Genetic association between leg conformation in young pigs and sow reproduction

Livestock Science 178 (2015) 9–17

Contents lists available at ScienceDirect

Livestock Science journal homepage: www.elsevier.com/locate/livsci

Genetic association between leg conformation in young pigs and sow reproduction Hong Thu Le a,b,n, Katja Nilsson a, Elise Norberg b, Nils Lundeheim a a b

Swedish University of Agricultural Sciences, Department of Animal Breeding and Genetics, Box 7023, SE-750 07 Uppsala, Sweden Aarhus University, Department of Molecular Biology and Genetics, P.O. Box 50, Tjele DK-8830, Denmark

a r t i c l e i n f o

abstract

Article history: Received 19 May 2014 Received in revised form 11 May 2015 Accepted 14 May 2015

Lameness is an issue of concern in pig production due both to animal welfare and to economical aspects. Lame sows are believed to suffer from pain and stress which is reported to have a negative influence on reproduction. Leg conformation and locomotion traits in young animals are associated with the risk of lameness at higher age. The purpose of this study was to estimate the genetic parameters of leg conformation traits recorded at performance testing (around 5 months of age) and their genetic correlations with reproduction traits. Information on leg conformation traits from 123,307 pigs scored and on reproduction traits from 22,204 litters in the first and second parity from Swedish Yorkshire nucleus herds were available for genetic analysis. Eight conformation and locomotion traits, coming from the old or the new scoring system in Sweden, included old movement, old overall leg score, new movement, new toes quality, new front leg quality, new rear leg quality, standing-under-position syndrome and new overall score. Four reproduction traits were analyzed by parity: the number of total born piglets, the number of liveborn piglets, the number of stillborn piglets and weaning to service interval. Estimates of heritabilities and genetic correlations between traits were obtained using a multi-trait linear animal mixed model. The heritability estimates were low to moderate, ranging from 0.02 to 0.20 for conformation traits and from 0.06 to 0.10 for reproduction traits. Significant genetic correlations were found between new toes quality and new overall score and the number of liveborn piglets in the 1st parity (
0.35 and
0.31, respectively), indicating that sows with even toes and better overall leg score tend to have higher number of liveborn piglets. Old movement score showed significant correlations with number of total born and number of liveborn piglets in both parities (0.20 to 0.36) and with weaning to service interval in the 2nd parity (
0.35 70.11). Similarly, standingunder-position syndrome was highly associated with number of total born and number of liveborn piglets in both parities (
0.54 to
0.35), indicating that sows with better movement and not suffering from standing-under-position syndrome are likely to have larger litter size and shorter interval to return heat after weaning. Heritabilities and significantly favorable genetic correlation estimates suggest the possibility of simultaneous improvement of both leg quality and reproduction performance by selecting on sound leg conformation and locomotion of young pigs. & 2015 Elsevier B.V. All rights reserved.

Keywords: Genetic correlation Lameness Leg conformation Pig Reproduction

n Corresponding author at: Swedish University of Agricultural Sciences, Department of Animal Breeding and Genetics, Box 7023, SE-750 07 Uppsala, Sweden. E-mail address: [email protected] (H.T. Le).

http://dx.doi.org/10.1016/j.livsci.2015.05.025 1871-1413/& 2015 Elsevier B.V. All rights reserved.

1. Introduction Lameness is not only a welfare issue of great concern but also a major source of economic loss in pig production.

10

H.T. Le et al. / Livestock Science 178 (2015) 9–17

Lameness is likely to be associated with pain and distress. The general influence of stress on the reproduction of sows was reviewed by Einarsson et al. (2008). Stress is believed to have a negative influence on the reproductive cycle, resulting in lower number of ovulated eggs and higher risk for re-mating (Fitzgerald et al., 2012; Heinonen et al., 2006; Wischner et al., 2009). In addition, Jensen et al. (2007) found that lame boars, in spite of treatment with antibiotics for arthritis, have reduced daily weight gain compared with boars without lameness. Sows with leg weakness have a higher frequency of uncontrolled lyingdown behavior, which probably causes higher risk of crushing the piglets, resulting in lower litter size at weaning (Heinonen et al., 2006; Pluym et al., 2013; Wischner et al., 2009). Also, leg weakness is reported as one of the most common reasons for premature culling of sows. From 9% to 13% of sows removed from commercial herds in Sweden, Finland and Denmark were done so due to lameness, as reported in several studies (Engblom et al., 2007; Heinonen et al., 2006; Jorgensen, 2003). Thus improving leg quality in pig herds is expected to increase profitability as well as animal welfare. Lameness has several causes, including claw lesion, trauma, different manifestations of osteochondrosis, skin lesion and arthritis, as reviewed by Heinonen et al. (2013). Among these, osteochondrosis is probably the main contributing cause of leg weakness in pigs (Lundeheim, 1987; Jørgensen and Andersen, 2000). Osteochondrosis is a disorder of the joints due to a failure in the endochondral

ossification of the articular cartilage and the growth plate, which is likely to cause deformation of the articular surface, leading to abnormal conformation and locomotion traits of affected animals. On the other hand, abnormal conformation and locomotion seem to increase the severity of osteochondrosis. For instance, Ytrehus et al. (2004) suggested that biomechanical pressure within joints may be involved in osteochondrosis development. Several studies have reported correlations between osteochondrosis and conformation and locomotion traits (Lundeheim, 1987; Jørgensen and Andersen, 2000; Luther et al., 2007). Koning et al. (2012) found significant genetic correlations between the prevalence and severity of osteochondrosis and several conformation traits and gait characteristics. They suggested that leg weakness caused by osteochondrosis can be predicted by exterior traits assessment; thus conformation and locomotion can be included in the breeding goal for selection for better leg quality. The association between conformation traits and production traits (e.g. growth rate, backfat thickness etc.) has been exploited in many studies, but not between conformation traits and reproduction traits. In fact, both conformation/osteochondrosis and reproduction traits have been included in genetic evaluations in almost all Nordic countries (Rydhmer, 2005). But the way these traits influence each other remains unclear. Our hypothesis is that inferior leg conformations can cause pain and distress to the sow, resulting in reduced reproduction. Thus selection for better leg conformations in a breeding program

Table 1 Description of conformation traits analyzed in this study. Traits

Abbrev.

Range Optimum Description

Old movement

o_move

1–3

3

Old overall leg score

o_all

1–3

3

New movement

n_move

1–7

4

New toes quality

n_toes

4–7

4

New front leg quality

n_front

1–7

4

New rear leg quality

n_rear

1–7

4

New standing-underposition

n_under 4–7

4

New overall score

n_all

1

1–6

Movement 1 ¼not good 3 ¼excellent Overall leg score 1 ¼not good 3 ¼excellent Movement 1 ¼stiff/rigid movement 4 ¼excellent movement (like a cat) 7 ¼winding movement Evenness of claw and space between claws (average score of four legs) 4 ¼optimal: even claws and space between claws 7 ¼severe: uneven claws and very narrow claws Front view and side view of front leg 1 ¼too flexible: bow-legged stance; turn-in pastern (front view); sickle-legged pastern (side view); crooked knee 4 ¼optimal: straight stance; straight pastern with toes face forwards (front view); intermediate pastern (side view); intermediate knee 7 ¼too rigid: cow-legged stance; turn-out pastern (front view); post-legged pastern (side view); straight knee Side view and behind view of rear leg 1 ¼too flexible: bow-legged stance; sickle-legged pasterns (side view); crooked hocks 4 ¼optimal: straight stance; straight pastern (rear view); intermediate pasterns (side view); intermediate hocks 7 ¼too rigid: cow-legged stance; turn-out pastern (rear view); post-legged pastern (side view); straight hocks Center of gravity on rear legs 4 ¼normal 7 ¼severe: center of gravity behind feet Total assessment 1 ¼excellent; 2¼ very good; 3¼ good; 4 ¼average; 5¼ unsatisfactory; 6¼ failed

H.T. Le et al. / Livestock Science 178 (2015) 9–17

is expected to improve the reproductive performance. For this purpose, genetic parameters such as heritabilities and genetic correlations between conformation traits and reproduction traits need to be known. In Sweden, conformation traits are recorded at performance testing in nucleus herds when animals are around 5 months old and weigh approximately 100 kg. However, little is known about how well leg quality recorded in young animals predicts leg soundness in the adult animal, and how it affects reproduction performance of gilts and sows. Therefore the objective of this study was to investigate the genetic association between leg conformation in young animals recorded at performance testing and the reproduction capacity of gilts and sows in a Yorkshire pig population.

2. Materials and methods 2.1. Animal management and data collection This study is based on data recorded on purebred Yorkshire pigs in nucleus herds within the breeding company Nordic Genetics (www.nordicgenetics.se). For conformation traits, the original data set included records from 125,770 purebred Yorkshire pigs born between 2005 and 2012. For the reproduction traits, data on 67,150 litters from 25,448 gilts and sows that farrowed between 2005 and July 2013 was available. Each year, approximately 20,000 purebred Yorkshire pigs are born and registered in these nucleus herds, representing the entire Swedish Yorkshire population. On average 80% of the registered pigs are performance tested at around 5 months of age and 100 kg of weight. Body weight, side-fat thickness, number and quality of teats as well as exterior conformation

11

focusing on leg quality are recorded by skilled technicians from the breeding company. Information about reproduction including date of farrowing, mating and weaning, number of total born piglets and number of born alive piglets are documented by the herd staff. In this study eight conformation traits were included. There were two different scoring systems used during the study period due to the implementation of a new scoring system for performance testing in Sweden in 2011. The old system included two traits: old movement (o_move) and old overall leg score (o_all). The new system includes six traits: new movement (n_move), new toes quality (n_toes), new front leg quality (n_front), new rear leg quality (n_rear), standing-under-position syndrome (n_under) and new overall score (n_all). Criteria for scoring and the description of scores are shown in Table 1 in which the old scoring system judges animals from bad to good, and the new scoring system describes the appearance of animals. The majority of the animals were scored in the old scoring system, one third was scored in the new system, and a few animals in the first six months of 2011 were scored in both systems. Four reproduction traits were included in this study: the number of total born piglets (NTB), the number of piglets born alive (NBA), the number of stillborn piglets (NSB); and weaning to service interval (WSI). Weaning to service interval was defined as the number of days from date of weaning to date of next insemination. In order to obtain normal distribution for the genetic analysis, WSI was logarithmic transformed from day 6 and forward following Ten Napel et al. (1995): 2.2. Data editing Data editing and phenotypic analyzes were performed

Table 2 Descriptive statistics of untransformed conformation traits and reproduction traits together with corresponding heritability estimates. Traits Conformationa o_move o_all n_move n_toes n_front n_rear n_under n_all Reproductionb NTB1 NTB2 NBA1 NBA2 NSB1 NSB2 WSI1 WSI2

N

Mean

SD

Optimum

Min

Max

97,348 97,530 30,912 30,881 30,910 30,912 30,886 30,909

2.8 2.6 4.2 4.2 4.1 4.4 4.2 2.8

0.4 0.6 0.6 0.5 0.8 0.8 0.4 1.3

3 3 4 4 4 4 4 1

1 1 1 4 1 1 4 1

3 3 7 7 7 7 7 6

13,872 8332 13,872 8332 13,872 8332 8540 5269

12.3 13.3 11.2 12.2 1.13 1.05 5.5 5.0

3.3 3.6 3.1 3.4 1.54 1.51 1.8 1.4

1 1 0 0 0 0 1 1

27 26 22 23 15 19 14.6 14.6

Median

Mode

h2 7SE

3 3 4 4 4 4 4 3

3 3 4 4 4 4 4 2

0.050.01 0.020.01 0.050.01 0.070.01 0.190.02 0.170.02 0.020.01 0.200.02 0.070.01 0.100.02 0.060.01 0.080.02 0.070.01 0.060.01 0.070.01 0.090.02

N ¼number of observations; SD¼ standard deviation; Min ¼minimum; Max ¼ maximum; h2 ¼ eritability; SE ¼standard error. a o_move¼ old scoring of movement; o_all ¼old scoring of overall leg score; n_move ¼ new scoring of movement; n_toes¼ uneven toes and width between toes; n_front¼front and side view of front legs; n_under ¼standing-under-position of rear leg; n_rear ¼ rear and side view of rear legs; n_all¼ new overall score. b NTB1,2 ¼ number of total born in parity 1,2; NBA1,2 ¼ number of born alive in parity 1,2; NSB1,2 ¼number of stillborn in parity 1,2; WSI1,2 ¼weaning to service interval in parity 1,2.

12

H.T. Le et al. / Livestock Science 178 (2015) 9–17

82.2

100 %

50

100 %

16.4

1.4

0

50

2

1

2

50 0

2

52.9 24.0 16.6

3

4

5

Score

2

3.6 0.6

6

7

50 0

3

4

5

3.0 0.3

6

0.1 0.6 9.1

1

2

3

49.3 33.1

4

5

80.2

50

%

17.9

0

7

4

5

Score

100 6.4 1.3

6

7

Score

%

1.8

0.1

6

7

Score

n_under

100 %

20.2

0.0 0.1 2.5

1

n_rear

0.3 2.1

1

3

100

73.9

Score

n_front 100

50 0

Score

%

%

4.0

3

100

61.6

34.4

0

1

n_toes

n_move

o_all

o_move

n_all

83.3

50

100 15.9

0 4

5

0.9

0.0

6

7

%

50

14.2

33.6 26.8

15.9

0 1

2

Score

3

4

4.7 4.9

5

6

Score

Fig. 1. Distribution of 8 conformation traits: old movement (o_move); old overall leg score (o_all); new movement (n_move); new toes quality (n_toes); new front leg quality (n_front); new rear leg quality (n_rear); standing-under-position (n_under); new overall score (n_all). The optimal scores are circled.

using SAS v9.3 (SAS Inst. Inc., Cary, NC; http://www.sas. com/en_us/home.html). The range of values used for data editing were based on the practical situation in herds in Sweden (standard deviation and frequency calculation) as well as the accepted range issued by Nordic Genetics from where the data came. Pigs weighing less than 70 kg or more than 130 kg at performance testing were excluded from the study. Data from nucleus herds with fewer than 500 animals performance tested during the study period were also excluded. After editing, data from 123,307 pigs with information on conformation traits were available for analysis. Of these, 97,530 used the old scoring system, 30,912 used the new scoring system, and approximately 5500 used both old and new scoring systems. The number of animals with records on each conformation score is presented in Table 2. The distributions of the 8 conformation traits are presented in Fig. 1. Data on reproduction traits included both purebred (Yorkshire  Yorkshire) and crossbred (Yorkshire  Landrace) litters. In this study, analyzes were restricted to the nucleus herds and to the litters in the 1st parity (NTB1, NBA1, NSB1, WSI1) and 2nd parity (NTB2, NBA2, NSB2, WSI2). Herds with fewer than 500 litters and with more than 90% of the litters being crossbred during the study period were excluded. Only litters with gestation length within 110 to 120 days were included for analysis. Weaning to service interval values before transformation, either outside the range of 1 to 30 days or when lactation length was outside the range of 25 to 45 days, were considered as missing observations. After editing, records on 22,204 litters (13,872 in the 1st parity and 8332 in the 2nd parity) from in total 14,329 sows were available for analysis. The distribution of WSI before and after logarithmic transformation is presented in Fig. 2. A normal scoring method was performed by the procedure RANK in SAS to transform the number of stillborn piglets and conformation traits, in order that they more closely follow the normal distribution. The normal score transformation ranks the score values from lowest to highest and matching these ranks to equivalent ranks generated from a normal distribution. The number of stillborn piglets was transformed by herd-year at

farrowing and conformation traits were transformed by sex and herd-year at testing. 2.3. Statistical analysis Fixed effects potentially influencing the traits were examined by the procedure MIXED in SAS. The results from this procedure were used to construct linear models for estimation of (co)variance component. Genetic analyzes were performed using AI-REML in the DMU package (Madsen and Jensen, 2013). The multi-trait linear animal mixed models for each group of traits are presented below: For conformation traits: yconf = hybir + sex + litter + hysp + a + eyconf

= hybir + sex + litter + hysp + a + e For litter size traits by parity (NTB, NBA and NSB): yfert = hyfarrow + boar + hysfarrow + a + eyfert

= hyfarrow + boar + hysfarrow + a + e For weaning to service interval trait by parity (WSI): yWSI = hywean + hyswean + a + eyWSI

= hywean + hyswean + a + e where yi is the transformed score for conformation traits yconf , the number of total born/born alive/ transformed number of stillborn piglets yfert and transformed weaning to service interval yWSI ; hyi the fixed effect of the combination of herd and year at birth hybir , at farrowing hyfar or at weaning hywean ; sex is the fixed effect of sex; boar is the fixed effect of breed of sire of the litters (Yorkshire or Landrace). The models included the random effects of birth litter (litter ); effect of combination of herd_year_batch_pen at testing (hysp) to account for the influence of the testing environment (pen) on the performance of the animals; effect of herd_year_season at farrowing hysfarrow or at weaning (hyswean) to consider how the farrowing and weaning environment affect the sows' reproduction performance; effect of direct genetic of animal (a) and residual effect (e ). For genetic correlation estimation, the two conformation

(

)

H.T. Le et al. / Livestock Science 178 (2015) 9–17

13

50 40 30 %

20 10 0

1 2 3 4 5 6 7 8 9 1011121314151617181920212223242526272829 days

50 40 30 %

20

10 0

1

2

3

4

5

6

7

8 9 days

10

11

12

13

14

15

Fig. 2. Distribution of untransformed WSI (A) and transformed WSI (B) in two first parities.

traits scored in the old system were analyzed jointly (i.e. [o_move o_all]). For conformation traits recorded in the new system, three traits were analyzed simultaneously (e.g. [n_move n_front n_rear]). For correlations between old score traits and new score traits, bivariate genetic analyzes were performed (e.g. [o_move n_front]). Because of the small number of observation overlapping between two scoring systems, the residual covariances between old score traits and new score traits were set to zero. For reproduction traits, genetic analyzes of four traits including two different traits in both parities were performed. Due to the non-convergence of some specific fourtrait analysis, the association between weaning to service interval with number of born alive and number of stillborn were analyzed as bivariate, including [NBA WSI1], [NBA

WSI2], [NSB WSI1], [NSB WSI2]. Genetic correlations between conformation and reproduction traits were estimated between three traits: [one conformation trait and one reproduction trait in both parities] (e.g. [o_move NTB1 NTB2]). Heritabilities were defined as:

(

)

2 For conformation traits: h2 = σa2conf / σa2conf + σlitter + σe2 2

For litter size and WSI traits: h = Where

σa2i

σa2fert /

(

σa2fert

+

)

σe2

is the additive genetic variance of con-

2 formation traits (σa2conf ), litter size or WSI traits (σa2fert ), σlitter

is litter variance and σe2 is the residual variance.

Table 3 Estimated genetic correlations between conformation traits (standard error as subscripts). Estimates significantly different from zero are in bold. Conformation traits o_all n_move n_toes n_front n_rear n_under n_all

a

o_move

o_all

n_move

n_toes

n_front

n_rear

n_under

0.880.02
0.730.11
0.750.09
0.550.08
0.820.06
0.480.16
0.730.11

–
0.930.05
0.800.06
0.530.07
0.950.02
0.220.16
0.740.07

– 0.380.11 0.540.09 0.620.08
0.330.16 0.620.09

– 0.400.08 0.520.07
0.290.07 0.480.08

– 0.660.05
0.520.11 0.140.08

–
0.300.13 0.400.07

– 0.000.13

a o_move¼ old scoring of movement; o_all ¼old scoring of overall leg score; n_move ¼ new scoring of movement; n_toes¼ uneven toes and width between toes; n_front¼ front and side view of front legs; n_under ¼standing-under-position of rear leg; n_rear¼ read and side view of rear legs; n_all¼ new overall score.

14

H.T. Le et al. / Livestock Science 178 (2015) 9–17

3. Results Means and standard deviations for all conformation and reproduction traits are presented in Table 2. On average, the means of leg conformation traits were close to optimal scores, except for overall score in the new system ( X¯ ¼8 vs. optimal ¼1). For reproduction traits, the numbers of total born and liveborn piglets in second parity were higher compared with those in first parity ( X¯ ¼.3 vs. 12.3, 12.2 vs. 11.2 respectively). Both conformation and reproduction traits are heritable but at a relatively low level (Table 2). Heritability estimates for new front leg, new rear leg and new overall score were from 0.17 to 0.20, and heritability estimated for other traits were lower (0.02–0.10). The estimates of genetic correlations between conformation traits are presented in Table 3. Almost all conformation traits showed medium to high correlations with each other. The two traits recorded in the old system were highly positively correlated, indicating that sows with good movement also have a good overall leg score. Associations between traits in the new scoring system were on average somewhat weaker, the absolute values ranging from 0.00 to 0.66. The strongest correlation was found between new front leg and new rear leg quality. In general, traits in the two scoring systems were numerically negatively associated. Only the correlation between old overall leg score and new standing-under-position was not found to be significant, the other correlations between old traits and new traits were relatively high, ranging from
0.48 to
0.95. The estimated genetic correlations between reproduction traits are presented in Table 4. Litter size traits (number of total born, liveborn and stillborn piglets) showed relatively high correlations with each other. The positive correlations between them reflect that the numbers of liveborn and stillborn piglets increase with the number of total born piglets. Weaning to service interval in the two parities were highly correlated, with a genetic correlation estimated at 0.83. The estimated correlations between litter size and weaning to service interval were low and not significantly different from zero. The correlation between number of stillborn and weaning to service interval in parity 2 was slightly negative and significant (
0.38), meaning that sows having more stillborn piglets in parity 2 appear to have a shorter interval to the next insemination.

The estimates of genetic correlations between conformation and reproduction traits are presented in Table 5. Most of the estimates were not significantly different from zero. However, some significant correlation estimates were observed. Old movement showed a positive genetic association with number of total born and born alive piglets (0.20–0.36), indicating that sows with excellent movement had large litter size and more piglets born alive in both parities compared with sows with bad movement. Old movement also showed a favorable genetic association with weaning to service interval in second parity (
0.35). This negative genetic correlation suggests that sows having excellent movement tend to get back to heat after weaning faster than sows with bad movement. The number of piglets born alive in first parity showed negative correlations with new toes quality trait and new overall score trait (
0.35 and
0.31 respectively), meaning that sows with even claws and good space between claws and better overall score had more liveborn piglets. A weak positive correlation found between new front leg quality and number of still born in first parity (0.26) indicates that sows with cow-legged stance, turned-out pasterns (front view), post-legged pasterns (side view) and straight knee were likely to have more stillborn piglets in the first parity. The highest correlations estimated were between standing-under-position and litter size traits. Standing-underposition showed negative genetic correlation with the number of total born and liveborn piglets in both parities: a particularly strong association was observed in second parity (around
0.50). In other words, sows with higher risk to suffer from standing-under-position also had smaller litter size and fewer piglets born alive compared with healthy sows.

4. Discussion 4.1. Heritability estimates of conformation and locomotion traits Heritability estimates of conformation and locomotion traits found in this study were low to moderate (0.02– 0.20), and were similar to findings previously reported for the Swedish Yorkshire pig population (0.11 70.03, Lundeheim, 1987). In general, heritability estimates for conformation traits available in the literature vary, and our findings fall into the range reported for pigs (Hellbrugger,

Table 4 Estimated genetic correlations between reproduction traits (standard error as subscripts). Estimates significantly different from zero are in bold. Reproduction traits NTB2 NBA1 NBA2 NSB1 NSB2 WSI1 WSI2

a

NTB1

NTB2

NBA1

NBA2

NSB1

NSB2

WSI1

0.740.09 0.870.03 0.650.10 0.490.09 0.580.12
0.050.13 0.000.14

– 0.540.11 0.960.01 0.500.11 0.600.10 0.050.14
0.150.14

– 0.590.12
0.010.12 0.230.14
0.150.14
0.160.15

– 0.230.12 0.360.14 0.070.14
0.040.16

– 0.790.11 0.090.14 0.270.14

– 0.000.17
0.380.17

– 0.880.12

a NTB1,2 ¼ number of total born in parity 1,2; NBA1,2 ¼ number of born alive in parity 1,2; NSB1,2 ¼ number of stillborn in parity 1,2; WSI1,2 ¼ weaning to service interval in parity 1,2.

H.T. Le et al. / Livestock Science 178 (2015) 9–17

15

Table 5 Estimated genetic correlations between reproduction traits and conformation traits (standard error as subscripts). Estimates significantly different from zero are in bold. Conformationa

Reproductionc NTB1 NTB2 NBA1 NBA2 NSB1 NSB2 WSI1 WSI2

o_move b 1–3*

o_all 1–3*

n_move 1–4*–7

n_toes 4*–7

n_front 1–4*–7

n_rear 1–4*–7

n_under 4*–7

n_all 1–4*–6

0.200.09 0.250.10 0.250.10 0.360.10 0.010.09
0.190.11
0.070.11
0.350.11


0.010.08 0.130.09 0.030.09 0.160.09
0.090.08 0.010.10 0.000.10
0.190.11

0.080.15
0.250.16
0.050.17
0.230.17 0.240.15 0.010.19 0.030.17 0.340.20


0.180.13
0.150.14
0.350.13
0.160.14 0.260.13 0.020.16
0.020.15 0.170.17

0.160.10 0.220.11 0.070.11 0.150.12 0.260.10 0.190.12
0.040.12 0.030.13

0.110.11 0.090.12 0.190.12 0.100.13
0.050.11
0.030.14
0.070.13 0.030.14


0.390.16
0.540.18
0.350.18
0.530.18
0.130.18
0.020.21 0.020.20 0.010.23


0.140.12
0.200.13
0.310.13
0.220.14 0.170.12 0.130.15
0.180.13 0.080.15

* Indicates the optimal score on linear scale. a o_move¼ old scoring of movement; o_all ¼old scoring of overall leg score; n_move ¼ new scoring of movement; n_toes¼ uneven toes and width between toes; n_front¼ front and side view of front legs; n_under ¼standing-under-position of rear leg; n_rear¼ read and side view of rear legs; n_all¼ new overall score. b Second row indicates the scoring scale for conformation traits. c NTB1,2 ¼ number of total born in parity 1,2; NBA1,2 ¼ number of born alive in parity 1,2; NSB1,2 ¼ number of stillborn in parity 1,2; WSI1,2 ¼weaning to service interval in parity 1,2.

2007; Jørgensen and Andersen, 2000; Knauer et al., 2010; López-Serrano et al., 2000; Luther et al., 2007; Nikkilä et al., 2013; Serenius and Stalder, 2004). The wide range of heritability estimates can be caused by many factors, such as testing scheme, the scale for scoring and the subjectivity of evaluators. While some studies dealt with conformation data recorded on adult animals (Hellbrugger, 2007), others analyzed records on young animals at performance testing. Also, conformation traits themselves can be different in different studies: Hellbrugger (2007) and Luther et al. (2007) treated front view, side view and pastern of front leg as different traits while these traits were combined into one trait in our study. Taken together, the low to medium estimates of heritabilities for conformation and locomotion traits found in our study and the literature suggest that these traits should respond to selection. However, one should not expect a rapid improvement because of the low to moderate heritability estimates. 4.2. Genetic correlations between conformation traits and reproduction traits Published estimates of the associations between conformation/locomotion traits and reproduction performance in pigs are few. Previous studies have focused more on the causal relationship between lameness or leg weakness due to osteochondrosis, and fertility. They have reported a low, non-significant but favorable genetic association between these traits. Serenius and Stalder (2004) showed that sows with severe leg problems tend to have lower number of piglets born alive during their reproductive lifetime. There are also publications reporting significant associations between conformation and reproductive traits (Knauer et al., 2011). Previously Rothschild et al. (1988) found a disparity in reproductive capacity between three lines selected for different front-leg structure: the “no leg-weakness” line had larger litter size

and higher number of liveborn piglets compared with the “intermediate or severe leg-weakness” lines. Genetic associations between leg conformation traits and reproductive efficiency were also reported by Nikkilä et al. (2013). In their study, sows with slightly outward turned front leg, less upright rear leg posture and intermediate rear leg foot size had larger litters and longer productive lifetime. Thus good structural conformation and locomotion are likely to have a favorable relationship with reproduction traits: larger litter size, higher number of born alive, fewer stillborn piglets and shorter weaning to service interval. This association tendency is in agreement with findings in the present study. The relationships of leg conformation and lameness with other reproduction traits rather than litter size or weaning to service interval traits have also been investigated in several studies. Heinonen et al. (2006) reported that lame sows were less likely to become pregnant compared with the non-lame sows. The tendency of lame sows to be less reproductive was consistent with studies of Heinonen et al. (2002) and Knauer et al. (2012). In their studies, sows with poor locomotion showed a reduced reproductive performance in that they were unlikely to reach puberty, conceive or farrow. The consequence of abnormal leg structure and lameness on reproduction has not only been found in pigs but also in dairy cattle. Lameness in dairy cows has been found to be associated with longer calving-first service interval, calving–conception interval, lower conception rate and higher number of services required per conception (Collick et al., 1989; Hernandez et al., 2001; Lucey et al., 1986; Melendez et al., 2003). Lameness can be a stressor contributing to ovulation failure. Lame cows tent to fail to show estrus, or to form the follicles with hormone stimulation, or showed lower proportion of ovulation compared with healthy cows (Crowe and Williams, 2012; Morris et al., 2011, 2009). In summary, studies in different species indicate that bad conformation/locomotion traits/ lameness have a negative impact on reproductive

16

H.T. Le et al. / Livestock Science 178 (2015) 9–17

performance of animals. The biological mechanism for how abnormal conformation and lameness reduce reproduction performance is unclear. Our hypothesis is that inferior leg strength can cause pain to the animals (Heinonen et al., 2013; Whay et al., 1998). Pain is a cause of stress, which has a negative influence on reproduction of sows as reviewed by Einarsson et al. (2008). Other authors (Morris et al., 2011; Walker et al., 2008) have also suggested that lameness can be considered a natural chronic stressor. Lame sows spend more time sitting or lying, possibly due to the pain in changing posture between standing and sitting (Madec et al., 1986). According to the review of Heinonen et al. (2013), this inactive behavior can lead to an increase in microorganisms around the perineal region, resulting in higher risk of urogenital infections. These authors also suggested that a lower frequency of urination due to lameness can worsen the urogenital infections. Infections in the reproductive tracts are expected to reduce the fertility capacity of affected animals. To obtain a better understanding of these relationships, further studies of the associations of different conformation traits with the frequency or duration of sitting and lying behavior, and with the clinical pathology of urogenital infection need to be conducted. The correlations between leg conformation/ locomotion traits and reproduction traits indicate that selection for one trait can influence the other correlated traits. According to our findings, on the one hand, animals with optimal leg structure and good movement might be desirable for selection to obtain the sows with larger litter size, more liveborn and fewer stillborn piglets, and shorter interval from weaning to service. On the other hand, selection for reproductive performance would to some extent have a positive impact on leg conformation and locomotion.

5. Conclusion Leg conformation and locomotion traits are heritable, so it is possible to change these traits by selection. Favorable estimates of genetic correlations found in this study imply that good conformation/ locomotion traits are likely to be genetically associated with good litter size and shorter time to return heat after weaning. In other words, there is a potential to simultaneously improve pigs with sound leg structure and efficient reproduction performance by selection on leg conformation and locomotion traits recorded at young age. Standing-under-position syndrome should be avoided in breeding due to high correlation of this trait with number of total born and piglets born alive.

Acknowledgment Le Hong Thu benefited from a joint grant from the European Commission within the framework of the Erasmus-Mundus joint doctorate “EGS-ABG”. We are grateful EGS ABG for the funding and Nordic Genetics for the data

provision. We would like to thank David Edwards at Center for Quantitative Genetics and Genomics (Aarhus University) for critical comments and proof reading of the manuscript.

References Collick, D.W., Ward, W.R., Dobson, H., 1989. Associations between types of lameness and fertility. Vet. Rec. 125, 103–106. Crowe, M., Williams, E., 2012. Triennial lactation symposium : effects of stress on postpartum reproduction in dairy cows. J. Anim. Sci. 90, 1722–1727, http://dx.doi.org/10.2527/jas2011-4674. Einarsson, S., Brandt, Y., Lundeheim, N., Madej, A., 2008. Stress and its influence on reproduction in pigs: a review. Acta Vet. Scand. 50, 48, http://dx.doi.org/10.1186/1751-0147-50-48. Engblom, L., Lundeheim, N., Dalin, A.-M., Andersson, K., 2007. Sow removal in Swedish commercial herds. Livest. Sci. 106, 76–86, http://dx. doi.org/10.1016/j.livsci.2006.07.002. Fitzgerald, R.F., Stalder, K.J., Karriker, L. a, Sadler, L.J., Hill, H.T., Kaisand, J., Johnson, A.K., 2012. The effect of hoof abnormalities on sow behavior and performance. Livest. Sci. 145, 230–238, http://dx.doi.org/10.1016/ j.livsci.2012.02.009. Heinonen, M., Oravainen, J., Orro, T., Virolainen, J., Tast, A., Peltoniemi, O. A.T., 2006. Lameness and fertility of sows and gilts in randomly selected loose-housed herds in Finland. Vet. Rec. 159, 383–387. Heinonen, M., Oravainen, J., Tast, A., Peltoniemi, O.A.T., 2002. Lameness and fertility in sows and gilts–a pilot study. Reprod. Domest. Anim. 37, 236. Heinonen, M., Peltoniemi, O., Valros, A., 2013. Impact of lameness and claw lesions in sows on welfare, health and production. Livest. Sci. 156, 2–9. Hellbrugger, B., 2007. Genetic Aspect of Piglet Losses and the Maternal Behaviour of Sows. Christian-Albrechts-University, Kiel Doctoral thesis. Hernandez, J., Shearer, J.K., Webb, D.W., 2001. Effect of lameness on the calving-to-conception interval in dairy cows. J. Am. Vet. Med. Assoc. 218, 1611–1614. Jensen, T.B., Baadsgaard, N.P., Houe, H., Toft, N., Østergaard, S., 2007. The effect of lameness treatments and treatments for other health disorders on the weight gain and feed conversion in boars at a Danish test station. Livest. Sci. 112, 34–42, http://dx.doi.org/10.1016/j. livsci.2007.01.153. Jorgensen, B., 2003. Influence of floor type and stocking density on leg weakness, osteochondrosis and claw disorders in slaughter pigs. Anim. Sci. 77, 439–449. Jørgensen, B., Andersen, S., 2000. Genetic parameters for osteochondrosis in Danish Landrace and Yorkshire boars and correlations with leg weakness and production. Anim. Sci. 71, 427–434. Knauer, M., Stalder, K.J., Serenius, T., Baas, T.J., Berger, P.J., Karriker, L., Goodwin, R.N., Johnson, R.K., Mabry, J.W., Miller, R.K., Robison, O.W., Tokach, M.D., 2010. Factors associated with sow stayability in 6 genotypes. J. Anim. Sci. 88, 3486–3492, http://dx.doi.org/10.2527/ jas.2009-2319. Knauer, M.T., Cassady, J.P., Newcom, D.W., See, M.T., 2011. Phenotypic and genetic correlations between gilt estrus, puberty, growth, composition, and structural conformation traits with first-litter reproductive measures. J. Anim. Sci. 89, 935–942, http://dx.doi.org/10.2527/ jas.2009-2673. Knauer, M.T., Cassady, J.P., Newcom, D.W., See, M.T., 2012. Gilt development traits associated with genetic line, diet and fertility. Livest. Sci. 148, 159–167, http://dx.doi.org/10.1016/j.livsci.2012.05.024. Koning, D.B., De, Groot, P.N., De, Hazeleger, W., Kemp, B., Grevenhof, E.M., Van, Laurenssen, B.F.A., Ducro, B.J., Heuven, H.C.M., 2012. Associations between osteochondrosis and conformation and locomotive characteristics in pigs. J. Anim. Sci. 90, 4752–4763, http://dx.doi.org/ 10.2527/jas2012-5310. López-Serrano, M., Reinsch, N., Looft, H., Kalm, E., 2000. Genetic correlations of growth, backfat thickness and exterior with stayability in large white and landrace sows. Livest. Prod. Sci. 64, 121–131, http: //dx.doi.org/10.1016/S0301-6226(99)00169-4. Lucey, S., Rowlands, G.J., Russell, A.M., 1986. The association between lameness and fertility in dairy cows. Vet. Rec. 118, 628–631. Lundeheim, N., 1987. Genetic analysis of osteochondrosis and leg weakness in the Swedish pig progeny testing scheme. Acta Vet. Scand. 37, 159–173. Luther, H., Schwörer, D., Hofer, a, 2007. Heritabilities of osteochondral

H.T. Le et al. / Livestock Science 178 (2015) 9–17

lesions and genetic correlations with production and exterior traits in station-tested pigs. Animal 1, 1105–1111, http://dx.doi.org/10.1017/ S1751731107000493. Madec, F., Cariolet, R., Dantzer, R., Croix, L., Carreire, D. De, 1986. Relevance of some behavioural criteria concerning the cow (motor activity and water intake) in the intensive pig farming and veterinary practice. Ann. Vet. Res. 17, 177–184. Madsen, P., Jensen, J., 2013. A User's Guide to DMU. Melendez, P., Bartolome, J., Archbald, L.F., Donovan, a, 2003. The association between lameness, ovarian cysts and fertility in lactating dairy cows. Theriogenology 59, 927–937. Morris, M.J., Kaneko, K., Walker, S.L., Jones, D.N., Routly, J.E., Smith, R.F., Dobson, H., 2011. Influence of lameness on follicular growth, ovulation, reproductive hormone concentrations and estrus behavior in dairy cows. Theriogenology 76, 658–668, http://dx.doi.org/10.1016/j. theriogenology.2011.03.019. Morris, M.J., Walker, S.L., Jones, D.N., Routly, J.E., Smith, R.F., Dobson, H., 2009. Influence of somatic cell count, body condition and lameness on follicular growth and ovulation in dairy cows. Theriogenology 71, 801–806, http://dx.doi.org/10.1016/j.theriogenology.2008.10.001. Nikkilä, M.T., Karriker, A., Boggess, M.V., Serenius, T.V., 2013. Genetic associations for gilt growth, compositional, and structural soundness traits with sow longevity and lifetime reproductive performance. J. Anim. Sci., 1570–1579, http://dx.doi.org/10.2527/jas2012-5723. Pluym, L.M., Van Nuffel, a, Van Weyenberg, S., Maes, D., 2013. Prevalence of lameness and claw lesions during different stages in the reproductive cycle of sows and the impact on reproduction results. Animal 7, 1174–1181, http://dx.doi.org/10.1017/S1751731113000232. Rothschild, M.F., Christian, L.L., Jung, Y.C., 1988. Genetic control of frontleg weakness in Duroc swine. II. Correlated responses in growth rate,

17

backfat and reproduction from five generations of divergent selection. Livest. Prod. Sci. 19, 473–485, http://dx.doi.org/10.1016/03016226(88)90013-9. Rydhmer, L., 2005. Swine breeding programmes in the Nordic countries, National Swine Improvement Federation. Serenius, T., Stalder, K.J., 2004. Genetics of length of productive life and lifetime prolificacy in the Finnish landrace and large white pig populations. J. Anim. Sci. 82, 3111–3117. Ten Napel, J., de Vries, A.G., Buiting, G.G., Luiting, P., Merks, J.W., Brascamp, E.W., 1995. Genetics of the interval from weaning to estrus in first-litter sows: distribution of data, direct response of selection, and heritability. J. Anim. Sci. 73, 2193–2203. Walker, S.L., Smith, R.F., Jones, D.N., Routly, J.E., Dobson, H., 2008. Chronic stress, hormone profiles and estrus intensity in dairy cattle. Horm. Behav. 53, 493–501, http://dx.doi.org/10.1016/j.yhbeh.2007.12.003. Whay, H.R., Waterman, a E., Webster, a J.F., O’Brien, J.K., 1998. The influence of lesion type on the duration of hyperalgesia associated with hindlimb lameness in dairy cattle. Vet. J. 156, 23–29, http://dx.doi. org/10.1016/S1090-0233(98)80058-0. Wischner, D., Kemper, N., Stamer, E., Hellbruegge, B., Presuhn, U., Krieter, J., 2009. Characterisation of sows' postures and posture changes with regard to crushing piglets. Appl. Anim. Behav. Sci. 119, 49–55, http: //dx.doi.org/10.1016/j.applanim.2009.03.002. Ytrehus, B., Andreas Haga, H., Mellum, C.N., Mathisen, L., Carlson, C.S., Ekman, S., Teige, J., Reinholt, F.P., 2004. Experimental ischemia of porcine growth cartilage produces lesions of osteochondrosis. J. Orthop. Res. 22, 1201–1209, http://dx.doi.org/10.1016/j. orthres.2004.03.006.