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Inheritance of Breast Muscle Morphology in a Line of Turkeys Selected for Increased Egg Production, Its Randombred Control Line, and Reciprocal Crosses Between Them¹

Department of Animal Sciences, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster 44691

² Corresponding author: velleman.1{at}osu.edu

	ABSTRACT

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Breast muscle morphology was studied at 16 wk of age in a line (E) selected over 45 generations for increased egg production, its randombred control line (RBC1), and reciprocal crosses between the E and RBC1 lines. A sample of 10 birds per genetic group-sex subgroup was killed with restraint to prevent flapping of the wings. The skin was removed from the breast region and a sample of breast muscle was obtained in a manner to prevent contraction. The muscle samples were dehydrated, cleared, embedded in paraffin, sectioned, incubated, and rehydrated before staining with hematoxylin and eosin. Four sections from the same muscle from each bird were placed on a slide and the slides were viewed for muscle morphology characteristics with a microscope and digitally recorded. Five fields of each section were viewed. Representative sections of each bird were given a score by 4 individuals based on breast muscle morphology. The scores ranged from 1 (little extracellular matrix and indistinct muscle fibers) to 5 (large extracellular space and distinct muscle fibers). Scores from 2 to 4 were intermediate to these extremes. The data were analyzed for sexes separate and combined.

The E line had lower breast muscle morphology scores than the RBC1 line for males and sexes combined, indicating additive genetic variation in the scores. Nonadditive genetic variation was not an important source of variation for breast muscle morphology scores based on the contrast of the average of the parental lines with the average of the reciprocal crosses for males, females, or sexes combined. In 5 of 6 possible comparisons, the breast muscle morphology scores of the reciprocal cross were not significantly different from the line of the dam in the reciprocal cross. The only exception was for the E sire x RBC1 dam cross based on the data for females, wherein the breast muscle morphology scores were higher in the cross than in the pure RBC1 line. The results of the current study confirm the maternal inheritance of breast muscle morphology scores at 16 wk of age that has been previously reported.

Key Words: turkey • breast muscle morphology • maternal inheritance • additive genetic variation • nonadditive genetic variation

	INTRODUCTION

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Growth, feed conversion, and muscling have improved in commercial turkeys (Nestor et al., 1969; Havenstein et al., 2004a,b), but meat quality has been altered. The turkey processing industry is experiencing a meat quality problem that is similar to the pale, soft, and exudative (PSE) condition in swine (Sosnicki and Wilson, 1991). When cooked, turkey PSE meat has a soft texture, poor meat binding, poor juiciness due to reduced water-holding capacity, and increased yield losses.

The inheritance of breast muscle morphology in turkeys has been studied during the embryonic (Velleman et al., 2002) and posthatch (Velleman et al., 2003b) periods. For these studies, comparisons were made among a randombred control line (RBC2), a subline (F) of the RBC2 line selected long term for increased 16-wk BW, and a commercial sire line (B). In most of the muscle traits measured, additive genetic variation was an important source of variation during the embryonic and posthatch periods as indicated by line differences. Nonadditive genetic variation, as measured by contrasts of the average of reciprocal crosses of the F and B lines with the average of the parental lines, was a more important source of variation at 20 d of incubation than at 25 d of incubation (Velleman et al., 2002). In general, nonadditive genetic variation was not an important source of variation posthatch (Velleman et al., 2003b).

Development of the breast muscle in turkeys is altered by genetic increases in BW during the embryonic period (Velleman et al., 2002) and posthatch (Velleman et al., 2003b). Wilson et al. (1990) reported that more degenerating muscle fibers were found in rapidly growing turkey lines than in slower growing lines and the damage increased with age. Velleman et al. (2003a) studied damage to the turkey pectoralis major muscle in the B, F, and RBC2 lines during the embryonic (25 d) and posthatch (from 1 to 20 wk) periods. Beginning at 8 wk posthatch, differences in muscle fiber morphology were observed among the different lines. The RBC2 line maintained well-organized muscle fibers and muscle fiber bundles with large capillary networks throughout the study. In contrast, the BW-selected F line began to show muscle fiber degeneration at 8 wk posthatch, and limited capillary beds were observed as development proceeded. The B line had intermediate muscle morphology between the RBC2 and F lines, but by 20 wk posthatch, significant muscle fiber degeneration was present with limited capillary supply. The results indicated that genetic increases in BW were associated with muscle damage.

Velleman and Nestor (2005) studied breast muscle morphology at 8 and 16 wk of age in a line (E) selected over 44 generations for increased egg production and its randombred control (RBC1). Based on a sample of 20 birds per sex-line-age subgroups, breast muscle morphology scores [1 (little extracellular matrix and indistinct muscle fibers) to 5 (large extracellular space and distinct muscle fibers)] did not differ between lines or ages, but there was a significant interaction between lines and ages. The scores increased in the RBC1 line from 8 to 16 wk of age but the reverse was true for the E line.

Velleman et al. (2003c) found evidence of maternal inheritance in breast muscle morphology scores at 16 wk of age in reciprocal crosses of the F and B lines and F and RBC2 lines. In both crosses, the averages of the reciprocal crosses were similar to the average of the parental lines. Velleman and Nestor (2004) studied the inheritance of breast muscle morphology scores in the RBC2 and F lines and the F₁ and F₂ crosses of the lines. Possible maternal inheritance was observed in the crosses.

The objective of the present experiment was to study the inheritance of breast muscle morphology scores of turkeys at 16 wk of age. For this purpose, the E and RBC1 lines and their reciprocal crosses were compared.

	MATERIALS AND METHODS

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Genetic Stocks and Matings
The RBC1 line is a randombred control line that was developed by crossing 4 commercial strains of turkeys in all possible combinations (McCartney, 1964) and was closed in 1960. The RBC1 line has been maintained without conscious selection using a paired mating system (Nestor, 1977b). The number of parental pairs used in the reproduction of the RBC1 line was 48 in generations 1 and 2 and 36 pairs thereafter. With the system of maintenance of the RBC1 line, little genetic change was expected or observed (Nestor, 1977a; Noble et al., 1995).

The E line was a subline of the RBC1 line that was developed by selecting only for increased egg production for various periods (84 d in generations 1 to 3, 180 d in generations 4 through 26, and 250 d thereafter). The E line was maintained with 48 parental pairs in the first 2 generations, 36 parental pairs in generations 3 to 5, and 72 parental pairs thereafter. Details of the maintenance of the E line and response to selection in the E line have been given previously (McCartney et al., 1968; Nestor, 1971; Anthony et al., 1991; Nestor et al., 1996). The E line was in the 45th generation of selection at the time of the present study.

Reciprocal crosses of the E and RBC1 lines were produced using 14 females from each line. The males used in the reciprocal crosses were those used in the reproduction of the pure lines and were mated to a single female at each weekly insemination. To obtain as large a genetic base as possible, the male assigned to a female in the crosses was different at each artificial insemination. For simplicity, the sire will always be listed first in the reciprocal cross designations.

Management of Birds
The birds were produced in a single 2-wk hatch, grown, sexes separate, in confinement in different houses. All birds were provided a declining protein ration system (Naber and Touchburn, 1970) based on the schedule for males. Continuous lighting was provided from hatching to 8 wk of age, at which time daylight was reduced to 12 h and remained at that level until the end of the experiment.

Immunohistochemistry
A sample of 10 birds per genetic group-sex subgroup was killed at 16 wk of age by severing the jugular vein with restraint to prevent flapping of the wings. The skin was immediately removed from the breast region and a sample of the pectoralis major muscle was obtained by carefully dissecting the muscle as described by Velleman et al. (2003b). The muscle samples were dehydrated, cleared, embedded in paraffin, sectioned at 5 µm, and mounted on slides as previously reported (Velleman et al., 2002). Before staining with hematoxylin and eosin, the muscle tissue sections were incubated at 55°C for 20 min and then rehydrated for 10 min in ProPar Clearant (Anatech, Battle Creek, MI): 2 min in 100% ethanol, 2 min in 95% ethanol, 2 min in 70% ethanol, 2 min in 50% ethanol, and 2 min in distilled H₂O. Staining with hematoxylin and eosin was as described in Velleman et al. (2002). The stained sections were viewed for muscle morphological characteristics with an Olympus XI 70 microscope and digitally recorded with an Olympus Magna Fire digital camera (Olympus America, Inc., Melville, NY). Four sections from each bird were placed on a slide; 5 fields of each section were viewed.

Muscle Measurements and Statistical Analysis
Representative sections were rated by 4 individuals based on breast muscle morphology (Velleman et al., 2003c). In brief, the ratings ranged from 1 (little extracellular matrix and indistinct muscle fibers) to 5 (large extracellular space and distinct muscle fibers). Ratings of 2 to 4 were intermediate to these extremes. The average rating scores for the 4 individuals were analyzed.

The data were analyzed with genetic group and sex as main effects. The data for the 2 sexes were also analyzed separately with genetic group as the main effect. A comparison of the E and RBC1 lines was used as a measure of additive genetic variation. Heterosis, a measure of non-additive genetic variation, was calculated as the percentage deviation of the mean of the 2 reciprocal crosses from the mean of the parental lines.

Differences between reciprocal crosses were a measure of maternal effects or sex linkage (confounded). Contrasts were used to test the significance of line effects, heterosis, and maternal or sex-linked effects.

	RESULTS

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The E and RBC1 lines differed significantly in breast muscle morphology scores when the analysis was based on males and sexes combined (Table 1). The reciprocal crosses differed in breast muscle morphology scores in all 3 analyses. When the E line was used as the dam in the reciprocal cross, the breast morphology score in the reciprocal cross did not differ from that of the pure E line when the analysis was based on males, females, or sexes combined. When the RBC1 line was used as the dam in the reciprocal cross, the breast morphology scores did not differ from that of the pure RBC1 line for males and sexes combined, but the breast morphology score for the E x RBC1 crosses was higher than that of the RBC1 line when only females were included in the analysis. Heterosis was not an important source of variation in breast morphology scores for males, females, or sexes combined.

	DISCUSSION

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Scheuermann et al. (2004) evaluated muscle morphology in broiler and Leghorn lines at 7 and 21 d of age and found highly significant Pearson correlation coefficients between myofiber density (number of fibers per mm²) and BW (–0.85), breast weight (–0.83), and breast yield (–0.88). Considering the line differences in BW and the apparent correlations with weight, yield, and myofiber density, it is somewhat surprising that muscle morphology scores were reduced regardless of whether selection directly or indirectly influenced BW.

It is curious that the selection for increased BW (Velleman and Nestor, 2004) and increased egg production (Velleman and Nestor, 2005; current study) resulted in declines in breast muscle morphology as measured by subjective scoring. It appears that, although muscle morphology scores have declined in both selection studies, it may be for different reasons. The subjective scoring system (Velleman et al., 2003c) was established on 2 components: the amount of extracellular space and the presence of distinct muscle fibers. Selection for increased egg production has clearly resulted in correlation reductions in BW (McCartney et al., 1968; Nestor, 1971, 1980; Anthony et al., 1991; Nestor et al., 1996) and breast yield on an absolute and relative basis (Nestor et al., 1995). Consistent with that observed for leghorns (Scheuermann et al., 2004), E-line turkeys appear to have more myofibers per mm² than the RBC1 line and relatively less extracellular space. Although the previously studied weight-selected population (Velleman and Nestor, 2004) had unchanged myofiber cross-sectional area when compared with the randombred population of origin, they appeared less distinct. In addition, the amount of extracellular space was reduced for the weight-selected population (Velleman and Nestor, 2004). Although the E line (current study) and the weight-selected line (Velleman and Nestor, 2004) had reduced extracellular space relative to their respective randombred control, the muscle morphology of the weight-selected line was further exacerbated by reduced myofiber quality.

Direction changes observed for muscle morphology in E-line turkeys relative to the RBC1 line were not as great as observed for the weight-selected line of turkeys relative to the line of origin. In fact, Velleman and Nestor (2004) reported that the subjective muscle morphology score of the weight-selected line was half that of the RBC2 line (1.77 and 3.72, respectively). In the current study, muscle morphology scores of the E line was 3.16 compared with 3.84 for the RBC1 line. It is clear that muscle morphology was altered more by selection for increased BW than for increased egg production.

One possible explanation for increases and decreases in BW being associated with a similar change in breast muscle morphology is that long-term selection for either increased BW or increased egg production has influenced genetic homeostasis. Lerner (1954) defined genetic homeostasis as the property of the population to equilibrate its genetic composition and to resist sudden changes. One contributing mechanism to genetic homeostasis is the superiority with respect to fitness of the heterozygous over the homozygote genotype (Lerner, 1954). It has been well established that long-term selection decreases the frequency of heterozygotes (Falconer, 1982). Thus, it would be expected that heterozygosity would be reduced in the E and F lines that had been selected long term for increased egg production and increased 16-wk BW, respectively. With the system of maintenance of the randombred control line in the long-term selection studies, little genetic change was expected or observed (Nestor, 1977a; Noble et al., 1995). However, Nestor et al. (2000) found that developmental stability of turkey populations, as measured by bilateral asymmetry, was influenced more by BW differences than by homozygosity.

The reduction in breast muscle morphological scores may also be attributable to the amount of perimysial space surrounding the muscle fibers. The perimysial spacing is where capillary beds are located; the capillary beds are necessary to remove lactic acid from the muscle. The pectoralis major muscle is a glycolytic muscle that through its anaerobic respiration results in the formation of lactic acid. If less lactic acid could be removed from the muscle, this would result in a decrease in pH and increase in muscle damage (Velleman et al., 2003a). A reduction in perimysial spacing surrounding the muscle fibers may be the result of a lower expression of chondroitin sulfate–containing proteoglycans during early embryonic muscle formation. It has been postulated that the chondroitin sulfate proteoglycans, because of their high negative charge, ionically bind to water and result in the spacing of the developing muscle fibers (Fernandez et al., 1991). Thus, reduced expression of chondroitin sulfate proteoglycans during early embryonic muscle development would lead to muscle fibers being closer to one another with a reduced area for capillary bed formation. In cartilage, the absence of the chondroitin sulfate proteoglycan leads to the structural collapse of the limb and tracheal cartilage, and chondrocytes that have limited spacing between them due to a decrease in extracellular spacing (Pennypacker and Goetinck, 1976). In chickens, this condition is called nanomelia. Future studies need to address the expression levels of the chondroitin sulfate proteoglycan during early embryonic muscle development because this may serve as an important predictive marker for muscle integrity in the posthatch bird.

Velleman et al. (2003c) and Velleman and Nestor (2004) presented evidence of maternal inheritance of breast muscle morphology of turkeys at 16 wk of age. The results of the current study support the maternal inheritance of the breast muscle morphology scores. In 5 of 6 possible comparisons, the breast muscle morphology scores of the reciprocal cross were not significantly different from the line of the dam in the reciprocal cross. The only exception was for the E x RBC1 cross in females in which the breast muscle morphology scores were higher in the cross than in the pure RBC1 line.

	FOOTNOTES

 
¹ Salaries and research support provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University.

Received for publication June 28, 2006. Accepted for publication July 29, 2006.

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