REALIZED HERITABILITY ESTIMATES IN BOARS DIVERGENTLY SELECTED FOR TESTOSTERONE LEVELS
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1 Running Head: Divergent selection for testosterone REALIZED HERITABILITY ESTIMATES IN BOARS DIVERGENTLY SELECTED FOR TESTOSTERONE LEVELS D. Lubritz, B. Johnson and O.W. Robison North Carolina State University, Raleigh, Abstract Data were collected from 1982 through 1992 from 100 sires and 891 Duroc boars. Testosterone production was measured from peripheral blood samples before (PRE) and after (POST) GnRH challenge. Additionally, data were collected on testes volume at 168 d (TVOL), days to 104 kg (DAYS104), number born alive (NBA) and backfat adjusted to 104 kg body weight (FAT). Realized heritabilities were estimated from the regression of response on cumulative selection differentials. Heritabilities for POST were. 15 and.24 in the low and high lines, respectively. This compares to the estimate of.26 from sire-son regressions. The regression of other traits on cumulative selection differentials can be viewed as realized correlated responses to selection. After 10 generations, the high line was approximately three times the low line for both PRE and POST levels of testosterone. Selection for increased POST would be expected to increase PRE, DAYS 104, and NBA while decreasing FAT and TVOL. Selection for decreased POST should decrease PRE, FAT, NBA and TVOL while increasing DAYS 104. Key Words (boars, selection, testosterone) Introduction The production of faster growing, more feed efficient, leaner pigs is of primary interest in the swine industry. Boars grow faster, convert feed more efficiently and grade le_er than barrows. The higher rate of gain seen in intact males relative to castrates is related to differences in endogenous testosterone levels (Gotsema et al., 1974). Positive correlations exist between growth and blood concentrations of testosterone (Lubritz et al., 1991). The early determination of testosterone levels in addition to other criteria represents a novel approach in identifying superior breeding animals. The potential impact of intense selection for male traits on reproductive and(or) production efficiency in swine is largely overlooked. Female reproductive traits are lowly 53
2 heritable, but moderate to high heritabilities have been reported for testosterone and testicular measures in boars (Legault et al., 1979; Toelle et al., 1984; Robison, 1986; and Lubritz et al., 1991). It seems likely that some predictor traits in the male can be identified to aid in selection for female reproduction. Land (1973) suggested the existence of favorable genetic associations between male testicular and female reproductive traits based on knowledge that the pituitary hormones stimulating the gonads are the same for both sexes. Additionally the steroidogenic pathways involved in synthesis of estrogens are the same as those for testosterone (Ewing and Brown, 1977), while theca and granulosa cells have roles analagous to leydig and sertoli cells (Tepperman, 1980). Selection intensity is much higher in the male than in the female, and if moderate favorable genetic corrlations between measures of male and female reproduction exist, it could lead to very large rates of genetic progress compared to female selection only. This experiment was designed to investigate the possibility of changing the concentration of testosterone in the blood of boars by divergen.t selection, and to evaluate the realized responses of various production and reproductive traits to this selection. Materials and Methods Data were obtained from 100 sires and 891 Duroc boars over the period 1982 to 1992 at North Carolina State University, Raleigh. These boars represented part of two fines in a study of divergent selection for high and low testosterone response to GnRH challenge. Each generation, blood samples were obtained from fifty boars (25 from each line). An indwelling catheter was inserted into the jugular vein. Over an 8 h period, 10 ml blood samples were drawn from the jugular vein via the catheter. Between 0700 and 0900, one blood sample was drawn every 30 min from each boar. These were the five pre-gnrh testosterone measures (PRE). After the 0900 bleeding, the GnRH challenge was given. From 0900 to 1100, boars were bled every 15 min. These constitute eight of the twelve post-gnrh testosterone samples (POST). The remainder of the post-gnrh samples were drawn every 30 min from 1100 to The PRE value was the area under the curve for basal levels, and POST was the area under the curve for 4 h after the GnRH challenge. Area under the curve was measured in nanogram,_milfiliter" Xohourl. The five boars with the highest and lowest post-gnrh testosterone levels were selected as sires for the next generation. Concentrations of testosterone were determined in duplicate 100 #1 aliquots of serum by a previously validated RIA procedure (Juniewicz et al., 1984). Testosterone was extracted from serum using anhydrous ethyl ether, with an average recovery of > 95 %. Testosterone was measured against standard curves of recrystallized 17/3-hydroxy-4- androsten-3-one, which ranged from 0 to 4 ng. Measures for testes length (TL168), testes width (TW168), and testes volume (TVOL) were taken at 168 d of age. Testes volume was estimated as TVOL = (TW168/2) 2 * TL168. Growth data were collected for days to 104 kg (DAYS104). Backfat depth was measured by ultrasound behind the shoulder at the seventh rib and at the middle of the loin approximately 3.8 cm off the midline, and adjusted to 104 kg BW (FAT) (Robison, 1981). 54
3 Son-sire regressions were estimated for all traits. Realized heritabilities were estimated from the linear regression of response on cumulative selection differentials. Results and Discussion Estimates of heritabilities and genetic correlations from sire-son regressions are presented in tables 1 and 2. These results suggest that all traits, except FAT are moderately heritable. Further the correlations point to increased testes size and growth rate with increased testosterone levels. Means for PRE and POST by line and generation are given in tables 3 and 4, respectively. By generation 10 both PRE and POST measures of testosterone production were about 3 times higher in the high line than in the low line. There was a positive association between means and variances in the two lines. Because we were unable to maintain a control it is impossible to determine if the response is asymmetrical. However it appears that, due to lower cumulative selection differentials (CSD) and lower estimated heritability in the low line, that more response was obtained in the high line. Realized heritabilities for POST are given in table 5 and the response of PRE and POST are presented graphically in Figures 1 and 2. The realized heritability in the high line is very close to that estimated from sire-son regression while that in the low line is somewhat lower. These estimates are considerably lower than the estimates of Bonneau and Sellier (1986) and Willeke et al. (1987) for 5a-androstenone (.61 and.56, respectively), but comfortably within the range of estimates reported by Toelle et al.(1984) and Eden et al. (1978) for testicular traits; Jonsson and Andresen (1979) for 5a-androstenone and Lubritz et al. (1991) for testosterone. The increase in testosterone production above generation zero in the low line was attributed to environmental trends and is accounted for by generation effects. Nevertheless, a pronounced difference in pre- and post-gnrh testosterone production existed at the end of the selection experiment. Selection response and selection differentials differed considerably between the two lines, and since the ratio between the two also differed, the realized heritabilities of the high and low lines differed accordingly (.24 and. 15, respectively). Cumulative selection differentials are in table 6. Actual CSD in the high line were approximately 2.7 times higher than CSD in the low line. Standardized CSD for the high line were about 1.4 times that of the low line (table 6). In order to illustrate how response was related to selection ifferential, response was expressed as a proportion of the selection differential. Because of differences in selection intensity both between generations and between lines, a more critical summary of selection responses was provided by plotting the generation means for POST against the standardized cumulative selection differentials. These responses expressed as deviations from the foundation 55
4 animals are shown in Figure 3. The average value of the ratio of response to selection differential (R/S) is the slope of the line, and equals the estimate of heritability in table 5. Perhaps the most interesting point about Figure 3 is that selection differentials were generally lower for the low testosterone line than for the high line. Standardized cumulative selection differentials were similar' between lines in the early generations, but began to diverge in later generations. Biological limits were approached in the later generations of selection for low testosterone production, resulting in delayed puberty, and poor libido. Thus the low end extremes could not be selected. Willeke et al. (1987) found similar results selecting for high and low levels of 5a-androstenone. These researchers also showed asymmetric response in the high and low line which was mainly caused by the very small selection differential in the low line and probably by the approach of the concentration to the absolute limit. Selection experiments for physiological traits have shown that selection response and differential response in high and low lines are influenced by the level of concentration at generation zero. If the physiological trait approaches a limit as in the low line of our study, the efficiency of selection is higher in the high line than in the low line. Least-squares means by line and generation are in tables 7 to 10 for TVOL, NBA, FAT and DAYS104, respectively. By generation 10, the high line had larger testes, larger litter size and fewer days. Because of a lack of a control line, it is not determined whether responses were asymmetrical. However the regressions in table 11 suggest more change in the low line. These results do not agree with those of Toelle et al. (1985) and Lubritz et al. (1991). Based on genetic correlations they suggested that increases in testicular and growth traits would occur concomittant with increased testosterone production. This study is the first to show differences in litter size of female relatives to boars with differing testosterone production. Tepperman (1980)discussed many similarities among male and female reproductive systems. Land (1973) suggested the existence of favorable genetic correlations among male testicular traits and female reproductive traits based on the knowledge that the pituitary hormones stimulating the gonads are the same for both sexes. Islam et al. (1976) reported improved ovulation rates in mice selected for increased testes size. In pigs, age at first farrowing and NBA were favorably correlated with 140 d testes measures (Toelle and Robison, 1985). Willeke et al. (1987) observed that boars selected for high levels of 5c_- androstenone had a significantly higher level of conjugated oestrogen than males of the low line. Willeke also observed that gilts of the high line exhibited first estrus 14 d earlier than gilts of the low line. Prior to the experiment it was expected that FAT would decrease in the high line. However this does not appear to be the case. The means presented suggest little if any change in the high line but a possible decrease in the low line. We have no satisfactory explanation for this. 56
5 Implications This study suggests that selection for testosterone production would be effective, and should favorably impact on growth. Also, the realized correlated responses in NBA suggest that selection for increased testosterone production should indirectly improve female reproduction. Female reproductive traits are lowly heritable, but the moderate heritabilities reported for testosterone in this study suggest it may be useful as a predictor trait to aid in selection for female reproduction. Literature Cited Bonneau, M. and P. Sellier Fat androstenone content and development of genital system in young Large White boars: Genetic aspects. World Rev. of Anim. Prod. 22:3. Ewing, L. L., and B. L. Brown Testicular steroidogenesis. In Johnson, A. D. and W. R. Gomes, (Ed.) The Testis: Vol. IV. Advances in physiology, biochemistry and function. Academic Press, New York. Falconer, D. S Patterns of response in selection experiments with mice. Cold Springs Harbor Symp. Quant. Biol. 20:178. Gotsema, S. R., J. A. Jacobs, R. G. Sasser, T. L. Gregory and R. C. Bull Effects of endogenous testosterone on production and carcass traits in beef cattle. J. Anim, Sci. 39:680. Hill W. G Estimation of realized heritabilities from selection experiments I. Divergent selection. Biometrics. 28:747. Islam, A. B. M. M., W. G. Hillard, and R. B. Land Ovulation rate of lines of mice selected for testes weight. Genet. Res. 27:23. Jonsson, P. and O. Andersen Experience during two generations of within lines boar performance testing, using 5a-androst-16-en-3-one and an olfactory judgement of boar taint. Ann. Genet. Sel. Anim. 11:241. Juniewicz, P. E., V. D. Toelle, O. W. Robison and B. H. Johnson Variation in testosterone production among boars and its relationship to sexual interest and breeding performance. Theriogenology. 22:259. Land, R. B The expression of female, sex-limited characters in the male. Nature. 241, 208. Legault, C., J. Gruand and F. Oulin Mise au point et interest genetique d'une methode d'appreciation sur le vivant du poids des testicles chez le jeune verrat. Jour. Rech. Porcine. en France. 1979,
6 Lubritz, D. L., B. Johnson and O. W. Robison Genetic parameters for testosterone production in boars. J. Anim. Sci. 69:3220. Robison, O. W Genetic control ofreproduction in non-ruminants: The male influence. Third WOrld Congress on Genetics Applied to Livestock Production. XI: 180. SAS SAS users guide: Statistics. SAS Inst., Cary, NC. Tepperman, J Metabolic and endocrine physiology. (4th Ed.) Year Book Medical Publishers, Chicago, IL. Toelle, V. D., B. H. Johnson and O. W. Robison Genetic parameters for testes traits in swine. J. Anim. Sci. 59:967. Toelle, V. D. and O. W. Robison Estimates of genetic relationships between testes measurements and female reproductive traits in swine. Zeitschrift fur Tierzuchtung und Zuchtungsbiologie. 102:125. Willeke, H., B. Claus, E. Miller, F. Pirchner and H. Karg Selection for high and low level of 5o_-androst-16-en-3-one in boars. J. Anita. Breed. Genet. 104:64. 58
7 Table 1. HERITABILITY ESTIMATES AND STANDARD ERRORS Trait" h2 SE PRE" POST FAT TVOL Day PRE = basal testosterone, POST = testosterone levels after GnRH, TVOL = testes volume at 168 days, DAY 104 = days to 104 kg, FAT = backfat adjusted to 104 kg. 59
8 Table 2. PHENOTYPICaAND GENETIC b CORRELATIONS Trait c Trait PRE POST TWI68 TLI68 TVOL DAY104 FAT PRE i *** *** *** *** + ns POST *** *** *** ns ms TWI *** *** *** ms TLI *** *** ns TVOL *** ns DAY ns a phenotypic correlations above the diagonal b genetic correlations below the diagonal _ P<.IO * P<.05 ** P<.01 *** P<
9 3. MEANS AND STANDARD DEVIATIONS FOR PRE-GnRH TESTOSTERONE LEVELS BY LINE AND GENERATION, Low Line High Line Generation Mean SD Mean SD Table 4. MEANS AND STANDARD DEVIATIONS FOR POST-GnRH TESTOSTERONE LEVELS BY LINE AND GENERATION Low Line High Line Generation Mean SD Mean SD
10 TABLE 5. REGRESSION OF PRE- AND POST-GnRH TESTOSTERONE LEVEL ON CUMULATIVE SELECTION DIFFERENTIALS _ STANDARD ERRORS) Regression Coefficients "' Low Line High Line Trait _ POSTCSD POSTCSD PRE b POST b.1513c c+.08 "PRE= pre-gnrh testosterone level, POST= post-gnrh testosterone level, b measured as ngeml'loh -1 realized heritability estimates for post-gnrh testosterone level. Table 6. CUMULATIVE SELECTION DIFFERENTIALS FOR POST-GnRH TESTOSTERONE LEVEL BY LINE AND GENERATION Low Line High Line Generation ACSD a SCSD b ACSD SCSD a ACSD =actual cumulative selection differential b SCSD=standardized cumulative selection differential 62
11 TABLE 7. LEAST-SQUARES MEANS AND STANDARD ERRORS FOR TESTES VOLUME BY LINE AND GENERATION LOW LINE HIGH LINE Generation Mean ' S.E. Mean S.E TABLE 8. LEAST-SQUARES MEANS AND STANDARD ERRORS FOR NUMBER BORN ALIVE BY LINE AND GENERATION LOW LINE HIGH LINE Generation Mean S.E. Mean S.E
12 TABLE 9. LEAST-SQUARES MEANS AND STANDARD ERRORS FOR BACKFAT LOW LINE HIGH LINE Generation Mean S.E. Mean S.E TABLE 10. LEAST-SQUARES MEANS AND STANDARD ERRORS FOR DAYS TO 104 kg BY LINEAND GENERATION LOW LINE HIGH LINE Generation Mean S.E. Mean S.E :
13 TABLE 11. REGRESSION OF PRODUCTION TRAITS ON POST-GnRH CUMULATIVE SELECTION DIFFERENTIALS _ STANDARD ERRORS) Regression Coefficients ' Low Line High Line Trait* POSTCSD POSTCSD DAYS104, d FAT, mm NBA TVOL, cm _ t-. 10 ' POSTCSD = cumulative selection differential for post-gnrh testosterone level, DAYS104= days to 104 kg, FAT= backfat adjusted to 104 kg BW, NBA= number born alive, TVOL= testes volume. 65
14 FIGURE I.ACTUAL AND EXPECTED RESPONSE BY GENERATION FOR POST-GnRH TESTOSTERONE PRODUCTION 95 O--Oexpected mean low line A 85 A--Aexpected mean high line z 75 aclual mean low line A actual mean high line I-O 65 / o 55 /A _o A..._ A.,-,- 25 / F 7 I _ 15 oaw o -25 _ _--0---_0 i.- w t I i I t I I I t GENERATION 66
15 FIGURE 2. ACTUAL AND EXPECTED RESPONSE BY GENERATION FOR PREIGnRH TESTOSTERONE PRODUCTION 67
16 FIGURE 3. SELECTION RESPONSE OF POST-GnRH TESTOSTERONE PRODUCTION RELATIVETO GENERATION ZERO PLOTTED AGAINST STANDARDIZED CUMULATIVE SELECTION DIFFERENTIALS low line high line / 150 1, _ _0 o 90 O_ co 80 c 100 _0_0\ / 50 O_ 10 4O / 2O _ / Stondordized Cumulotive Selection Differentiol (obsolute volue units) 68
17 Question: Henry Kohl Did high line boars reach puberty earlier than low line boars as the high line females did? Response: O.W. Robison I have no measure of puberty in boars; this is extremely hard to quantify in boars. The gilts do reach puberty earlier. Question: Dan Zelenka Have you measured correlated responses to skatole, and are you aware of similar selection experiments geared toward the reduction of skatole, the substance thought to influence boar taint. Response: O.W. Robison We have not measured skatole or 5 alpha-androstenone, both of which have been implicated in boar taint. Bonneau and Sellier (1968), Willeke et al (1987) and Jonsson and Andersen (1979) have studied 5 alpha-androstenone. I believe their results suggest a reduction inthis hormone lowers boar taint.... Bonneau & Sellier. World Rev. of Anim. Prod. 22:3 Jonsson & Andersen. Ann. Genet. Sel. Anim. 11:241 Willeke et al. J. Anim. Breed. Genet. 104:64 In literature cited. Question: Dan Zelenka Have you looked for correlated responses of hormone levels in females to account for the reduction in litter size. Response: O.W. Robison No, we have not done that. the low line. However, ovulation rate is increased in the high line vs 69
18 Question: Dan Zelenka In your response to a previous question, you stated that female puberty has changed between the lines. Can you elaborate? Response: O.W. Robison The high line reaches puberty about two weeks earlier and conception rates appear to be higher. Question: David Pollock What obvious behavioral differences exist between the two lines? Response: O.W. Robison We have not noticed any behavior differences, other than libido. Libido is certainly higher in the high line. Question: Koos Van Middelkoop Testosterone went up in the high line, but also you got a higher fat content. Did you get a higher oestrogen level in the sows? Response: O.W. Robison We have not measured estrogen. It is possible that estrogen is enhanced and thus causes an increase in fat. Question: Gerald Herbert Were there any changes in the exhibition of aggressiveness and competitive behavior among "high" line males (and females)? (In poultry the ability of males to compete with females for feed when feed restriction is being practiced is very important.) Response: O.W. Robison Other than increased libido, we have not noticed any change. conducted studies to measure this. However, we have not 7O
19 Question: John Tierce DO you have measurements of semen Characteristics between the two lines? Response: O.W. Robison._ We do not have measures of semen quality or quantity. Conception rates are higher in the high line, but I do not know if this reflects changes in semen quantity or quality. Question" E. G. Buss How early in life can the measurement of testosterone be made? Response: O.W. Robison I do not know. Question: Dale Van Vleck Why were high and low lines so similar in generation 6? Response: O.W. Robison Probably.due to chance. :Assays for hormone levels vary. We purchased assay kits each year. Even though the company provides a standard to use in establishing a base, I am convinced that a great deal of year to year variation exists due to the assay. Question: Dr. Edward Smith Cholesterol is a major intermediate in the biosynthesis of steroid hormones like testosterone - Is it possible that the increase in fat levels in the high line is a result of increase in cholesterol level? Response: O.W. Robison We have not checked cholesterol levels. However, it certainly is feasible that cholesterol levels have increased in order to manufacture testosterone. 71
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