Published December 4, 2014
Estimates of inbreeding depression for serum insulin-like growth factor I concentrations, body weights, and body weight gains in Angus beef cattle divergently selected for serum insulin-like growth factor I concentration1,2,3 M. E. Davis*4 and R. C. M. Simmen† *Department of Animal Sciences, The Ohio State University, Columbus 43210-1095; and †Department of Physiology and Biophysics, University of Arkansas for Medical Sciences, Little Rock 72202
ABSTRACT: Data for the current study were obtained from a divergent selection experiment in which the selection criterion was the average serum IGF-I concentration of 3 postweaning blood samples collected from purebred Angus calves. Multiple trait derivativefree REML procedures were used to obtain estimates of inbreeding depression for IGF-I concentration and for BW and BW gains measured from birth to the conclusion of a 140-d postweaning performance test. Included in the analysis were 3,243 animals in the A−1 matrix, 2,182 of which had valid records for IGF-I concentration. Over the course of the entire selection experiment, inbreeding of the calf averaged 3.3% (SD = 3.1%) and inbreeding of the dam averaged 1.8% (SD = 2.7%). Mean inbreeding levels at the end of the study were 6.82 ± 0.38% and 4.20 ± 0.36% for calves and dams, respectively. Annual rates of increase in inbreeding of calves and dams were 0.36 ± 0.01 (P < 0.0001) and 0.25 ± 0.01%/yr (P < 0.0001), respectively. Insulinlike growth factor I concentration at d 28 (IGF28), 42 (IGF42), and 56 (IGF56) of the 140-d postweaning test and mean IGF-I concentration decreased by 0.62 ± 0.88, 1.86 ± 0.96, 1.92 ± 0.89, and 1.48 ± 0.76 ng/mL per
1% increase in inbreeding of calf. Only the regression coefficient for IGF56 differed significantly from zero, although the regression coefficients for IGF42 and mean IGF-I approached significance (P < 0.10). Increases in inbreeding levels of the dams also tended to result in reduced IGF-I concentrations, although the regression coefficients were not significantly different from zero. Inbreeding of calf had highly significant negative effects on all BW and BW gain traits examined, except for birth weight, with regression coefficients ranging from −0.74 ± 0.20 kg/% increase in calf inbreeding for postweaning BW gain to −1.68 ± 0.33 kg/% increase in calf inbreeding for off-test BW. Inbreeding of dam had a significant negative effect on birth weight of progeny and tended to have a negative effect on postweaning BW gain (P < 0.10). Preweaning gain of the progeny and BW other than birth weight were not influenced by increases in dam inbreeding. Results indicate that reductions in serum IGF-I concentration due to inbreeding may contribute to the decline in BW and BW gains that is typically associated with increases in inbreeding within populations.
Key words: beef cattle, growth, inbreeding depression, insulin-like growth factor, selection ©2010 American Society of Animal Science. All rights reserved.
J. Anim. Sci. 2010. 88:552–561 doi:10.2527/jas.2009-2232
INTRODUCTION Insulin-like growth factor I is a polypeptide hormone that regulates growth and cellular metabolism during all stages of development. Circulating IGF-I is synthesized and secreted primarily by the liver, although several fetal and adult tissues also synthesize IGF-I (D’Ercole et al., 1984; Murphy et al., 1987). Inbreeding increases the probability that the 2 alleles at a locus in an individual are identical by descent, which in turn causes an increase in the proportion of homozygous loci in the inbred animal or population. A consequence of the inbreeding process is that increased
1 Salaries and research support were provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University. 2 This experiment was a contributing project to North Central Regional Project NC-1010, “Interpreting Cattle Genomic Data: Biology, Applications, and Outreach.” 3 The authors thank W. D. Shriver, J. D. Wells, and C. A. Clark (Eastern Agricultural Research Station, Belle Valley, OH) and F. J. Michel (University of Florida, Gainesville)for their excellent technical assistance. 4 Corresponding author:
[email protected] Received June 18, 2009. Accepted October 7, 2009.
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Inbreeding depression estimates for insulin-like growth factor I
homozygosity has generally been associated with a decline in reproductive performance, survival, and growth rate (Brinks and Knapp, 1975; Kristensen and Sorensen, 2005). The rate of inbreeding is accelerating in most species, and economic losses in production, growth, health, and fertility due to inbreeding depression are a serious concern (Weigel, 2001; Weigel and Lin, 2002; Kristensen and Sorensen, 2005). Numerous authors have reported that increased inbreeding of the animal is associated with reduced growth, especially during the preweaning period (Brinks and Knapp, 1975; Burrow, 1993). Smaller detrimental effects of inbreeding have been observed for birth weight and postweaning growth (Brinks and Knapp, 1975; Burrow, 1993). Little is known, however, about the physiological changes that result from inbreeding and that lead to reduced growth rates. Therefore, the objective of the current study was to determine if inbreeding results in reduced serum IGF-I concentrations, which may in turn be associated with reduced growth.
MATERIALS AND METHODS Procedures involving use of animals were approved by the Institutional Animal Care and Use Committee of The Ohio State University.
Selection Procedures Divergent selection for blood serum IGF-I concentration was initiated at the Eastern Agricultural Research Station (EARS), Belle Valley, OH, in 1989 using 100 spring-calving (n = 50 high line and n = 50 low line) and in 1990 using 100 fall-calving (n = 50 high line and n = 50 low line) purebred Angus cows with unknown IGF-I concentrations. Cows from the initial base population were randomly assigned to the selection lines. Different sets of 4 bulls with unknown IGF-I concentrations were used to produce the spring 1989 and 1990 and fall 1990 calf crops. Each year, the 4 bull calves with the greatest (i.e., most positive) and the 4 with the least (i.e., most negative) residuals (from the model: mean IGF-I = µ + age of dam + age of calf + residual) for IGF-I concentrations were saved for breeding within the respective selection lines. In fall 1990, the same bulls were used for breeding that had been used in the spring 1990 breeding season, with the exception that 1 of the 4 bulls in the low IGF-I line was replaced with 1 of the 2 backup bulls that had been saved for the spring breeding season. In all other years, selections of breeding bulls were done strictly on a within-season basis. Selection was based solely on the mean IGF-I concentration of 3 blood samples [taken at d 28 (IGF28), 42 (IGF42), and 56 (IGF56) of the 140-d postweaning test]. No emphasis was placed on growth traits, conformation, or other characteristics of the bulls. Yearling bulls were used for breeding to minimize the generation interval. Approximately 8 cows were culled from each line each year (based on physical unsoundness, reproductive fail-
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ure, and oldest age) and replaced with approximately 8 pregnant heifers with the greatest (i.e., most positive) or least (i.e., most negative) residuals (from the model: mean IGF-I = µ + age of dam + age of calf + residual) for serum IGF-I concentrations. Selection of heifers was based solely on the mean IGF-I concentration of 3 blood samples collected at d 28, 42, and 56 of the 140d test period with no emphasis given to growth rate, conformation, or other phenotypic traits. All available heifers were bred and selections were made among heifers that conceived. In 1990, excess heifers were available at the end of the spring breeding season and additional females were needed for the fall replicates of the selection lines. Therefore, 7 heifers that were pregnant at the end of the spring breeding season were aborted and transferred from the high line of the spring replicate to the high line of the fall replicate. Three open heifers were also transferred from the spring high line to the fall high line. In addition, 7 heifers that were open at the end of the spring breeding season were transferred from the low line of the spring group to the low line of the fall group.
Mating Scheme Selected heifers within the high IGF-I line were stratified such that 1 of the 4 heifers with the greatest IGF-I concentrations, 1 of the 4 heifers with the next greatest concentrations, and so on, were assigned to each bull. The same mating procedure was followed in the low line using males and females with the least IGF-I concentrations. This mating scheme was intended to increase the probability of producing at least 1 replacement bull and 2 replacement heifers from each sire each year. Cows 2 yr old and older were randomly assigned to bulls for mating. Half-sib and closer matings were avoided for heifers and cows to minimize increases in inbreeding.
Management Scheme Spring-born calves were reared by their dams without creep feed until weaning at approximately 7 mo of age. Males were left intact with the exception of those born in spring 2003, which were castrated before weaning. After weaning, bull calves (steer calves born in 2003) were given ad libitum access to a corn-soybean meal-based concentrate diet, plus grass hay in large round bales. Heifers born from spring 1989 through fall 1993 were given ad libitum access to NPN (feed grade urea)-treated corn silage, in addition to grass hay in large round bales. Heifers born in spring 1994 and later were fed a corn-soybean meal diet designed to result in postweaning BW gains of approximately 0.75 kg/d. Throughout the study, bulls (steers in 2003) and heifers were allowed 2 to 3 wk to adjust to the postweaning diet and then were fed for a 140-d test period. Male calves were fed in a 3-sided barn with adjoining ex-
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Table 1. Means, SD, and CV for serum IGF-I concentrations, BW, and BW gains Trait 1
IGF28, ng/mL IGF42, ng/mL IGF56, ng/mL Mean IGF-I,2 ng/mL Birth wt, kg Weaning wt, kg On-test BW, kg d 28 BW, kg d 42 BW, kg d 56 BW, kg Off-test BW, kg Preweaning BW gain, kg Postweaning BW gain, kg Weaning age, d On-test age, d CALFF,3 % DAMF,4 %
n
Mean
SD
CV
Minimum value
Maximum value
2,122 2,051 2,125 2,182 2,507 2,114 2,190 2,185 2,056 2,183 2,136 2,113 2,136 2,114 2,182 2,182 2,182
239.6 263.5 256.7 245.4 33.7 202.1 223.4 258.0 275.9 292.0 388.0 168.3 165.0 225.9 252.3 3.3 1.8
166.9 177.1 176.9 166.7 4.8 32.1 36.8 45.2 50.4 55.4 82.6 31.1 62.1 20.9 18.8 3.1 2.7
69.7 67.2 68.9 68.0 14.3 15.9 16.5 17.5 18.3 19.0 21.3 18.5 37.7 9.2 7.4 94.5 153.5
4.2 15.4 3.4 4.1 11.3 90.7 83.9 97.5 93.0 102.1 147.4 49.9 18.1 148.0 183.0 0.0 0.0
1,025.8 1,031.4 974.7 913.3 56.7 299.4 347.0 408.2 437.7 460.4 607.8 263.1 329.8 276.0 307.0 25.2 25.0
1
IGF28, IGF42, and IGF56 represent serum IGF-I concentrations at d 28, 42, and 56, respectively, of the postweaning test. Mean IGF-I = (IGF28 + IGF42 + IGF56)/3. 3 CALFF = inbreeding coefficient of calf. 4 DAMF = inbreeding coefficient of dam. 2
ercise lots located at EARS. Heifers born from spring 1989 through fall 1993 were fed in a drylot with access to an enclosed barn located at the North Appalachian Experimental Watershed, Coshocton, OH. Heifers born in spring 1994 and later were fed in a 3-sided barn with adjoining exercise lots located at EARS. Fall-born male calves were left intact with the exception of those born in fall 2003, which were castrated before weaning. Fall-born calves were weaned at approximately 140 d of age and then fed a corn-soybean meal diet formulated to yield BW gains of 0.9 kg/d, plus grass hay, in drylot for 112 d. Fall-born calves were weighed near the end of the 112-d growing period. This BW was used as a weaning weight in the data analysis so that the BW of the fall-born calves was taken at a similar age as for the spring-born calves. After the 112d growing period, bull calves (steers in 2003) remained at EARS and were managed in the same manner as spring-born bulls. Heifer calves born during fall 1993 and earlier were transported to the North Appalachian Experimental Watershed and managed in the same manner as spring-born heifers. Heifers born during fall 1994 and later remained at EARS and were fed the same diet as spring-born heifers. Average weaning and on-test ages of all spring- and fall-born calves combined were 226 (SD = 21 d; Table 1) and 252 d (SD = 19 d; Table 1), respectively.
Data Collection Calves were weighed at birth, weaning, beginning of the 140-d postweaning performance test, and every 28 d thereafter. In addition, calves born after 1989 were weighed on d 42 of the postweaning period, when 1 of the 3 blood samples was collected for each calf. The
fall-calving herd was sold for financial reasons before weaning of the calves born in fall 2004. Therefore, the only dependent variable available for these calves was birth weight. In addition, calves born in spring 2004 were transported to Texas A & M University for a feed efficiency study after collection of d-56 measurements. Calves born in spring 2005 were also transported to Texas A & M after weaning. Therefore, numbers of observations available for this study were 2,122, 2,051, and 2,125 for IGF-I concentration at d 28, 42, and 56, respectively, of the postweaning period, 2,182 for mean IGF-I concentration of each calf, 2,507 for birth weight, 2,114 for weaning weight, and ranged from 2,056 to 2,190 for postweaning BW and BW gains. Fewer observations were available at d 42 because BW and blood samples were not taken at that time for calves born in spring 1989. In addition, serum samples for heifers born in spring 1990 were damaged due to a freezer malfunction, which necessitated resampling of the heifers at d 84, 98, and 112 of the postweaning period. The d 84, 98, and 112 IGF-I concentrations were used to calculate the mean IGF-I values of these heifers. The resampling likely resulted in greater mean IGF-I concentrations for the heifers born in spring 1990 than would have been observed if the d 28, 42, and 56 serum samples had been available for analysis, based on the postweaning increases in serum IGF-I concentration observed in bulls and heifers by Bishop (1991). Therefore, 2,182 observations were available for mean IGF-I concentration, but fewer numbers of observations were available for IGF-I concentration on d 28, 42, and 56. On rare occasions, glass tubes were broken during centrifugation, which also contributed to differing numbers of observations for IGF-I concentrations on d 28, 42, and 56, and for mean IGF-I concentration.
Inbreeding depression estimates for insulin-like growth factor I
Collection of Blood Samples and Determination of IGF-I Concentration Approximately 25 mL of blood was collected into sterile 16- × 150-mm glass tubes via jugular venipuncture of each animal. The blood was allowed to clot for 24 h at 4°C. Serum was obtained by centrifugation (1,800 × g for 20 min at room temperature) and frozen at −20°C until it was assayed. The RIA for IGF-I concentration was performed at the University of Florida using antiserum raised against human IGF-I in rabbits (UBK487), following procedures described by Bishop et al. (1989).
Statistical Analysis Inbreeding coefficients of calves (calf F) and their dams (dam F) were obtained using PROC INBREED (SAS Inst. Inc., Cary, NC). Pedigrees of base population animals were traced back 3 generations for the calculation of inbreeding coefficients. The average generation coefficient of the calves born in spring 2005 was 5.24. General linear models procedures (PROC GLM; SAS) were used to derive least squares means and SE for calf F and dam F by year. The statistical model included fixed effects of birth year of calf (1989 through 2005), season of birth (spring vs. fall), selection line (high vs. low IGF-I), sex of calf (bull, heifer, or steer), and age of dam (2, 3, 4, 5 to 9, ≥10 yr). Two- and 3-way interactions involving year, season, and line were tested for significance. Annual rate of inbreeding was also evaluated by regressing calf F and dam F on birth year of calf. Slopes of the linear regression lines were tested for significant differences between selection lines, as well as between seasons of birth. Seasonal effects were tested because different bulls were used for breeding in each season. The distribution of inbreeding levels over the course of the entire selection experiment and during the final year of the study was determined by assigning calves and dams to 1 of 5 inbreeding groups: F = 0; 0 < F ≤ 6.25; 6.25 < F ≤ 12.5; 12.5 < F ≤ 25; or F > 25. To determine effects of calf F and dam F on IGF-I concentration at the various time points, BW, and BW gains, the data were analyzed using an animal model with a set of multiple trait, derivative-free REML (MTDFREML) computer programs written by Boldman et al. (1993). Pedigrees of base population animals were traced back 3 generations to create the numerator relationship matrix. A total of 3,243 animals were included in the A−1 matrix. The model for these analyses included fixed effects of birth year of calf, season of birth, IGF-I selection line, sex of calf, and age of dam, and random animal, maternal genetic, and maternal permanent environmental effects, as well as linear covariates for age of calf (omitted in analysis of birth weight), calf F, and dam F. Maternal genetic and maternal permanent environmental effects were deleted from the final model if determined by likelihood ratio
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tests to be unimportant sources of variation for a given trait. Significance of the regression coefficients for the regression of the dependent variables on calf F and dam F was determined using t-tests with n – 2 df. Convergence was declared when the change in the variance of the simplex between successive rounds of iteration was less than 10−9. Cold restarts of the MTDFREML programs were performed using the converged values to ensure that the log-likelihood was the global, and not a local, maximum. Restarts were performed until −2 times the log-likelihood values used in the simplex search algorithm did not change to the second decimal place from one restart to the next.
RESULTS AND DISCUSSION The number of observations, simple means, SD, and coefficients of variation for serum IGF-I concentrations, weaning age, on-test age, BW, BW gains, calf F, and dam F are presented in Table 1.
Inbreeding Levels in IGF-I Selection Lines Over the course of the entire selection experiment, the calf F averaged 3.3% (SD = 3.1%) and ranged from 0.0 to 25.2%, whereas the dam F averaged 1.8% (SD = 2.7%) and varied from 0.0 to 25% (Table 1). Least squares means (±SE) for calf F and dam F by year are shown in Table 2. Mean inbreeding levels in 2005 were 6.82 ± 0.38% and 4.20 ± 0.36% for calves and dams, respectively. The year × line interaction was highly significant (P = 0.009) for calf F due to changes in rank of the high and low lines from year to year. Therefore, yearly means for calf F are presented separately by high and low IGF-I selection lines in Table 3. In addition, the line × season interaction was significant (P = 0.049) for dam F. The mean dam F was greater in the fall than in the spring for the high IGF-I line, whereas the opposite was true for the low IGF-I line (Table 4). The high line had a greater average dam F than the low line in the spring- and fall-calving herds, but the magnitude of the difference was greater in the fall herd. Line differences in inbreeding levels were not significant for calf F (P = 0.27 and 0.57 for 2005-spring calves and 2004-fall calves, respectively) or dam F (P = 0.57 and 0.65 for 2005-spring calves and 2004-fall calves, respectively) when values from the final year of the study were analyzed separately by season (Table 5). Annual rates of increase in inbreeding coefficients of calves and dams were 0.36 ± 0.01 (P < 0.0001) and 0.25 ± 0.01%/yr (P < 0.0001), respectively. The slopes of the regression lines for calf F differed by season of birth (0.33 ± 0.02%/yr for spring vs. 0.40 ± 0.02%/yr for fall; P < 0.01). The distributions of inbreeding coefficients of calves and dams over all years of the study are presented in Table 6. Most calves and dams (74.7% of calves and 63.3% of dams) had inbreeding coefficients between 0 and 0.0625. Forty-six calves (1.8% of the total) and 22
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Table 2. Least squares means (±SE) for inbreeding coefficients by year Year
n
1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005
82 135 144 161 155 162 170 170 165 169 181 164 176 169 121 125 62
1 2
CALFF,1 %
DAMF,2 %
1.56 1.23 1.90 2.07 2.17 2.11 2.76 3.54 3.35 3.96 4.49 4.88 5.28 5.63 5.40 6.39 6.82
0.77 0.84 0.78 0.88 1.30 1.14 1.55 1.59 1.84 2.20 2.60 2.84 3.19 3.58 4.05 4.22 4.20
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.34 0.28 0.28 0.27 0.27 0.27 0.26 0.27 0.27 0.27 0.26 0.27 0.26 0.27 0.26 0.29 0.38
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.32 0.27 0.26 0.25 0.25 0.25 0.25 0.25 0.25 0.25 0.25 0.25 0.25 0.25 0.25 0.27 0.36
CALFF = inbreeding coefficient of calf. DAMF = inbreeding coefficient of dam.
dams (0.9% of the total) had inbreeding coefficients between 0.125 and 0.25, whereas only 1 calf and 0 dams had inbreeding coefficients exceeding 0.25. Distributions of inbreeding coefficients in the final year of the study are shown in Table 7. The most frequent calf F class for the fall 2004 calves (55.3% of the total) was 0.0625 to 0.125, whereas the class with the greatest frequency for the spring 2005 calves (61.3% of the total) was 0 to 0.0625. The most frequent dam F class was from 0 to 0.0625 for both the fall 2004 and spring 2005 groups (76.3 and 83.9%, respectively).
Inbreeding Depression for IGF-I Estimates of inbreeding depression are presented in Table 8. Insulin-like growth factor I concentration at
d 28, 42, and 56 of the 140-d postweaning test and mean IGF-I concentration decreased by 0.62 ± 0.88, 1.86 ± 0.96, 1.92 ± 0.89, and 1.48 ± 0.76 ng/mL per 1% increase in inbreeding of calf. Only the regression coefficient for IGF56 differed significantly from zero, although the regression coefficients for IGF42 and mean IGF-I approached significance (P < 0.10). Increases in inbreeding levels of the dams also resulted in reduced IGF-I concentrations, although the regression coefficients were not significantly different from zero (P > 0.10). The lack of an inbreeding of dam effect on IGFI concentration is not surprising given that the blood samples were collected during the postweaning period. To the knowledge of the authors, no previous estimates of inbreeding depression for IGF-I are available in the literature.
Table 3. Least squares means (±SE) for calf inbreeding (%) by line-year subclass1 Year
n
1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005
44 75 70 85 80 88 88 85 86 84 87 88 89 81 62 64 36
1
High 1.27 1.39 2.14 2.12 2.24 2.12 2.41 3.44 3.07 4.20 4.12 4.79 4.79 5.93 4.62 6.63 7.20
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.44 0.35 0.36 0.33 0.34 0.33 0.33 0.33 0.33 0.34 0.33 0.33 0.33 0.34 0.35 0.37 0.48
Significance level for line × year interaction; P = 0.0089.
n 38 60 74 76 75 74 82 85 79 85 94 76 87 88 59 61 26
Low 1.87 1.02 1.69 2.03 2.11 2.10 3.15 3.65 3.66 3.74 4.85 4.99 5.78 5.37 6.20 6.15 6.28
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.47 0.38 0.35 0.35 0.35 0.35 0.34 0.33 0.34 0.33 0.32 0.35 0.33 0.33 0.36 0.38 0.55
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Inbreeding depression estimates for insulin-like growth factor I 1
Table 4. Least squares means (±SE) for dam inbreeding (%) by line-season subclass Season
n
High
n
Low
Spring Fall
696 596
2.20 ± 0.17 2.54 ± 0.18
668 551
2.06 ± 0.17 2.01 ± 0.18
1
Significance level for line × season interaction; P = 0.0489.
Inbreeding Depression for Growth Traits Inbreeding depression for growth traits in beef cattle and other species has been well documented (e.g., Burrow, 1993), but estimates are reported here for comparison purposes with those obtained for serum IGF-I concentrations. Inbreeding of calf had a positive, though nonsignificant (P > 0.10), effect on birth weight. Inbreeding of calf had highly significant (P < 0.01) negative effects on all other BW and BW gain traits examined, with regression coefficients ranging from −0.74 ± 0.20 kg/% increase in calf F for postweaning BW gain to −1.68 ± 0.33 kg/% increase in calf F for off-test BW (i.e., BW at the end of the 140-d postweaning test). The regression coefficients for the BW traits became increasingly negative with advancing age, in agreement with the results for IGF-I. In a review of several inbreeding studies conducted in the 1940s, 1950s, and 1960s, Brinks and Knapp (1975) also concluded that inbreeding of calf is associated with reduced growth rates, particularly during the preweaning period. Smaller detrimental inbreeding effects were apparent for birth weight and postweaning growth. In a review of inbreeding effects in beef cattle, Burrow (1993) reported that the inbreeding of a calf had a consistent adverse effect on growth traits with an increase of 1% in inbreeding resulting in a decrease of 0.06, 0.44, 0.69, and 1.30 kg in BW at birth, weaning, 1 yr, and maturity, respectively. Therefore, the negative effects of inbreeding on BW of calf increased with age in agreement with the findings of the current study. Gengler et al. (1998) reported a decline in postweaning BW gain of 0.24 kg per percentage increase in inbreeding of Limousin calves. In a recent study, Carolino and Gama (2008) found that regression coefficients of performance traits on inbreeding in the Alentejana breed were small, indicating a minor, but detrimental, effect of individual inbreeding on most traits. The traits with the greatest percentage impact
of individual inbreeding were total number of calvings throughout life and calf BW at 3 mo of age. Inbreeding of dam had a significant negative effect on birth weight of progeny and tended to have a negative effect on postweaning BW gain (P < 0.10; Table 8). Preweaning BW gain of the progeny and BW other than birth weight were not influenced by increases in dam F. In summarizing several inbreeding studies, Burrow (1993) reported that inbreeding of dam decreased weaning and yearling weights by 0.30 and 0.21 kg for each 1% increase in inbreeding, suggesting decreased milk yield in inbred dams, whereas the effect of inbreeding of the dam on birth weight was inconsistent and overall was near zero. Brinks and Knapp (1975), based on several early inbreeding studies, also concluded that inbreeding of dam had little effect on birth weight of calves, but had a sizeable detrimental effect on preweaning BW gain and weaning weight. Inbreeding of dam had little effect, or possibly even a compensatory effect, on postweaning BW gain of calves. Most studies have shown that inbreeding has a negative effect on milk production of dairy cows, particularly during the first lactation (Brinks and Knapp, 1975; Burrow, 1993; Smith et al., 1998; Cassell et al., 2003). Carolino and Gama (2008) found that the greatest effect of maternal inbreeding in the Alentejana breed was on calf BW at 3 mo of age. In the present study, inbreeding of calf had highly significant (P < 0.01) negative effects on all BW and BW gains other than birth weight, whereas inbreeding of dam had nonsignificant effects on all BW and BW gains except birth weight. MacNeil et al. (1992) reported that inbreeding of a calf had more than 7 times greater negative effect on birth weight than inbreeding of dam in Line 1 Herefords. On the other hand, inbreeding of dam had more than 7 times greater negative effect on preweaning daily BW gain than inbreeding of calf. However, MacNeil et al. (1992) pointed out
Table 5. Least squares means (±SE) for calf and dam inbreeding at the end of the study Year – season
Line
n
CALFF,1 %
DAMF,2 %
2005 – spring 2004 – fall
High Low High Low
36 26 41 35
P = 0.27 6.22 ± 0.60 5.22 ± 0.74 P = 0.57 7.41 ± 0.52 7.02 ± 0.60
P = 0.57 4.39 ± 0.49 3.96 ± 0.61 P = 0.65 4.56 ± 0.52 4.23 ± 0.60
1 2
CALFF = inbreeding coefficient of calf. DAMF = inbreeding coefficient of dam.
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Table 6. Distribution of inbreeding coefficients (all years) Inbreeding level F=0 0 < F ≤ 0.0625 0.0625 < F ≤ 0.125 0.125 < F ≤ 0.25 F > 0.25 Total
CALFF1
DAMF2
211 1,876 377 46 1 2,511
741 1,590 158 22 0 2,511
0.18 observed by Herd et al. (1995) at birth; 0.32 ± 0.06 by Johnston et al. (2001) at 8 to 10 mo of age; 0.34 ± 0.09 and 0.43 ± 0.12 by Johnston et al. (2002) at 9 and 22 mo, respectively, in cattle fed at 2 different locations in Australia; and 0.32 ± 0.06 at weaning (average age = 201 d) and 0.30 ± 0.07 during the postweaning period (average age = 310 d) by Moore et al. (2005) in Angus seedstock cattle fed on pasture in Australia. Results from the present and previous studies provide ample evidence that serum IGF-I concentration is moderately to highly heritable in beef cattle. Estimates of hd2 for BW ranged from 0.32 ± 0.06 for birth weight to 0.43 ± 0.06 for weaning weight (Table 9). Estimates of hd2 for BW gain from birth to weaning and from d 0 to 140 of the postweaning period were 0.42 ± 0.06 and 0.39 ± 0.07, respectively. These estimates of direct heritability of BW and BW gains generally agree well with average estimates from many studies as summarized by Woldehawariat et al. (1977), Mohiuddin (1993), and Koots et al. (1994a). Results of the current study indicated that the direct heritability of IGF-I was similar to that of weaning weight, postweaning BW, and pre- and postweaning BW gain. Therefore, it might be expected that serum IGF-I concentration would experience a similar degree of inbreeding depression as BW and BW gain traits. Estimates of maternal heritability (hm2) were 0.14 ± 0.04, 0.15 ± 0.05, 0.09 ± 0.04, and 0.16 ± 0.05 for IGFI concentration at d 28, 42, and 56 of the postweaning test, and for mean IGF-I concentration, respectively (Table 9). These estimates are similar to those reported by Davis and Simmen (2006), and indicate that postweaning IGF-I concentration is determined more by the genetic characteristics of the calf than by those of the dam. Estimates of maternal heritabilities of BW traits varied from 0.03 ± 0.03 for off-test BW to 0.17 ± 0.05 for birth weight. Mohiuddin (1993) and Koots et al. (1994a) also found low hm2 for birth, weaning, and yearling BW. In the present study, estimates of hm2 were 0.13 ± 0.05 for BW gain from birth to weaning and 0.02 ± 0.03 for BW gain during the postweaning test. In agreement with the results of Davis and Simmen (2006), the proportion of phenotypic variance due to permanent environmental effects of the dam (c2) was
1
CALFF = inbreeding of calf. DAMF = inbreeding of dam.
2
that results for Line 1 Herefords were somewhat atypical when compared with those of 48 inbred lines of beef cattle from 10 experiment stations located in 8 western states that participated in the W-1 Regional Beef Cattle Breeding Project and were summarized by Brinks and Knapp (1975). In their analysis, the linear effect of inbreeding of a calf was highly significant for preweaning growth traits in both sexes, except for birth weight in females, in which case the effect was significant. Inbreeding of male calves was significant for initial BW and highly significant for ADG on test and for final BW off test. Inbreeding of heifers had negative, though nonsignificant, effects on the postweaning traits. The linear effect of inbreeding of dam was highly significant for preweaning ADG and weaning weight in both sexes, but was nonsignificant for birth weight in both sexes. Inbreeding of dam had nonsignificant effects on postweaning growth traits for both sexes. Inbreeding of dam had a greater effect for male calves, but a slightly smaller effect for females, than inbreeding of calf for preweaning ADG and weaning weight. Inbreeding of calf had a much larger effect than inbreeding of dam on postweaning BW gain and final BW. Estimates of heritabilities obtained for serum IGF-I concentration are shown in Table 9. Direct heritability (hd2) of IGF-I concentration at d 28, 42, and 56 of the postweaning test and of mean IGF-I concentration was 0.41 ± 0.07, 0.41 ± 0.07, 0.33 ± 0.06, and 0.46 ± 0.07, respectively. These estimates agree well with those obtained by Davis and Simmen (2006) using data from earlier years of the same selection experiment. The estimates are somewhat larger than the values of 0.31 ±
Table 7. Distribution of inbreeding coefficients (final year of study) CALFF1 Inbreeding level
Fall 2004
Spring 2005
Fall 2004
Spring 2005
3 28 42 3 0 76
0 38 21 3 0 62
3 58 14 1 0 76
0 52 10 0 0 62
F=0 0 < F ≤ 0.0625 0.0625 < F ≤ 0.125 0.125 < F ≤ 0.25 F > 0.25 Total 1
CALFF = inbreeding of calf. DAMF = inbreeding of dam.
2
DAMF2
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Inbreeding depression estimates for insulin-like growth factor I
Table 8. Estimates of inbreeding depression due to inbreeding of calf and inbreeding of dam CALFF1 Reg. coeff.3 ± SE
Trait 4
IGF28, ng/mL IGF42, ng/mL IGF56, ng/mL Mean IGF-I,5 ng/mL Birth wt, kg Weaning wt, kg On-test BW, kg d 28 BW, kg d 42 BW, kg d 56 BW, kg Off-test BW, kg Preweaning BW gain, kg Postweaning BW gain, kg
−0.62 −1.86 −1.92 −1.48 0.04 −0.87 −0.97 −1.23 −1.31 −1.39 −1.68 −0.91 −0.74
± ± ± ± ± ± ± ± ± ± ± ± ±
0.88 0.96 0.89 0.76 0.03 0.20 0.22 0.25 0.26 0.27 0.33 0.19 0.20
DAMF2 t
Reg. coeff. ± SE
0.70 1.94† 2.16* 1.94† 1.11 4.42** 4.45** 5.00** 4.98** 5.18** 5.10** 4.75** 3.66**
−1.19 −1.25 −0.55 −0.45 −0.11 0.13 0.01 0.01 0.05 0.09 −0.35 0.26 −0.37
± ± ± ± ± ± ± ± ± ± ± ± ±
0.95 1.05 0.98 0.85 0.04 0.33 0.36 0.39 0.40 0.41 0.45 0.32 0.22
t 1.25 1.19 0.57 0.53 2.53* 0.40 0.04 0.04 0.11 0.21 0.79 0.80 1.71†
1
CALFF = inbreeding of calf. DAMF = inbreeding of dam. 3 Reg. coeff. = regression coefficient. 4 IGF28, IGF42, and IGF56 represent serum IGF-I concentration at d 28, 42, and 56, respectively, of the postweaning test. 5 Mean IGF-I is the average of serum IGF-I measurements for a given calf. †P < 0.10. *P < 0.05. **P < 0.01. 2
zero for all measures of IGF-I (Table 9). Estimates of c2 were near zero for birth weight, 0.23 ± 0.04 for weaning weight, 0.22 ± 0.04 for on-test BW, and then declined to 0.09 ± 0.03 for off-test BW. In his review, Mohiuddin (1993) found that estimates of c2 averaged 0.03, 0.07, and 0.03 for birth, weaning, and yearling weight, respectively. Correlations between direct and maternal genetic effects (ram) were large and negative for all measures of IGF-I (ram ≥ −0.87) and for all BW (ram ≥ −0.48) and BW gain (ram ≥ −0.77) traits other than birth weight (Table 9). Studies summarized by Mohiuddin (1993)
reported that ram averaged −0.35, −0.15, and −0.26 for birth, weaning, and yearling BW, respectively. Koots et al. (1994b) found that ram averaged −0.27 for birth weight and −0.30 for weaning weight. The large directmaternal correlations in the present study may have been due, in part, to the relatively small maternal variances, which may have been a result of the selection criterion employed (i.e., serum IGF-I concentration during the postweaning period). The direct-maternal covariances and the proportions of total phenotypic variance accounted for by these covariances are shown in Table 9. The covariance between direct and mater-
Table 9. Parameter estimates (±SE) for serum IGF-I concentrations, BW, and BW gains derived from the full animal model1 Trait IGF282 IGF42 IGF56 Mean IGF-I3 Birth wt Weaning wt On-test wt d 28 BW d 42 BW d 56 BW Off-test BW Preweaning BW gain Postweaning BW gain
σ2p 11,385.1 13,338.6 11,855.7 9,070.5 19.8 687.2 835.0 1,038.9 1,110.4 1,193.9 1,709.2 646.1 620.0
h2d 0.41 0.41 0.33 0.46 0.32 0.43 0.36 0.39 0.39 0.39 0.41 0.42 0.39
± ± ± ± ± ± ± ± ± ± ± ± ±
0.07 0.07 0.06 0.07 0.06 0.06 0.06 0.06 0.06 0.06 0.07 0.06 0.07
h2m 0.14 0.15 0.09 0.16 0.17 0.13 0.11 0.10 0.09 0.10 0.03 0.13 0.02
± ± ± ± ± ± ± ± ± ± ± ± ±
0.04 0.05 0.04 0.05 0.05 0.05 0.05 0.05 0.05 0.05 0.03 0.05 0.03
c2 0.00 0.00 0.00 0.00 0.01 0.23 0.22 0.18 0.17 0.14 0.09 0.25 0.00
± ± ± ± ± ± ± ± ± ± ± ± ±
ram 0.02 0.02 0.02 0.02 0.03 0.04 0.04 0.03 0.04 0.03 0.03 0.04 0.02
−0.92 −0.90 −0.87 −0.90 −0.27 −0.71 −0.66 −0.57 −0.52 −0.56 −0.48 −0.77 −1.00
± ± ± ± ± ± ± ± ± ± ± ± ±
0.06 0.07 0.09 0.06 0.15 0.12 0.14 0.16 0.18 0.15 0.29 0.12 0.36
covam
covam/σ2p
−2,516.9 −2,930.3 −1,743.0 −2,235.3 −1.3 −118.0 −108.3 −114.8 −104.7 −131.2 −88.7 −117.3 −61.3
0.22 0.22 0.15 0.25 0.07 0.17 0.13 0.11 0.09 0.11 0.05 0.18 0.10
1 2 σ p = phenotypic variance; h2d = heritability (direct effect); h2m = maternal heritability; c2 = proportion of phenotypic variance due to permanent environmental effect of dam; ram = correlation between direct and maternal effects; covam = covariance between direct and maternal effects. 2 IGF28, IGF42, and IGF56 represent serum IGF-I concentration at d 28, 42, and 56, respectively, of the postweaning test. 3 Mean IGF-I is the average of serum IGF-I measurements for a given calf.
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Davis and Simmen
nal genetic effects accounted for less than 25% of the total variance in each trait, even though the values for ram were large. The large direct-maternal correlations may also have been an artifact of the divergent selection for IGF-I. Insulin-like growth factor I is known to be associated with several physiological processes in addition to those that lead to growth. For example, IGF-I is a growth factor for the immune system, increasing lymphocyte number and function via greater lymphocyte generation and survival (Clark, 1997; Hinton et al., 1998). Clark (1997) put forth the hypothesis that the anabolic hormones (GH, prolactin, and IGF), which regulate whole body growth, metabolism, tissue repair, and cell survival, also play an integrating role in the growth, maintenance, repair, and function of the immune system. Results of this analysis indicate that postweaning serum IGF-I concentration is a moderately heritable trait. Estimates of direct heritability of IGF-I concentration at d 28, 42, and 56 of the postweaning test and of mean IGF-I concentration were 0.41 ± 0.07, 0.41 ± 0.07, 0.33 ± 0.06, and 0.46 ± 0.07, respectively. Inbreeding depression generally shows an inverse relationship with the heritability of traits (i.e., lowly heritable traits exhibit the most inbreeding depression and highly heritable traits exhibit the least inbreeding depression; Bourdon, 2000). Therefore, it might be expected that a moderately heritable characteristic, such as serum IGF-I concentration, would exhibit intermediate levels of inbreeding depression. This seemed to be the case in the current study because increases in inbreeding of calf tended to result in reduced postweaning serum IGF-I concentrations. For example, mean IGF-I concentration decreased by 1.48 ± 0.76 ng/mL per 1% increase in inbreeding of calf, which was significant at the P < 0.10 level. Inbreeding of calf also resulted in highly significant reductions in all BW and BW gain traits examined other than birth weight; regression coefficients ranged from −0.74 ± 0.20 kg/% increase in calf inbreeding for postweaning BW gain to −1.68 ± 0.33 kg/% increase in calf inbreeding for off-test BW. Increases in inbreeding of dam were associated with reduced, albeit nonsignificant, IGF-I concentrations, as well as reductions in birth weight (P < 0.05) and postweaning BW gain (P < 0.10). Therefore, reduced serum IGF-I concentrations may be a contributing factor to the declines in BW and BW gains that are typically associated with increases in inbreeding levels within populations.
LITERATURE CITED Bishop, M. D. 1991. Insulin-like growth factor I in beef cattle: Gene location, repeatability of measurement and criteria for selection. PhD Diss. The Ohio State Univ., Columbus. Bishop, M. D., R. C. M. Simmen, F. A. Simmen, and M. E. Davis. 1989. The relationship of insulin-like growth factor-I with postweaning performance in Angus beef cattle. J. Anim. Sci. 67:2872–2880. Boldman, K. G., L. A. Kriese, L. D. Van Vleck, and S. D. Kachman. 1993. A Manual for Use of MTDFREML. A Set of Programs
to Obtain Estimates of Variances and Covariances [DRAFT]. ARS, USDA, Washington, DC. Bourdon, R. M. 2000. Understanding Animal Breeding. 2nd ed. Prentice-Hall Inc., Upper Saddle River, NJ. Brinks, J. S., and B. W. Knapp. 1975. Effects of inbreeding on performance traits of beef cattle in the western region. Technical Bulletin 123. Colorado State Univ. Exp. Stn., Fort Collins. Burrow, H. M. 1993. The effects of inbreeding in beef cattle. Anim. Breed. Abstr. 61:737–751. Carolino, N., and L. T. Gama. 2008. Inbreeding depression on beef cattle traits: Estimates, linearity of effects and heterogeneity among sire-families. Genet. Sel. Evol. 40:511–527. Cassell, B. G., V. Adamec, and R. E. Pearson. 2003. Effect of incomplete pedigrees on estimates of inbreeding and inbreeding depression for days to first service and summit milk yield in Holsteins and Jerseys. J. Dairy Sci. 86:2967–2976. Clark, R. 1997. The somatogenic hormones and insulin-like growth factor-1: Stimulators of lymphopoiesis and immune function. Endocr. Rev. 18:157–179. Davis, M. E., and R. C. M. Simmen. 2006. Genetic parameter estimates for serum insulin-like growth factor I concentrations, and body weight and weight gain in Angus beef cattle divergently selected for serum insulin-like growth factor I concentration. J. Anim. Sci. 84:2299–2308. D’Ercole, A. J., A. D. Stiles, and L. E. Underwood. 1984. Tissue concentrations of somatomedin-C: Further evidence for multiple sites of synthesis and paracrine or autocrine mechanisms of actions. Proc. Natl. Acad. Sci. USA 81:935–939. Gengler, N., I. Misztal, J. K. Bertrand, and M. S. Culbertson. 1998. Estimation of the dominance variance for postweaning gain in the U.S. Limousin population. J. Anim. Sci. 76:2515–2520. Herd, R. M., P. F. Arthur, K. Zirkler, C. Quinn, and V. H. Oddy. 1995. Heritability of IGF-1 in beef cattle. Page 694 in Proc. Aust. Assoc. Anim. Breed. Genet. Univ. Adelaide, Adelaide, South Australia, Australia. Hinton, P. S., C. A. Peterson, E. M. Dahly, and D. M. Ney. 1998. IGF-I alters lymphocyte survival and regeneration in thymus and spleen after dexamethasone treatment. Am. J. Physiol. Regul. Integr. Comp. Physiol. 274:R912–R920. Johnston, D. J., R. M. Herd, M. J. Kadel, H.-U. Graser, P. F. Arthur, and J. A. Archer. 2002. Evidence of IGF-I as a genetic predictor of feed efficiency traits in beef cattle. Proc. 7th World Congr. Genet. Appl. Livest. Prod., Montpellier, France, CDROM Commun. No. 10-16. Johnston, D. J., R. Herd, A. Reverter, and V. H. Oddy. 2001. Heritability of IGF-I in beef cattle and its association with growth and carcase traits. Pages 163–166 in Proc. Assoc. Adv. Anim. Breed. Genet., Queenstown, New Zealand. Koots, K. R., J. P. Gibson, C. Smith, and J. W. Wilton. 1994a. Analyses of published genetic parameter estimates for beef production traits. 1. Heritability. Anim. Breed. Abstr. 62:309– 338. Koots, K. R., J. P. Gibson, and J. W. Wilton. 1994b. Analyses of published genetic parameter estimates for beef production traits. 2. Phenotypic and genetic correlations. Anim. Breed. Abstr. 62:825–853. Kristensen, T. N., and A. C. Sorensen. 2005. Inbreeding—Lessons from animal breeding, evolutionary biology and conservation genetics. Anim. Sci. 80:121–133. MacNeil, M. D., J. J. Urick, S. Newman, and B. W. Knapp. 1992. Selection for postweaning growth in inbred Hereford cattle: The Fort Keogh, Montana line 1 example. J. Anim. Sci. 70:723– 733. Mohiuddin, G. 1993. Estimates of genetic and phenotypic parameters of some performance traits in beef cattle. Anim. Breed. Abstr. 61:495–522. Moore, K. L., D. J. Johnston, H.-U. Graser, and R. Herd. 2005. Genetic and phenotypic relationships between insulin-like growth factor-I (IGF-I) and net feed intake, fat, and growth traits in Angus beef cattle. Aust. J. Agric. Res. 56:211–218.
Inbreeding depression estimates for insulin-like growth factor I Murphy, L. J., G. I. Bell, and H. G. Friesen. 1987. Tissue distribution of insulin-like growth factor I and II messenger ribonucleic acid in the adult rat. Endocrinology 120:1279–1282. Smith, L. A., B. G. Cassell, and R. E. Pearson. 1998. The effects of inbreeding on the lifetime performance of dairy cattle. J. Dairy Sci. 81:2729–2737. Weigel, K. A. 2001. Controlling inbreeding in modern breeding programs. J. Dairy Sci. 84 (E. Suppl.):E177–E184. Weigel, K. A., and S. W. Lin. 2002. Controlling inbreeding by constraining the average relationship between parents of young
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bulls entering AI progeny test programs. J. Dairy Sci. 85:2376– 2383. Woldehawariat, G., M. A. Talamantes, R. R. Petty Jr., and T. C. Cartwright. 1977. A summary of genetic and environmental statistics for growth and conformation characters of young beef cattle (2nd ed.). Texas Agric. Exp. Stn. Tech. Rep. 103. Texas A&M Univ., College Station.
