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ANIMAL GENETICS |
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* Department of Animal Sciences, The Ohio State University, Columbus 43210-1095 and
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Department of Animal Science and Interdisciplinary Concentration in Animal Molecular and Cell Biology, University of Florida, Gainesville 32611-0901
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResults and DiscussionImplicationsLiterature Cited |
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Key Words: Beef Cattle • Heritability • Insulin-Like Growth Factor-I • Physiology • Reproduction • Selection
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionImplicationsLiterature Cited |
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), with number of calves weaned per cow mated being of economic importance. A decrease in age of heifers at first calving also would increase lifetime productivity (Patterson et al., 1992).
Male and female reproductive traits can be improved by selection. Selection for scrotal circumference provides a method of reproductive improvement in a herd (Keeton et al., 1996) due to correlated response for reproductive traits of both male and female progeny. Scrotal circumference is related to percentage of abnormal sperm cells (Christmas et al., 2001), calving dates (Meyer et al., 1991), and age at puberty (Evans et al., 1999).
Concentration of IGF-I in the serum is a candidate for selection to improve reproductive performance because it is moderately to highly heritable, is associated with economically important traits, and its release is not pulsatile. Insulin-like growth factor-I has been isolated from components of the male and female reproductive tract (Dombrowicz et al., 1992; Robinson et al., 2002). The local concentration of IGF-I is correlated with male (Glander et al., 1996) and with female (Woad et al., 2000) reproductive traits. Selection for circulating high IGF-I concentration does not change conception rate in mice (Kroonsberg et al., 1989), and it is associated with earlier calving in heifers (Davis and Bishop, 1991).
Estimates of genetic correlations of reproductive traits with IGF-I concentration are needed to determine which traits can be genetically improved by selecting for IGF-I concentration. The objective of the current study was, therefore, to obtain estimates of heritability, along with genetic, environmental, and phenotypic correlations of scrotal circumference, percentage of morphologically normal and motile sperm cells, age at first calving, and calving rate with IGF-I concentration in beef cattle.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionImplicationsLiterature Cited |
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. Age at first calving was the age in days when a heifer gave birth to her first calf. Calving rate reflected whether a palpable fetus was present or a calf was born given the cow or heifer was mated. The calving rate data were entered arbitrarily as either 1 (if calved) or 100 (if not calved). Estimates for calving rate in this study were approximate because calving rate was treated as a continuous variable.
Selection Procedures.
Data for the current study were taken from an ongoing divergent selection experiment for blood serum IGF-I concentration initiated in 1989 using 100 spring-calving (50 high line and 50 low line) and in 1990 using 100 fall-calving (50 high line and 50 low line) purebred Angus cows with unknown IGF-I levels located at the Eastern Ohio Resource Development Center (EORDC). Cows from the initial base population were randomly assigned to the high- or low-IGF-I selection lines in spring- or fall-breeding herds.
Selection of replacement breeding animals was based on the linear residuals (adjusted for age of calf and age of dam) for mean IGF-I concentration of three blood samples taken at d 28, 42, and 56 of the 140-d postweaning test, which are abbreviated as IGF28, IGF42, and IGF56, respectively. The fall- and spring-breeding herds were replicates of each other. Animals in each of the four groups (e.g., high- and low-IGF-I lines in spring- and fall-breeding herds) were mated only within their groups. The four bull calves with the highest and the four with the lowest linear residuals for mean IGF-I concentration were saved each year and each season for breeding within the corresponding selection lines. Selected bulls were used for breeding only as yearlings. All available heifers were bred and selections were made among heifers that conceived. Approximately eight cows were culled from each line each year (based on physical unsoundness, failure to conceive in two consecutive years, and oldest age) and replaced with approximately eight pregnant heifers having the highest or lowest linear residuals (adjusted for age of calf and age of dam) for serum IGF-I concentration.
Matings were by natural service except that some artificial insemination was used from spring 1991 through fall 1994 breeding seasons to create ties between the EORDC herd and herds contributing to North Central Regional Project NC-196, the Genetics of Body Composition in Beef Cattle. Approximately 10 cows per selection line were randomly chosen and artificially inseminated each breeding season using semen from an Angus reference sire. In 1990, when excess heifers were available at the end of the spring breeding season and additional heifers were needed for the fall breeding season in the high- and low-IGF-I selection lines, pregnant heifers were aborted and transferred from the spring to fall-breeding herd without changing their IGF-I selection lines. The number of heifers transferred from the spring to fall herd in the high- and low-IGF-I lines were 10 and 7, respectively. Heifers that were transferred from the spring- to the fall-calving herd were considered as 2 yr of age at first calving for purposes of data analysis, although they were approximately 2.5 yr old. This transfer should not have affected the analysis of heifer age at first calving because numbers of animals transferred in the high- and low-IGF-I lines were similar (i.e., 10 vs. 7) and small. Further details regarding selection procedures can be found elsewhere (Davis et al., 1995; Davis and Simmen, 1997).
Management Procedures.
Calves were maintained in either drylot or a three-sided barn with adjoining exercise lots located at EORDC. Bulls and heifers were fed in separate barns. Spring-born calves were weaned at approximately 210 d and were subjected to an adjustment period of approximately 2 wk. Fall-born calves were weaned at an average age of 140 d and additionally fed a diet formulated to yield gains of approximately 0.9 kg/d in drylot for 112 d after weaning. Both spring- and fall-born calves were fed a corn/soybean meal-based diet plus hay as previously described (Davis et al., 2003). All animals were maintained at EORDC, except that heifers born from spring 1989 through fall 1993 were transported to the North Appalachian Experimental Watershed (NAEW), Coshocton, OH, and were given ad libitum access to nonprotein nitrogen (feed grade urea)-treated corn silage, in addition to grass hay, in drylot. Further details regarding management procedures were described by Davis and Simmen (1997).
Serum Samples.
At d 28, 42, and 56 of the postweaning test, approximately 25 mL of blood was collected into sterile glass tubes, allowed to clot for 24 h at 4°C, and centrifuged at 1,800 x g for 20 min. Serum was drawn off and frozen at –20°C until assayed.
RIA for IGF-I.
The RIA for IGF-I was performed in the laboratory of R.C.M. Simmen at the University of Florida using antiserum raised against human IGF-I in rabbits (UBK487), following previously described procedures (Bishop et al., 1989). The number of observations for IGF28, IGF42, IGF56, and mean IGF-I differed because IGF42 was not measured in calves born in 1989 and a few of the blood samples were lost during the experimental procedure. In addition, the IGF-I measurements for d 28, 42, and 56 were unavailable for heifers born in spring 1990 owing to a freezer malfunction. Heifers born in the spring 1990 calving season were resampled on d 84, 98, and 112 of the postweaning test, and these samples were used to obtain the mean IGF-I concentration.
Breeding Soundness Examinations.
On bulls that were approximately 12 to 14 mo old, breeding soundness exams were performed by Ohio Agricultural Research and Development Center (OARDC) veterinarians immediately following the postweaning test. The exams were performed on all bulls except that, before 1995, exams were performed on only bulls that were saved for breeding. The number of observations for each of the male reproductive traits differed because ejaculates collected from some of the bulls were not of sufficient quantity or quality to allow accurate measurement. Data in this study were collected from bulls born in 1990 through 2001. Ejaculates were collected by electroejaculation.
Statistical Analyses.
All data were analyzed using the GLM procedure of SAS (SAS Inst. Inc., Cary, NC) and a set of MTDFREML programs written by Boldman et al. (1995). First, the fixed effects and covariates for each trait shown in Table 1 were tested for significance using SAS and only effects with a P-value of less than 0.10 were included in the subsequent MTDFREML analyses. Reproductive traits in the current study were treated as a trait of the calf, except that calving rate was treated as a trait of the cow.
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Pedigrees of base population animals were traced back three generations to create the numerator relationship matrix. Total number of animals in the numerator relationship matrix, including base animals, was 2,864, of which 1,861 were inbred. The average inbreeding coefficient was 0.03. Age of dam was the age of the dam of heifers or cows and not the age of heifers or cows themselves. All of the traits were first analyzed using a full animal model that included direct genetic effects, maternal genetic effects, permanent environmental effect of the dam, and the covariance between direct and maternal genetic effects, as well as all of the fixed effects that accounted for more than 10% of the observed variance (i.e., P > 0.10) as determined in the SAS analysis.
In a second analysis, IGF-I values, along with reproductive traits, were included in bivariate analyses to estimate direct genetic (rA1A2), environmental (rE1E2), and phenotypic (rP1P2) correlations between IGF-I measurements and the reproductive traits. Maternal genetic or permanent environmental effects were not included in the bivariate analyses because these effects contributed less than 21% of the total variance and removing these effects significantly decreased the number of (co)variances that needed to be "guessed" and used in MTDFREML as the starting values.
In all analyses, "cold restarts" of the MTDFREML programs were performed, using the converged values, until –2 times the log likelihoods used in the simplex search algorithm did not change to the second decimal place from one restart to the next. Iterations were assumed to have converged when the variance of –2 times the log likelihood of the simplex algorithm was less than 10–9. Approximate standard errors for estimates of 
and genetic correlations were obtained using previously reported procedures by Swiger et al. (1964) and Falconer and Mackay (1996), respectively.
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Results and Discussion |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionImplicationsLiterature Cited |
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. Number of observations for analyses of calving rate and age at first calving differed because age at first calving analysis included only data from heifers, whereas calving rate analysis included data from both heifers and cows. The IGF-I measurements had higher coefficients of variation than did the reproductive traits.
Significance levels of fixed effects from the PROC GLM analysis are shown in Table 2. Effects of birth year on all of the traits analyzed in the current study were significant at the P < 0.10 level. The IGF-I selection line effects on all of the IGF-I measurements, as well as on scrotal circumference and age at first calving, were significant. The IGF-I line effect on scrotal circumference was not significant in an earlier study by Yilmaz et al. (1999) in the same herd but was significant in the current study, likely because of the larger sample size in the current study (n = 825 vs. 385). Heifers in the high-IGF-I line calved 4.02 ± 2.18 d earlier than did the low-IGF-I line heifers (P = 0.07; our unpublished data). Effects of seasons on IGF-I measurements other than IGF28 were significant. Effects of seasons on scrotal circumference, age at first calving, and calving rate were also significant. Seasonal changes in IGF-I concentration in cattle could be due to changes in temperature (Sarko et al., 1994) or feed intake (Stick et al., 1998). Age of dam effects on IGF-I measurements, with the exception of IGF56, were not significant, a result that agrees with the findings of Davis et al. (1995). Age of dam effects on scrotal circumference and calving rate were significant. In earlier years of the current study, however, Yilmaz et al. (1999) reported nonsignificant age of dam effects on scrotal circumference when a smaller sample was analyzed. The age of dam effects on percent motile and normal sperm cells were nonsignificant in both studies. Sex effects on IGF-I measurements were significant. In addition, effect of mating number on calving rate was significant. On-test age of calf, with the exception of CR, was significant for all of the traits analyzed in this study. Bishop (1991) monitored IGF-I concentration during developmental stages of cattle. He reported dramatic increases in IGF-I concentration of bulls between 10 and 14 mo of age. The IGF-I concentration increased in heifers at the time of puberty (i.e., approximately 12 mo of age).
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are direct () heritability estimates for IGF-I measurements and reproductive traits (with comparison with earlier estimates reported in the literature), maternal (
) heritability estimates, the proportion of phenotypic variance due to permanent environmental effects of the dams (c2), and the correlation between direct and maternal genetic effects (ram). Direct heritabilities were estimated using an animal model that included maternal genetic and permanent environmental effects, as well as fixed effects. Direct heritability estimates ranged from 0.41 ± 0.08 to 0.51 ± 0.13, except that estimates for percent motile sperm cells and calving rate were 0.08 ± 0.12 and 0.11 ± 0.05, respectively. Heritability for age at first calving converged to 1.00 ± 0.28, but decreased to 0.26 ± 0.28 when the data were reanalyzed after deleting maternal effects from the model. Direct heritability estimates were in general agreement with the literature. The observed differences in current and previously reported heritability estimates for IGF-I measurements from this herd may be due to the larger sample size in the current study. Sample size and mean IGF-I concentration were 1,283 and 225.8 ng/mL in a study by Davis and Simmen (2000) compared with 1,848 and 238.8 ng/mL in the current study. Another reason for the observed differences could be that Davis and Simmen (2000) included all of the fixed effects in the models regardless of contribution of these effects to the total observed variance.
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and c2 were smaller than 0.21, except that and c2 for age of heifers at first calving were 0.77 and 0.28, respectively. Davis and Simmen (2000) also reported estimates of and c2 that were less than 0.20 for IGF-I measurements. The unusually large estimates of , , and c2 for age of heifers at first calving in the current study were likely due to small sample size or confounding between direct and maternal genetic effects. Deleting the maternal genetic and permanent environmental effects from the model decreased the heritability from 1.00 ± 0.28 to 0.26 ± 0.28, a result in agreement with the literature (Table 3). Estimates of the correlation between direct and maternal genetic effects ranged from –0.40 to –1.00, a result consistent with that of Davis and Simmen (1997).
A data set was created for analysis of calving rate by entering an IGF-I measurement for the first mating only and missing values for the remaining matings (Table 4). Heritability for calving rate was 0.13 and agreed well with the estimates reported in the literature. Evans et al. (1999) and Doyle et al. (1996) reported heritability estimates of 0.13 and 0.26, respectively, for heifer pregnancy rate. Entering IGF-I measurements once per animal allowed estimation of genetic correlations, but it ignored environmental correlations for matings other than the first.
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2 test was used to determine whether ignoring environmental covariance for matings other than the first had an influence on the estimates of genetic, environmental, and phenotypic correlations. Calving rate and IGF-I measurements, along with significant fixed effects, were included in reduced (i.e., with no maternal genetic or permanent environmental effects) bivariate models in MTDFREML. The program was first run using a zero starting value for environmental covariance. The run was repeated with a nonzero starting value for environmental covariance and the difference in log likelihood values from the two runs were tested for significance against the 2 distribution with a single degree of freedom. The difference in minimum function values exhibits a 2 distribution (Van Tassell and Van Vleck, 1996), and the difference between the values from two different runs can be used to compare models with different numbers of (co)variances. The one degree of freedom is the difference in the number of (co)variance components in the two models. The minimum function values when calving rate was paired with IGF28, IGF42, IGF56, and mean IGF-I and zeros were used as the starting value for environmental covariance remained the same when a nonzero starting value was used for environmental covariance, indicating that environmental correlations of calving rate with IGF-I measurements were not important when all of the matings were included in the data set.
Genetic correlations of IGF-I measurements with scrotal circumference were larger than the correlations with the percentage of normal sperm cells, but smaller than the correlations with the percentage of motile sperm cells (Table 5). Genetic correlations of mean IGF-I concentration with scrotal circumference, and the percentage of motile and normal sperm cells were 0.35 ± 0.11, 0.43 ± 0.32, and 0.00 ± 0.03, respectively. Genetic correlations of IGF-I measurements with calving rate and age at first calving were negative, indicating a tendency toward an increase in calving rate and a decrease in age at first calving with increased IGF-I concentration. Moderate genetic correlations of calving rate with IGF-I measurements were obtained (Table 5). The genetic correlations ranged from –0.41 ± 0.16 to –0.48 ± 0.16, indicating that cows with high breeding values for IGF-I measurements also had high breeding values for calving rate. Coding calving rate as either 1 (if calved) or 100 (if not calved) resulted in favorable negative genetic correlations between calving rate and IGF-I measurements. These genetic correlations indicate that selection for increased IGF-I should improve both male and female reproductive traits, but little or no improvement would be expected in the percentage of normal sperm cells.
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). Thus, phenotypic changes in IGF-I concentrations were not associated with phenotypic changes in the reproductive traits analyzed, a result in agreement with Yilmaz et al. (1999), who reported nonsignificant residual correlations of IGF-I measurements with scrotal circumference and the percentage of motile and normal sperm cells. In addition, residual correlations between age at first calving and IGF-I concentrations were nonsignificant (our unpublished data).
Correlations of reproductive traits with each of the IGF-I measurements were generally similar because IGF-I concentrations at d 28, 42, and 56 are controlled by the same genes (Davis and Simmen, 1997). Those authors reported that genetic correlations among IGF-I measurements at these points in time were close to 1.00. In their study, phenotypic correlations among IGF-I measurements averaged 0.68.
Genetic and environmental correlations of circulating IGF-I concentration with reproductive traits included in the current study have not been reported previously in the literature. Although local expression of IGF-I in both male and female reproductive tracts has been well documented, only phenotypic relationships of local IGF-I measurements with reproductive traits have been reported previously. Significant phenotypic correlations of seminal plasma IGF-I with sperm motility (Breier et al., 1996) and the percentage of normal sperm cells (Glander et al., 1996) have been reported in rats and humans, respectively.
Concentration of IGF-I in blood serum is related to reproductive, growth, and nutritional status of animals and may be the link between nutritional status and reproductive performance in cattle (Zulu et al., 2002). Concentration of circulating IGF-I is related to not only concentration of several metabolites in blood—including urea, nitrogen, and free fatty acids—but also ovarian production of gonadotropins and function of the corpus luteum. Zulu et al. (2002) concluded that changes in plasma IGF-I concentration could be predictive of nutritional and reproductive status in cattle.
Moderate genetic correlations of blood serum IGF-I concentration with calving rate and age at first calving in the current study are not surprising because IGF-I is known to play an important role in follicular development and ovulation in cattle. Production of IGF-I in the ovary has been reported, suggesting local action of IGF-I (Lucy, 2000). Growth-promoting effects of circulating and locally produced IGF-I on ovarian cell growth is synergistic. Therefore, effects of circulating IGF-I on the ovary may be as important as those of locally produced IGF-I. Local production of IGF-I in the ovary increases before the late stages of follicular development and results in increases in sensitivity of the granulosa cells to follicle-stimulating hormone in the ovary (Monget and Bondy, 2000).
Concentration of IGF-I also is involved in pregnancy. Uterine IGF-I expression has been detected during the estrous cycle and early pregnancy, indicating that its expression may play a role in embryonic development and uterine function (Robinson et al., 2000). Expression of IGF-I differs in various regions of the uterus and at different stages of pregnancy, suggesting that these changes may play a role in pregnancy and early development of the embryo (Robinson et al., 2000). Insulin-like growth factor-I may be important in the course of pregnancy in rats (Davenport et al., 1992). In pigs, expression of IGF-I mRNA in the uterus was highest in early pregnancy (Tavakkol et al., 1988). Kroonsberg et al. (1989) reported no difference in conception rates of female mice divergently selected for high or low plasma IGF-I concentration. They reported greater weights and number of fetuses in high-IGF-I line mice, but the difference could have been due to differences in maternal body weight and the ability of the dam to provide nutrients for the fetus, rather than to direct effects of IGF-I in the selection line.
Expression of IGF-I has also been well documented in the male reproductive tract (Dombrowicz et al., 1992). Insulin-like growth factor-I stimulates testicular development by inhibiting aromatase enzyme activity, which results in decreased estrogen production in the testis (Rappaport and Smith, 1996). Injection of growth hormone-deficient mice with IGF-I increases the number of motile sperm cells, as well as the number of sperm cells with normal morphology (Vickers et al., 1999). Concentration of IGF-I has a nonlinear relationship with scrotal circumference (Yilmaz et al., 1999). Bulls with intermediate concentration of IGF-I have larger scrotal circumferences than bulls with high or low concentration of IGF-I.
In summary, current and previous data suggest that concentration of blood serum IGF-I is involved in growth and reproductive performance of beef cattle. Phenotypic correlations of concentration of IGF-I with weaning weight and postweaning weights are small, but genetic correlations of IGF-I with birth, weaning, and postweaning weights and with postweaning weight gain are strongly negative (Davis and Simmen, 1997). These results indicate that selection for increased postweaning concentration of IGF-I results in decreases in performance traits. High concentrations of IGF-I in cattle are associated with decreases marbling score, quality grade, backfat thickness (Davis and Simmen, 2000), and age at first calving (current study). Furthermore, a high concentration of IGF-I is associated with increases in scrotal circumference, percentage of sperm motility, and calving rate. Therefore, selection for high serum concentration of IGF-I is associated with improved reproductive performance, and changes in growth rate and carcass composition in beef cattle.
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Implications |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionImplicationsLiterature Cited |
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Footnotes |
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2 This experiment was a contributing project to North Central Regional Project NC-196, the Genetics of Body Composition in Beef Cattle.
3 The authors respectfully acknowledge the invaluable advice from L. D. Van Vleck (Univ. of Nebraska at Lincoln) and H. C. Hines (The Ohio State Univ.) in MTDFREML analyses.
5 Current address: Dept. of Physiology & Biophysics, Univ. of Arkansas for Med. Sci. and Senior Investigator in Developmental Biology, Arkansas Children’s Nutrition Center, 1120 Marshall Street, R-2027, Slot 512, Little Rock 72202.
4 Correspondence: Dept. of Poultry Sci., 419 Kleberg Center, Texas A&M University, College Station 77840 (phone: 979-845-9444; fax: 979-845-1921; e-mail: ahmetyilmazyilmaz{at}yahoo.com).
Received for publication April 16, 2003. Accepted for publication April 19, 2004.
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionImplicationsLiterature Cited |
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