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Dam Line and Sire Line Effects on Turkey Embryo Survival and Thyroid Hormone Concentrations at the Plateau Stage in Oxygen Consumption¹

V. L. Christensen^*,2, G. B. Havenstein^*, D. T. Ort^*, J. P. McMurtry and K. E. Nestor

^* Department of Poultry Science, College of Agriculture and Life Sciences, North Carolina State University, Raleigh 27695; Growth Biology Laboratory, Agricultural Research Service, USDA, Beltsville, MD 20705; and Department of Animal Science, Ohio State University, Wooster 44691

² Corresponding author: vern_christensen{at}ncsu.edu

	ABSTRACT

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Inheritance of embryo thyroid function was measured in lines of turkeys. Two lines that had been selected for either increased egg production (E) or increased 16-wk BW (F) and their respective randombred controls (i.e., RBC1 and RBC2) were examined. Reciprocal crosses of dams and sires from each selected line and its randombred control were made to estimate sire line and dam line effects. Orthogonal contrasts were used to determine if the differences found were due to the presence of additive, nonadditive, or maternal, sex-linked, or both, gene effects. With the data involved, sex-linkage and maternal effects could not be separated. Embryo survival was measured for all lines and their reciprocal crosses. Crossing the RBC1 sire and E dam also resulted in better embryo survival and lower death losses at pipping than for the other cross- or purelines. Reciprocal crosses of the F and RBC2 lines showed better total embryo survival, and they survived pipping better than the F or RBC2 purelines. Thyroxine (T₄) and triiodothyronine (T₃) concentrations differed between the reciprocal crosses at external pipping, but the effects were inconsistent for the 2 data sets. Reciprocal tests indicated that maternal, sex-linked, or both, effects were present for T₃ concentrations at internal pipping in the E and RBC1 lines and at external pipping for the F and RBC2 lines. Reciprocal effects were significant for T₄ at internal pipping for both data sets. The RBC1 sire embryos had significantly higher T₃:T₄ ratios than the E line sire embryos at internal and external pipping, and the pureline RBC1 embryos had consistently higher ratios than the pureline E embryos. The differences for the T₃:T₄ ratios between these 2 lines at internal pipping, external pipping, and hatch appeared to be consistently additive in nature, although significant nonadditive or heterotic effects were present for the ratio at external pipping. Similar effects on the T₃:T₄ ratio were observed for the F and RBC2 lines at external pipping.

Key Words: turkey • embryo survival • thyroid • thyroxine • triiodothyronine

	INTRODUCTION

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Evidence suggests that maternal DNA dominates breast muscle inheritance (Velleman et al., 2003; Velleman and Nestor, 2004) and gene expression for disease resistance (Allen, 1962), but current genetic theory suggests that imprinting of male or female gene DNA does not occur in birds (Moore and Haig, 1991). With turkeys, increased embryo deaths during tucking have been associated with the dam line, but increased deaths at pipping have been associated with the sire line (Christensen et al., 2004, 2005b). Little is known about the mechanisms that may underlie such a dichotomy. One possible explanation for divergent dam line and sire line effects on embryo viability may be related to embryo thyroid function. The embryonic thyroid controls maturation of functions that characterize the precocial or altricial nature of hatchlings that is characteristic of a species (Christensen and Biellier, 1982; Christensen et al., 2002; Christensen and Davis, 2004).

Commercial turkeys are the product of 3- or 4-way crosses that utilize 1 sire or a cross of 2 growth-selected sire lines and usually a cross of 2 reproduction-selected dam lines. Therefore, knowledge of the gene expression from the sire and dam lines on embryo thyroid function may be important for understanding the viability of commercial turkey embryos and neonates. So, a hypothesis was proposed that the dam line and the sire line may independently affect embryo thyroid hormone concentrations and that such differences may be due to different types of gene action.

	MATERIALS AND METHODS

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Breeder turkeys for the current experiments were produced during the 40th generation of line F, which had been selected for increased 16-wk BW, and from the 46th generation of line E, which had been selected for increased egg production for various periods of time. The 2 randombred control lines from which the F and E lines had been derived [i.e., RBC2 and RBC1, respectively (Nestor, 1984; Nestor and Noble, 1995)] were compared with the selected line and the reciprocal crosses of each selected line with the control line from which it had been derived. Day-old poults were delivered from the Ohio Agricultural Research and Development Center, Wooster, to the North Carolina State University Turkey Research Unit, Raleigh, in April and were grown using accepted practices (Grimes et al., 1989; Christensen et al., 1993). At 37 wk of age, egg production was induced by photostimulation in all 4 lines (15.5 h of light/d; 0500 to 2030 h). Thereafter, hens within lines were divided randomly into 24 pens with 6 hens each (36 hens per line). Half of the pens of hens from the E and RBC1 lines were artificially inseminated with pooled semen from 9 hatchmate males to reproduce the 2 purelines (i.e., from RBC1 x RBC1 and E x E matings), and the remaining hens were inseminated with the same pooled semen but from the opposite line to reproduce the 2 reciprocal crosses (i.e., from RBC1 x E and E x RBC1 matings). Similar pure and reciprocal cross-matings using pooled semen from 9 males were made to produce the RBC2 x RBC2, F x F, RBC2 x F, and F x RBC2 offspring. Hatching eggs were subsequently collected from the nests 5 times per day, sanitized, placed into a room kept at 12.8°C and 75% RH, and stored for up to 7 d before setting. Eggs were removed from the room at weekly intervals, sorted by day and pen, allowed to warm overnight at room temperature, and placed into machines for incubation. Eggs were incubated at 37.5°C and 53% RH using a multiple-stage incubation system such that eggs from 4 wk of production were in the incubator at 1 time. Following 25 d of incubation, all eggs were transferred to hatching baskets and were placed into an incubator operating at 36.9°C and 75% RH. Eggs were collected for a 20-wk laying period and were set weekly for 17 of the 20 wk to determine embryo livability for each of the crosses. Eggs that did not hatch were broken, and embryos were examined to categorize deaths according to the criteria of Hamburger and Oppenheim (1967). Eggs produced at 9, 12, and 16 wk of production were sampled at similar stages of development to determine plasma thyroid hormone concentrations.

Sampled embryos were selected randomly from each treatment at d 25, 26, 27, and 28 of development using the morphological criteria of Hamburger and Oppenheim (1967) to represent the following stages of development. These criteria were identical to those used to categorize eggs that did not hatch. Day 25 of incubation was utilized to represent the time when the embryo is tucking its head beneath its wing. Day 26 was used as the time when internal pipping occurs with the beak penetrating the air space, and d 27 was utilized as the time when external pipping occurs or when the beak of the embryo penetrates the eggshell. On the 28th day of incubation, newly hatched poults, who had completely freed themselves from the shell and whose down feathers were nearly dry, were randomly selected for use in the posthatch part of the study. Embryo survival and morphology of tucking and internal pipping were visualized using a candling light before selection for sampling. Each hatch included a comparison of each selected line, its randombred control, and their reciprocal crosses. Within each of the 3 sampling hatches, 3 embryos or neonates were selected randomly from each pureline and from each reciprocal cross at each stage of development, for a total sample size of 9 for each line or cross subgroup. Blood samples were collected from embryos and neonates following decapitation. The blood was centrifuged (700 x g at 4°C), and the plasma was decanted and frozen (–20°C) for later analysis.

Plasma was analyzed for triiodothyronine (T₃) and thyroxine (T₄) concentrations by RIA as described previously (McMurtry et al., 1988). All samples were assayed in a single assay to avoid interassay variation. Intraassay CV was determined to be 3.4% for T₃ and 2.0% for T₄.

Weekly data for embryo survival and deaths were collected for 17 wk. The data for percentage of dead embryos at internal pipping were not normally distributed; therefore, the internal pipping mortality data were pooled with the tucking mortality for analysis. Both stages constitute the plateau stage for turkey embryos. Percentage data for each pen were subjected to the arcsine of the square root of the percentage of transformation before analysis. The data were sorted by lines, and each selected line was compared with its randombred control line (i.e., the E line was compared with RBC1, and the F line was compared with RBC2). Therefore, 2 separate sets of data were analyzed, each consisting of the pure selected line and its pure randombred control and their 2 reciprocal crosses. Thus, each analysis was done as a 2 x 2 factorial when the purelines were used as sires and as dams in both pureline and crossline combinations. All main effects and interactions were tested, and means determined to differ significantly were separated using the least square means procedure (SAS Institute, 1998). Additive genetic variation (line effect) was estimated by the orthogonal contrast of the purelines. The values for heterosis were obtained by dividing the average of the reciprocal crosses by the average of the parental lines and multiplying by 100. The significance of the heterosis was obtained by contrasting the average of the parental lines and the average of the reciprocal crosses. The significance of reciprocal effects (a confounded measure of sex linkage and maternal effects) was obtained by contrasting the reciprocal crosses.

	RESULTS

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Embryo Survival to 25 d, Mortality at Head Tucking, and Internal and External Pipping
The week of lay of the flock when the hatching eggs were collected was included as a fixed factor in all analyses. No significant week of lay x treatment interactions were observed, but the embryo livability across all lines and crosses differed as the hens aged, with deaths occurring early in development declining but those occurring late in development increasing. Crossing of the E dams, which had been long-term selected for increased egg production, with RBC1 sires (from which the selected E line had been derived) produced embryos that survived better than either pureline or the other reciprocal cross (Table 1). Offspring of the RBC1 line sires had higher embryo survival than did the offspring of the E line sires (P 0.0005), and E line dams had higher embryo survival than did RBC1 dams (P 0.0001). This resulted in a highly significant sire line x dam line interaction (P 0.0001). The orthogonal contrasts for embryo survival for the purelines and their crosses indicated a negative 15.8% heterosis was present (P 0.0008), and the reciprocal cross contrast indicated the presence of maternal or sex-linked gene expression (P 0.0001). Crossing of the E dam with the RBC1 sire also reduced the number of embryos dying at tucking and internal pipping (i.e., on d 25 and 26) in comparison with the mortality of embryos produced by the 2 purelines and the other reciprocal cross. The RBC1 sires had significantly less embryo mortality at tucking and internal pipping (P = 0.0038), but the sire x dam interaction was also highly significant (P = 0.0216) due to an inverse relationship between the 2 lines when used as sires in comparison with the difference between the 2 lines when used as dams. The orthogonal contrast for reciprocal effects at tucking and internal pipping for the E and RBC1 matings indicated that the differences in mortality were influenced (P < 0.03) by sex-linked or maternal effects. The reciprocal crosses of the E and RBC1 lines had lower external pipping mortality than did either of the 2 purelines, and the sire line effect was significant (P < 0.0308), indicating the RBC1 sires had a higher percentage of deaths at external pipping than did the E line sires. The dam line, and sire line x dam line interaction effects were not significant for external pipping deaths. The orthogonal contrasts showed a highly significant (P 0.00001) degree of negative heterosis (–41.7%) was present; however, significant (P = 0.0128) sex-linked or maternal effects were also present for external pipping deaths.

Plasma T₃ Concentrations
Comparisons of the embryo plasma T₃ concentrations in the pure E and RBC1 line embryos and their reciprocal cross embryos are summarized in Table 2. No significant effects were observed for embryo plasma T₃ concentrations at tucking between embryos from the pure E and RBC1 lines and their reciprocal crosses or between the embryos from the pure F and RBC2 lines and their reciprocal crosses. Neither were any of the genetic tests significant for embryo plasma T₃ concentrations for either of the 2 sets of data. At internal pipping, however, embryonic T₃ concentrations were significantly affected by the E and RBC1 data set when used both as sire lines (P = 0.0239) and as dam lines (P 0.0519). The embryos from the RBC1 pureline matings had less than half the concentration of T₃ at internal pipping than did the embryos from the 2 reciprocal cross-matings, which were intermediate in their T₃ concentrations between the 2 purelines. The orthogonal contrasts for the E and RBC1 data set at internal pipping indicated that only additive gene effects significantly (P = 0.007) affected the T₃ concentration. Growth selection in the F line had a similar effect on embryonic T₃ concentration at internal pipping (Table 2). Although the difference in internal pipping deaths between the 2 lines when used as sires was not significant, the difference between the 2 lines when used as dams was significant (P 0.0466), and, as with the E and RBC1 comparisons, the growth-selected F pureline embryos had less than one-third the T₃ concentration at internal pipping than did the RBC2 pureline embryos. Unlike the E and RBC1 comparison, however, the reciprocal cross embryo T₃ concentrations in the F and RBC2 data were similar to the concentrations found in the pure RBC2 embryos. None of the orthogonal contrasts were significant at internal pipping for T₃ concentration for the F and RBC2 data set.

Plasma T₄ Concentrations
None of the sire line, dam line, or sire line x dam line interactions or any of the genetic tests were significant for plasma T₄ concentrations at head tucking for either data set (Table 3). At internal pipping, however, the embryos from the RBC1 line when used both as sires and as dams had significantly higher plasma T₄ levels (P = 0.0413, 0.0021, respectively). Similarly, embryos from the RBC2 dams had significantly higher T₄ concentrations than did the embryos from the growth rate-selected F line dams. Significant reciprocal effects were present (P = 0.0379) for both data sets, indicating that maternal or sex-linked effects were contributing to T₄ concentrations at internal pipping. At external pipping, embryos from E line sires had significantly (P 0.0521) higher T₄ concentrations (21.7 ng/mL) than did the embryos from RBC1 line sires (17.8 ng/mL). This effect was not present in the F and RBC2 data set. None of the genetic tests at external pipping were significant for T₄ concentrations for either data set. At hatch, RBC1 line dams had significantly higher (21.4 ng/mL, P = 0.0430) T₄ concentrations than did hatched poults from E line dams (9.2 ng/mL). A significant sire line x dam line interaction indicated that the difference in T₄ concentrations between the offspring of the E line and RBC1 sires was significantly larger (P < 0.0430) than between the offspring of the E line and RBC1 dams. The orthogonal contrasts for the E line and RBC1 line data set indicated that both heterosis (P < 0.0421) and sex-linked or maternal effects (P < 0.0526) were present for concentrations in hatched poults. None of the sire line, dam line, or sire x dam effects or any of the genetic tests for T₄ concentrations in hatched poults were significant for the F line and RBC2 data set.

A highly significant (P = 0.005) sire line x dam line interaction for the T₃:T₄ ratio was present at internal pipping for the F line and RBC2 line matings, indicating that the difference in the ratios between the offspring from the F line and RBC2 line sires was larger than it was between the offspring from the F line and RBC2 line dams (Table 4). The genetic tests at internal pipping for the T₃:T₄ ratio indicated that a significant level (78.1%, P = 0.0277) of heterosis existed in the F and RBC2 data set.

At external pipping (Table 4), the T₃:T₄ ratios for the E and RBC1 data set were significantly affected by both the line of the sire (P = 0.0107) and the line of the dam (P = 0.0374). Embryos produced by the RBC1 line when used as sires had significantly higher (P = 0.0107) T₃:T₄ ratios (0.37) at external pipping than did embryos from E line sires (0.28). The genetic tests for the T₃:T₄ ratio at external pipping (Table 4) indicated that the effects were additive in nature (P = 0.0199) for the E line and RBC1 line data set.

Sire line and dam line effects for the T₃:T₄ ratio at internal pipping for the F and RBC2 data set (Table 4) were not significant. However, a significant (P = 0.0050) sire line x dam line interaction was present at internal pipping for these lines, indicating that the difference in the T₃:T₄ ratio between the lines when used as sires (0.07) was significantly larger than it was when the lines were used as dams (0.05). Embryos from F line sires had significantly (P = 0.0006) higher T₃:T₄ ratios at external pipping (0.36) than did embryos from RBC2 line sires (0.24). A significant sire x dam interaction (P = 0.0380) was also present at external pipping for the F and RBC2 data set, indicating that the difference between the T₃:T₄ ratios at external pipping for the F line and RBC2 line sires (0.12) was significantly larger than was the difference between the ratios in the offspring from the F and RBC2 dams (0.03). Sex-linked and maternal effects contributed (P = 0.0015) to the T₃:T₄ ratios at external pipping for the F and RBC2 data set. Both data sets showed thst 20.4% heterosis was present for the T₃:T₄ ratios at external pipping, but neither estimate was significant (Table 4).

Hatched poults from E line dams had significantly higher (P = 0.007) T₃:T₄ ratios (0.41) than did hatched poults from RBC1 dams (0.31), and the differences in the ratios at hatch were additive in nature (P = 0.0199, Table 4). None of the sire, dam, or sire x dam effects for T₃:T₄ ratios were significant for the F line and RBC2 data set, but the orthogonal contrasts indicated that significant (P = 0.0017) sex-linked or maternal effects were present.

	DISCUSSION

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Long-term selection for increased egg production in the E line of turkeys and for increased 16-wk BW in the F line of turkeys appear to have resulted in different effects on the development and function of the embryonic thyroid. The use of long-term selected genetic lines and the randombred lines from which they were derived, when mated in both pure and crossline combinations, show differences in embryo survival and mortality at specific ages of development as well as different types of gene action involved in the significant differences observed.

The long-term selected E and F turkey lines, along with their respective randombred control lines and their reciprocal crosses, were used in this study, and those lines affected embryo survival as well as the development and function of the embryonic thyroid. The effects observed, however, were in many cases dependent upon whether the lines were being used as sire lines or as dam lines, as well as on the stage of development involved and on which of the 2 selected lines its randombred control was being studied. Orthogonal contrasts were used to show whether the effects observed were due to additive or nonadditive (heterotic) gene actions or to sex-linked or maternal effects. The latter 2 effects could not be separated with the available data sets. Embryo survival was significantly affected by sex-linked or maternal effects at all of the embryonic developmental stages tested in both data sets. As was pointed out earlier, these results could be due to sex-linked gene effects, but more likely, they are due to maternal effects related to hatching egg size. The E line dams produce eggs that are much smaller than the eggs of the randombred line (RBC1) from which they are derived, and F line dams produce hatching eggs that are much larger than the eggs of the randombred line (RBC2) from which they are derived. Thus, one might expect that the nutrition provided to the embryos from different sized eggs would be very different and might affect survival. The data herein, however, are difficult to interpret, because crossline embryos from the smaller E line eggs survived much better than did the crossline embryos from the larger RBC1 eggs. On the other hand, crossline embryos from the larger F line eggs survived poorer than did embryos from the smaller eggs of the RBC2 line. Nonadditive gene action or heterosis was also present for embryo survival in both data sets at 25 and 27 d of incubation.

Thyroid hormone responses in avian embryos have been suggested to be of 2 types, developmental and functional (Christensen et al., 2005a). Embryos from different lines of turkeys may have the same general developmental thyroid characteristics but may differ in functional response to temperature or ambient O₂ concentrations. The environment of the incubator stimulates functional thyroid responses in unique ways (Christensen et al., 2002). Embryos from different genetic backgrounds have been shown to survive differently when exposed to elevated temperatures. Turkey embryos with greater T₄ concentrations and perhaps greater hypothalamic maturity survive better than do those with depressed levels (Christensen and Biellier, 1982; Christensen and Phelps, 2001). Comparing embryos of different lines to their randombred controls has revealed that both developmental and functional responses are essential to embryo survival (Christensen et al., 2002). Plasma thyroid hormone concentrations have been found to be depressed in weak neonatal turkeys, as identified by characteristic flip-over behavior (Christensen et al., 2003), as well as in hypercapnic embryos (Donaldson et al., 1995). Tona et al. (2005) also have related higher T₃:T₄ ratios to improved chick quality. Thus, better thyroid responses may also indicate not only improved embryo viability but better neonatal poult survival as well.

The line of the dam, the line of the sire, or the interaction of the line of the sire and the line of the dam when used as parents affected embryo plasma ratio of T₃ to T₄ divergently in the current study at the external pipping stage of development. Thyroid function at external pipping when measured as ratios was affected more when the line was used as the sire than when used as the dam. External pipping is the most critical stage for thyroid function and embryo survival (Christensen and Biellier, 1982). Velleman et al. (2003) and Velleman and Nestor (2004) have suggested that 16-wk breast muscle morphology (in the same growth-selected line used in the present study) results primarily from maternal DNA. Befkre that work, Allen (1962) reported possible maternal inheritance of factors affecting pullet mortality along with many egg characteristics. Evidence indicates maternal mitochondrial inheritance in some species of animals, but the mechanisms regulating such inheritance in birds are still obscure (Birky, 2001). Thus, paternal and maternal DNA may have distinctive roles in developmental and functional thyroid activity. Although Moore and Haig (1991) have theorized that no imprinted genes exist in avian species, this does not preclude a graded expression of maternal or paternal DNA for thyroid function or a time-dependent response. It may also simply indicate sex-linked inheritance for that particular trait in turkeys. No matter the mechanism of embryo thyroid inheritance, the type of mating used in the production of commercial crosses (i.e., using the line as the sire or as the dam) may affect embryonic thyroid function and survival.

One cannot, however, rule out that simple maternal effects due to the size of the hatching eggs involved may have contributed to the results found herein concerning embryo survival and thyroid function. The reciprocal cross-orthogonal contrasts are a test of confounded maternal and sex-linked effects, and in numerous cases, they were significant for embryo survival and for embryonic T₃ and T₄ levels. As was pointed out by Christensen et al. (2006), egg size in the E and F lines has changed dramatically with long-term selection, and as was discussed by Nestor et al. (1996) and by Emmerson et al. (2002), the genetic correlation between egg production and BW has changed several times during the 38 generations of selection in the E line and has resulted in a dramatic decrease in BW and egg size as concomitant effects of selecting for increased egg number. On the other hand, the BW of the F pureline poults has dramatically increased from the BW of the RBC2 line from which it was derived (Nestor et al., 1996). Egg weight has also increased substantially (0.32 g/generation of selection, Nestor et al., 1996) in the F line. These changes are in good agreement with changes that have taken place in the growth rate of commercial turkeys, in which it has recently been shown that commercial turkeys in 2003 were approximately twice as large at a given age as the RBC2 (Havenstein et al., 2004, 2006, 2007).

Based on the above, it is suspected that the presence of positive reciprocal effects (i.e., confounded maternal and sex-linked effects) in both the E x RBC1 and F x RBC2 data sets are at least partially due to the changes that have taken place in egg size for the 2 selected lines. The E line currently has much smaller egg size than the RBC1 from which it originated (Nestor, personal communication), and the change in egg size has been documented in several published studies by Emmerson et al. (2002), Nestor et al. (1982, 1996), and Nestor and Noble (1995). The reduced egg size (19 g per egg, unpublished data reported by Emmerson et al., 2002) is an expected genetically correlated response to selection for increased egg number (Arthur and Abplanalp, 1975). Long-term selection for increased 16-wk BW has also resulted in an increase in the egg weight (Nestor et al., 1982, 1996; Nestor and Noble, 1995) and poult weight of the F line (Christensen et al., 2006). Again, this is expected, because BW and egg weight have a strong positive genetic correlation in avian species (Kinney, 1969), and, therefore, selection for growth rate should concomitantly increase egg weight.

Sire effects cannot be eliminated entirely, however, because when the F and E sires have been mated to dams of the same commercial line (Christensen et al., 2004), hatchability of the F sire embryos has been improved significantly because of reduced embryo mortality occurring late in development. Further evidence has indicated that sire effects have been present for embryo organ growth and metabolism. The E line sire increased poult weight at hatching, but the F line sire enhanced embryo yolk utilization, jejunum, and skeletal muscle growth compared with the E line sire. The E line sires shortened the developmental period by shortening the time their embryos spent at internal and external pipping compared with the embryos from F or commercial line sires.

Residual yolk was also measured at all developmental stages by Christensen et al. (2006), and the amount of yolk was consistently reduced at all times in the poults from RBC1 line dams compared with those from E line dams. This was not consistent with the findings of Nestor and Noble (1995), who found that the reduction of egg weight in the E line was due to a proportional reduction in all component parts of the egg. This leads one to the conclusion that some of the effects observed could simply be due to differences in embryonic nutrition due to the increased intake of yolk between the selected and randombred lines when used as sires or as dams. This explanation is not supported, however, by the findings of Christensen et al. (2004), in which embryos from E line sires showed depressed yolk utilization in comparison with embryos from F line sires when used with a line producing eggs of the same size. Also, RBC1 embryos utilized more yolk than did embryos from the E line, because they had less residual yolk at hatching.

Egg and RBC1 Lines
Selection for economically important traits caused turkey embryos to respond differently. In agreement with a prior study (Christensen et al., 2005b), reciprocal crosses of E and RBC1 lines in the current study affected embryos differently in the last week of development. The data herein show that heterosis, maternal or sex-linked, and additive effects all contribute to embryo survival. Embryos dying between tucking and external pipping showed significant maternal or sex-linked effects. For example, when the RBC1 sire was used with the E line dam, fewer embryos died at those stages of development than from the reciprocal cross or from the 2 pureline matings. Because T₃ is the more metabolically active hormone, the deiodination of T₄ to T₃ is critically important to thyroid and metabolic responses. Ratios may be indicative of at least 3 physiological responses (Decuypere et al., 1991). Plasma T₃ may increase due to increased monodeiodinase I activity without an increase in T₄, or it may be increased because of reduced monodeiodinase III activity converting T₃ to the biologically inactive form T₂. Secretion of T₄ may also increase or decrease without a concomitant change in T₃ or decreases in activities of either or both monodeiodinase I and III. The unique thyroid response from the cross with the best embryo livability (RBC1 line sire x E line dam) was the increase in the T₃ to T₄ ratio at internal and external pipping from elevated T₃ and T₄, and monodeiodination increased T₃ to a greater extent than T₄ levels. This may be explained by an increase in type I deiodination or a decrease in type III deiodination. When ratios were elevated by increasing T₃ or decreasing T₄ concentrations, survival was reduced, as was the case with crossing E line dams and sires. This may be due to a decrease in thyroid secretion rates, a decrease in type I deiodination, or an increase in type III deiodination. Additional factors that may be involved in the responses seen in the current study could be the effects of corticosterone and thyroid-stimulating hormone on T₄ secretion (Tona et al., 2005). It was clear from the current data that the increased hatchability of embryos from the RBC1 sire crossed with the E line dam was associated with the former case. Dams and sires acted independently until hatching to influence T₃ or T₄ concentrations. However, when the ratios of T₃ to T₄ were examined at external pipping, it was clear that sires influenced the ratio more than dams. Depressed ratios were noted predominantly in the progeny from the E line sires, regardless of the dam used. Thus, a failure of the mechanism controlling T₄ and T₃ ratios in progeny from E line sires may increase embryo death immediately before hatching.

Comparison of F and RBC2 Lines
Embryos from the reciprocal crosses of the RBC2 and F lines survived better than did embryos from either pure-line. The reciprocal crosses also had considerably less mortality at external pipping than did the purelines.

The F line dams had improved embryo survival at tucking and internal pipping compared with RBC2 dams, and crossing dams and sires of F and RBC2 lines improved embryo viability at external pipping compared with the purelines. Embryos from F line dams had consistently about half the concentration of T₃ at internal pipping than did embryos from the RBC2 line dams. This difference disappeared, however, at external pipping and in hatched poults. At the same time, T₄ levels in the F and RBC2 line embryos did not differ, except at internal pipping when the embryos from the RBC2 dams had higher T₄ levels than did the embryos from F line dams. In the F pureline, the T₃:T₄ ratios were greatly depressed at internal pipping, and nearly one-fourth of the embryos died at external pipping. However, when the F sire was crossed with the RBC2 dam, the ratio was elevated; embryo viability improved and resulted in the greatest percentage of embryonic survival. Evidently, increased ratios at these stages of development are critically important to survival of growth-selected embryos. One remarkable observation of embryos from F pureline cross was the extremely low plasma T₃ to T₄ ratio at internal pipping. This was due to a depression in both circulating T₃ and T₄ concentrations as mentioned previously. The F sires and dams exhibited the lowest ratios at both internal and external pipping. This observation may indicate that selection for increased BW interferes with deiodination of T₄ to T₃ in embryos, as has been suggested in chickens (McNabb et al., 1993).

It is clear from the current data that the dam line and the sire line have distinct effects on turkey embryo thyroid function and viability, but the effects observed appear to be line-specific and dependent upon the selection history of the line. The data suggest that either sex-linked or maternal effects are strongly involved in the responses observed. It is not known, however, if they are developmental or functional responses (Christensen et al., 2005a). Although it is known that selection for growth increases avian embryo T₃ (McNabb et al., 1993), separate roles for the effects on thyroid function of the lines when used as dams or as sires was not known. Thus, the current data are the first to describe separate dam and sire effects on the inheritance of embryo thyroid function.

	FOOTNOTES

 
¹ The mention of trade names in this publication does not imply endorsement of the products mentioned nor criticism of similar products not mentioned.

Received for publication October 4, 2006. Accepted for publication January 18, 2007.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Allen, C. P. 1962. The contribution of the plasmon to specific reciprocal cross differences in poultry. Poult. Sci. 41:825–839.[ISI]

Arthur, J. A., and H. Abplanalp. 1975. Linear estimates of heritability and genetic correlation for egg production, body weight, conformation and egg weight of turkeys. Poult. Sci. 54:11–23.[ISI]

Birky, C. W., Jr. 2001. The inheritance of genes in mitochondria and chloroplasts: Laws, mechanisms and models. Annu. Rev. Genet. 35:125–128.[ISI][Medline]

Christensen, V. L., and H. V. Biellier. 1982. Physiology of turkey embryos during pipping and hatching. IV. Thyroid function in embryos from selected hens. Poult. Sci. 61:2482–2488.[ISI][Medline]

Christensen, V. L., and G. S. Davis. 2004. Maternal dietary iodide influences embryonic thyroid hormone levels in turkeys. Int. J. Poult. Sci. 3:550–557.

Christensen, V. L., G. S. Davis, and K. E. Nestor. 2002. Environmental incubation factors influence embryonic thyroid hormones. Poult. Sci. 81:442–450.[Abstract/Free Full Text]

Christensen, V. L., W. E. Donaldson, and K. E. Nestor. 1993. Hatchability and embryonic metabolism in turkey lines selected for egg production and growth. Poult. Sci. 72:829–838.[ISI]

Christensen, V. L., B. D. Fairchild, D. T. Ort, and K. E. Nestor. 2005a. Dam and sire effects on sperm penetration of the perivitelline layer and resulting fecundity of different lines of turkeys. J. Appl. Poult. Res. 14:483–491.[Abstract/Free Full Text]

Christensen, V. L., G. B. Havenstein, D. T. Ort, and K. E. Nestor. 2007. Genetic control of neonatal growth and intestinal maturation in turkeys. Poult. Sci. 86:476–487.[Abstract/Free Full Text]

Christensen, V. L., D. T. Ort, and J. L. Grimes. 2003. Physiological factors associated with weak neonatal poults (Meleagris gallopavo). Int. J. Poult. Sci. 2:7–14.

Christensen, V. L., D. T. Ort, M. J. Wineland, and J. L. Grimes. 2004. Turkey sire effects on embryonic survival and physiology. Int. J. Poult. Sci. 3:80–88.

Christensen, V. L., and P. Phelps. 2001. Injection of thyrotrophin-releasing hormone to turkey embryos elevates plasma thyroxine concentrations. Poult. Sci. 80:643–646.[Abstract/Free Full Text]

Christensen, V. L., M. J. Wineland, I. Yildrum, B. D. Fairchild, D. T. Ort, and K. M. Mann. 2005b. Incubator temperature and oxygen concentrations during the plateau stage in oxygen uptake affect turkey embryo plasma T₄ and T₃ concentrations. Int. J. Poult. Sci. 4:268–273.

Decuypere, E., E. Dewil, and E. R. Kuehn. 1991. The hatching process and the role of hormones. Pages 239–256 in Avian Incubation. S. G. Tullett, ed. Butterworth-Heinemann, London, UK.

Donaldson, W. E., V. L. Christensen, J. D. Garlich, J. P. McMurtry, and N. C. Olson. 1995. Exposure to excessive carbon dioxide: A risk factor for early poult mortality. J. Appl. Poult. Res. 4:249–253.[Abstract/Free Full Text]

Emmerson, D. A., S. G. Velleman, and K. E. Nestor. 2002. Genetics of growth and reproduction in the turkey. 15. Effect of long-term selection for increased egg production on the genetics of growth and egg production traits. Poult. Sci. 81:316–320.[Abstract/Free Full Text]

Grimes, J. L., J. F. Ort, and V. L. Christensen. 1989. Effect of different protein levels fed during the prebreeder period on performance of turkey breeder hens. Poult. Sci. 68:1436–1441.[ISI][Medline]

Hamburger, V., and R. Oppenheim. 1967. Prehatching motility and hatching behavior in the chick. J. Exp. Zool. 166:171–203.[ISI][Medline]

Havenstein, G. B., P. R. Ferket, J. L. Grimes, M. A. Qureshi, and K. E. Nestor. 2004. Performance of 1966 vs. 2003-type turkeys when fed representative 1966 and 2003 turkey diets. Page 112 in Proc. XXII World’s Poult. Congr., Istanbul, Turkey. CD-ROM.

Havenstein, G. B., P. R. Ferket, J. L. Grimes, M. A. Qureshi, and K. E. Nestor. 2007. Comparison of the performance of the 1966- versus 2003-type turkeys when fed representative 1966 and 2003 turkey diets: Growth rates, livability, and feed conversion. Poult. Sci. 86:232–240.[Abstract/Free Full Text]

Havenstein, G. B., P. R. Ferket, J. L. Grimes, M. A. Qureshi, and K. E. Nestor. 2006. Comparison of the performance of 1966 vs. 2003-type turkeys when fed representative 1966 and 2003 turkey diets. 1. Growth rate, livability, and feed conversion. Poult. Sci. 86:232–240.[ISI]

Kinney, T. B. 1969. A summary of reported estimates of heritabilities and of genetic and phenotypic correlations for traits in chickens. Agric. Handbook No. 363. USDA-ARS, Washington, DC.

McMurtry, J. P., I. Plavnik, R. W. Rosebrough, N. C. Steele, and J. A. Proudman. 1988. Effect of early feed restriction in male broiler chicks on plasma metabolic hormones during feed restriction and accelerated growth. Comp. Biochem. Physiol. A 91:67–70.

McMurtry, J. P., R. W. Rosebrough, and N. C. Steele. 1988. Effect of early feed restriction in male broiler chicks on plasma metabolic hormones during feed restriction and accelerated growth. Comp. Biochem. Physiol. A 91:61–70.

McNabb, F. M., E. A. Dunnington, P. B. Siegel, and S. Suvarna. 1993. Perinatal thyroid hormones and hepatic 5'deiodinase in relation to hatching time in weight-selected chickens. Poult. Sci. 72:1764–1771.[ISI][Medline]

Moore, T., and D. Haig. 1991. Genomic imprinting in mammalian development: A parental tug of war. Trends Genet. 17:45–49.

Nestor, K. E. 1984. Genetics of growth and reproduction in the turkey. 9. Long-term selection for increased sixteen-week body weight. Poult. Sci. 56:2114–2122.

Nestor, K. E., and D. O. Noble. 1995. Influence of selection for increased egg production, body weight, and shank width of turkeys on egg composition and the relationship of egg traits to hatchability. Poult. Sci. 74:427–433.[ISI][Medline]

Nestor, K. E., D. O. Noble, J. Zhu, and Y. Moritsu. 1996. Direct and correlated responses to long-term selection for increased body weight and egg production in turkeys. Poult. Sci. 75:1180–1191.[ISI][Medline]

Nestor, K. E., C. F. Strong Jr., and W. L. Bacon. 1982. Influence of strain and length of lay on total egg weight and weight of the component parts of turkey eggs. Poult. Sci. 61:18–24.[ISI]

SAS Institute. 1998. A User’s Guide to SAS 98. Sparks Press Inc., Raleigh, NC.

Tona, K., V. Bruggeman, O. Onagbesan, F. Bamelis, F. Gbeassor, K. Mertens, and E. Decuypere. 2005. Day-old chick quality: Relationship to hatching egg quality, adequate incubation practice and prediction of broiler performance. Avian Poult. Biol. Rev. 16:109–119.

Velleman, S. G., C. S. Coy, J. W. Anderson, R. A. Patterson, and K. E. Nestor. 2003. Effect of selection for growth rate and inheritance on posthatch muscle development in turkeys. Poult. Sci. 82:1365–1372.[Abstract/Free Full Text]

Velleman, S. G., and K. E. Nestor. 2004. Inheritance of breast muscle morphology in turkeys at sixteen weeks of age. Poult. Sci. 83:1060–1066.[Abstract/Free Full Text]

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