Effect of Maternal Dietary Triiodothyronine on Embryonic Physiology of Turkeys1

PHYSIOLOGY AND REPRODUCTION Effect of Maternal Dietary Triiodothyronine on Embryonic Physiology of Turkeys1 V. L. CHRISTENSEN and W. E. DONALDSON Department of Poultry Science, Box 7608, North Carolina State University, Raleigh, North Carolina 27695-7608 K. E. NESTOR

ABSTRACT The objective of the present experiment was to feed triiodothyronine (T3) to lines of turkey breeders selected for egg production and growth, and an unselected control line. The data were collected to determine a genetic basis for thyroid-mediated maternal effects on embryonic physiology and livability. At 30 wk of age, turkeys of the three lines were photostimulated and half of each line was fed a diet containing .5 ppm T3. Maternal dietary T3 increased egg weight, reduced yolk solids and eggshell conductance constants, and increased albumen solids and water in eggs in all lines compared with control eggs. Hatchability in all lines was not affected by the dietary treatment (Control = 72.2%; T3 treatment = 70.7%), but there was a significant interaction between dietary T3 and line of turkey for the time of embryonic mortality, time of hatching, and carbohydrate metabolism of the embryo. The T3 increased mortality of the Egg line and unselected line during pipping, increased mortality of the Growth line in the plateau stage, but decreased its mortality during internal pipping. Reduced glycogen in liver as well as a reduced gluconeogenesis were evident in embryos of the two selected lines fed T3. It is concluded that genetic lines may have different metabolic patterns based on their genetic constitution in order to compensate for variations in egg solids and eggshell conductance constants. The metabolic patterns are reflected in different levels of embryonic blood plasma glucose, glycogen, and gluconeogenesis. (Key words: turkeys, embryonic development, thyroid, hatchability, energy budget) 1993 Poultry Science 72:2316-2327

ences in the abilities of turkey embryos from different lines to create or utilize Glycogen is accumulated in vital tissues tissue glycogen during pipping and hatchof avian embryos during their incubation ing (Christensen et al., 1993). Specifically, period to serve as an energy source during embryos from lines selected for increased pipping and hatching (John et al., 1987). growth or egg production had less cardiac Previous experiments indicated differ- and hepatic glycogen than those from randombred control lines prior to as well as following pipping. Thyroid hormones play a major role in Received for publication February 12, 1993. Accepted for publication August 27, 1993. tissue differentiation and in the final 1 The use of trade names in this publication does not maturation of many tissues just prior to imply endorsement by the North Carolina Agricultural Research Service, nor criticism of similar ones not hatching (Black, 1978; Mallon and Betz, 1982) as well as improve survival rates of mentioned. INTRODUCTION

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Department of Poultry Science, Ohio State University, Ohio Agriculture Research and Development Center, Wooster, Ohio 44691

MATERNAL THYROID

MATERIALS AND METHODS Fertile turkey eggs from lines selected for increased egg production (E), increased 16-wk body weight (F), and the line from which the F line was derived, a randombred control (RBC2), were ob-

2Catalog Number T2752 Sodium Salt 3,3',5Tmodo-L-Thyronine, Sigma Chemical Co., St. Louis, MO 63178-9916. 3 Aqua-Magic Model 50, National Poultry Equipment Co., Renton, WA 98055. 4 Jamesway Model 252B, Jamesway Incubator Co., Ft. Atkinson, WI 53538.

tained from Ohio Agricultural Research and Development Center, Wooster, OH, in May and were hatched in June, 1990 (McCartney et al, 1968; Nestor et al, 1985). The hatched poults were randomly distributed into the growing house and grown to sexual maturity using commercially accepted practices. At maturity, the hens were moved to an open-sided, fan-ventilated laying house in January and photostimulated using 15.5 h of daylight (0500 to 2030 h) to begin egg laying. Natural daylight was supplemented each morning and night with incandescent lights to provide the appropriate light period throughout the experiment. There were eight replicate pens of six hens each per line. Half of the hens from each line (four pens) were fed a basal diet (Grimes et al, 1989) and was designated as controls (CON), whereas the remaining half was fed the same basal diet containing .5 ppm T3.2 The effective dose for elevating plasma T3 was determined in prior studies (Queen, 1990; Christensen et al, 1992) by sampling blood from the hens at Weeks 0, 4, 8, 12, 16, and 20 of lay. The line and dietary treatments were randomly assigned to pens using a random numbers table. On Days 14 and 17 following photostimulation, the hens were inseminated using pooled semen from hatchmate toms from their own line. Weekly inseminations were performed thereafter for the duration of the experiment. Eggs were collected five times daily, sanitized,3 and stored at 12.8 C and 75% RH for 2 to 15 days prior to setting in incubators. Immediately prior to setting, the eggs were sorted by pen and date of oviposition. Each pen was then randomly assigned a position in the incubator. All eggs were incubated using the manufacturer's recommended procedures.4 At hatching the poults of each pen were counted, and the unhatched eggs were broken and examined macroscopically using a prepared chart of turkey embryo morphology to estimate embryonic development at the time of death. Hatchability and embryonic mortality were measured in four replicate trials using pens as repeated measures. Within each trial and at each of four stages of development, as described previ-

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chicks exposed to anoxia (McCartney and Shaffner, 1949). The neonatal thyroid is also necessary for forming glycogen in tissues other than liver and kidney, which can utilize gluconeogenesis to form precursors for synthesis of glycogen (Nobukuni et al, 1989; Czarnecki, 1991). Prior work with turkeys (Christensen et al, 1982) suggested that embryos from dams with poor hatchability have reduced blood plasma concentrations of thyroxine (T4). In subsequent work (Queen, 1990; Christensen et al, 1992), the concentrations of maternal blood plasma triiodothyronine (T3) were shown to negatively influence embryonic plasma T3 concentrations and hatchability. Thus, maternal deiodination of T4 to T3 may affect embryonic tissue glycogen (Christensen et al, 1991b) and thereby cause late developmental deaths in turkey embryos. Growth hormone (GH) in avian species is known to augment the conversion of T4 to T3 (Harvey et al, 1991). Genetic lines of turkeys selected for rapid growth have been observed to have a reduced amount of GH (Bacon et al, 1989). A consequence of reduced GH in turkey breeder hens from lines selected for rapid growth may be a reduced monodeiodination of T4 to T3. In the current study it was hypothesized that turkey lines selected for increased body weights may lack an adequate T3 concentration, therefore the objective of this study was to determine the effects of supplementing T3 in the maternal diet on embryo physiology and survival.

2317

2318

CHRISTENSEN ET AL.

analysis. Least square means differing significantly were separated by the LSD means separation procedure, and probability was based on P < .05. RESULTS Dietary T3 affected every measurement of egg quality except for percentage shell (Table 1). Eggshell conductance constants and the amount of dried yolk in each egg were decreased by the addition of dietary T3, whereas the amount of dried albumen increased compared with CON. Feeding T3 decreased the percentage of solids in each egg compared with CON regardless of line of turkey and despite an increase in egg weight. Both selected lines had eggs with less solids than those of the RBC2 line. There were significant line effects for all egg measurements. Weights of the F strain eggs were heavier than those of the RBC2, which were heavier than those from the E line. The F line eggs contained a higher percentage of albumen than the RBC2 eggs, which had a higher percentage than the E eggs. The RBC2 line eggs had a higher percentage yolk than the F or E eggs, which did not differ. Significant line by diet interaction effects were observed at the plateau stage and indicated that hepatic glycogen concentration was reduced by maternal dietary T3 among the E line embryos, but among the F or RBC2 embryos dietary T3 did not display a significant effect (Table 2). At internal pipping, the RBC2 line possessed greater amounts of glycogen per unit of weight of liver tissue than did the E or F line embryos, and E embryos had more than those from the F line. Line differences persisted at the external pipping of the shell stage, but the interaction effects were no longer significant. At external pipping, E embryos had higher concentrations of hepatic glycogen than F or RBC2 embryos. The plateau stage interaction effects of the E and F lines and dietary T3 were reversed in hatched poults compared with prepipping embryos. The hatchlings from the E line fed T3 had greater hepatic glycogen reserves than those from E dams not fed T^ but dietary T3 did not influence the concentrations of hepatic glycogen in either the F or RBC2 lines.

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ously by Christensen et al. (1991b), three embryos were selected randomly from each treatment and were sampled for subsequent physiological analyses. The stages were prepipping or plateau (25 days of incubation), internal pipping (26 days of incubation), external pipping (27 days of incubation), and hatched poults (28 days of incubation). Embryo body weight (with yolk sac), liver and heart weight, cardiac and hepatic glycogen, and blood plasma glucose concentrations were measured in two replicate trials (Dreiling et al, 1987; Christensen et al, 1991b). Hepatic glucose-6-phosphatase (G-6-P) activity (an index or gluconeogenesis) was measured (Donaldson and Liou, 1976) in two replicate trials. Measurements of egg weight and eggshell water vapor conductance were made for three eggs per pen in each of eight trials. Egg components were determined by separating the shell, yolk, and albumen and drying each to a constant weight in a drying oven at 65 C. Percentage water was determined by summing the amounts of dried egg components and dividing the sum by the initial egg mass. Twenty eggs from each treatment group were used to determine the treatment effects on egg components. Time of hatching was observed in three trials. Beginning on the 24th day, incubators were opened at 2-h intervals for 72 h, and the number of poults from each pen that had hatched was counted. Poults that had completely freed themselves from the shell were counted regardless of whether they were wet or dry. The data were analyzed as the percentage of poults hatched at each time. The data were summarized as a moving average pooled over 12-h time intervals for analysis. All data were analyzed using the General Linear Models procedure of SAS® software (SAS Institute, 1989) as a completely randomized design with two levels of diet (T3 or no T3) by three lines of turkey in a factorial arrangement of treatments (Snedecor and Cochran, 1967). All main and interaction effects were tested for significance, and the residual mean square error was used as the error term. All percentage data were transformed using arc sine transformations prior to

V
X

CON T3

X

.006 .001 .485 65.1 ± 2.0

64.9 66.3 65.6* 64.7 67.2 65.9* 62.6 65.1 63.9B

(g) 67.8 70.0 68.9C 89.2 94.8 90.9* 85.6 85.8 85.7B

.001 .045 .274 81.1 ± 5.8

Water

Weight <°f»\

.001 .485 34.9 ± 2.0

.006

36.1A

37.4 34.9

34.1"

35.3 32.8

34.4B

35.1 33.7

Total solids 3

.001 .001 .181 7.1 ± .7

7.1 7.1 7.1B

7.2 8.0 7.6*

6.6 6.8 6.7C

Albumen 3 ( %

of t 1 1 1 1 1 1 2 1 2

1

HG3T1C ^r*

•

Y

Least squares means in a column with no common superscript differ significantly (P £ .01). ^Least squares means in a column with no common superscript differ significantly (P S .05). *E = line selected for increased 180-day egg production; F = line selected for increased 16-wk body weight; RBC2 = 2CON = basal diet containing 16.5% crude protein and 2,760 kcal ME/kg of feed. T3 = basal diet plus .5 p 3 Percentages were calculated by dividing the dried weight by the initial egg mass. "•Milligrams of water vapor lost per day per millimeter of mercury water vapor pressure gradient in 28-day incubation period.

A_c

Line Diet Line x diet 5c±SEM

S U I U L C \Jl

^rvtiTW f\f v a r i ;»*•''"»*»

RBC2

CON T3

X

CON T3

E

F

Diet 2

Line1

TABLE 1. Egg weights and components of eggs produced by lines of turkey hens fed a triiodothyro

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CHRISTENSEN ET AL.

other), but the diet and line interaction effects were not significant. Hatchability of fertile eggs was significantly lower in the F line than in the E and RBC2 lines (Table 6). The addition of dietary T3 did not affect hatchability nor did it show an interaction with line. When embryonic mortality was examined, significant line by diet interactions were observed at the plateau and internal pipping stages (Table 7). At the plateau stage, dietary T3 increased F embryo mortality, decreased mortality in E embryos, but had no effect on RBC2 embryonic death. At internal pipping, dietary T3 increased mortality in the E and RBC2 lines, but had no effect on mortality in F embryos. Line differences were observed at external pipping with F line embryos having greater mortality than RBC2 embryos. Mortality of E line embryos was intermediate and did not differ significantly from the other two lines. A significant line by diet interaction was observed in the length of incubation

TABLE 2. Hepatic glycogen in turkey embryos from hens of different lines fed a triiodothyronine- (T3) supplemented or control diet Stage! Of development 3 Line1

Diet 2

Plateau

Internal pip

E

CON T3 5c CON T3 5c CON T3 5c

27.3AB 19.8C

21.7 19.5 20.6B

External pip

Hatched

/gc

F

RBC2

Source of variation Line Diet Line x diet 5c±SEM A

23.6 23.3BC 26.3BC 24.8 28.3AB 32.0*

17.3 15.3 16.2C

30.2

28.6 20.2 24.4 A

.009 .842 .010 25.1 ± 15.1

.003 .016 .180 20.4 ±

15.9 15.9 15.9* 11.6 13.0 12.3B 12.3 12.3 12.3B Probabilities .004 .583 .740 13.5 ± 1.6 3.1

12.7B 17.4* 15.1 ll.lBC 10.4C 10.7 10.2C 11.7BC 10.9 .002 .017 .010 12.2 ± 1.3

-CLeast squares means in a column with no common superscript differ significantly (P £ .01). E = line selected for increased 180-day egg production; F = line selected for increased 16-wk body weight; RBC2 = unselected controls from which line F was derived. 2CON = basal diet containing 16.5% crude protein and 2,760 kcal ME/kg of feed. T3 = basal diet plus .5 ppm T3. 3 Plateau = embryos just prior to pipping; Internal pip = beak had entered the air space; External pip = beak had broken the shell; Hatched = embryo had freed itself from the shell. J

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Only two significant differences were noted in cardiac glycogen, and both were line effects (Table 3). Concentrations of glycogen in the hearts of embryos from the F line were reduced compared with the other lines at the plateau stage, and heart glycogen was reduced in RBC2 hatchlings compared with those from the E or F lines. A significant interaction of line with dietary T3 was observed in blood plasma glucose concentrations at external pipping (Table 4). Dietary T3 elevated blood plasma glucose in the E embryos, but not F embryos, and depressed glucose in the RBC2 embryos. Specific hepatic G-6-P activity was affected at external pipping as shown by the interaction of line with dietary T3 (Table 5). Dietary T3 decreased G-6-P activity in RBC2 embryos, but failed to affect the activity in E or F line embryos. Line differences persisted in hatched poults (RBC2 and E embryo G6-P activities were greater than those of F embryos, but did not differ from each

MATERNAL THYROID

2321

periods (Table 8). As indicated by a significant interaction in the percentage of poults hatched at 660 h of incubation, dietary T3 shortened the incubation period of E embryos, lengthened that of the F embryos, but had no effect on that of the RBC2 embryos.

TABLE 3. Cardiac glycogen in turkey embryos from hens of different lines fed a triiodothyronine- (T3) supplemented or a control diet Stage of development3 1

2

Line

Diet

Plateau

Internal pip

E

CON T3 S CON T3 S CON T3 X

4.4 4.2 4.3» 4.0 3.5 3> 4.2 4.3 4.3»

3.9 4.3 4.1 4.0 3.2 3.6 4.2 3.9 4.1

.046 .429 .430 4.1 ± .4

.174 .397 .200 3.9 ±

,

F

RBC2

Source of variation Line Diet Line x diet 5c±SEM ab

External pip

Hatched

,'go 3.7 3.9 3.8 4.1 3.5 3.8 4.1 3.9 4.0 Probabilities .805 .363 .390 3.9 ± .5 .4

4.3 4.0 4.1> 4.2 3.8 4.0* 3.6 3.5 3.5" .040 .147 .670 3.9 ± .3

' Least squares means in a column with no common superscript differ significantly (P £ .05). *E = line selected for increased 180-day egg production; F = line selected for increased 16-wk body weight; RBC2 = unselected controls from which line F was derived. 2CON = basal diet containing 16.5% crude protein and 2,760 kcal ME/kg of feed. T3 = basal diet plus .5 ppm T3. 3 Plateau = embryos just prior to pipping; Internal pip = beak had entered the air space; External pip = beak had broken the shell; Hatched = embryo had freed itself from the shell.

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laying and declines when lay ceases. Sharp et al. (1979) have shown similar results for chickens. The data in the current study may suggest an important role for GH in avian reproduction. The F line, which has been shown to have depressed plasma GH concentrations prior to 24 wk of age in relation to the control (RBC2) from which it was derived (Bacon DISCUSSION et al, 1989) produced embryos that had Maternal dietary T3 and line of turkey the lowest tissue glycogen concentrations affected energy budgets (Ar et al, 1987; and G-6-P activity, and it also suffered the Vleck, 1991) and developmental patterns greatest embryonic mortality during the in the present study. Ar et al. (1987) and plateau and external pipping stages. The Vleck (1991) suggest that based on inter- supplementation of T3 to the maternal diet specific comparisons, all avian species of F line hens lengthened the incubation utilize the same amount of energy for period for F embryos compared with F growth, although maternal investments in embryos from CON dams. The length of eggs may differ widely. Thus, the data the incubation period has been increased may suggest that one way in which previously by the addition of thyroprotein genetic selection may have influenced to the diet of chickens (McCartney and embryo survival is through maternal or Shaffner, 1949), but the differential effects embryonic thyroid function effects on of dietary T3 on the incubation period of energy budgets of eggs. Scanes et al. (1979) different genetic lines was evident in the showed clearly that plasma GH concentra- present study. The T3 treatment increased tion increases when turkey hens begin mortality in F line embryos at the plateau

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CHRISTENSEN ET AL.

TABLE 4. Blood plasma glucose of turkey embryos from hens of different lines fed a triiodothyronine- (T3) supplemented or a control diet Stage of development3 Line1

Diet2

Plateau

Internal pip

External pip

Hatched

fmrrMT 1

E

F

RBC2

CON T3 X CON T3 3c CON T3 X

Source of variation Line Diet Line x diet 5c ±SEM ab

161 136 148 122 82 102 150 164 158 .426 .638 .822 136 ± 76

211b 232» 221 205" 222ab 214 232» 209b 221 Probabilities .691 .308 .796 .527 .265 .050 219 ± 16 224 ± 16<

222 210 216 229 227 228 219 239 229

258 276 267 239 253 246 263 255 259 .158 .350 .406 257 ± 17

' Least squares means in a column with no common superscript differ significantly (P £ .05). E = line selected for increased 180-day egg production; F = line selected for increased 16-wk body weight; RBC2 = unselected controls from which line F was derived. 2CON = basal diet containing 16.5% crude protein and 2,760 kcal ME/kg of feed. T3 = basal diet plus .5 ppm T3. 'Plateau = embryos just prior to pipping; Internal pip = beak had entered the air space; External pip = beak had broken the shell; Hatched = embryo had freed itself from the shell. !

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stage but had no significant effect on 6-P (Donaldson and Liou, 1976). The level mortality at internal pipping. Preparation of gluconeogenesis of F line embryos for pipping in F line embryos was charac- remained low during external pipping and terized by a decline in stored glycogen hatching. Dietary T3 may have resulted in between the plateau and internal pipping induced glucose-6-phosphatase activity stages (earlier in development than the but failed to improve livability during other lines) leaving little stored glycogen internal and external pipping, probably for energy at pipping. because of the lengthened incubation Wittmann and Weiss (1981) reported an period and lack of energy resources of F experiment in which air cells of incubating line embryos from dams fed T3. This eggs toward the end of incubation were seems contradictory to the original ventilated with oxygen or nitrogen. When hypothesis that GH may have reduced T3 ventilated with oxygen, no decrease of in F line hens involved and that replacehepatic glycogen or ATP was noted: ment therapy might improve hatchability. However, there are many physiological however, when hypoxia was produced by ventilating the air cell with nitrogen, an factors that are integrated at mis time, and accelerated depletion of glycogen and the data may suggest that a different dose ATP was produced. An accelerated deple- of T3 and T4 may be effective in improving tion of glycogen was seen in F line hatchability. The hatchability data from embryos (Table 2). In animals deprived of the present study contradict those in a feed or in animals with little or no prior study in which hatchability was carbohydrate intake (e.g., avian embryos), improved by feeding T3 to turkey breeder reduced blood glucose concentrations in- hens (Christensen et ah, 1991b). Two duce increased activity of hepatic observations may aid in clarifying the gluconeogenetic enzymes such as G- contrasting observations. First, the F line

2323

MATERNAL THYROID TABLE 5. Hepatic glucose-6-phosphatase activity of turkey embryos from hens of different lines fed a triiodothyronine- (T3) supplemented or a control diet Stage of development 3 Line1

Diet 2

Internal pip

Plateau

External pip

Hatched

881* 104»" 96 65 d 74cd

93 74 83 A 71 56 63» 85 105 95 A

of CON T3 3c

F

CON T3 x" CON T3 3c

RBC2

Source of variation Line Diet Line x diet 5c±SEM

76 49 88 68 92 85 88

103 110 107 94 110 102 141 112 127

.430 .374 .286 78 ± 2 5

.411 .899 .490 112 ± 32

76 77

69 110» g7bc 99 Probabilities .010 .917 .011 88 ± 15

.010 .559 .119 81 ± 16

A B

- Least squares means in a column with no common superscript differ significantly (P £ .01). Least squares means in a column with n o common superscript differ significantly (P <, .05). J E = line selected for increased 180-day egg production; F = line selected for increased 16-wk body weight; RBC2 = unselected controls from which line F w a s derived. 2CON = basal diet containing 16.5% crude protein and 2,760 kcal M E / k g of feed. T 3 = basal diet plus .5 p p m T3. 3 Plateau = embryos just prior to pipping; Internal pip = beak had entered the air space; External pip = beak had broken the shell; Hatched = embryo h a d freed itself from the shell. a_d

TABLE 6. Hatchability (percentage of fertile eggs) of eggs produced by genetic lines of turkey hens fed a triiodothyronine- (Tj) supplemented or a control diet Line 1

Diet 2

E

CON

73.1

T3

78.5

5? CON T3 J? CON T3 5c

75.9A 67.0 59.6 63.3B 75.8 74.7 74.9A Probabilities of transformed means .001 .524 .200 71.5 ± 18.0

F

RBC2

Source of variation Line Diet Line x diet x±SEM AB

Hatchability

' Least squares means in a column with no common superscript differ significantly (P £ .01). •E = line selected for increased 180-day egg production; F = line selected for increased 16-wk body weight; RBC2 = unselected controls from which line F was selected. ^ O N = basal diet containing 16.5% crude protein and 2,760 kcal ME/kg of feed. T3 = basal diet plus .5 ppm T3.

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E

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CHRISTENSEN ET AL.

more hepatic glycogen following hatching. To survive hatching, the E embryos from dams fed T3 did not increase gluconeogenesis during external pipping as did their counterparts from the RBC2 line. This physiological mechanism used by E line embryos was probably beneficial for preparation for pipping because the T3 diet reduced mortality during the plateau stage but was not effective for internal pipping because it resulted in more mortality in internally pipped embryos from E dams fed T3 than those from E dams fed the basal diet. Embryos from the RBC2 line possessed greater amounts of hepatic glycogen at the plateau and internal pipping stages. They also utilized the greatest amount of stored glycogen. Both of these functions are mediated by thyroid hormones (Wittmann and Weiss, 1981). This observation confirms earlier published results (Christensen el al, 1993). The RBC2 embryos also

TABLE 7. Embryonic mortality in eggs from hens of different lines fed a triiodothyronine- (Tj) supplemented or a control diet Stage of death3 Line1

Diet2

Week 1

Plateau

Internal pip

External pip

1.9* 4.6» 3.3 2.4* .6* 1.5 2.6b 1.5

12.0 11.6 11.8* 17.2 14.8 16.0» 8.3 9.9 9.1b

.020 .106 .050 2.1 ± 1.5

.038 .931 .820 12.2 ± 11.5

(% of 1 E

F

RBC2

Source of variation Line Diet Line x diet 5c ± SEM*

CON T3 S CON T3 X CON T3 5c

7.0 5.9 6.4<* 4.6 4.5 4.5b 8.3 8.5 8.4" .019 .760 .809 6.5 ± 3.8

6.8B 4.7C 5.7 9.9B 18.2A 14.0 6.1BC 5.4C 5.7 .003 .768 .004 8.3 ± 7.7

A-CLeast squares means in a column with no common superscript differ significantly (P <, .01). "Least squares means in a column with no common superscript differ significantly (P £ .05). : E = line selected for increased 180-day egg production; F = line selected for increased 16-wk body weight; RBC2 = unselected controls from which line F was derived. 2CON = basal diet containing 16.5% crude protein and 2,760 kcal ME/kg of feed. T3 = basal diet plus .5 ppm T3. 3 Plateau = embryos just prior to pipping; Internal pip = beak had entered the air space; External pip = beak had broken the shell; Hatched = embryo had freed itself from the shell. 4 Overall mean ± SEM. Means and standard errors used in the analysis were transformed.

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in the present study was from a different strain than that observed previously, and second, dietary T3 reduced eggshell conductance in the F line in the present study but did not in the strain observed previously (Christensen et al, 1991b). The most interesting observed changes in embryo physiology resulting from perturbation of the maternal thyroid were those noted among E line embryos. Plasma GH in the E line is higher than in its randombred control line at hatching but higher in the randombred control line from Weeks 7 to 28 of growth (Anthony et al, 1990). Eggs from the E line were smaller and contained less solids than those of the RBC2 line. When dams were fed T3, which reduced the solids in the incubating eggs, the E embryos made large adjustments to survive hatching. They shortened the developmental period, which was accompanied by reduced hepatic glycogen prior to pipping but left

2325

MATERNAL THYROID

incubation) were reduced in the selected lines and when dietary T3 was fed. The lack of adequate oxygen at the plateau stage in oxygen consumption would require a greater reliance on anaerobic metabolism and glycogen for survival (Beattie, 1964; Freeman, 1965; Wittmann and Weiss, 1981). Thus, egg protein (gluconeogenic amino acids) in albumen would assume a greater role in energy metabolism than long chain fatty acids in yolk, which require aerobic metabolism. The replacement of yolk fat with albumen protein in eggs from hens of the E and F lines as well as in eggs from all hens fed T3 may represent a mechanism to stimulate glycogen production. The additional glycogen would be required for embryonic survival under the anaerobic conditions of pipping (Wittmann and Weiss, 1981) and hatching from eggshells that provide less oxygen. If such an assumption were true, differences in intermediary metabolism of developing embryos should be discernible. Tissue glycogen, blood plasma glucose, and gluconeogenesis were all measured to

TABLE 8. Percentage of poults hatched at 624 to 672 h of incubation from turkey hens of different lines fed a triiodothyronine- (Tj) supplemented or a control diet Time of hatching (hours of incubation) 1

2

Line

Diet

E

CON T3 X

F

CON T3 X CON T3 X

RBC2

624 .5 2.4 1.4 .5 .5 .5 .9 1.7 1.3

QnillVA f*f x w « a t i r t « kA/UltC

648

660

672

75.0b 82.2" 78.6 81.4a 62.9c 72.2 80.0» 80.2» 80.1

100 100 100 100 100 100 100 100 100

^ _ PmVlflhiliHpd rttf iiwfi»a«cfi"M"tir»<»/1 m a a n c ^_^_

\

Line Diet Line x diet X ± SEM3

636

— (% of cumulative total poults 6.6 37.9 4.2 37.2 5.4 37.5 48.2 9.6 8.8 45.7 9.2 47.0 48.2 9.5 4.8 43.4 48.8 6.3

.398 .166 .374 1.1 ± 2.1

.810 .258 .776 7.1 ± 6.4

.597 .520 .964 43.1 ± 22.8

.612 .713 .042 77.4 ± 6.2

"Least squares interaction means in a column with no common superscript differ significantly (P £ .05). *E = line selected for increased 180-day egg production; F = line selected for increased 16-wk body weight; RBC2 = unselected controls from which line F was selected. ZCON = basal diet containing 16.5% crude protein and 2,760 kcal ME/kg of feed. T3 = basal diet plus .5 ppm T3. 3 Overall mean ± SEM. Means and standard errors used in the analysis were transformed.

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had the genetic ability to increase gluconeogenesis to a greater extent at pipping than did F or E line embryos. However, maternal dietary T3 interacted with RBC2 embryos at external pipping to decrease gluconeogenesis. These metabolic adjustments were accompanied by increased mortality at internal pipping. Dietary T3 decreased maternal investments in each egg regardless of line. The amount of yolk and total solids deposited per egg were decreased, whereas the amounts of albumen and water were increased. It was assumed that these changes may enhance embryo survival because similar differences have been reported in maternal investments in eggs by populations of lizards and turkeys kept at high altitudes or sea level (Sinervo and Huey, 1990; Christensen et at, 1991a). In addition to changes in egg composition, the ability of the embryos to obtain oxygen to drive metabolism was limited by both line and dietary T3. Conductance constants (the measure of the ease with which a gas diffuses through the shell per unit of egg mass multiplied by time of

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Thyroid hormones, specifically T4, have been observed to increase hepatic glycogenolysis (Wittm?.in and Weiss, 1981) and at the same time increase accrual of glycogen in tissues other than liver and kidney (Nobukuni et al, 1989; Czarnecki, 1991). The accrual of glycogen in neonatal turkey heart has been shown to be influenced directly by dietary T4. It is possible that the embryonic thyroid may have been influencing glycogenolysis and accrual of cardiac glycogen in the present study. If such an hypothesis were true, then blood glucose, the product of gluconeogenesis and breakdown product of hepatic glycogen, should be increased in embryos from dams fed T3. Dietary T3 elevated blood glucose in the E line, depressed it in RBC2 embryos, but had no effect in F line embryos. This suggests that maternal dietary T3 may have influenced the embryonic thyroid (Christensen et al, 1991b) in the E and RBC2 lines but not the F line or the single dose level of T3 fed in the current study may not have been appropriate for the F line. No difference in hatchability could be attributed to dietary T3, but the failure to

REFERENCES Anthony, N. B., R. Vasilatos-Younken, D. A. Emmerson, K. E. Nestor, and W. L. Bacon, 1990. Pattern of growth and plasma growth hormone secretion in turkeys selected for increased egg production. Poultry Sci. 69:2057-2063. Ar, A., B. Arieli, A. Belinsky, and Y. Yom-Tov, 1987. Energy in avian eggs and hatchlings: utilization and transfer. J. Exp. Zool. 235(Suppl. 1):151-164. Bacon, W. L., R Vasilatos-Younken, K. E. Nestor, B. J. Andersen, and D. W. Long, 1989. Pulsatile patterns of plasma growth hormone in turkeys: effects of growth rate, age and sex. Gen. Comp. Endocrinol. 75:417-426. Beattie, J., 1964. The glycogen content of skeletal muscle, liver and heart in late chick embryos. Br. Poult. Sci. 5:285-293. Black, B. L., 1978. Morphological development of the epithelium of the embryonic chick intestine in culture: influence of thyroxine and hydrocortisone. Am. J. Anat. 153:573-600. Christensen, V. L., H. V. Biellier, and J. F. Forward, 1982. Physiology of turkey embryos during pipping and hatching, m. Thyroid function. Poultry Sci. 61:367-374. Christensen, V. L., W. E. Donaldson, and T. Hardy, 1991a. Effect of altitute on fitness of turkey embryos and poults. Poultry Sci. 70(Suppl. 1): 26.(Abstr.) Christensen, V. L., W. E. Donaldson, and K. E. Nestor, 1992. Effect of maternal blood concentrations of triiodothyronine on embryonic

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observe how embryos from hens of each show such differences may have been due line of turkey fed T3 regulated their energy to embryos altering incubation periods in budgets to survive given the different the selected lines. Dietary T3 increased maternal investment and eggshell conduc- embryonic developmental periods for the tance values. It is speculated that the F line, but shortened them for the E line. increased gluconeogenesis occurred in re- The length of an incubation period is sponse to the limitations in oxygen availa- adjusted frequently among wild species of bility and reliance of hepatic glycogen birds to enhance embryonic survival by (Wittmann and Weiss, 1981) due to the improving the energetics of growth (Ar et reduced eggshell conductance. The E and al, 1987). Shorter incubation periods have F line embryos seemed unable to increase also been noted for lines of chickens gluconeogenic activity, perhaps because of selected for increased body weights comdifferences in their egg size or eggshell pared with those with low body weight conductance as a correlated response to (Dunnington et al, 1992). selection for increased egg production or The data from the present study sugbody weight. Alternately, the dose of T3 gest that genetic lines selected for infed in the current study may have been creased egg production or body weight inadequate or excessive to elicit a favorahave adjusted maternal investments in ble hatchability response among selected eggs when compared with the RBC2 embryos. Increased mortality of E line control line. Alterations in maternal inembryos from hens fed T3 was observed at internal pipping, but no other mortality vestments have resulted in changes in the effects were observed between control and energetics of embryonic development. T3 treatments for E embryos. Thus, inter- Feeding the single .5 ppm of T3 to dams, nal pipping may be a critical developmen- which was intended to compensate for GH tal event for E line embryos because of the limitations on monodeiodination, was not reduced amount of hepatic glycogen at the an effective means for improving turkey egg hatchability. plateau stage.

MATERNAL THYROID

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growth and metabolism of large white turkeys. Poultry Sci. (Suppl. l):24.(Abstr.) Christensen, V. L., W. E. Donaldson, and K. E. Nestor, 1993. Hatchability and embryonic metabolism in turkey lines selected for egg production or growth. Poultry Sci. 72:829-838. Christensen, V. L., W. E. Donaldson, J. F. Ort, and J. L. Grimes, 1991b. Influence of diet-mediated maternal thyroid alterations on hatchability and metabolism of turkey embryos. Poultry Sci. 70: 1594-1601. Czarnecki, C. M., 1991. Influence of exogenous T4 on body weight, feed consumption, T4 levels, and myocardial glycogen in furazolidone-fed turkey poults. Avian Dis. 35:930-936. Donaldson, W. E., and G. I. Liou, 1976. Lipogenic enzymes: Parallel responses in liver to glucose consumption by newly-hatched chicks. Nutr. Rep. Int. 13:471-476. Dreiling, E. E., D. E. Brown, L. Casale, and L. Kelly, 1987. Muscle glycogen: comparison of iodine binding and enzyme digestion assays and application to meat samples. Meat Sci. 20: 167-177. Dunnington, E. A., F.M.A. McNabb, T. B. Freeman, N. O'Sullivan, and P. B. Siegel, 1992. Genetic analyses of incubation time in weight-selected lines of chickens and their crosses. Arch. Geflugelkd. 56:77-80. Freeman, B. M., 1965. The importance of glycogen at the termination of the embryonic existence in Gallus domesticus. Comp. Biochem. Physiol. 28: 1169-1170. Grimes, J. L., J. F. Ort, V. L. Christensen, and H. R. Ball, 1989. Effect of different protein levels fed during the prebreeder period on performance of turkey breeder hens. Poultry Sci. 68:1436-1441. Harvey, S., R. A. Fraser, and R. W. Lea, 1991. Growth hormone secretion in poultry. Crit. Rev. Poult. Biol. 3:239-282. John, T. M., J. C. George, and E. T. Moran, Jr., 1987. Pre- and post-hatch ultrastructural and metabolic changes in the hatching muscle of turkey embryos from antibiotic and glucose treated eggs. Cytobios 49:197-210. Mallon, D. L., and T. W. Betz, 1982. The effects of hydrocortisone and thyroxine treatments on duodenal morphology, alkaline phosphatase, and sugar transport in chicken (Gallus gallus) embryos. Can. J. Zool. 60:3447-3455. McCartney, M. G., K. E. Nestor, and W. R. Harvey, 1968. Genetics of growth and reproduction in

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