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Myogenesis and postnatal skeletal muscle cell growth as

influenced by selection

*

C. Rehfeldt , I. Fiedler, G. Dietl, K. Ender

Divisions of Muscle Biology and Growth and Genetics and Biometry, Research Institute for the Biology of Farm Animals,

Wilhelm-Stahl-Allee2, D-18196 Dummerstorf, Germany

Abstract

The major component of a given muscle is the constituent muscle fibres. Lean growth and ultimate muscle mass are therefore largely determined by the number of muscle fibres and the size of those fibres. During myogenesis, myoblasts develop from mesenchymal precursor cells by proliferation and myogenic commitment. Myoblasts subsequently fuse to form multinucleated myofibres. Postnatal growth of skeletal muscle is mainly realised through increases in length and girth of the muscle fibres, but not by increases in muscle fibre number. Postnatal fibre hypertrophy, associated with accumulation of myonuclei (satellite cell proliferation) and muscle-specific proteins, is inversely correlated with the number of prenatally formed muscle fibres. On the other hand, both fibre number and fibre thickness are positively correlated with muscle mass and lean meat percentage. Both fibre number and fibre size are influenced by selection as shown by differences between breeds and correlated responses to (lean) growth selection. Increases in muscle mass solely by fibre hypertrophy, as observed particularly in meat-type pigs and chickens, may be associated with problems in stress adaptability and ultimate meat quality. Genetic variability and heritability of muscle fibre number and size are sufficiently high to include these traits in farm animal selection in addition to commonly used selection criteria for improving lean meat content and meat quality.  2000 Elsevier Science B.V. All rights reserved.

Keywords: Muscle fibre; Growth; Meat; Selection; Heritability; Genetic correlation

1. Introduction muscle fibres and the size of those fibres. Current research suggests that animals with greater numbers

The understanding of the growth and development of muscle fibres of moderate size produce more meat

of skeletal muscle is one of the most important goals of better quality. During myogenesis, the extent of

in animal science. The major component of a given muscle cell multiplication largely determines how

muscle is the constituent muscle fibres. Muscle mass many muscle fibres are formed. Therefore, the

is therefore largely determined by the number of number of muscle fibres is mainly determined by

genetic factors and those environmental factors

which are capable of influencing prenatal

*Corresponding author. Tel.: 149-38208-68853; fax: 1

49-myogenesis. The aim of this paper is to describe the

38208-68852.

E-mail address: [email protected] (C. Rehfeldt). principles of skeletal muscle growth, to highlight the

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importance of muscle cell growth in animal per- Myonuclei themselves remain mitotically quiescent.

formance and to explain how it is influenced by The importance and relations of the different

selection. myogenic lineages (primary and secondary) are not

yet clarified. It seems, however, that the lineage’s are not related to fibre type composition (Hughes and

2. Principles of skeletal muscle growth Blau, 1992).

2.1. Prenatal development 2.2. Postnatal growth

During embryonic development, myoblasts de- During postnatal growth, the increase in skeletal

velop from myogenic precursor cells which are of muscle mass is mainly due to an increase in muscle

mesodermal origin (Fig. 1). These cells are de- fibre size (hypertrophy). This process is

accom-termined to enter the myogenic lineage and are able panied by the proliferative activity of satellite cells

to proliferate and divide to establish a pool of which are the source of new nuclei incorporated into

myoblasts. Special signals cause the myoblasts to the muscle fibres. After birth, total muscle fibre

exit the cell cycle, to stop dividing and to differen- number has been reported to remain unchanged in

tiate. They begin to express muscle cell-specific mammals and birds by most authors. No significant

proteins and finally fuse to form multinucleated changes in postnatal fibre number have been found in

myotubes. mice (e.g., Rowe and Goldspink, 1969; Nimmo and

During myogenesis, muscle fibres develop from Snow, 1983), rat (e.g., Brown, 1987; Rosenblatt and

two distinct populations. Fibres which form during Woods, 1992; Schadereit et al., 1995), pig (e.g.,

the initial stages of myoblast fusion are primary Fiedler, 1983), cattle (e.g., Wegner et al., 2000),

myofibres which provide a framework for the larger chicken (e.g., Smith, 1963) and quail (e.g., Fowler et

population of smaller secondary fibres (e.g., Beer- al., 1980).

mann et al., 1978; Miller et al., 1993). These are Some reports have indicated increases in muscle

formed from foetal myoblasts during a second wave fibre number shortly after birth in rodents (e.g.,

of differentiation. Another population of myoblasts Rehfeldt and Fiedler, 1984; Summers and Medrano,

does not form fibres but stays close to the myofibres; 1994) and pigs (Swatland, 1975; Fiedler et al.,

these are termed satellite cells and they are able to 1998). In these studies, fibre counts were done on

divide and serve as the source of new myonuclei histological transverse sections. It is possible that the

during postnatal growth (Moss and Leblond, 1971; increase in fibre number during the first days of

Schultz, 1974). They contribute to growth of the postnatal life in rodents is a result of maturation and

fibres and also participate in regeneration processes. elongation of the existing myotubes rather than due

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to production of new fibres (Ontell and Kozeka, 1984). This may be true also for pig muscle, since fibre formation is known to be finished at about day 70 of gestation (Swatland, 1973).

Fig. 2 depicts the postnatal development of muscle fibre thickness and muscle fibre number in different muscles of the mouse and pig. Muscle fibres grow in size towards a plateau, whereas fibre number remains constant after initial increases shortly after birth. Decreases in fibre number with ageing (e.g.,

Faul-Fig. 3. Relationships by linear phenotypic correlation coefficients

kner et al., 1972) are possibly related to a reduction

between muscle cross-sectional area, muscle fibre size (diameter

in physical exercise. Activity stimuli are able to

or cross-sectional area) and muscle fibre number per cross-section

induce increases whereas disuse of muscles may be _{(Staun, 1968, 1972; Osterc, 1974; Rehfeldt and Fiedler, 1984;}

followed by decreases in muscle fibre number (see Locniskar et al., 1980; Rehfeldt et al., 1988, 1989; Fiedler et al.,

1997; Larzul et al., 1997).

Rehfeldt et al., 1999).

At this point, an interesting phenomenon of mus-cle growth should be emphasised. Postnatal musmus-cle

fibre hypertrophy depends on the total number of clear antagonism between fibre thickness and fibre

muscle fibres within a muscle. The postnatal growth number would be that nutritional energy is

distribut-rate of the individual muscle fibre is lower when ed evenly among all fibres. However, the correlation

there are high numbers of fibres and higher when coefficient is not 21.0 which means that some

there are low numbers of fibres. This can be con- animals exhibit fast-growing fibres despite high fibre

cluded from the fact that muscle fibre number is numbers.

inversely correlated with muscle fibre thickness at the end of the intensive growth period. Negative

correlation coefficients were estimated when the 3. Importance of muscle fibre number and size

animals were slaughtered at the same age (mouse: for animal performance

Rehfeldt et al., 1988, 1989; chicken: Locniskar et al.,

1980; pig: Fiedler et al., 1997), at almost the same 3.1. Lean growth

weight (pig: Staun, 1968, 1972; Larzul et al., 1997)

or at a different age and weight (cattle: Osterc, From the principles of skeletal muscle growth, it

1974). On the other hand, both fibre number and becomes clear that lean growth depends on the

fibre thickness are positively correlated with muscle number of the prenatally formed fibres and on the

cross-sectional area (Fig. 3). An explanation for this degree of their postnatal hypertrophy. This has been

Fig. 2. Postnatal development of muscle fibre thickness (cross-sectional area or diameter) and total muscle fibre number per muscle cross-section in: (a) rectus femoris muscle of laboratory mice (Rehfeldt and Fiedler, 1984); (b) semitendinosus muscle of German Landrace pigs (Fiedler, 1983; Rehfeldt et al., 1993).

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confirmed by significant positive correlation coeffi- Wegner et al., 2000). This increase in muscle fibre

cients of muscle mass or lean meat percentage with number is associated with increases in muscle mass

both fibre number and size (Otto and Wegner, 1976; of $ 20% (Shahin and Berg, 1985; Wegner et al.,

Fiedler and Otto, 1982; Klosowska et al., 1985; 2000). Another example of muscular hypertrophy is

Larzul et al., 1997; Henckel et al., 1997). On the the callipyge condition in sheep which is associated

other hand, it seems to be important to which extent with selective fibre hypertrophy (Carpenter et al.,

each of the two fibre characteristics contribute to 1996).

lean growth. The potential for lean growth of an

animal largely depends on the number of the prenat- 3.2. Meat quality /stress susceptibility

ally formed muscle fibres, because the postnatal

increase in muscle fibre size is limited by genetic and It was discussed above that low muscle fibre

physiological reasons. The latter is supported by the number correlates with fibres which exhibit greater

following results. A 15-week treatment with porcine hypertrophy. However, strong fibre hypertrophy

somatotrophin (pST), which repartitions nutrients to seems to reduce the capacity of the fibres to adapt to

muscle, was able to accelerate fibre growth in activity-induced demands which in turn may be

Landrace pigs, but the maximum fibre size did not associated with stress susceptibility and poor meat

exceed that of the control pigs attained 5 weeks later quality in modern meat-type pig breeds (Cassens et

(Rehfeldt et al., 1996). In Pietrains, representing the al., 1975; Fiedler et al., 1993, 1999; Wicke et al.,

pig breed with the largest muscle fibres, exogenous 1991; Lengerken et al., 1997). Possibly energy and

pST was not capable at all of increasing fibre size oxygen supply are limited with increasing fibre size

(Rehfeldt and Ender, 1995) and, similarly, Sørensen due to reduced capillary density (Cassens and

et al. (1996) suggested that pig genotypes with larger Cooper, 1971; Fiedler et al., 1993) and nuclear

muscle fibres are less responsive to pST treatment control of cellular processes may be impaired in

than genotypes with smaller fibres. On the other large fibres which often exhibit a low

nuclear:cytop-hand, pigs are mostly slaughtered before their po- lasm ratio (Cheek et al., 1970; Rehfeldt and Ender,

tential for lean growth is exhausted, so that in most 1995). Particularly in modern meat-type pigs and

cases the rate of lean growth, depending on the rate chickens, larger fibres tend to have lower numbers of

of muscle fibre hypertrophy (e.g., Larzul et al., mitochondria, and they belong to the white,

fast-1997), seems to be of greater interest than the contracting type. In pigs, higher white fibre

per-potential of lean growth. Although within breed centages have been shown to correlate with the PSE

phenotypic correlation coefficients are mostly in- (pale, soft, exudative) meat condition (Linke, 1972;

significant (e.g., Fiedler and Otto, 1982; Larzul et al., Larzul et al., 1997; Fiedler et al., 1999) and with

1997), there is some evidence that pigs with more stress susceptibility (Nelson and Schochet, 1982;

muscle fibres exhibit less fat (Stickland and Fiedler et al., 1993, 1999). These fibres produce

Goldspink, 1975; Kuhn et al., 1998). This may be energy for contraction mainly by the glycolytic

related to the fact that the plateau of muscle fibre pathway and, under energy-demanding conditions

growth is achieved earlier at lower fibre numbers, (e.g., before slaughter), their metabolism contributes

and that afterwards available nutrients are preferen- to a very fast pH decline by over-production of

tially used for fat deposition. In part, this may lactate which cannot be removed. This in turn is

explain the fact that the highest lean meat percentage related to the PSE condition after slaughter.

cannot be expected at the maximum fibre size Lengerken et al. (1997) investigated the

relation-(Lengerken et al., 1997). ship between muscle fibre number and pH value of

The relationship between muscle fibre number and pig longissimus muscle and meat percentage after

lean growth becomes very obvious by the example of slaughter. They were able to demonstrate that there

double-muscled cattle which exhibit almost double is a range of optimum muscle fibre number which

the number of muscle fibres compared with other guarantees both high meat percentage and good meat

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Table 1

a ´

Meat characteristics dependent on the total muscle fibre number of longissimus muscle in Pietrain pigs (mean6S.D.) 3

Class of muscle fibre number (310 )

Low Middle High

800–1000 .1000–1200 .1200–1600

Number of animals 9 9 8

Total fibre number (310 ) 908656 1112657 13256110

Fibre diameter (mm) 86.068.2 77.568.6 67.165.4

Lean meat (%) 60.062.3 59.862.4 59.163.4

Loin muscle area (cm ) 54.962.0 57.266.0 58.267.5

pH 45 min p.m. 5.9560.36 6.0160.44 6.2060.39

Reflectance 17 h p.m. 4863 4964 4663

Drip loss (%) 4.0162.21 4.3962.85 2.9161.45

Halothane status as the number of homozygous negative / homozygous positive pigs: low, 3 / 6; middle, 4 / 5; high, 2 / 6.

Pietrain pigs with the highest number of low-size Larzul et al. (1997), Klont et al. (1998) and Karlsson

fibres in the longissimus muscle tended to exhibit the et al. (1999).

best meat quality without significant differences in lean meat percentage and loin muscle area. From

data reported by Maltin et al. (1997), it may be 4. Influence of selection on muscle fibre size and

suggested that strong muscle fibre hypertrophy con- number

tributes to poor tenderness of pig muscle. Similarly,

extreme muscle fibre hypertrophy in callipyge lambs 4.1. Genetic variability /heritability

has been reported to be associated with poor meat

quality such as reduced tenderness and juiciness Whether and to what extent a biological trait is

(Shackelford et al., 1997). inherited and can be changed by selection largely

The relationships between fibre number, fibre size depends on its genetic variability, heritability and

and meat quality are most obvious when comparing genetic correlation to the criteria used in selection.

genotypes or groups of pigs with extremely different As shown in Table 2, about half (mouse) or

two-lean percentage or meat quality, whereas significant thirds (pig) of the phenotypic standard deviation in

within-breed correlations are scarcely presented. muscle fibre number is due to genetic origin. This

Also, within normal cattle breeds, no correlations proportion is relatively high as compared with

between fibre characteristics and meat quality traits performance traits commonly used in selection of

were found in (e.g., Wegner et al., 2000). However, farm animals.

double-muscled cattle exhibit paler meat and higher Several studies have been conducted to estimate

proportions of glycolytic fibres despite higher fibre

numbers and similar fibre size compared with other _{Table 2}

cattle breeds (e.g., Holmes and Ashmore, 1972; Phenotypic and genetic variation coefficients (CV , CV ; %) ofp g

a muscle fibre number and size (cross-sectional area or diameter)

Wegner et al., 2000).

The results suggest that fibre size and fibre Species / muscle Fibre number Fibre size

metabolism may be also independently related to

CVp CVg CVp CVg

ultimate meat quality and that only one small part of

Mouse / extensor 18.9 9.3 17.8 8.2

its phenotypic variation is due to variations in muscle

digitorum longus

fibre characteristics. The relationships between meat

Pig / longissimus 25.9 17.1 13.6 7.6

quality and muscle fibre type composition are not

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Table 3

2 a

Estimates of heritability (h ) for muscle structure traits 2

Species: Heritability (h )

muscle Fibre number (area or diameter) Fibre size Reference

Mouse:

extensor digitorum longus 0.23–0.24 0.16–0.21 Rehfeldt et al. (1988)

soleus 0.44–0.68 0.07 Nimmo et al. (1985)

Chicken:

pectoralis superficialis 0.12–0.49 0.00–0.26 Locniskar et al. (1980)

Pig:

longissimus 0.66–0.88 0.17–0.31 Staun (1968)

0.43–0.48 0.30–0.50 Staun (1972)

0.28–0.41 0.22–0.34 Fiedler et al. (1991),

Dietl et al. (1993)

0.22 0.34 Larzul et al. (1997)

Cattle:

longissimus ND 0.29 Gravert (1963)

0.35 0.74 Osterc (1974)

ND 0.39 Andersen et al. (1977)

Ranges arise from the application of different methods of heritability estimation. ND, not determined.

the heritability of muscle fibre traits by use of 4.2. Differences between breeds

different methods. Heritability has been defined in

both a broad sense and a narrow sense (Falconer, The influence of growth selection on muscle fibre

1981). Estimated by the twin method (e.g., Komi and number or size is also apparent from differences

Karlsson, 1979), the heritability is the extent to between animals of different breeds or between wild

which individual variation of a population is ge- and domestic types of the same species.

netically determined. On the other hand, heritability The European domestic pig, which was derived

in a narrow sense can be estimated by the use of from the European wild pig, exhibits larger fibres

artificial selection experiments (e.g., Nakamura et al., (Bader, 1983; Szentkuti and Schlegel, 1985; Weiler

1993), that is, the extent to which the individual et al., 1995) but also higher numbers of fibres (e.g.,

variation within a population is passed on to the next semitendinosus muscle, Table 4). Clear differences

generation. The coefficients of heritability estimated in muscle fibre number, but not in muscle fibre

for muscle fibre number (Table 3) range from 0.12 to 0.88, most lying between 0.2 and 0.5. These results

Table 4

demonstrate that muscle fibre number is not

exclu-Muscle fibre number and muscle fibre cross-sectional area

sively determined genetically as has been previously

(LSMeans6S.E.) in the semitendinosus muscle of wild-type (WP)

presumed owing to its relative constancy during _{and domestic pigs (DP) at 7 and 20 weeks of age}

postnatal life. Probably, maternal factors

(environ-Weeks of age

mental and genetic) are significant determinants of

7 20

muscle fibre number as the formation of fibres occurs

prenatally. Maternal influence on fibre number has Fibre number (310 ) WP 611638 554629

DP 908654** 860654**

been estimated for mouse Extensor digitorum longus

muscle and reported to be about 17% of the pheno- Fibre cross-sectional WP 407636 14406136

area (mm ) DP 1082651*** 38556255***

typic variance (Rehfeldt et al., 1988). Heritability

estimates for muscle fibre size range from low to **P,0.01, ***P,0.001 for differences between DP (German

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thickness, were reported between Large White and factor (GDF-8) that belongs to the transforming

miniature pigs of the same age (Stickland and growth factor-b (TGF-b) superfamily and has been

Handel, 1986). No marked differences in muscle identified as an important negative regulator of

fibre number and size of the longissimus muscle muscle development in a mouse model of gene

were apparent between different modern meat-type deletion (McPherron et al., 1997). The callipyge

pig breeds and crosses in contrast to the ‘older’ fatty condition in sheep as a further example of extreme

Saddle Back breed which has a lower fibre number muscular hypertrophy is caused by a mutation of the

and size (Table 5). When comparing the same callipyge gene located on ovine chromosome 18

muscle of several European pig breeds 20 years ago, (Cockett et al., 1994). In contrast to the

double-Staun (1963) found differences in muscle fibre size muscled condition in cattle, muscular enlargement in

and number. Possibly, in modern meat-type pig callipyge lambs seems mainly to be due to muscle

breeds, e.g., Pietrain or Large White, fibre number fibre hypertrophy (Carpenter et al., 1996).

and size are at the limits of their correlated responses

to selection for leanness, and new strategies must be 4.3. Correlated selection responses

applied to attain further changes.

There are no obvious differences in muscle fibre 4.3.1. Selection experiments

number and size in most of the cattle breeds (e.g., Genetic relationships between animal performance

Osterc, 1974; Wegner et al., 2000). However, an and muscle fibre characteristics can be derived from

exception are double-muscled cattle which exhibit both selection experiments and from genetic

correla-almost double the number of muscle fibres compared tion coefficients.

with other cattle breeds, whereas no differences in Differences in muscle mass obtained by breeding

fibre size are apparent (Ouhayoun and Beaumont, and selection are due to changes in both muscle fibre

1968; Holmes and Ashmore, 1972; Wegner et al., number and muscle fibre size. This can be concluded

2000). Prenatal studies with double-muscled cattle from a series of selection experiments for large body

suggest that the higher number of muscle fibres is a size or rapid growth rate with several species

includ-consequence of delayed differentiation and extended ing the mouse (Luff and Goldspink, 1967; Hanrahan

myoblast proliferation (Picard et al., 1995), and et al., 1973; Aberle and Doolittle, 1976; Penney et

serum from double-muscled foetuses induced higher al., 1983; Rehfeldt and Otto, 1985; Timson et al.,

proliferative responses in L6 myoblasts compared 1985; Rehfeldt and Bunger, 1990; Brown and

Stick-with serum of normal cattle foetuses (Gerrard and land, 1994; Summers and Medrano, 1994), pig

Judge, 1993). The double-muscled phenotype arises (Wicke, 1989; Wicke et al., 1991; Brocks et al.,

from mutations in the myostatin gene (Grobet et al., 1998), chicken (Smith, 1963; Mizuno and Hikami,

1997; Kambadur et al., 1997; McPherron and Lee, 1971; Aberle and Stewart, 1983; Remignon et al.,

1997). Myostatin is a growth and differentiating 1994, 1995), quail (Fowler et al., 1980) and turkey

(Cherel et al., 1994).

Growth selection leads to increases in myoblast and / or satellite cell proliferation rates as indicated

Table 5

by higher myonuclear numbers (e.g., Knizetova et

Muscle fibre number and diameter (mean6S.D.) in the

longis-al., 1972; Penney et longis-al., 1983; Brown and Stickland,

simus muscle of different pig breeds (Fiedler et al., 1989; Kuhn et

1994), higher DNA synthesis rate (Knizetova et al.,

al., 1998)

1972) and higher total muscle DNA content (e.g.,

Pig breed (n) Fibre number Fibre diameter

6 Knizetova et al., 1972; Martin and White, 1979;

(310 ) (mm)

Fowler et al., 1980; Campion et al., 1982; Jones et

German Landrace (694) 1.04160.280 68.969.5

al., 1986; Mitchell and Burke, 1995). We also

German Large White (137) 1.01660.251 70.068.4

recently demonstrated this by the in vitro growth of

Leicoma (1052) 1.06160.275 68.669.4

Schwerfurter (77) 1.10960.309 68.9610.7 satellite cells derived from differently selected mouse

Pietrain (26) 1.10760.178 71.368.8 _{lines (Fig. 4). According to the principles of skeletal} Saddle Back (17) 0.90960.178 67.167.8

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Burke, 1995), but no increases in IGF-I concen-trations were found. The correlated responses of these and other hormones and growth factors to growth selection need to be further investigated. 4.3.2. Genetic correlation coefficients

Changes that are to be expected in response to selection can be predicted from genetic correlation coefficients. It has been found consistently that the antagonism between fibre size and number men-tioned above is based on a genetic relationship. The genetic correlation coefficients between fibre size and number estimated for the mouse, chicken and

Fig. 4. DNA accumulation in cultures of satellite cells isolated

pig were found to range from 20.4 to 20.8 (Staun,

from mouse lines selected for 6-week protein accretion (DU-6P),

body weight (DU-6) or an index from body weight and treadmill 1972; Locniskar et al., 1980; Rehfeldt et al., 1988;

performance (DU-61LB) over 71 generations, and from a _{Fiedler et al., 1997; Larzul et al., 1997).} Conse-control (DU-Ks). FBS, foetal bovine serum (Walther, 1999).

quently, selection of animals with high muscle mass due mainly to large fibres will in turn produce offspring with low fibre number.

to the formation of higher muscle fibre numbers and, In pigs, positive genetic correlations were

ob-postnatally, to the accumulation of more myofibre served for muscle fibre number or size with lean

nuclei. There is some evidence that selection for meat percentage (Table 6), which is consistent with

growth or body weight mainly stimulates myoblast results reported previously by Dietl et al. (1993) and

proliferation and muscle fibre formation without a Larzul et al. (1997). We did not find significant

change in muscle DNA:protein ratio (Martin and correlations for both fibre characteristics with backfat

White, 1979; Fowler et al., 1980; Campion et al., thickness (Table 6). In contrast, Larzul et al. (1997)

1982; Penney et al., 1983). In contrast, for modern reported a negative correlation (20.26) of fibre size

meat-type chickens (Knizetova et al., 1972; Jones et with backfat thickness. The genetic correlations of

al., 1986; Mitchell and Burke, 1995), pigs selected fibre size and number with average daily gain seem

for meat content (Nøstvold et al., 1984) and mice to be contradictory as the estimated coefficients

selected long-term for protein content (Rehfeldt and range from 20.49 to 10.46 for fibre number and

Bunger, 1990), decreased muscle DNA:protein or from 0.03 to 0.74 for fibre size (Table 6; see also,

nuclear:cytoplasm ratios have been reported. There are suggestions that the extent of

hyper-trophic and / or proliferative response depends on Table 6

Genetic correlations of longissimus muscle fibre number and fibre

how the applied selection leads to changes in the

cross-sectional area (rg6S.E.) with traits of growth and pork

hormonal system, especially in the growth hormone

quality estimated from data of half- and full-sib groups (n51997)

(GH) / insulin-like growth factor-I (I) axis.

IGF-from 514 sires and 1078 dams of four German pig genotypes

I is an important growth factor which stimulates _{(REML procedure)}

myoblast and satellite cell proliferation (White and

Trait Fibre number Fibre

cross-Esser, 1989; Florini et al., 1991). Plasma concen- _{sectional area}

trations of GH were significantly decreased and a

Average daily gain (g / day) 0.4660.15 0.0360.19

plasma IGF-I was increased in response to growth

Backfat thickness (mm) 20.0560.11 20.1260.18

selection in mice (Medrano et al., 1991; Moride and _{Lean meat percentage} _0.3860.12 _0.5260.08

Hayes, 1993; Schadereit et al., 1998). Similarly, Drip loss (%) 20.0560.19 0.6460.25

Reflectance 17 h p.m. 20.0560.14 0.3260.14

plasma GH concentrations were lower in broiler

pH 45 min p.m. 0.1360.14 20.3760.19

chickens highly selected for muscle mass compared

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Staun, 1972; Dietl et al., 1993; Larzul et al., 1997). low line and the proportion of stress-susceptible

As shown by Larzul et al. (1997), lean tissue growth (halothane-positive) pigs shifted from about 50% to

rate correlates with fibre size (rg50.47) but not with zero in the low line and to 70% in the high line.

fibre number (rg50.08). Fibre size in turn correlates Moreover, it has also been demonstrated by

simu-negatively with good pork quality, as exemplified by lated selection with mouse and pig data that, if

genetic correlations with different quality charac- muscle structure traits were included in selection

teristics, such as drip loss, lightness and pH value indices, selection responses in commonly used

per-(Table 6; see also, Staun, 1972; Larzul et al., 1997), formance traits could be markedly improved

(Re-and the genetic correlations are numerically higher hfeldt et al., 1989; Dietl et al., 1993). This is of

than the phenotypic ones. The genetic correlation importance with regard to a possible use of muscle

between fibre number and meat quality is less clear, structure characteristics in farm animal selection.

but the individual coefficients bear the opposite sign which appears logically consistent due to the

antago-nistic relationship of fibre number and size. 5. Conclusions

4.3.3. Selection criteria including muscle fibre The number of muscle fibres formed during

characteristics prenatal myogenesis and the degree of postnatal fibre

From genetic correlation coefficients and results of hypertrophy are significant in determination of lean

selection experiments, it is suggested that increases growth and ultimate meat quality after slaughter.

in muscle mass solely through muscle fibre hy- Both of the muscle fibre traits are inversely

corre-pertrophy are, at least in pigs, associated with lated with each other. Differences in muscle mass

problems in stress adaptability and meat quality. In caused by selection are due to changes in both

contrast, selection for high fibre numbers at a muscle fibre number and muscle fibre size. The

moderate fibre size are presumed to be advantageous genetic background of the different selection

re-in achievre-ing both high meat content and good meat sponses in relation to the criteria of selection remains

quality. to be further investigated. At least in pigs, increases

That it is possible to produce more meat by high in muscle fibre size rather than number are to be

muscle fibre numbers has been shown by a selection expected when using selection programmes which

experiment with pigs (Wicke, 1989). Divergent are preferentially directed to increased lean growth

selection on high or low muscle fibre diameter in the rate. This in turn may be associated with changes

longissimus muscle, with each of them associated towards poor pork quality. Genetic variability and

with a low backfat:muscle ratio, increased muscle heritability are sufficiently high to use muscle fibre

thickness in equal terms but produced meat of number and muscle fibre size as criteria in selection.

extremely different structure and quality (Table 7). From genetic correlations and correlated responses of

The quality was poor in the high line and good in the selection, it is suggested that both muscle mass and

meat quality / stress adaptability could be significant-ly influenced when considering muscle structure

Table 7

traits in farm animal selection.

Results of a four-generation divergent selection on high and low longissimus muscle fibre diameter together with a low backfat-:muscle ratio in German Landrace pigs (Wicke, 1989)

References

Trait High Low Difference

(n531) (n568) low / high (%)

Aberle, E.D., Doolittle, D.P., 1976. Skeletal muscle cellularity in Muscle thickness (mm) 49.3 49.4 0

mice selected for large body size and in controls. Growth 40, Fibre diameter (mm) 90.0 81.6* 91

133–146. 3 a

Fibre number index (310 ) 310 379* 122

Aberle, E.D., Stewart, T.S., 1983. Growth of fiber types and a

Calculated from ultrasound-measured muscle thickness and apparent fiber number in skeletal muscle of broiler- and layer-fibre number per unit area in muscle biopsy sections. type chickens. Growth 47, 135–144.

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J.P., 1977. Growth, feed utilization, carcass quality and meat Fiedler, I., Ender, K., Domrose, H., 1989. [Results on muscle quality in Danish dual-purpose cattle. Genetic analysis con- structure in pigs of different sex and breeds] Genetische cerning 5 years data from progeny tests for beef production at Probleme in der Tierzucht. Akad. Landwirtschaftswissenschaf-Egtved. 453. Beretning fra statens hysdyrbrugforsøg, pp. 1–83. ten, Berlin, Germany 20, 95–101.

Bader, R., 1983. [Histometrical and histological investigations of _{Fiedler, I., Rehfeldt, C., Ender, K., 1991. [Muscle fibre} charac-¨

muscles of domestic pigs and of wild boars]. Berl. Munch. _{teristics-new selection criteria?]. Tierzuchter 43, 444–445.}_¨ ¨

Tierarztl. Wschr. 96, 89–97. _{Fiedler, I., Ender, K., Wicke, M., von Lengerken, G., 1993.} Beermann, D.H., Cassens, R.G., Hausman, G.J., 1978. A second _{[Relationships between micro-structure of muscle tissue and} look at fibre type differentiation in porcine skeletal muscle. J. _{stress susceptibility in Landrace pigs (halothane sensitivity)].} Anim. Sci. 46, 125–132.

Arch. Anim. Breed. 36, 525–538. Brocks, L., Hulsegge, B., Merkus, G., 1998. Histochemical

Fiedler, I., Rehfeldt, C., Dietl, G., Ender, K., 1997. Phenotypic characteristics in relation to meat quality properties in the

and genetic parameters of muscle fiber number and size. J. longissimus lumborum of fast and lean growing lines of Large

Anim. Sci. 75 (Suppl. 1), 165. White pigs. Meat Sci. 4, 411–420.

Fiedler, I., Rehfeldt, C., Ender, K., Henning, M., 1998. His-Brown, M., 1987. Change in fibre size, not number, in ageing

tophysiological features of skeletal muscle and adrenal glands skeletal muscle. Age Ageing 16, 244–248.

in wild-type and domestic pigs during growth. Arch. Anim. Brown, S.C., Stickland, N.C., 1994. Muscle at birth in mice

Breed. 41, 489–496. selected for large and small body size. J. Anat. 184, 371–380.

Fiedler, I., Ender, K., Wicke, M., Maak, S., von Lengerken, G., Campion, D.R., Marks, H.L., Richardson, R.L., 1982. An analysis

Meyer, W., 1999. Structural characteristics of muscle fibres in of satellite cell content in the semimembranosus muscle of

pigs with different malignant hyperthermia susceptibility and Japanese quail (Coturnix coturnix japonica) selected for rapid

different meat quality. Meat Sci. 53, 9–15. growth. Acta Anat. 112, 9–13.

Florini, J.R., Ewton, D.Z., Magri, K.A., 1991. Hormones, growth Carpenter, C.E., Rice, O.D., Cockett, N.E., Snowder, G.D., 1996.

factors, and myogenic differentiation. Am. Rev. Physiol. 53, Histology and composition of muscles from normal and

201–216. callipyge lambs. J. Anim. Sci. 74, 388–393.

Cassens, R.G., Cooper, C.C., 1971. Red and white muscle. Adv. Fowler, S.P., Campion, D.R., Marks, H.L., Reagan, J.O., 1980. An Food Res. 19, 1–74. analysis of skeletal muscle response to selection for rapid Cassens, R.G., Marple, D.N., Eikelenboom, G., 1975. Animal growth in quail (Coturnix coturnix japonica). Growth 44,

physiology and meat quality. Adv. Food Res. 21, 71–155. 235–252.

Cheek, D.B., Hill, D.B., Cornando, A., Graham, G.G., 1970. Gerrard, D.E., Judge, M.D., 1993. Induction of myoblast prolifer-Malnutrition in infancy: changes in muscle and adipose tissue ation in L6 myoblast cultures by fetal serum of double-muscled before and after rehabilitation. Pediatr. Res. 4, 135–144. and normal cattle. J. Anim. Sci. 71, 1464–1470.

Cherel, Y., Hurtrel, M., Gardahaut, M.F., Merly, F., Magrasresch, Gravert, H.O., 1963. [Investigations on the heritability of meat C., Fontaineperus, J., Wyers, M., 1994. Comparison of postnat- characteristics in cattle II. protein content, pH value, colour, al development of anterior latissimus dorsi (ALD) muscle in muscle fibre thickness, tenderness]. Arch. Anim. Breed. Genet. heavy- and light-weight strains of turkey (Meleagris gal- 78, 139–178.

lopavo). Growth Dev. Aging 58, 157–165. Grobet, L., Martin, L.J., Poncelet, D., Pirottin, D., Brouwers, B., Cockett, N.E., Jackson, S.P., Shay, T.L., Nielsen, D., Moore, S.S., Riquet, J., Schoeberlein, A., Dunner, S., Menissier, F., Mas-Steele, M.R., Barendse, W., Green, R.D., Georges, M., 1994. sabanda, J., Fries, R., Hanset, R., Georges, M., 1997. A Chromosomal localization of the callipyge gene in sheep (Ovis deletion in the bovine myostatin gene causes the

double-ariens) using bovine DNA markers. Proc. Natl. Acad. Sci. muscled phenotype in cattle. Nat. Genet. 17, 71–74. USA 91, 3019–3023. Hanrahan, J.P., Hooper, A.C., McCarthy, J.C., 1973. Effects of Dietl, G., Groeneveld, E., Fiedler, I., 1993. Genetic parameters of divergent selection for body weight on fiber number and

muscle structure traits in pig. In: Proc. 44th Annual Meeting diameter in two mouse muscles. Anim. Prod. 16, 7–16. EAAP, Aarhus, 16–19 August 1993, Vol. II, 1.8. Henckel, P., Oksbjerg, N., Erlandsen, E., Barton-Gade, P., Bejer-Falconer, D.S., 1981. In: Introduction to Quantitative Genetics. holm, C., 1997. Histo- and biochemical characteristics of the Ronald Press, New York. longissimus dorsi muscle in pigs and their relationships to Faulkner, J.A., Maxwell, L.C., Lieberman, D.A., 1972. Histo- performance and meat quality. Meat Sci. 47, 311–321.

chemical characteristics of muscle fibers from trained and Holmes, J.H., Ashmore, C.R., 1972. A histochemical study of detrained guinea pigs. Am. J. Physiol. 222, 836–840. development of muscle fiber type and size in normal and Fiedler, I., 1983. [Postnatal growth of muscle fibres in pigs]. double muscled cattle. Growth 36, 351–372.

Tagungsber. Akad. Landwirtschaftswissenschaften, Berlin, Hughes, S.M., Blau, H.M., 1992. Muscle fibre pattern is in-Germany 209, 87–94. dependent of cell lineage in postnatal rodent development. Cell Fiedler, I., Otto, E., 1982. [Number and size of Longissimus 68, 659–671.

muscle fibres in relation to carcass traits in pigs]. Fleisch 11, Jones, S.J., Aberle, E.D., Judge, M.D., 1986. Skeletal muscle 213–214. protein turnover in broiler and layer chicks. J. Anim. Sci. 62, Fiedler, I., Dietl, G., 1992. [Muscle structure traits as criteria of 1576–1583.

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Muta-tions in myostatin (GDF8) in double-muscled Belgian Blue and development: news from in vitro and in vivo. Bioessays 15, Piedmontese cattle. Genome Res. 7, 910–916. 191–196.

Karlsson, A.H., Klont, R.E., Fernandez, X., 1999. Skeletal muscle Mitchell, R.D., Burke, W.H., 1995. Posthatching growth and fibres as factors for pork quality. Livest. Prod. Sci. 60, 255– pectoralis muscle development in broiler strain chickens,

269. bantam chickens and the reciprocal crosses between them.

Klont, R.E., Eikelenboom, G., Brocks, L., 1998. Muscle fibre type Growth Dev. Aging 59, 149–161.

and meat quality. In: Proc. 44th Int. Congr. Meat Sci. Tech., Mizuno, T., Hikami, J., 1971. Comparison of muscle growth Barcelona, L9, pp. 98–105. between meat-type and egg-type chickens. Jpn. J. Zootech. Sci. Klosowska, D., Klosowski, B., Fiedler, I., Wegner, J., 1985. 42, 526–532.

[Changes in fibre type distribution and muscle fibre thickness Moride, Y., Hayes, J.F., 1993. Correlated responses in growth in porcine M. longissimus dorsi during growth and relation- hormone to selection for weight gain in mice. J. Anim. Breed. ships between histological characteristics and carcass parame- Genet. 110, 450–458.

ters]. Arch. Anim. Breed. 5, 171–180. Moss, F.P., Leblond, C.P., 1971. Satellite cells as the source of Komi, P.V., Karlsson, J., 1979. Physical performance, skeletal nuclei in muscle of growing rats. Anat. Rec. 170, 421–436.

muscle enzyme activities, and fibre types in monozygous and Nakamura, T., Masui, S., Wada, M., Kotoh, H., Mikami, H., dizygous twins of both sexes. Acta Physiol. Scand. 462, 1–28. Katsuta, S., 1993. Heredity of muscle fibre type composition Knizetova, H., Knize, B., Kopezny, V., Fulka, J., 1972. Con- estimated from a selection experiment in rats. Eur. J. Appl.

centration of nuclei in chicken muscle fibre in relation to the Physiol. 66, 85–89.

intensity of growth. Ann. Biol. Anim. Bioch. Biophys. 12, Nelson, T.E., Schochet, Jr. S.S., 1982. Malignant hyperthermia: a 321–328. disease of specific myofiber type? Can. Anaesth. Soc. J. 29,

Kuhn, G., Hartung, M., Nurnberg, K., Fiedler, I., Falkenberg, H., 163–167. ¨

Nurnberg, G., Ender, K., 1998. [Body composition and muscle Nimmo, M.A., Snow, D.H., 1983. The effect of ageing on skeletal structure in genetically different pigs is dependent on MHS muscle fibre characteristics in two inbred strains of mice. J. status]. Arch. Anim. Breed. 41, 589–596. Physiol. 40, 24–25.

Larzul, C., Lefaucheur, L., Ecolan, P., Gogue, J., Talmant, A., Nimmo, M.A., Wilson, R.H., Snow, D.H., 1985. The inheritance Sellier, P., Monin, G., 1997. Phenotypic and genetic parameters of skeletal muscle fibre composition in mice. Comp. Biochem. for Longissimus muscle fibre characteristics in relation to Physiol. A 81, 109–115.

growth, carcass and meat quality traits in Large White pigs. J. Nøstvold, O., Schie, K.A., Frøystein, T., 1984. Muscle fiber Anim. Sci. 75, 3126–3137. characteristics in lines of pigs selected for rate of gain and Lengerken, G., Wicke, M., Maak, S., 1997. [Stress susceptibility backfat thickness. Acta Agric. Scand. Suppl. 21, 136–142.

and meat quality-situation and prospects in animal breeding Ontell, M., Kozeka, K., 1984. Organogenesis of the mouse and research]. Arch. Anim. Breed. 40 (Suppl.), 163–171. extensor digitorum longus muscle: a quantitative study. Am. J. Linke, H., 1972. [Histological studies on exudative, pale pork]. Anat. 171, 149–161.

Fleischwirtsch. 52, 493–507. Osterc, J., 1974. Diameter and number of muscle fibers in Locniskar, F., Holcman, A., Zagozen, F., 1980. Muscle fibre musculus longissimus dorsi in connection with production investigations in poultry. Zb. Biotehniske Fa. Univ. Ljubliani properties of some cattle breeds. PhD Thesis, University of

Kmetistvo 35, 7–24. Ljubljana, pp. 1-67.

Luff, A.R., Goldspink, G., 1967. Large and small muscles. Life Otto, E., Wegner, J., 1976. [Quantitative microscopic studies of the Sci. 6, 1821–1826. muscle fibre and its relationship with meat deposition in Maltin, C.A., Warkup, C.C., Matthews, K.R., Grant, C.M., Porter, swine]. Arch. Anim. Breed. 19, 419–429.

A.D., Delday, M.I., 1997. Pig muscle fibre characteristics as a Ouhayoun, J., Beaumont, A., 1968. [Investigation of the double-source of variation in eating quality. Meat Sci. 47, 237–248. muscled characteristic: III. Anatomical microscopic compari-Martin, R., White, J., 1979. Muscle and adipose cell development son of muscle tissue from normal and double-muscled, male

in mice selected for postweaning growth rate. Growth 43, Charolais]. Ann. Zootech. 17, 213–223.

167–173. Penney, R.K., Prentis, P.F., Marshall, P.A., Goldspink, G., 1983. McPherron, A.C., Lee, S.J., 1997. Double muscling in cattle due Differentiation of muscle and the determination of ultimate

to mutations in the myostatin gene. Proc. Natl. Acad. Sci. USA muscle size. Cell Tissue Res. 228, 375–388.

94, 12457–12461. Picard, B., Gagniere, H., Robelin, J., Geay, Y., 1995. Comparison McPherron, A.C., Lawler, A.M., Lee, S.J., 1997. Regulation of of the foetal development of muscle in normal and

double-skeletal muscle mass in mice by a new TGF-beta superfamily muscled cattle. J. Muscle Res. Cell Motil. 16, 629–639. ¨

member. Nature 387, 83–90. Rehfeldt, C., Bunger, L., 1990. [Effects of long-term selection of Medrano, J.F., Pomp, D., Sharrow, L., Bradford, G.E., Downs, laboratory mice on parameters of muscle growth and muscle

T.R., Frohman, L.A., 1991. Growth hormone and insulin-like structure]. Arch. Anim. Breed. 33, 507–516.

growth factor-1 measurements in high growth (hg) mice. Rehfeldt, C., Ender, K., 1995. Somatotropin action on skeletal Genet. Res. Camb. 58, 67–74. muscle and backfat cellularity in pigs of different breed and Miller, J.B., Everitt, E.A., Smith, T.H., Block, N.E., Dominov, halothane sensitivity. Arch. Anim. Breed. 38, 405–415.

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fibres in growing skeletal muscle of laboratory mice]. Arch. Sørensen, M.T., Oksbjerg, N., Agergaard, N., Søholm Petersen, J., Exp. Vet. med. 38, 178–192. 1996. Tissue deposition rates in relation to muscle fibre and fat Rehfeldt, C., Otto, E., 1985. [Changes in muscle structure in cell characteristics in lean female pigs (Sus scrofa) following response to selection for growth and fitness-studies on labora- treatment with porcine growth hormone. Comp. Biochem. tory mice]. Arch. Anim. Breed. 5, 465–475. Physiol. 113A, 91–96.

Rehfeldt, C., Bunger, L., Dietl, G., Fiedler, I., Wegner, J., 1988. Staun, H., 1963. Various factors affecting number and size of [On the heritability of muscle structure characters and their muscle fibers in the pig. Acta Agric. Scand. 13, 293–322. genetic relationships with growth and fitness in laboratory Staun, H., 1968. [Diameter and number of muscle fibres and their mice]. Arch. Anim. Breed. 31, 185–195. relation to meatiness and meat quality in Danish Landrace

Rehfeldt, C., Bunger, L., Dietl, G., Ender, K., 1989. [Usefulness pigs]. 366. Beretning fra førsøgslaboratoriet. National Res. Inst. of muscle structure characteristics for selection — model Anim. Sci., Copenhagen, Denmark, pp. 1–121.

experiment on laboratory mice]. J. Anim. Breed. Genet. 106, Staun, H., 1972. The nutritional and genetic influence on number 208–216. and size of muscle fibres and their response to carcass quality Rehfeldt, C., Fiedler, I., Weikard, R., Kanitz, E., Ender, K., 1993. in pigs. World Rev. Anim. Prod. 3, 18–26.

It is possible to increase skeletal muscle fibre number in utero. Stickland, N.C., Goldspink, G., 1975. A note on porcine skeletal Biosci. Rep. 13, 213–220. muscle parameters and their possible use in early progeny

Rehfeldt, C., Ender, K., Nurnberg, K., Hackl, W., 1996. Cellular testing. Anim. Prod. 21, 93–96.

aspects of the repartitioning process induced by somatotropin Stickland, N.C., Handel, S.E., 1986. The numbers and types of in pigs up to 150 kg live weight in relation to growth and muscle fibres in large and small breeds of pigs. J. Anat. 147, carcass characteristics. Arch. Anim. Breed. 39, 169–184. 181–189.

Rehfeldt, C., Stickland, N.C., Fiedler, I., Wegner, J., 1999. Summers, P.J., Medrano, J.F., 1994. Morphometric analysis of Environmental and genetic factors as sources of variation in skeletal muscle growth in the high growth mouse. Growth Dev. skeletal muscle fibre number. Basic Appl. Myol. 9, 235–253. Aging 58, 135–148.

Remignon, H., Lefaucheur, L., Blum, J.C., Ricard, F.H., 1994. Swatland, H.J., 1973. Muscle growth in the fetal and neonatal pig. Effects of divergent selection for body weight on three skeletal J. Anim. Sci. 37, 536–545.

muscles characteristics in the chicken. Br. Poul. Sci. 35, 65–76. Swatland, H.J., 1975. Myofibre number and myofibrillar develop-Remignon, H., Gardahaut, M.F., Marche, G., Ricard, F.H., 1995. ment in neonatal pig. Zbl. Vet.-Med. 22, 756–764.

Selection for rapid growth increases the number and the size of Szentkuti, L., Schlegel, O., 1985. [Genetic and functional in-muscle fibres without changing their typing in chickens. J. fluences on fibre type proportions and fibre diameter in M. Muscle Res. Cell Motil. 16, 95–102. longissimus dorsi and M. semitendinosus of pigs. Studies on Rosenblatt, J.D., Woods, R.I., 1992. Hypertrophy of rat extensor trained domestic pigs and restrained wild type pigs]. Dtsch.

digitorum longus muscle injected with bupivacaine. A sequen- Tierarztl. Wschr. 92, 93–97.

tial histochemical, immunohistochemical, histological and mor- Timson, B.F., Bowlin, B.K., Dudenhoeffer, G.A., George, J.B., phometric study. J. Anat. 181, 11–27. 1985. Fiber number, area, and composition of mouse soleus Rowe, R.W.E., Goldspink, G., 1969. Muscle fibre growth in five muscle following enlargement. J. Appl. Physiol. 58, 619–624. different muscle in both sexes of mice. J. Anat. 104, 519–530. Walther, K., 1999. [In vitro study of basic processes of muscle cell Schadereit, R., Klein, M., Rehfeldt, C., Kreienbring, F., Krawie- growth of the laboratory mouse after long-term selection on litzki, K., 1995. Influence of nutrient restriction and realimen- different growth traits]. PhD Thesis, University of Rostock, tation on protein and energy metabolism, organ weights, and Germany, pp. 1–142.

muscle structure in growing rats. J. Anim. Physiol. Anim. Nutr. Wegner, J., Albrecht, E., Fiedler, I., Teuscher, F., Papstein, H.-J., 74, 253–268. Ender, K., 2000. Growth and breed-related changes of muscle Schadereit, R., Rehfeldt, C., Krawielitzki, K., Klein, M., Kanitz, fibre characteristics in cattle. J. Anim. Sci. 78, 1485–1496.

E., Kuhla, S., 1998. Protein turnover, body composition, Weiler, U., Appell, H.J., Kremser, M., Hofacker, S., Claus, R., muscle characteristics and blood hormones in response to 1995. Consequences of selection on muscle composition. A different direction of growth selection in mice. J. Anim. Feed comparative study on gracilis muscle in wild and domestic Sci. 7, 333–352. pigs. Anat. Histol. Embryol. 24, 77–80.

Schultz, E.A., 1974. A quantitative study of satellite cell popula- White, T.P., Esser, K., 1989. Satellite cell and growth factor tion in postnatal mouse lumbrical muscle. Anat. Rec. 180, involvement in skeletal muscle growth. Med. Sci. Sports

589–596. Exercise 21, 158–163.

Shackelford, S.D., Wheeler, T.L., Koohmaraie, M., 1997. Effect of Wicke, M., 1989. [Influences of a divergent selection for muscle callipyge phenotype and cooking method on tenderness of structure characteristics of M. longissimus dorsi on stress several major lamb muscles. J. Anim. Sci. 75, 2100–2105. susceptibility and carcass quality in pigs]. PhD Thesis, Uni-Shahin, K., Berg, R.T., 1985. Growth patterns of muscle, fat and versity of Leipzig, Germany, pp. 1–115.

bone, and carcass composition of double muscled and normal Wicke, M., Lengerken, G., Fiedler, I., Altmann, M., Ender, K., cattle. Can. J. Anim. Sci. 65, 279–294. 1991. [Effects of selection for muscle structure characteristics Smith, J.H., 1963. Relation of body size to muscle cell size and of M. longissimus dorsi on stress susceptibility and meat

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thickness, were reported between Large White and

factor (GDF-8) that belongs to the transforming

miniature pigs of the same age (Stickland and

growth factor-b

(TGF-b) superfamily and has been

Handel, 1986). No marked differences in muscle

identified as an important negative regulator of

fibre number and size of the longissimus muscle

muscle development in a mouse model of gene

were apparent between different modern meat-type

deletion (McPherron et al., 1997). The callipyge

pig breeds and crosses in contrast to the ‘older’ fatty

condition in sheep as a further example of extreme

Saddle Back breed which has a lower fibre number

muscular hypertrophy is caused by a mutation of the

and size (Table 5). When comparing the same

callipyge gene located on ovine chromosome 18

muscle of several European pig breeds 20 years ago,

(Cockett et al., 1994). In contrast to the

double-Staun (1963) found differences in muscle fibre size

muscled condition in cattle, muscular enlargement in

and number. Possibly, in modern meat-type pig

callipyge lambs seems mainly to be due to muscle

´

breeds, e.g., Pietrain or Large White, fibre number

fibre hypertrophy (Carpenter et al., 1996).

and size are at the limits of their correlated responses

to selection for leanness, and new strategies must be

4.3. Correlated selection responses

applied to attain further changes.

There are no obvious differences in muscle fibre

4.3.1. Selection experiments

number and size in most of the cattle breeds (e.g.,

Genetic relationships between animal performance

Osterc, 1974; Wegner et al., 2000). However, an

and muscle fibre characteristics can be derived from

exception are double-muscled cattle which exhibit

both selection experiments and from genetic

correla-almost double the number of muscle fibres compared

tion coefficients.

with other cattle breeds, whereas no differences in

Differences in muscle mass obtained by breeding

fibre size are apparent (Ouhayoun and Beaumont,

and selection are due to changes in both muscle fibre

1968; Holmes and Ashmore, 1972; Wegner et al.,

number and muscle fibre size. This can be concluded

2000). Prenatal studies with double-muscled cattle

from a series of selection experiments for large body

suggest that the higher number of muscle fibres is a

size or rapid growth rate with several species

includ-consequence of delayed differentiation and extended

ing the mouse (Luff and Goldspink, 1967; Hanrahan

myoblast proliferation (Picard et al., 1995), and

et al., 1973; Aberle and Doolittle, 1976; Penney et

serum from double-muscled foetuses induced higher

al., 1983; Rehfeldt and Otto, 1985; Timson et al.,

¨

proliferative responses in L

myoblasts compared

1985; Rehfeldt and Bunger, 1990; Brown and

Stick-with serum of normal cattle foetuses (Gerrard and

land, 1994; Summers and Medrano, 1994), pig

Judge, 1993). The double-muscled phenotype arises

(Wicke, 1989; Wicke et al., 1991; Brocks et al.,

from mutations in the myostatin gene (Grobet et al.,

1998), chicken (Smith, 1963; Mizuno and Hikami,

1997; Kambadur et al., 1997; McPherron and Lee,

1971; Aberle and Stewart, 1983; Remignon et al.,

1997). Myostatin is a growth and differentiating

1994, 1995), quail (Fowler et al., 1980) and turkey

(Cherel et al., 1994).

Growth selection leads to increases in myoblast

and / or satellite cell proliferation rates as indicated

Table 5

by higher myonuclear numbers (e.g., Knizetova et

Muscle fibre number and diameter (mean6S.D.) in the

longis-al., 1972; Penney et longis-al., 1983; Brown and Stickland,

simus muscle of different pig breeds (Fiedler et al., 1989; Kuhn et

1994), higher DNA synthesis rate (Knizetova et al.,

al., 1998)

1972) and higher total muscle DNA content (e.g.,

Pig breed (n) Fibre number Fibre diameter

Knizetova et al., 1972; Martin and White, 1979;

(310 ) (mm)

Fowler et al., 1980; Campion et al., 1982; Jones et

German Landrace (694) 1.04160.280 68.969.5

al., 1986; Mitchell and Burke, 1995). We also

German Large White (137) 1.01660.251 70.068.4

recently demonstrated this by the in vitro growth of

Leicoma (1052) 1.06160.275 68.669.4

Schwerfurter (77) 1.10960.309 68.9610.7

satellite cells derived from differently selected mouse

Pietrain (26) 1.10760.178 71.368.8

_{lines (Fig. 4). According to the principles of skeletal}

Saddle Back (17) 0.90960.178 67.167.8

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Burke, 1995), but no increases in IGF-I

concen-trations were found. The correlated responses of

these and other hormones and growth factors to

growth selection need to be further investigated.

4.3.2. Genetic correlation coefficients

Changes that are to be expected in response to

selection can be predicted from genetic correlation

coefficients. It has been found consistently that the

antagonism between fibre size and number

men-tioned above is based on a genetic relationship. The

genetic correlation coefficients between fibre size

and number estimated for the mouse, chicken and

Fig. 4. DNA accumulation in cultures of satellite cells isolated

pig were found to range from

2 0.4 to

2 0.8 (Staun,

from mouse lines selected for 6-week protein accretion (DU-6P),

body weight (DU-6) or an index from body weight and treadmill

1972; Locniskar et al., 1980; Rehfeldt et al., 1988;

performance (DU-61LB) over 71 generations, and from a

_{Fiedler et al., 1997; Larzul et al., 1997).}

Conse-control (DU-Ks). FBS, foetal bovine serum (Walther, 1999).

quently, selection of animals with high muscle mass

due mainly to large fibres will in turn produce

offspring with low fibre number.

to the formation of higher muscle fibre numbers and,

In pigs, positive genetic correlations were

ob-postnatally, to the accumulation of more myofibre

served for muscle fibre number or size with lean

nuclei. There is some evidence that selection for

meat percentage (Table 6), which is consistent with

growth or body weight mainly stimulates myoblast

results reported previously by Dietl et al. (1993) and

proliferation and muscle fibre formation without a

Larzul et al. (1997). We did not find significant

change in muscle DNA:protein ratio (Martin and

correlations for both fibre characteristics with backfat

White, 1979; Fowler et al., 1980; Campion et al.,

thickness (Table 6). In contrast, Larzul et al. (1997)

1982; Penney et al., 1983). In contrast, for modern

reported a negative correlation (20.26) of fibre size

meat-type chickens (Knizetova et al., 1972; Jones et

with backfat thickness. The genetic correlations of

al., 1986; Mitchell and Burke, 1995), pigs selected

fibre size and number with average daily gain seem

for meat content (Nøstvold et al., 1984) and mice

to be contradictory as the estimated coefficients

selected long-term for protein content (Rehfeldt and

range from

2 0.49 to

1 0.46 for fibre number and

¨

Bunger, 1990), decreased muscle DNA:protein or

from 0.03 to 0.74 for fibre size (Table 6; see also,

nuclear:cytoplasm ratios have been reported.

There are suggestions that the extent of

hyper-trophic and / or proliferative response depends on

Table 6

Genetic correlations of longissimus muscle fibre number and fibre

how the applied selection leads to changes in the

cross-sectional area (rg6S.E.) with traits of growth and pork

hormonal system, especially in the growth hormone

quality estimated from data of half- and full-sib groups (n51997)

(GH) / insulin-like growth factor-I (I) axis.

IGF-from 514 sires and 1078 dams of four German pig genotypes

I is an important growth factor which stimulates

_{(REML procedure)}

myoblast and satellite cell proliferation (White and

Trait Fibre number Fibre

cross-Esser, 1989; Florini et al., 1991). Plasma concen-

_{sectional area}

trations of GH were significantly decreased and

Average daily gain (g / day) 0.4660.15 0.0360.19

plasma IGF-I was increased in response to growth

Backfat thickness (mm) 20.0560.11 20.1260.18

selection in mice (Medrano et al., 1991; Moride and

_{Lean meat percentage} _0.3860.12 _0.5260.08

Hayes, 1993; Schadereit et al., 1998). Similarly,

Drip loss (%) 20.0560.19 0.6460.25 Reflectance 17 h p.m. 20.0560.14 0.3260.14

plasma GH concentrations were lower in broiler

pH 45 min p.m. 0.1360.14 20.3760.19

chickens highly selected for muscle mass compared

(3)

Staun, 1972; Dietl et al., 1993; Larzul et al., 1997).

low line and the proportion of stress-susceptible

As shown by Larzul et al. (1997), lean tissue growth

(halothane-positive) pigs shifted from about 50% to

rate correlates with fibre size (r

5 0.47) but not with

zero in the low line and to 70% in the high line.

fibre number (r

5 0.08). Fibre size in turn correlates

Moreover, it has also been demonstrated by

simu-negatively with good pork quality, as exemplified by

lated selection with mouse and pig data that, if

genetic correlations with different quality charac-

muscle structure traits were included in selection

teristics, such as drip loss, lightness and pH value

indices, selection responses in commonly used

per-(Table 6; see also, Staun, 1972; Larzul et al., 1997),

formance traits could be markedly improved

(Re-and the genetic correlations are numerically higher

hfeldt et al., 1989; Dietl et al., 1993). This is of

than the phenotypic ones. The genetic correlation

importance with regard to a possible use of muscle

between fibre number and meat quality is less clear,

structure characteristics in farm animal selection.

but the individual coefficients bear the opposite sign

which appears logically consistent due to the

antago-nistic relationship of fibre number and size.

5. Conclusions

4.3.3. Selection criteria including muscle fibre

The number of muscle fibres formed during

characteristics

prenatal myogenesis and the degree of postnatal fibre

From genetic correlation coefficients and results of

hypertrophy are significant in determination of lean

selection experiments, it is suggested that increases

growth and ultimate meat quality after slaughter.

in muscle mass solely through muscle fibre hy-

Both of the muscle fibre traits are inversely

corre-pertrophy are, at least in pigs, associated with

lated with each other. Differences in muscle mass

problems in stress adaptability and meat quality. In

caused by selection are due to changes in both

contrast, selection for high fibre numbers at a

muscle fibre number and muscle fibre size. The

moderate fibre size are presumed to be advantageous

genetic background of the different selection

re-in achievre-ing both high meat content and good meat

sponses in relation to the criteria of selection remains

quality.

to be further investigated. At least in pigs, increases

That it is possible to produce more meat by high

in muscle fibre size rather than number are to be

muscle fibre numbers has been shown by a selection

expected when using selection programmes which

experiment with pigs (Wicke, 1989). Divergent

are preferentially directed to increased lean growth

selection on high or low muscle fibre diameter in the

rate. This in turn may be associated with changes

longissimus muscle, with each of them associated

towards poor pork quality. Genetic variability and

with a low backfat:muscle ratio, increased muscle

heritability are sufficiently high to use muscle fibre

thickness in equal terms but produced meat of

number and muscle fibre size as criteria in selection.

extremely different structure and quality (Table 7).

From genetic correlations and correlated responses of

The quality was poor in the high line and good in the

selection, it is suggested that both muscle mass and

meat quality / stress adaptability could be

significant-ly influenced when considering muscle structure