Evaluation of genetic resistance to Salmonella Pullorum in three chicken lines

Evaluation of genetic resistance to Salmonella Pullorum in three chicken lines Abstract Resistance to diseases varies considerably among populations of the same species and can be ascribed to both genetic and environmental factors. Salmonella Pullorum (SP) is responsible for significant losses in the poultry industry, especially in developing countries. To better understand SP resistance in chicken populations with different genetic backgrounds, we orally challenged 3 chicken lines with SP—a highly selected commercial breed (Rhode Island Red, RIR), a local Chinese chicken (Beijing You, BY), and a synthetic layer line (dwarf, DW)—at 4 d of age. Two traits related to SP resistance, survival, and bacterial carriage in the spleen were evaluated after infection. Survival rates were recorded up to 40 d of age when all chickens still alive were killed to verify the presence of SP in the spleen to determine carrier state. Mortalities for RIR, BY, and DW chicks were 25.1%, 8.3%, and 22.7%, respectively, and the corresponding carrier-states in the spleens were 17.9%, 0.6%, and 15.8%. Survival and carrier-state heritabilities were estimated using an animal threshold model. Survival heritability was 0.197, 0.091, and 0.167 in RIR, BY, and DW populations, respectively, and the heritabilities of carrier state for DW and RIR were 0.32 and 0.16, respectively. This is the first time that the heritability of the SP carrier state has been evaluated in chickens. Our study provides experimental evidence that chickens with various genetic background exhibited significantly different SP-resistant activities and heritabilities. These results may be useful for selecting lines with better disease resistance. INTRODUCTION Pullorum disease is caused by Salmonella Pullorum (SP) and represents a serious threat to the poultry industry. Pullorum disease has been eradicated from commercial flocks in the U.S, Canada, Japan, and most European countries through collective control measures (Shivaprasad, 2000). However, in Asia and South America, pullorum disease is still a cause of high poultry mortality rates and huge economic losses due to reduced hygienic conditions and complex rearing facilities (Wigley et al., 2002). Moreover, with increasing requests from the public to ban antibiotics, an alternative strategy for controlling the disease may lie in genetic resistance. Disease resistance is determined by both genetics and the environment (Lamont, 1998). Chickens from different populations present dramatically different levels of resistance to certain diseases or immunogens, such as Marek's disease (Steadham et al., 1987; Yu et al., 2011; Li et al., 2013; Yan et al., 2015), avian leucosis (Bearse et al., 1963; Crittenden et al., 1974; Okazaki et al., 1982), Salmonella enteritidis (SE) (Protais et al., 1996; Swaggerty et al., 2005), avian flu (Li et al., 2006), Newcastle disease (Cole and Hutt, 1961), Escherichia coli (Leitner et al., 1992; Sandford et al., 2012), Campylobacter (Boyd et al., 2005; Li et al., 2010), and even some immunogens like sheep red blood cells (Dunnington et al., 1989; Yang et al., 1999). The strategy to control SP or Salmonella disease by breeding disease-resistant chickens was adopted as early as the 1930s (Roberts and Card, 1935) when acute salmonellosis, such as pullorum disease, was threatening the poultry industry. Afterwards, Hutt and Scholes (1941) presented evidence that Leghorn chicks were more resistant to SP than Rhode Island Reds. As the measures to control the disease produced good results, breeding of disease-resistant chickens was interrupted because of slow progress and high costs. In the 1980s, interest in the selection of more resistant animals was renewed due to an outbreak of Salmonella enteritidis (Calenge et al., 2010). Bumstead and Barrow (1993) proposed that a general mechanism of resistance might apply to Salmonella gallinarum (SG), SP, and SE (Bumstead and Barrow, 1993). Wigley and colleagues (2001) showed that SP could persist in splenic macrophages for long periods. On the other hand, the use of comparative genomics and the development of sequencing technologies led to the identification of many salmonella-resistant genes and quantitative trait loci (QTLs) (Hu et al., 1997; Fife et al., 2011). In the present study, we aimed at clarifying whether chicken populations from 3 different genetic backgrounds developed different SP resistance after being orally challenged with the bacteria. We also estimated heritabilities of survival and SP carrier ability in the 3 chicken populations. MATERIALS AND METHODS Ethics Statement. All experiments were approved by the Committee for Animal Care and Use of China Agricultural University (Approval ID: XXCB-20,090,209). All animals were fed and handled according to the regulations and guidelines established by this committee, and all efforts were made to minimize suffering. Chickens. A commercial layer line (Rhode Island Red, RIR), a local Chinese chicken (Beijing You, BY), and a synthetic layer line (dwarf, DW) bearing the sex-linked dw allele were selected for the experiments. All 3 lines derived from completely different genetic backgrounds. A total of 646 RIR, 681 DW, and 542 BY chicks were produced in a single hatch by mating 11 males with 93 females, 13 males with 114 females, and 21 males with 87 females, respectively. A detailed pedigree was kept for each chicken. All parents were serologically tested twice through a commercial antigen developed for standard rapid whole-blood plate agglutination for Salmonella pullorum to ensure that the chicks were salmonella-free and to avoid the presence of maternal antibodies. All chicks were hatched in the same place and transferred to the same isolation room on the d of hatching. Each population was split into 4 isolators (produced by Suzhou Fengshi Laboratory Animal Equipment Co. Ltd, model GJ-1) and a total of 12 isolators were used under the same environmental condition. To confirm that the chicks were free from Salmonella, we randomly selected 60 chicks (20 per line) and tested them for the presence of Salmonella antibodies. Further, another 120 chicks (40 per line) were randomly selected as controls and put in 2 separate isolators (one for 60 males and another for 60 females) in another room. All chicks had free access to sterile water and sterile feed. In total, we had 586 RIRs, 621 DWs, and 482 BYs available to challenge with SP. Bacterial Challenge. SP strain 533 was obtained from the China Institute of Veterinary Drug Control (Beijing, China). The challenge dose was slightly below the 50% lethal dose (LD50), which was estimated in a preliminary experiment by challenging 120 Rhode Island Red chicks with 5 different concentrations (data not shown). The bacteria were routinely grown under aerobic conditions at 37°C in Luria Bertani (LB) broth for 12 h. The bacterial suspension was adjusted to a concentration of 109 colony-forming units (CFUs) per milliliter and stored at −80°C. On inoculation day, the bacterial concentration was confirmed by plating and counting colonies, and the suspension was diluted in sterile phosphate buffer saline to obtain an inoculum concentration of 9.6 × 107 CFU/mL. All chicks were orally inoculated with 0.5 mL of SP culture containing 4.8 × 107 CFU at 4 d of age, and the control chicks were treated with the same amount of sterile phosphate buffer saline. Chicks were observed every 2 h. Dead chicks were removed from the isolators as soon as they were discovered. After 40 d, all chicks still alive were killed by neck dislocation, and their spleens were removed aseptically and then immediately plated onto MacConkey agar median using an inoculation loop without enrichment to check for the presence of SP. There was no antibiotics in the MacConkey plates. Trait Definitions. The resistance of different chicken lines was evaluated by the population survival rate. Chicks that died within 36 d after inoculation were classified as “0”, while those that were still alive after 36 d were classified as “1”. For the resistance to carrier- state, chicks whose spleens carried SP were classified as “1”, while those without SP on their spleens were classified as “0”. Statistical Analysis. The variance and covariance components were estimated using the DMU software package (Madsen and Jensen, 2008). Two analyses were used to calculate genetic parameters: a classic animal model and a threshold animal model. The heritability of mortality and the carrier state were analyzed using the animal threshold model. Both models included the cage as a fixed effect and additive genetic effects as random effects. In the threshold model, observed binary records (Yij) are assumed to be determined by an underlying liability (λij) as shown below:   \begin{equation*}{{\rm{Y}}_{\rm{ij}}}\,{\rm{ = }}\left\{\!\! {\ \begin{array}{@{}*{1}{c}@{}} {{\rm{0\ for}}\ {{\rm{\lambda }}_{{\rm{ij}}}}{\rm{\ }} \le {\rm{\ 0}}}\\ {{\rm{1\ for}}\ {{\rm{\lambda }}_{{\rm{ij}}}}{\rm{\ > \ 0}}} \end{array}} \right.,\end{equation*}$\ $The animal threshold in matrix notation is   \begin{equation*}y{\rm{ }} = {\rm{ }}X\beta {\rm{ }} + Za{\rm{ }} + e\end{equation*} where y is a vector of a phenotypic values; β and a are the fixed and random additive effect vectors, respectively; X and Z are appropriate incidence matrices of the fixed and random additive effects, respectively; and e represents the random residuals. The animal threshold was analyzed using the Gibbs sampling module included in the DMU software package (Ødegård et al., 2010), and the classical animal model was analyzed with the DMUAI module in DMU using the average information restricted maximum likelihood (AI-REML) algorithm. RESULTS Challenge Test. After the serological tests of the parent generation, we obtained 128 Salmonella-free chickens from 140 DWs, 103 from 160 RIRs, and 132 from 172 BYs. In addition, healthy parents that laid only a few eggs were also discarded from our study. The 60 sampled chicks (n = 20/line) all proved to be free from SP. During the course of the challenge, only one DW chick from the control group (with a thin and weak body) died; however, we did not find Salmonella in its liver or spleen. Every dead chick in the challenge group was necropsied and the spleen was cultured, as the survivors were, and they all proved to be infected. Most chicks that died from challenging showed typical SP infection symptoms such as hepatosplenomegaly, white diarrhea, cecal cores, etc. In addition, 5 samples were randomly selected for PCR identification, and all 5 proved to be SP. The 3 chicken lines had different survival curves as shown in Figure 1. Overall, 382 out of 621 DWs, 334 out of 586 RIRs, and 439 out of 482 BYs survived the SP challenge. The DW chicks were most sensitive to SP in the first days after the challenge, but they became insensitive around 10 d of age. However, RIR chickens exhibited a more constant death rate through 25 d. As for the BY, only a few birds died in the early days post infection. After 10 d of age, no more deaths appeared in BY. Overall, our results indicated that the order of resistance to SP was BY > DW > RIR. Figure 1. View largeDownload slide Survival curves for 3 chicken lines after infection with SP. •, Rhode Island Red (RIR); ○, Dwarf (DW); ▵, Beijing You (BY). Figure 1. View largeDownload slide Survival curves for 3 chicken lines after infection with SP. •, Rhode Island Red (RIR); ○, Dwarf (DW); ▵, Beijing You (BY). Mortality and Carrier-state Statistics. Death rate and carrier state data are presented in Figure 2. Mortality in RIR, BY, and DW were 25.1%, 8.3%, and 22.7% respectively. Carriage rates were 17.9%, 0.6%, and 15.8% for RIR, BY, and DW, respectively. These results showed that carrier state and mortality seem to be positively related; BY chicken were almost completely free of bacteria. Figure 2. View largeDownload slide The number and proportion of dead, carrier, and clear (not carrying SP) chickens from 3 lines, respectively. All traits were determined within 40 d of age, namely, within 36 d post-inoculation. 1DW, dwarf chicken; RIR, Rhode Island Red; and BY, Beijing You. Figure 2. View largeDownload slide The number and proportion of dead, carrier, and clear (not carrying SP) chickens from 3 lines, respectively. All traits were determined within 40 d of age, namely, within 36 d post-inoculation. 1DW, dwarf chicken; RIR, Rhode Island Red; and BY, Beijing You. Heritabilities. Estimated genetic parameters for survival and the carrier state are presented in Table 1. Survival heritabilities were 0.197, 0.091, and 0.167 for the RIR, BY, and DW populations, respectively, heritabilities for the carrier state in DW and RIR were 0.32 and 0.16. The heritability of the carrier state in BY could not be estimated because of too few carrier chickens. These disease-resistance traits presented low to moderate heritabilities in line with previous research (Beaumont et al., 1999; Girard-Santosuosso et al., 2002). The heritability of survival in BY was lower than it was for the other lines. This may be the result of the very low death rate in this line, which may cause a biased estimation of heritability. Table 1. Heritabilities of survival and the carrier state. Traits  Line1  Heritability  SE2  Survival  DW  0.167  0.091    RIR  0.197  0.100    BY  0.091  0.062  Carrier-state  DW  0.320  0.106    RIR  0.161  0.097    BY  –  –  Traits  Line1  Heritability  SE2  Survival  DW  0.167  0.091    RIR  0.197  0.100    BY  0.091  0.062  Carrier-state  DW  0.320  0.106    RIR  0.161  0.097    BY  –  –  1DW, dwarf chicken; RIR, Rhode Island Red; and BY, Beijing You 2SE, standard error View Large DISCUSSION Various responses by chickens with different genotypes to certain pathogens have been reported (Briles et al., 1977; Swaggerty et al., 2009; Beaumont et al., 2010; Calenge and Beaumont, 2012). For example, the ADOL chicken lines N and P have exhibited differing resistance to Marek's disease (Bacon et al., 2000). The important role the MHC and B complexes play for these 2 chicken lines is also well documented (Briles et al., 1977; Powell et al., 1982). In the current study, we found dramatically different resistances to SP among the 3 populations of chicks. We found that the BY chickens exhibited much higher resistance to SP, either in terms of lower mortality or via an increased number of carriers. These observations provide an explicit explanation for the large differences in disease resistance among chicken populations. The survival curves for the 3 populations indicated that the 3 chicken lines responded differently to SP infection. Some DW chicks died in the first few days after infection and others who survived mostly grew normally. However, many RIR chicks, which struggled for longer, could not avoid death in the end. From our observations, the RIR chicks that died were the ones that exhibited low body weight and poor growth (data not shown). We speculated that these characteristics could result from a different immune response occurring in the different chick lines because disease resistance may correlate with growth traits (Dorshorst et al., 2011; Lee et al., 2014; Nikbakht and Esmailnejad, 2015). There is a general view that native poultry, which have not been subject to intensive selection, are usually more resistant to diseases (Alvarez et al., 2003; Schou et al., 2010; Han et al., 2013). Considering the origin of the 3 lines, RIR has experienced the most intense selection for performance in production (Hays, 1955). Comparatively, DW chickens are a newly developed commercial line. As a local breed, BY chickens have not been intensively selected and thus might have higher genetic diversity. This view is in agreement with the fact that indigenous chicken lines that have not undergone extensive artificial selection are more resistant to infectious diseases (Jie and Liu, 2011). Breeders might choose to breed indigenous chickens like BY to produce more resistant chicken lines as this could reduce the risk of an outbreak of Salmonella. Furthermore, it could benefit conservation of the breed and improve genetic diversity in commercial chicken flocks. Here we report the first estimated heritability of SP resistance among chicken populations, which varies among chicken lines. The heritability of mortality estimated here is close to that reported for Salmonella Enteritidis (Beaumont et al., 1999), and heritability of the carrier state, based on investigation of the spleen, was higher than what has been reported for the heritability of the carrier state based on investigation of the ceca (Berthelot et al., 1998). The heritability of disease resistance usually ranges from low to moderate. However, values of 0.16 to 0.32 are sufficiently high, and it is worth investigating QTLs or candidate genes (Girard-Santosuosso et al., 2002). The carrier state is an important trait in SP resistance. The high heritability reported for the first time here indicated that it is possible to breed chickens without carrying SP in the spleen, which is very important for SP purification in breeding population. On chicken farms, we typically use serological tests to identify and then eliminate infected chickens. However, we could infer here that the traditional serological test may not be suitable for indigenous chickens because many BY chickens with SP antibodies were found to be free from SP. Based on the fairly low percentage of SP carriers in the BY chicks that survived the challenge, serological tests for SP, which have been used principally as a screening tool for SP infection, could not accurately confirm the infection. In several studies, SP from tissues of seropositive hens could not be isolated (Waltman and Horne, 1993; Gast, 1997). According to our results, serological tests were still meaningful for RIR and DW. However, the carrier state should be better investigated in local chicken breeds, and alternative strategies should be developed for Salmonella tests in indigenous chickens. In conclusion, our results showed that BY chickens are more resistant to SP than RIR or DW chickens are and that genetic variance plays an important role in SP resistance in different chicken lines, either in terms of mortality or as a carrier state. Selecting more resistant lines could help to reduce the risk of poultry infections and subsequent economic losses. ACKNOWLEDGMENTS This work was supported by the earmarked fund for the Beijing Innovation Team of the Modern Agro-industry Technology Research System (BAIC04–2016), National Scientific Supporting Projects of China (2015BAD03B03), and Chinese Agricultural Research System (CARS-41). 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Abstract

Abstract Resistance to diseases varies considerably among populations of the same species and can be ascribed to both genetic and environmental factors. Salmonella Pullorum (SP) is responsible for significant losses in the poultry industry, especially in developing countries. To better understand SP resistance in chicken populations with different genetic backgrounds, we orally challenged 3 chicken lines with SP—a highly selected commercial breed (Rhode Island Red, RIR), a local Chinese chicken (Beijing You, BY), and a synthetic layer line (dwarf, DW)—at 4 d of age. Two traits related to SP resistance, survival, and bacterial carriage in the spleen were evaluated after infection. Survival rates were recorded up to 40 d of age when all chickens still alive were killed to verify the presence of SP in the spleen to determine carrier state. Mortalities for RIR, BY, and DW chicks were 25.1%, 8.3%, and 22.7%, respectively, and the corresponding carrier-states in the spleens were 17.9%, 0.6%, and 15.8%. Survival and carrier-state heritabilities were estimated using an animal threshold model. Survival heritability was 0.197, 0.091, and 0.167 in RIR, BY, and DW populations, respectively, and the heritabilities of carrier state for DW and RIR were 0.32 and 0.16, respectively. This is the first time that the heritability of the SP carrier state has been evaluated in chickens. Our study provides experimental evidence that chickens with various genetic background exhibited significantly different SP-resistant activities and heritabilities. These results may be useful for selecting lines with better disease resistance. INTRODUCTION Pullorum disease is caused by Salmonella Pullorum (SP) and represents a serious threat to the poultry industry. Pullorum disease has been eradicated from commercial flocks in the U.S, Canada, Japan, and most European countries through collective control measures (Shivaprasad, 2000). However, in Asia and South America, pullorum disease is still a cause of high poultry mortality rates and huge economic losses due to reduced hygienic conditions and complex rearing facilities (Wigley et al., 2002). Moreover, with increasing requests from the public to ban antibiotics, an alternative strategy for controlling the disease may lie in genetic resistance. Disease resistance is determined by both genetics and the environment (Lamont, 1998). Chickens from different populations present dramatically different levels of resistance to certain diseases or immunogens, such as Marek's disease (Steadham et al., 1987; Yu et al., 2011; Li et al., 2013; Yan et al., 2015), avian leucosis (Bearse et al., 1963; Crittenden et al., 1974; Okazaki et al., 1982), Salmonella enteritidis (SE) (Protais et al., 1996; Swaggerty et al., 2005), avian flu (Li et al., 2006), Newcastle disease (Cole and Hutt, 1961), Escherichia coli (Leitner et al., 1992; Sandford et al., 2012), Campylobacter (Boyd et al., 2005; Li et al., 2010), and even some immunogens like sheep red blood cells (Dunnington et al., 1989; Yang et al., 1999). The strategy to control SP or Salmonella disease by breeding disease-resistant chickens was adopted as early as the 1930s (Roberts and Card, 1935) when acute salmonellosis, such as pullorum disease, was threatening the poultry industry. Afterwards, Hutt and Scholes (1941) presented evidence that Leghorn chicks were more resistant to SP than Rhode Island Reds. As the measures to control the disease produced good results, breeding of disease-resistant chickens was interrupted because of slow progress and high costs. In the 1980s, interest in the selection of more resistant animals was renewed due to an outbreak of Salmonella enteritidis (Calenge et al., 2010). Bumstead and Barrow (1993) proposed that a general mechanism of resistance might apply to Salmonella gallinarum (SG), SP, and SE (Bumstead and Barrow, 1993). Wigley and colleagues (2001) showed that SP could persist in splenic macrophages for long periods. On the other hand, the use of comparative genomics and the development of sequencing technologies led to the identification of many salmonella-resistant genes and quantitative trait loci (QTLs) (Hu et al., 1997; Fife et al., 2011). In the present study, we aimed at clarifying whether chicken populations from 3 different genetic backgrounds developed different SP resistance after being orally challenged with the bacteria. We also estimated heritabilities of survival and SP carrier ability in the 3 chicken populations. MATERIALS AND METHODS Ethics Statement. All experiments were approved by the Committee for Animal Care and Use of China Agricultural University (Approval ID: XXCB-20,090,209). All animals were fed and handled according to the regulations and guidelines established by this committee, and all efforts were made to minimize suffering. Chickens. A commercial layer line (Rhode Island Red, RIR), a local Chinese chicken (Beijing You, BY), and a synthetic layer line (dwarf, DW) bearing the sex-linked dw allele were selected for the experiments. All 3 lines derived from completely different genetic backgrounds. A total of 646 RIR, 681 DW, and 542 BY chicks were produced in a single hatch by mating 11 males with 93 females, 13 males with 114 females, and 21 males with 87 females, respectively. A detailed pedigree was kept for each chicken. All parents were serologically tested twice through a commercial antigen developed for standard rapid whole-blood plate agglutination for Salmonella pullorum to ensure that the chicks were salmonella-free and to avoid the presence of maternal antibodies. All chicks were hatched in the same place and transferred to the same isolation room on the d of hatching. Each population was split into 4 isolators (produced by Suzhou Fengshi Laboratory Animal Equipment Co. Ltd, model GJ-1) and a total of 12 isolators were used under the same environmental condition. To confirm that the chicks were free from Salmonella, we randomly selected 60 chicks (20 per line) and tested them for the presence of Salmonella antibodies. Further, another 120 chicks (40 per line) were randomly selected as controls and put in 2 separate isolators (one for 60 males and another for 60 females) in another room. All chicks had free access to sterile water and sterile feed. In total, we had 586 RIRs, 621 DWs, and 482 BYs available to challenge with SP. Bacterial Challenge. SP strain 533 was obtained from the China Institute of Veterinary Drug Control (Beijing, China). The challenge dose was slightly below the 50% lethal dose (LD50), which was estimated in a preliminary experiment by challenging 120 Rhode Island Red chicks with 5 different concentrations (data not shown). The bacteria were routinely grown under aerobic conditions at 37°C in Luria Bertani (LB) broth for 12 h. The bacterial suspension was adjusted to a concentration of 109 colony-forming units (CFUs) per milliliter and stored at −80°C. On inoculation day, the bacterial concentration was confirmed by plating and counting colonies, and the suspension was diluted in sterile phosphate buffer saline to obtain an inoculum concentration of 9.6 × 107 CFU/mL. All chicks were orally inoculated with 0.5 mL of SP culture containing 4.8 × 107 CFU at 4 d of age, and the control chicks were treated with the same amount of sterile phosphate buffer saline. Chicks were observed every 2 h. Dead chicks were removed from the isolators as soon as they were discovered. After 40 d, all chicks still alive were killed by neck dislocation, and their spleens were removed aseptically and then immediately plated onto MacConkey agar median using an inoculation loop without enrichment to check for the presence of SP. There was no antibiotics in the MacConkey plates. Trait Definitions. The resistance of different chicken lines was evaluated by the population survival rate. Chicks that died within 36 d after inoculation were classified as “0”, while those that were still alive after 36 d were classified as “1”. For the resistance to carrier- state, chicks whose spleens carried SP were classified as “1”, while those without SP on their spleens were classified as “0”. Statistical Analysis. The variance and covariance components were estimated using the DMU software package (Madsen and Jensen, 2008). Two analyses were used to calculate genetic parameters: a classic animal model and a threshold animal model. The heritability of mortality and the carrier state were analyzed using the animal threshold model. Both models included the cage as a fixed effect and additive genetic effects as random effects. In the threshold model, observed binary records (Yij) are assumed to be determined by an underlying liability (λij) as shown below:   \begin{equation*}{{\rm{Y}}_{\rm{ij}}}\,{\rm{ = }}\left\{\!\! {\ \begin{array}{@{}*{1}{c}@{}} {{\rm{0\ for}}\ {{\rm{\lambda }}_{{\rm{ij}}}}{\rm{\ }} \le {\rm{\ 0}}}\\ {{\rm{1\ for}}\ {{\rm{\lambda }}_{{\rm{ij}}}}{\rm{\ > \ 0}}} \end{array}} \right.,\end{equation*}$\ $The animal threshold in matrix notation is   \begin{equation*}y{\rm{ }} = {\rm{ }}X\beta {\rm{ }} + Za{\rm{ }} + e\end{equation*} where y is a vector of a phenotypic values; β and a are the fixed and random additive effect vectors, respectively; X and Z are appropriate incidence matrices of the fixed and random additive effects, respectively; and e represents the random residuals. The animal threshold was analyzed using the Gibbs sampling module included in the DMU software package (Ødegård et al., 2010), and the classical animal model was analyzed with the DMUAI module in DMU using the average information restricted maximum likelihood (AI-REML) algorithm. RESULTS Challenge Test. After the serological tests of the parent generation, we obtained 128 Salmonella-free chickens from 140 DWs, 103 from 160 RIRs, and 132 from 172 BYs. In addition, healthy parents that laid only a few eggs were also discarded from our study. The 60 sampled chicks (n = 20/line) all proved to be free from SP. During the course of the challenge, only one DW chick from the control group (with a thin and weak body) died; however, we did not find Salmonella in its liver or spleen. Every dead chick in the challenge group was necropsied and the spleen was cultured, as the survivors were, and they all proved to be infected. Most chicks that died from challenging showed typical SP infection symptoms such as hepatosplenomegaly, white diarrhea, cecal cores, etc. In addition, 5 samples were randomly selected for PCR identification, and all 5 proved to be SP. The 3 chicken lines had different survival curves as shown in Figure 1. Overall, 382 out of 621 DWs, 334 out of 586 RIRs, and 439 out of 482 BYs survived the SP challenge. The DW chicks were most sensitive to SP in the first days after the challenge, but they became insensitive around 10 d of age. However, RIR chickens exhibited a more constant death rate through 25 d. As for the BY, only a few birds died in the early days post infection. After 10 d of age, no more deaths appeared in BY. Overall, our results indicated that the order of resistance to SP was BY > DW > RIR. Figure 1. View largeDownload slide Survival curves for 3 chicken lines after infection with SP. •, Rhode Island Red (RIR); ○, Dwarf (DW); ▵, Beijing You (BY). Figure 1. View largeDownload slide Survival curves for 3 chicken lines after infection with SP. •, Rhode Island Red (RIR); ○, Dwarf (DW); ▵, Beijing You (BY). Mortality and Carrier-state Statistics. Death rate and carrier state data are presented in Figure 2. Mortality in RIR, BY, and DW were 25.1%, 8.3%, and 22.7% respectively. Carriage rates were 17.9%, 0.6%, and 15.8% for RIR, BY, and DW, respectively. These results showed that carrier state and mortality seem to be positively related; BY chicken were almost completely free of bacteria. Figure 2. View largeDownload slide The number and proportion of dead, carrier, and clear (not carrying SP) chickens from 3 lines, respectively. All traits were determined within 40 d of age, namely, within 36 d post-inoculation. 1DW, dwarf chicken; RIR, Rhode Island Red; and BY, Beijing You. Figure 2. View largeDownload slide The number and proportion of dead, carrier, and clear (not carrying SP) chickens from 3 lines, respectively. All traits were determined within 40 d of age, namely, within 36 d post-inoculation. 1DW, dwarf chicken; RIR, Rhode Island Red; and BY, Beijing You. Heritabilities. Estimated genetic parameters for survival and the carrier state are presented in Table 1. Survival heritabilities were 0.197, 0.091, and 0.167 for the RIR, BY, and DW populations, respectively, heritabilities for the carrier state in DW and RIR were 0.32 and 0.16. The heritability of the carrier state in BY could not be estimated because of too few carrier chickens. These disease-resistance traits presented low to moderate heritabilities in line with previous research (Beaumont et al., 1999; Girard-Santosuosso et al., 2002). The heritability of survival in BY was lower than it was for the other lines. This may be the result of the very low death rate in this line, which may cause a biased estimation of heritability. Table 1. Heritabilities of survival and the carrier state. Traits  Line1  Heritability  SE2  Survival  DW  0.167  0.091    RIR  0.197  0.100    BY  0.091  0.062  Carrier-state  DW  0.320  0.106    RIR  0.161  0.097    BY  –  –  Traits  Line1  Heritability  SE2  Survival  DW  0.167  0.091    RIR  0.197  0.100    BY  0.091  0.062  Carrier-state  DW  0.320  0.106    RIR  0.161  0.097    BY  –  –  1DW, dwarf chicken; RIR, Rhode Island Red; and BY, Beijing You 2SE, standard error View Large DISCUSSION Various responses by chickens with different genotypes to certain pathogens have been reported (Briles et al., 1977; Swaggerty et al., 2009; Beaumont et al., 2010; Calenge and Beaumont, 2012). For example, the ADOL chicken lines N and P have exhibited differing resistance to Marek's disease (Bacon et al., 2000). The important role the MHC and B complexes play for these 2 chicken lines is also well documented (Briles et al., 1977; Powell et al., 1982). In the current study, we found dramatically different resistances to SP among the 3 populations of chicks. We found that the BY chickens exhibited much higher resistance to SP, either in terms of lower mortality or via an increased number of carriers. These observations provide an explicit explanation for the large differences in disease resistance among chicken populations. The survival curves for the 3 populations indicated that the 3 chicken lines responded differently to SP infection. Some DW chicks died in the first few days after infection and others who survived mostly grew normally. However, many RIR chicks, which struggled for longer, could not avoid death in the end. From our observations, the RIR chicks that died were the ones that exhibited low body weight and poor growth (data not shown). We speculated that these characteristics could result from a different immune response occurring in the different chick lines because disease resistance may correlate with growth traits (Dorshorst et al., 2011; Lee et al., 2014; Nikbakht and Esmailnejad, 2015). There is a general view that native poultry, which have not been subject to intensive selection, are usually more resistant to diseases (Alvarez et al., 2003; Schou et al., 2010; Han et al., 2013). Considering the origin of the 3 lines, RIR has experienced the most intense selection for performance in production (Hays, 1955). Comparatively, DW chickens are a newly developed commercial line. As a local breed, BY chickens have not been intensively selected and thus might have higher genetic diversity. This view is in agreement with the fact that indigenous chicken lines that have not undergone extensive artificial selection are more resistant to infectious diseases (Jie and Liu, 2011). Breeders might choose to breed indigenous chickens like BY to produce more resistant chicken lines as this could reduce the risk of an outbreak of Salmonella. Furthermore, it could benefit conservation of the breed and improve genetic diversity in commercial chicken flocks. Here we report the first estimated heritability of SP resistance among chicken populations, which varies among chicken lines. The heritability of mortality estimated here is close to that reported for Salmonella Enteritidis (Beaumont et al., 1999), and heritability of the carrier state, based on investigation of the spleen, was higher than what has been reported for the heritability of the carrier state based on investigation of the ceca (Berthelot et al., 1998). The heritability of disease resistance usually ranges from low to moderate. However, values of 0.16 to 0.32 are sufficiently high, and it is worth investigating QTLs or candidate genes (Girard-Santosuosso et al., 2002). The carrier state is an important trait in SP resistance. The high heritability reported for the first time here indicated that it is possible to breed chickens without carrying SP in the spleen, which is very important for SP purification in breeding population. On chicken farms, we typically use serological tests to identify and then eliminate infected chickens. However, we could infer here that the traditional serological test may not be suitable for indigenous chickens because many BY chickens with SP antibodies were found to be free from SP. Based on the fairly low percentage of SP carriers in the BY chicks that survived the challenge, serological tests for SP, which have been used principally as a screening tool for SP infection, could not accurately confirm the infection. In several studies, SP from tissues of seropositive hens could not be isolated (Waltman and Horne, 1993; Gast, 1997). According to our results, serological tests were still meaningful for RIR and DW. However, the carrier state should be better investigated in local chicken breeds, and alternative strategies should be developed for Salmonella tests in indigenous chickens. In conclusion, our results showed that BY chickens are more resistant to SP than RIR or DW chickens are and that genetic variance plays an important role in SP resistance in different chicken lines, either in terms of mortality or as a carrier state. Selecting more resistant lines could help to reduce the risk of poultry infections and subsequent economic losses. ACKNOWLEDGMENTS This work was supported by the earmarked fund for the Beijing Innovation Team of the Modern Agro-industry Technology Research System (BAIC04–2016), National Scientific Supporting Projects of China (2015BAD03B03), and Chinese Agricultural Research System (CARS-41). 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Poultry ScienceOxford University Press

Published: Mar 1, 2018

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