cattle. Effects of cytoplasmic inheritance might have an impact on breeding policies. E m b r y o transfer might become economically feasible sooner, strategy in selection of y o u n g bulls for A.I. might be changed and there would possibly be some prospect for genetic manipulation. LITERATURE Bell et al. (1985) reviewed literature concerning cytoplasmic inheritance. Their review q u o t e d many studies, with various mammalian and plant species, that have shown the strict maternal inheritance of mitochondrial DNA (mtDNA). Relative homogeneity in m t D N A within maternal, derived lines and heterogeneity between these could give a genetic basis for differences in cytoplasmic effects between maternal lines. Maternal inheritance of m t D N A was confirmed in dairy cattle by Laipis and Hauswirth (1980) and Laipis et al. (1982). The rate of mutation in m t D N A appears to be much more rapid than the mutation rate in nuclear DNA (Laipis and Hauswirth, 1980). Individual variant m t D N A molecules resulting from mutational events can rapidly dominate the large intracellular m t D N A population (Olivo et al., 1983}. The question remains as to whether, despite these events which decrease relative h o m o g e n e i t y within maternal lines, a cytoplasmic effect on production traits can be detected. Other maternally inherited factors might also contribute to differences between maternal lines. In a review article, Gavora and Spencer (1983) quoted Harris et al. (1983) with observations on lymphoid leukosis, a congenitally transmitted viral disease of chickens. Individuals of lines infected with the virus had depressed egg production and depressed performances in other traits. Fischer Lindahl and Hausmann (1983) reported a maternally

13 transmitted cell surface-antigen in mice. However, recent research has indicated that the expression of maternally transmitted antigen in mice is controlled by mtDNA (Goodfellow, 1983). Since mitochondria play an important role in protein and energy metabolism in cells, and are involved in steroid hormone production and disease resistance {Bell et al., 1985), it has been assumed that cytoplasmic effects would be displayed in traits derived from these processes. Recent studies with reciprocal crosses in pigs (Dzapo et al., 1983; Dzapo and Wassmuth, 1983) gave a more fundamental basis for the mitochondrial involvement in production and reproduction traits. Three additional facts that might support the evidence of existence of maternal effects due to cytoplasmic inheritance on production traits in dairy cattle can be mentioned: 1. The generally lower heritability estimates from paternal half-sib correlation compared to those from daughter-dam regression (Rendel et al., 1957; Bradford and Van Vleck, 1964; Van Vleck and Bradford, 1965a, b, 1966; Van Vleck, 1966; Van Vleck and Hart, 1966b) and daughter- granddam iVan Vleck and Bradford, 1965b) regression analysis. 2. The significant differences in production traits between reciprocal crosses in crossbreeding studies with dairy cattle (Robertson, 1949; Bereskin and Touchberry, 1966; Donald et al., 1977; Robison et al., 1981). 3. The more than theoretically expected importance of cow's genetic evaluation on basis of her own performance in predicting daughter production (Powell et al., 1981) and the lower than expected importance of dam's estimated transmitting ability to predict son's progeny test (Powell et al., 1981; Rothschild et al., 1981; Murphy et al., 1982). In Bell's studies {Bell, 1983; Bell et al., 1985) of maternal inheritance on production traits in dairy cattle, pedigrees of 4461 cows were traced to determine the cytoplasmic origin of the cow. Cytoplasmic origin was a significant source of variation for production traits and days open. Adjusting yield traits for days open reduced the magnitude of the cytoplasmic effects, which suggested that reproductive performances may be influenced by a maternally inherited component. Heritability estimates were obtained from daughter--dam regression based on 3398 daughter--dam pairs. Heritability estimates were lowered by adjustment for cytoplasmic origin. Those derived from paternal half-sib correlations were unchanged after adjustment for cytoplasmic effects. A similar divergence in heritability estimates for days open from daughter--dam regression and paternal half-sib analysis was also reported by Seykora and McDaniel (1983). These results induced Bell (1983) to revise the definition of maternal effects. A maternal effect is any influence, other than the contribution resulting from nuclear genes, that the dam has on the phenotype of her progeny.

14 MATERIALS

Data were derived from 290 heifers in first lactation t h a t calved between 1976 and 1982 at an experimental farm of the Agricultural University of Wageningen. In two consecutive years {1968 and 1969) batches of 120 calves were purchased from different farms. Each calf came from a different herd, and therefore was assumed to have a different cytoplasmic source. Each batch of calves was composed of a random sample of two subpopulations of the Dutch Friesian (Friesland and North Holland). These districts had a different breeding policy for dairy and conformation traits. For a more detailed description of the composition of the foundation cows see Politiek (1974). After the purchase, a long-term breed comparison of the Black and White breed was started. Representative groups were formed, and their members and offspring were consistently bred by either the best Dutch Friesian (DF), Holstein Friesian (HF) or British Friesian (BF) proven bulls, selected on milk production (including components). Results showed genetic differences in production traits for breeds of sire and districts of origin. For more detailed information, see Politiek et al. (1982). In 1982 three generations of offspring were completed. By excluding the first generation, it became more feasible to distinguish cytoplasmic effects from the additive genetic influence. Table I shows the distribution of the records per trait over the different generations, subpopulations, and the districts of the cytoplasmic sources. TABLE I N u m b e r o f first l a c t a t i o n r e c o r d s b y g e n e r a t i o n a n d s u b p o p u l a t i o n s Generation

Subpopulations

Purebred DF a 75% HF, 25% D F 75% BF, 25% D F Total Purebred DF 8 7 . 5 % HF, 12.5% D F 8 7 . 5 % BF, 12.5% D F Total

Production

Reproduction

Production traits

NS1 b AGEFC

NS2 c

CALINT d

59 57 66

59 57 66

59 57 66

46 43 53

192

192

192

142

20 34 54

20 34 54

18 33 52

4 14 24

108

108

103

42

a D F = D u t c h Friesian, H F = H o l s t e i n Friesian, BF -- British Friesian. b N S 1 = n u m b e r o f i n s e m i n a t i o n s per c o n c e p t i o n for nullipara, A G E F C = age a t first calving. cNS2 = n u m b e r of i n s e m i n a t i o n s p e r c o n c e p t i o n for primipara. d C A L I N T = calving i n t e r v a l b e t w e e n first a n d s e c o n d calvings.

15 T A B L E II F r e q u e n c y d i s t r i b u t i o n o f c y t o p l a s m i c sources b y n u m b e r o f d e s c e n d a n t s for t h e respective traits Generation

Number of descendants 2

3

4

5

6

7

8

Total

2 3

P r o d u c t i o n traits, NS1, A G E F C 34 19 10 1 23 10 3 1

2 0

0 1

0 1

66 39

2 3

NS2 34 22

19 11

10 2

1 1

2 1

0 1

0 0

66 38

2 3

CALINT 32 12

12 1

9 1

0 1

1 1

0 0

0 0

54 16

NS1 = n u m b e r o f i n s e m i n a t i o n s per c o n c e p t i o n for nullipara. A G E F C = age at first calving. NS2 = n u m b e r o f i n s e m i n a t i o n s per c o n c e p t i o n for primapara. C A L I N T = calving interval b e t w e e n first a n d s e c o n d calving.

In the data the purchased calves (generation 0) were defined as the cytoplasmic sources. A cytoplasmic line was formed by all the female descendants of a certain cytoplasmic source. Cytoplasmic lines consisting of less than two members per generation were excluded. In the second and third generation 66 and 39 cytoplasmic lines were left, respectively. Table II shows the frequencies of cytoplasmic lines by number of descendants per generation. The number of members per cytoplasmic line for the second and the third generations averaged 2.76 and 2.77, respectively. Combining both generations resulted in 79 cytoplasmic lines with an average of 3.67 members. The production traits used were kg milk, fat %, protein %, kg fat and protein, and milk returns (Dfl.). All were standardized to a 305-day basis. Kilograms milk production with a lactation length of less than 305 days was extended to a 305
16 The considered reproduction traits were number of inseminations per conception as a nullipara (NS1) and primipara (NS2), age at first calving (AGEFC) and the interval between first and second calving (CALINT). Breeding of the nullipara started when the virgin heifers reached the age of 15 months. Breeding for primipara started at 60 days after calving. Cows that eventually failed to conceive were not excluded, but consequently had a high number of inseminations per conception. Breedings were not made in the period from September to January. Calving intervals (CALINT) which were affected by this, and therefore intervals longer than 530 days were excluded from the data. The number of CALINT records for the third generation was reduced, since some of the cows had not yet calved for the second time. The n u m b e r of records for reproduction traits over the different generations and subpopulations are also shown in Table I. METHODS Production

traits

Data of the second, third and combined generations were analyzed by least squares methods (Harvey, 1977) using the following model: Y z i j k l = u + SBDISi + YS/+ Ck: i + bBV:SBDI S + bag e + e i j k l

where Y z i i k l = z-th production trait of the n-th cow; u = overall mean; SBDISi = effect of the ith-sire's breed × district (i = 1,6) (fixed); YSj = effect of the j t h year × season of calving (generation 2: j = 1 , 1 6 ; generation 3: 1= 10,20; combined generations: j = 1,20) (fixed); C k : i = effect of the k-th cytoplasmic source (random); bBV:SBDIS = linear regression of the estimated breeding value of the cow on the basis of the breeding value of the cow's sire and maternal grandsire for the z-th production trait; bage = linear regression of the age at calving; e i j k l = random error. Calving seasons were divided into three sets per year: N o v e m b e r - J a n u a r y , February--March and April--May. The sires and maternal grandsires were randomly allocated over the cytoplasmic lines per generation within a SBDIS subclass. In the data of the combined generations a non-randomly additive genetic covariance existed. Therefore the sire and grandsire were taken into account. An additional advantage is t h a t smaller residual mean squares are given. Bell et al. (1985) observed no difference in adjusting between a model with a sire and maternal grandsire random c o m p o n e n t and a model with the estimated breeding values of the sires and maternal grandsires in the whole population, respectively. The number of daughters per sire and maternal grandsire were too small in this

17 material and therefore breeding values were used. (BBV:SBDIS = 1/2 X site's B V + 1/4X maternal grandsire's BV). Estimated breeding values were expressed as a deviation of the average breeding value of all cows of a SBDIS subclass. Breeding values for the sires were obtained from the Central Milk Recording Service (1983). For the estimated breeding values of milk returns (Dfl.), the weighing factors for the breeding values of kg milk, fat %, protein % were 0.316, 0.260, 0.500, respectively (Jansen et al., 1983). Each cytoplasmic source originating from a certain district was allocated to a certain breed. Hence, cytoplasmic sources were nested within sire's breed X district subclasses. For the data of the combined generations, a generation effect and a SBDIS X generation interaction effect were also included in the model. Reproduction

traits

Data of the second and third generations were analyzed separately by least squares methods (Harvey, 1977). The combined generations were not analyzed, because breeding values for the reproductive traits were not available. The following model was used: Y z i j k l = u + SBi + YSj + Ck:i + e i j k l

where Y z = z-th reproduction trait of the n-th cow; u = overall mean; SBi = effect of the i-th sire's breed 1i=1,3) (fixed); YS/ = effect of the j-th year X season (generation 2: j = l , 1 4 ; generation 3: j = 8,18; combined generation: j = 1,18) {fixed); Ck:i = effect of the k-th cytoplasmic source (random); e i j k l = random error. Reproduction measurements were expressed as logs to reduce the skewness of the distribution of these traits. Calving seasons for AGEFC and CALINT were divided into three sets per year: November--January, February--March and A p r i l - M a y . Year × season classes for NS1 and NS2 were based on the date of the insemination resulting in conception. These were also divided into three sets per year: F e b r u a r y April, May--June and July--August. In contrast to the analysis of the production traits, no district of origin of the cytoplasmic source was included in the model. Since the additive genetic variance is low for reproductive traits, any additive genetic influence of the breeding districts on cows of the second and third generation should be negligible for reproduction traits. Reproduction traits reflecting the results of an insemination are influenced by both male and female fertility. However, the large number of bulls used and the low number of cows per bull were justifications for omitting the male effect in the model.

18 T A B L E III F-values o f t h e sources of v a r i a t i o n a n d residual m e a n squares for p r o d u c t i o n a nd rep r o d u c t i o n t r a i t s o f t h e second, third, and c o m b i n e d g e n e r a t i o n s Source a

d.f.

kg m i l k

Fat %

Protein%

kg fat + protein

Milk r e t u r n s

Production traits Second g e n e r a t i o n SBDIS YS CYTOPL. S. Age Residual M.S.

5 15 60 1 94

16.35"* 1.62 1.17 1.20 433691.8

8.49** 1.75 1.00 0.04 514.9

5.06** 1.39 0.97 0.16 163.3

9.73** 1.74 1.59" 2.61 1751.4

7.32** 1.70 1.62" 2.47 34454.2

Third g e n e r a t i o n SBDIS YS CYTOPL. S. Age Resid ual M.S.

5 10 33 1 52

18.62"* 0.77 1.24 0.82 417157.4

5.48** 2.90** 1.17 0.86 597.3

4.91"* 1.31 1.79"* 1.17 147.0

11.68"* 1.37 1.10 0.02 1809.46

8.93** 1.80 1.10 0.35 34309.3

Second and third g e n e r a t i o n SBDIS 5 28.07** YS 19 1.82" GE N 1 0.79 SBDISXGEN 5 2.14" CYTOPL. S. 73 1.37" Age 1 2.90 R e s i d u a l M.S. 179 4 1 9 3 6 1 . 0

11.93"* 2.39** 4.99* 1.45 1.20 0.02 559.38

9.43** 1.92" 0.62 1.78 1.31 0.41 166.5

17.98"* 2.01"* 0.12 1.51 1.60"* 3.84* 1723.6

12.24"* 2.24** 0.01 1.61 1.71"* 5.14" 32807.8

Source

d.f.

NS1 b

AGFEC

d.f.

NS2

d.f.

CALINT

Second g e n e r a t i o n SB 2 YS 13 CYTOPL. S. 63 Error M.S. 103

2.177 2.239* 1.309 0.014587

1.080 1.245 0.901 0.000196

2 15 63 101

0.302 4.407** 0.826 0.019214

2 14 51 74

1.176 0.846* 0.717 0.001624

Third g e n e r a t i o n SB 2 YS 10 CYTOPL. S. 36 Error M.S. 59

0.298 3.786** 1.131 0.014529

1.392 2.508** 1.450 0.000173

2 11 35 54

0.821 3.212"* 1.175 0.016524

2 10 13 20

9.894** 0.553 0.873 0.001046

Reproduction traits

"0.01 < P < 0.05; **P < 0.01. aSBDIS = effect of t h e sire's breed x district; SB = effect of the sire's breed; YS = effect of year x season; GEN = effect of g e n e r a t i o n ; SBDIS x GE N = effect of i n t e r a c t i o n b e t w e e n SBDIS a nd GEN; CYTOPL. S. = effect of the c y t o p l a s m i c sources; BV = linear regression o f t h e b r e e d i n g values on a pedigree basis; Age = linear regression of age at calving. bNS1 = n u m b e r of i n s e m i n a t i o n s per c o n c e p t i o n for nullipara; A G E F C = age at first calving; NS2 = n u m b e r of i n s e m i n a t i o n s per c o n c e p t i o n for p r i m i p a r a ; C A L I N T = calving interval b e t w e e n first and second calving.

19 RESULTS

The results of the analyses of variance are summarized in Table III. The effect of sire's breed × district and year × season were significant for almost all production traits in the data. Age at first calving was significant in the combined data for kg milk, kg fat plus protein, and milk returns. Only in the case of fat % was the generation effect important. For the reproduction traits sire's breed was only significant for CALINT. The YS effect was significant in most cases. Of the production traits, cytoplasmic sources were significant (P < 0.05) for kg fat plus protein and milk returns in the second generation, and for protein % ( P < 0 . 0 1 ) in the third generation. In the combined data cytoplasmic sources were highly significant ( P < 0 . 0 1 ) for kg fat plus protein, T A B L E IV Overall means (~), p h e n o t y p i c standard deviation (Sp), standard deviation for cytoplasmic 2 2 effects (So) and its c o n t r i b u t i o n to p h e n o t y p i c variance (aC/ap) of p r o d u c t i o n and r e p r o d u c t i o n traits Traits

~

Sp

sC

2 2 a c /op

Second generation kg milk Fat % Protein % kg fat and protein Milk returns (Dfl.) NS1 AGEFC NS2 CALINT

5235 4.13 3.31 386 1753 0.259 2.864 0.272 2.568

912 0.28 0.16 56 239 0.131 0.014 0.157 0.039

178 0.00 0.02 20 94 0.042 -0.003 -0.036 -0.014

0.04 0.00 -0.01 0.13 0.15 0.10 -0.04 -0.05 -0.13

Third generation kg milk Fat % Protein % kg fat and protein Milk returns (Dfl.) NS1 AGEFC NS2 CALINT

5237 4.14 3.29 385 1748 0.264 2.864 0.271 2.575

985 0.30 0.17 60 250 0.140 0.015 0.145 0.038

209 0.07 0.07 9 40 0.028 0.006 0.035 -0.008

0.04 0.05 0.19 0.02 0.03 0.04 0.13 0.06 -0.04

939 0.29 0.16 57 243

224 0.06 0.04 18 86

Second and third generation c o m b i n e d kg milk 5236 Fat % 4.13 Protein % 3.30 kg fat and protein 386 Milk returns (Dfl.) 1751

0.06 0.05 0.06 0.10 0.13

20

milk returns and significant (P < 0.05) for kg milk, and approached significance (P <~0.10) for protein %. Table IV shows the overall means, phenotypic standard deviation, standard deviation for cytoplasmic effects and its contribution to phenotypic variance in production and reproductive traits. In the combined data phenotypic standard deviation amounted to 939 kg, 0.29%, 0.16%, 57 kg and 253 Dfl. for kg milk, fat %, protein %, kg fat plus protein and milk returns, respectively. The standard deviations of cytoplasmic effects of the former traits were 224 kg, 0.06%, 0.04%, 18 kg and 90 Dfl., respectively. Respective contributions of cytoplasmic effects to phenotypic variance in these production traits were 5.6, 4.8, 6.2, 10.1 and 12.5%. In the two generations phenotypic standard deviations of the nulliparous reproductive traits amounted to a range of 0.13-0.14 and 0.014-0.015 for NS1 and AGEFC, respectively. The standard deviation of cytoplasmic effects of these traits for the second and third generation ranged from 0.042 to 0.028 and from -0.003 to 0.006, respectively. The contribution of cytoplasmic effects to phenotypic variance in these reproductive traits amounted for the two generations to a range from 10% to 4% and from -4% to 13%, respectively. DISCUSSION

Production traits

The analyses suggest the presence of cytoplasmic effects for at least kg milk, kg fat plus protein, and milk returns. These results support the findings of Bell et al. {1985) that maternal effects due to mitochondrial inheritance have effects on yields. However, this evidence is not conclusive, as other maternally transmitted components might be involved. The results differ from those of Bell et al. (1985) in that Bell found greater cytoplasmic effects for fat % than for kg milk and fat yield. In our data additive genetic covariance between members of a cytoplasmic TABLE V Change in F-values for the cytoplasmic sources due to an a p p r o x i m a t e a d j u s t m e n t for additive genetic covariance in the p r o d u c t i o n traits of the c o m b i n e d generations Traits

F-value

F-value (adjusted)

kg milk Fat % Protein % kg fat and protein Milk returns (Dfl.)

1.37" 1.20 1.31 1.60"* 1.71"*

1.19 1.05 1.07 1.49" 1.60"*

*0.01 < P < 0.05; **P < 0.01.

21 line was partly c o n f o u n d e d with cytoplasmic effects. It is difficult to estimate the a m o u n t of covariance in our data, therefore we will discuss two approaches to adjusting cytoplasmic effects for this covariance. The remaining 25% of the additive genetic values, which is n o t adjusted for, is cause of the additive genetic covariance. The maximal impact of this 25% of the additive genetic values on the F-values of the cytoplasmic components can be approximated from the variance accounted for by the breeding values in the model. Multiply the added sums of squares (SS) due to covariates for breeding values by 4/3 and subtract the SS of cytoplasmic sources from the increase of the SS of breeding value covariates as is shown in the following equation: adjusted

SS(Ck:i)

=

SS(Ck:i) - (SS(bl:i) × 4/3 - SS(bI:i))

The changes in F-values of the cytoplasmic sources after these adjustments are shown in Table V. Cytoplasmic effects for kg fat plus protein, and milk returns remained significant after adjustment. The cytoplasmic lines of the second and third generation consist of maternal half-sibs, maternal cousins and maternal second cousins. Van Vleck and Hart (1966a) estimated genetic and genetic maternal additive components of variance and covariance between records of pairs of cousins. They could not find evidence for additive genetic maternal effects, and concluded that only additive genetic effects were important for first lactation production to cause covariance. However, t h e y did not a t t e m p t to estimate maternal effects due to cytoplasmic inheritance. In the case of cousins and second cousins additive genetic covariances are 1/16 and 1/64 of the additive genetic variance, respectively. Since the additive genetic influence of the maternal grandsire was adjusted for, the additive genetic covariance of maternal half sibs amounts to 1/8 of the additive genetic variance. Hence, the additive genetic covariance will vary between 1/8 and 1/64 of the additive genetic variances. Theoretically this corresponds with intervals of 3.125--0.039%, 6.25--0.78%, 6.25--0.78%, 3.125--0.39% (derived from the assumed heritabflities) of the phenotypic variance of kg milk, fat %, protein %, kg fat plus protein, respectively. Assuming average figures for the intervals none of them is as high as the contributions of cytoplasmic effects to phenotypic variance (Table IV). Irrespective of the approach, significance of cytoplasmic effects prevailed in kg fat plus protein, and milk returns. These traits express more than the others a total energy o u t p u t for the dairy cow. This agrees with the expectation that cytoplasmic effects would especially be exhibited in traits reflecting the energy o u t p u t of the individual. On the other hand some effects could lead to an underestimation of cytoplasmic effects. First, the SBDIS-effect in the model adjusts for differences in cytoplasmic sources between its subclasses. Further, it is likely that some of the different 'cytoplasmic sources' belong, in fact, to the same cytoplasmic line. The impact of these effects is n o t calculable.

22 In this study maternal effects due to cytoplasmic inheritance were a significant source of variance in kg fat plus protein and milk returns.

Reproductive traits The number of inseminations per conception in nullipara ( N S 1 ) p r o b a b l y better expresses the fertility of an animal than age at first calving (AGEFC). More inseminations needed for conception result in a higher age at calving. Variation in age at calving also includes variation in the interval between starting breeding at 15 months and first breeding of the heifer, and variation in gestation length. The fact that smaller cytoplasmic c o m p o n e n t s were found for the primiparous reproductive measurements can at least partially be explained by the greater error mean squares compared to those of the nulliparous reproductive measurements. Probably more factors play a role in fertility as a primipara than as a nullipara. Besides, whether or not heifer and cow fertility reflect the same trait is n o t clear (Maijala, 1974; Hansen et al., 1983; R o n et al., 1984). If reproductive traits in virgin heifers and first calvers are indeed based on a different genetic mechanism, it is possible that only reproductive measurements of virgin heifers are subjected to maternal effects due to cytoplasmic inheritance. Bell et al. (1985) showed a cytoplasmic effect in days open for primipara, which accounted for 2% of the phenotypic variation. The fact that a greater n u m b e r of records was involved in their analysis may have played a role. For a variety of fertility measures, heritability estimates and additive genetic contribution to variation in reproduction have been shown to be small, mostly lower than 5% and 10%, respectively (reviews by Maijala, 1976, 1978; Philipsson, 1981; Vinson, 1982; Jansen, 1985). Therefore, a cytoplasmic c o m p o n e n t has to be evaluated relative in this respect. Some of the cytoplasmic effects for nullipara from Table IV exceeded heritability estimates and most estimates of genetic variation in fertility traits. This suggests that the maternal c o m p o n e n t accounted for more variation in female fertility in nuUipara than the sire component. This means that in selection for female fertility, progress could be achieved via the maternal side. Whether or not this would be valid for selection on fertility in primipara is not clear. Further research on a larger data set is necessary for drawing definite conclusions. IMPLICATIONS If important effects of cytoplasmic inheritance exist in dairy cattle, which this paper strongly suggests at least for kg fat plus protein and milk returns, several conclusions referring to breeding policies may follow: 1. E m b r y o transfer and e m b r y o manipulation will have more importance in producing female offspring than predicted from additive genetic superiority if superior maternal lines can be identified.

23 2. S e p a r a t e s e l e c t i o n i n d e x e s s h o u l d b e d e v e l o p e d f o r s e l e c t i o n o f c o w s (a) t o p r o d u c e d a u g h t e r s , a n d ( b ) t o p r o d u c e s o n s : (a) T o p r o d u c e d a u g h t e r s , m o r e r e l a t i v e e m p h a s i s t h a n a t p r e s e n t s h o u l d b e g i v e n t o p r o d u c t i o n o f d a m s a n d o t h e r m a t e r n a l r e l a t i v e s in t h e cow's pedigree; ( b ) T o p r o d u c e s o n s , m o r e a t t e n t i o n s h o u l d b e p a i d t o sires in t h e c o w ' s p e d i g r e e a n d less t o t h e m o t h e r ' s p r o d u c t i o n a n d t h a t o f h e r m a t e r n a l relatives. 3. T h e i m p o r t a n c e a n d r o l e o f b r e e d s w i t h s u p e r i o r c y t o p l a s m i c e f f e c t s might be changed.

REFERENCES Bell, B.R., 1983. Effects of cytopla~nic inheritance on production traits in dairy cattle. Ph.D. Dissertation, North Carolina State University, Raleigh. Bell, B.R., McDaniel, B.T. and Robison, O.W., 1985. Effects of cytoplasmic inheritance on production traits of dairy cattle. J. Dairy Sci., 68: 2038--2051. Bereskin, B. and Touchberry, R.W., 1966. Crossbreeding dairy cattle. 3. First lactation production. J. Dairy Sci., 49: 659---667. Bradford, G.E. and Van Vleck, L.D., 1964. Heritability in relation to selection differential in cattle. Genetics, 49: 819---829. Central Milk Recording Service, 1983. Stier index en totaal publicatie. Arnhem, The Netherlands. Donald, H.P., Gibson, D. and Russell, W.S., 1977. Estimations of heterosis in crossbred dairy cattle. Anita. Prod., 25: 193--208. Dzapo, V., Schnarr, W. and Wassmuth, R., 1983. Mitochondrialer Stoffwechsel und heterotische Effekte beim Schwein. Ergebnisse eines reziproken Kreuzungsversuches. 1. Reproduktionsleistung, Wachstungsintensit~it und SchlachtkSrperqualit~it. Z. Tierz. Ztichtungsbiol., 100: 109--122. Dzapo, V. and Wassmuth, R., 1983. Mitochondrialer Stoffwechsel und heterotische Effekte beim Schwein. Ergebnisse eines reziproken Kreuzungsversuches. 2. Atmungsaktivit~it und oxydative Phosphorylierung in Herz-, Leber- und Hodenmitochondrien. Z. Tierz. Ziichtungsbiol., 100: 280--295. Fischer Lindahl, K. and Hausmann, B., 1983. Cytoplasmic inheritance of a cell surface antigen in the mouse. Genetics, 103: 483--494. Gavora, J.S. and Spencer, J.L., 1983. Breeding for immune responsiveness and disease resistance. Anita. Blood Groups Biochem. Genet., 14: 159--180. Goodfellow, P., 1983. Mitochondria and the major histocompatibility complex. Nature (London), 306: 539---540. Hansen, L.B., Freeman, A.E. and Berger, P.J., 1983. Association of heifer fertility with cow fertility and yield in dairy cattle. J. Dairy Sci., 66: 306--314. Harvey, W.R., 1977. Mixed model least-squares and maximum likelihood computer program. Ohio State University, 76 pp. Jansen, J., 1985. Genetic aspects of fertility in dairy cattle based on analysis of A.I. data -- a review with emphasis on areas for further research. Livest. Prod. Sci., 12: 1--12. Jansen, J., Dommerholt, J. and Wismans, W.M.G., 1983. Breeding values for milk production traits in the Netherlands. Report B-211 of the Research Institute for Animal Production, " S c h o o n o o r d " . Laipis, P.J. and Hauswirth, W.W., 1980. Variation in bovine mitochondrial DNAs between maternally related animals. In: A.M. Kroon and C. Saccone (Editors), Organization

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25 Van Vleck, L.D. and Hart, C.L., 1966b. Heritability estimates when dams and daughters are in the same and different herds. J. Dairy Sci., 49: 1676--1679. Vinson, W.E., 1982. Selection for secondary traits in dairy cattle. Proc. 2nd World Congress Genet. Applied to Livest. Prod., Vol. 5, pp. 370--386.

RESUME Huizinga, H.A., Korver, S., McDaniel, B.T. et Politiek, R.D., 1986. Effets maternels dus a une h~r~dite cytoplasmique chez les bovins laitiers. Livest. Prod. Sci., 15: 11-26 (en anglais). Cette 6tude a eu pour objet de mesurer les effets d'origine cytoplasmique sur les caract~res de production laiti~re et de reproduction. Les families de vaches de la ferme exp~rimentale sont issues de veaux collectSs au hasard dans 240 troupeaux de deux zones d'~levage. L'origine cytoplasmique a ~t~ d~finie par la femelle fondatrice de la lign~e maternelle. On a u t i l i ~ les productions laiti~res de 290 vaches en premiere lactation entre 1976 et 1982. Les caract~res de reproduction des m~mes animaux ont pu ~tre analys~s par famille de vaches. L'origine cytopia~nique a 6t~ une source significative (P < 0.01) de la variation des productions de mati~res grasses et de mati~res azot~es et de la vente de lait, apr~s ajustement pour la zone d'origne de la source cytoplaarnique, la race du p~re, l'ann~e et la saison de v~iage, l'index des p~res et des grand p~res maternels, et l'~ge au v~hge. L'origine cytoplasmique rend compte au maximum de 10 et 13% respectivement de la variation phSnotypique des deux caract~res. EUe n'a pas ~t6 une source significative de variation des caract~res de reproduction des multipares et des primipares, apr~s ajustement pour les effets de ia race, du l'ann~e et de la saison de v~lage. Bien que n o n significative, la composante cytoplasmique a rendu compte de 10 et 4% de la variation ph~notypique dans le nombre d ' i n s ~ m n a t i o n s pour la premiere f$condation et de - 0 . 0 4 et 13% de la variation ph~notypique de l'ige au premier v~iage, respectivement pour la premiere et la deuxi~me g~n~ration. Certaines de ces composantes cytoplasmiques expliquent une part plus grande de la variation ph~notypique des caract~res de reproduction des g6nisses multipares que la plupart des composantes g~n~tiques additifs rapport~es dans la litt~rature. Les effets de l'h~r~dit6 cytoplasmique sur les caract~res de production et de reproduction pourraient avoir des consequences sur la politique de s~lection des bovins laitiers. KURZFASSUNG Huizinga, H.A., Korver, S., McDaniel, B.T. und Politiek, R.D., 1986. Maternale Effekte infolge zytoplasmatischer Vererbung beim Milchvieh. Livest. Prod. ScL, 1 5 : 1 1 - - 2 6 (auf englisch). Ziel dieser Untersuchung war es, die Bedeutung zytoplasmatischer Effekte auf Milchleistung und Reproduktionsmerkmale festzustel]en. Die Kuhf~milian auf dem Versuchsbetrieh wurden mit K~Ibarn aufgebaut, die zufsllsm~ig aus 240 Harden in zwei Zuchtgebieten e n t n o m m e n worden waren. Zytoplasmatische Herkunft wurde definiert als das erste Tier in der nachweisbaren miitterlichen Linie. Fiir die Auswertung stand die Milchleistung yon 290 KiLhen in der 1. Laktation aus den Jahren 1976 bis 1982 zur Verf'dgung. Die Reproduktionsdaten derselben K~he v o r u n d nach der 1. Kalbung (nullipar und primipar) k o n n t e n innerhaIb der Kuhfamilien analysiert werden. Die zytoplasmatische Herkunft hatte einen signifikanten Einflu~ (P < 0.01) auf die Merkmale Fett + Eiwei~ -kg und den Milcherl~s (Dfl.) rmch Korrektur auf das Zuchtgebiet, die genetische Herkunft des Bullen, das Kalbejahr und die Saison, die Zuchtwerte der

26 Bullen und der miitterlichen Gro~v~iter sowie das Alter bei der Kalbung. Die zytoplasmatische Herkunft erkl/irtemaximal 10% bzw. 13% der phiinotypischen Variation in den 2 Merkmalen. Nach Korrektur auf die Effekte tiergenetischen Herkunft des Bullen, das Kalbejahr und die Saison hatte die zytoplasmatische Herkunft keinen signifikanten Einflu~ auf die Reproduktionsmerkmale. Trotz feb.lender Signifikanz erkli/rtedie zytophsmatische Herkunft 4 % bis 10% der ph/inotypischen Variation des Besamungsindexes bei F~irsen und -0.04% bis 13% der phiinotypischen Variation des Alters bei der ersten Kalbung fiir die I. bzw. 2. Generation. Einige dieser zytoplasmatischen Bestandteile erkl~ten mehr ph~inotypische Varianz bei den Reproduktionsmerkmalen von nuUiparen Fiirsen als die rneisten in der Literatur gefundenen additiv genetischen Komponenten. Die Auswirkungen zytoplasmatischer Vererbung auf Produktions- und Reproduktionsmerkmale diirfteneine Wirkung auf die Zuchtstrategie beim Milchvieh haben.