The genetics of resilience and its relationships with egg production traits and antibody traits in chickens.

BACKGROUND: Resilience is the capacity of an animal to be minimally affected by disturbances or to rapidly return to its initial state before exposure to a disturbance. Resilient livestock are desired because of their improved health and increased economic profit. Genetic improvement of resilience may also lead to trade-offs with production traits. Recently, resilience indicators based on longitudinal data have been suggested, but they need further evaluation to determine whether they are indeed predictive of improved resilience, such as disease resilience. This study investigated different resilience indicators based on deviations between expected and observed egg production (EP) by exploring their genetic parameters, their possible trade-offs with production traits, and their relationships with antibody traits in chickens. METHODS: Egg production in a nucleus breeding herd environment based on 1-week-, 2-week-, or 3-week-intervals of two purebred chicken lines, a white egg-laying (33,825 chickens) and a brown egg-laying line (34,397 chickens), were used to determine deviations between observed EP and expected average batch EP, and between observed EP and expected individual EP. These deviations were used to calculate three types of resilience indicators for two life periods of each individual: natural logarithm-transformed variance (ln(variance)), skewness, and lag-one autocorrelation (autocorrelation) of deviations from 25 to 83 weeks of age and from 83 weeks of age to end of life. Then, we estimated their genetic correlations with EP traits and with two antibody traits. RESULTS: The most promising resilience indicators were those based on 1-week-intervals, as they had the highest heritability estimates (0.02-0.12) and high genetic correlations (above 0.60) with the same resilience indicators based on longer intervals. The three types of resilience indicators differed genetically from each other, which indicates that they possibly capture different aspects of resilience. Genetic correlations of the resilience indicator traits based on 1-week-intervals with EP traits were favorable or zero, which means that trade-off effects were marginal. The resilience indicator traits based on 1-week-intervals also showed no genetic correlations with the antibody traits, which suggests that they are not informative for improved immunity or vice versa in the nucleus environment. CONCLUSIONS: This paper gives direction towards the evaluation and implementation of resilience indicators, i.e. to further investigate resilience indicator traits based on 1-week-intervals, in breeding programs for selecting genetically more resilient layer chickens.

Research Note: Genome-wide association study for natural antibodies and resilience in a purebred layer chicken line.

Resilience is the capacity of an animal to be minimally affected by disturbances or rapidly return to the state pertained before exposure to a disturbance. Resilience indicators can be estimated from longitudinal production data, using deviations of observed from expected production levels. One component of resilience is disease resilience, which includes general disease resistance. Natural antibodies (NAbs) are an indicator trait for general disease resistance. The aim of this study was to perform a genome-wide association study (GWAS) for resilience indicators and NAbs in a Rhode Island purebred layer line and study potential overlap in genomic regions detected for these traits. For 2,494 hens, deviations (i.e., differences) between observed weekly egg production and expected weekly egg production were calculated. Resilience indicators were then defined as the natural logarithm of the variance of deviations, skewness of deviations, and lag-one autocorrelation of deviations. For a subset of 1,221 hens genotyped with the 60 K Illumina SNP BeadChip, NAbs binding keyhole-limpet hemocyanin were available (isotypes IgM and IgG). Heritabilities, estimated with a linear mixed animal model, were 0.39 for IgM and 0.20 for IgG, and ranged from 0.03 to 0.18 for the resilience indicators. No significant associations were found in the GWAS, except for a single chromosomal region for the skewness of egg deviations in wk 25 to 83 of the laying period. The absence of significant peaks for NAbs and resilience indicators suggests that there are no genes with major effect and that the traits are likely under polygenic control in this line.

Using egg production longitudinal recording to study the genetic background of resilience in purebred and crossbred laying hens.

BACKGROUND: There is growing interest in using genetic selection to obtain more resilient farm animals (i.e. that are minimally affected by disturbances or rapidly recover from them). The aims of this study were to: (i) estimate the genetic parameters of resilience indicator traits based on egg production data, (ii) assess whether these traits are genetically correlated in purebreds and crossbreds, and (iii) assess the genetic correlations of these traits with egg production (EP) as total number of eggs between 25 and 83 weeks. Purebred hens (33,825 from a White Leghorn (WA) line and 34,397 from a Rhode Island (BD) line were housed in individual cages, while crossbred hens were housed in collective cages of 6 to 8 paternal half-sibs (12,852 WA and 3898 BD crossbred groups, where the name of the group refers to the line used as the sire). Deviations of a hen's weekly egg production from the average of the corresponding batch were calculated. Resilience indicator traits investigated were the natural logarithm of the variance (LNVAR), the skewness (SKEW), and the lag-one autocorrelation (AUTO-R) of these deviations. RESULTS: In both purebred lines, EP was estimated to be lowly heritable (WA: 0.11 and BD: 0.12). Resilience indicators were also estimated to be lowly heritable in both lines (LNVAR: 0.10 and 0.12, SKEW: 0.04 and 0.02, AUTO-R: 0.06 and 0.08 in WA and BD, respectively). In both crossbred groups, EP, AUTO-R, and SKEW were estimated to be less heritable than in purebreds (EP: [Formula: see text] ≤ 0.07; and resilience indicator traits: [Formula: see text] ≤ 0.03), while LNVAR had an [Formula: see text] estimate that was similar to or higher in crossbreds ([Formula: see text] ranged from 0.13 to 0.21) than in purebreds. In both purebreds and crossbreds, resilience indicator traits were estimated to have favorable genetic correlations with EP and between each other. For all traits and in both lines, estimates of genetic correlations between purebreds and crossbreds ([Formula: see text]) differed from 1 and ranged from 0.16 to 0.63. CONCLUSIONS: These results show that selection for resilience based on EP data can be considered in breeding programs for layers. Genetic improvement of resilience in crossbreds can be achieved by using information on purebreds, but would be greatly enhanced by the integration of information on crossbreds in breeding programs.

Divergent selection for natural antibodies in poultry in the presence of a major gene.

BACKGROUND: Natural antibodies (NAb) are antibodies that are present in a healthy individual without requiring previous exposure to an exogenous antigen. Selection for high NAb levels might contribute to improved general disease resistance. Our aim was to analyse the genetic background of NAb based on a divergent selection experiment in poultry, and in particular the effect of a polymorphism in the TLR1A gene. METHODS: The study population consisted of a base population from a commercial pure-bred elite white leghorn layer line and seven generations of birds from a High and Low selection line. Birds were selected for total KLH-binding NAb titer (IgTotal). An enzyme-linked immunosorbent assay was performed to determine NAb titers in blood plasma for IgTotal and the antibody isotypes IgM and IgG. NAb titers were available for 10,878 birds. Genotypes for a polymorphism in TLR1A were determined for chickens in generations 5, 6 and 7. The data were analysed using mixed linear animal models. RESULTS: The heritability estimate for IgM was 0.30 and higher than that for IgG and IgTotal (0.12). Maternal environmental effects explained 2 to 3% of the phenotypic variation in NAb. Selection for IgTotal resulted in a genetic difference between the High and Low line of 2.4 titer points (5.1 genetic standard deviation) in generation 7. For IgM, the selection response was asymmetrical and higher in the Low than the High line. The frequency of the TLR1A C allele was 0.45 in the base population and 0.66 and 0.04 in generation 7 of the High and Low line, respectively. The TLR1A polymorphism had large and significant effects on IgTotal and IgM. Estimated genotypic effects suggest full dominance of the TLR1A C allele. Significant TLR1A by generation interactions were detected for IgM and IgTotal. CONCLUSIONS: The effect of a polymorphism in the TLR1A gene on IgTotal and IgM NAb was confirmed. Furthermore, we provide experimental verification of changes in allele frequencies at a major gene with dominant gene action on a quantitative trait that is subjected to mass selection. TLR1A by generation interactions indicate sensitivity to environmental factors.

Does paternal immunocompetence affect offspring vulnerability to maternal androgens? A study in domestic chickens.

Exposure of yolk androgens can positively stimulate chick growth and competitive ability, but may negatively affect immunity. It has been hypothesized that only chicks from immunologically superior fathers can bear the cost of prenatal exposure to high androgen levels. To test this hypothesis, we paired roosters from two selection lines, one up- and one down-selected for natural antibodies (NAbs), with hens from a control line. We measured yolk testosterone and androstenedione levels, and we injected the treatment group of eggs of each female with testosterone suspended in sesame oil and the control group with sesame oil only. We then measured hatching success and growth, and characterized the humoral and cellular immune responses using three different challenges: a phyto-hemagglutinin, a lipopolysaccharide and a sheep red blood cell challenge. We found that the hatching success, body mass, initial levels of natural antibodies and the chicks' immunological responses to the three different challenges and development were affected neither by paternal immunocompetence nor by treatment. These results do not support the hypothesis that chicks from low-NAb line fathers are more sensitive to testosterone exposure during embryonic development than chicks from high-NAb line fathers.

Body Weight Deviations as Indicator for Resilience in Layer Chickens.

Resilience is the capacity of an animal to be minimally affected by disturbances or to rapidly return to the state pertained before exposure to a disturbance. Less resilient animals are expected to be more susceptible to environmental perturbations, such as diseases, and will consequently show more and/or greater fluctuations in production than more resilient animals. Natural antibodies (NAb) are antibodies recognizing antigens without previous exposure to these, and are hypothesized to be an indication of general disease resistance. The objective of this research was to investigate genetic parameters of resilience indicators based on standardized body weight (BW) deviations and to investigate its relation with immunity (i.e. NAb) and disease resistance. Keyhole limpet hemocyanin-binding NAb were measured in layer chickens, which were selectively bred for high and low keyhole limpet hemocyanin-binding NAb levels during six generations. In addition, BW data of these layers were collected on a four-weekly interval from 4 weeks of age until 32 weeks of age. Standardized deviations of BW from an individual were compared to lines' average BW (i.e. across individuals), and these were used to calculate resilience indicators: natural logarithm-transformed variance [ln(variance)], skewness, and lag-one autocorrelation of deviations (i.e. all within an individual). Heritabilities of resilience indicators were between 0.09 and 0.11. Genetic correlations between the three resilience indicators were between -0.20 and 0.40 (with high SE), which might suggest that the resilience indicators capture different aspects of resilience. Genetic correlations between resilience indicators and NAb were close to zero, which suggests that the resilience indicators and NAb capture different aspects of immunity. This might indicate that, in this dataset, environmental perturbations are only to a small extent affected by disease incidence, possibly due to a lack of disease occurrence. However, a lower estimated breeding value for ln(variance) was predictive for lower lesion scores after an avian pathogenic Escherichia coli inoculation and vice versa. In conclusion, this study shows that there is genetic variation in resilience indicators based on BW deviations in layer chickens, which opens up possibilities to improve resilience by means of selective breeding.

Opportunities to Improve Resilience in Animal Breeding Programs.

Resilience is the capacity of an animal to be minimally affected by disturbances or to rapidly return to the state pertained before exposure to a disturbance. However, indicators for general resilience to environmental disturbances have not yet been defined, and perhaps therefore resilience is not yet included in breeding goals. The current developments on big data collection give opportunities to determine new resilience indicators based on longitudinal data, which can aid to incorporate resilience in animal breeding goals. The objectives of this paper were: (1) to define resilience indicator traits based on big data, (2) to define economic values for resilience, and (3) to show the potential to improve resilience of livestock through inclusion of resilience in breeding goals. Resilience might be measured based on deviations from expected production levels over a period of time. Suitable resilience indicators could be the variance of deviations, the autocorrelation of deviations, the skewness of deviations, and the slope of a reaction norm. These (new) resilience indicators provide opportunity to include resilience in breeding programs. Economic values of resilience indicators in the selection index can be calculated based on reduced costs due to labor and treatments. For example, when labor time is restricted, the economic value of resilience increases with an increasing number of animals per farm, and can become as large as the economic value of production. This shows the importance of including resilience in breeding goals. Two scenarios were described to show the additional benefit of including resilience in breeding programs. These examples showed that it is hard to improve resilience with only production traits in the selection index, but that it is possible to greatly improve resilience by including resilience indicators in the selection index. However, when health-related traits are already present in the selection index, the effect is smaller. Nevertheless, inclusion of resilience indicators in the selection index increases the response in the breeding goal and resilience, which results in less labor-demanding, and thus easier-to-manage livestock. Current developments on massive collection of data, and new phenotypes based on these data, offer exciting opportunities to breed for improved resilience of livestock.

Genomic Region Containing Toll-Like Receptor Genes Has a Major Impact on Total IgM Antibodies Including KLH-Binding IgM Natural Antibodies in Chickens.

Natural antibodies (NAb) are antigen binding antibodies present in individuals without a previous exposure to this antigen. Keyhole limpet hemocyanin (KLH)-binding NAb levels were previously associated with survival in chickens. This suggests that selective breeding for KLH-binding NAb may increase survival by means of improved general disease resistance. Genome-wide association studies (GWAS) were performed to identify genes underlying genetic variation in NAb levels. The studied population consisted of 1,628 adolescent layer chickens with observations for titers of KLH-binding NAb of the isotypes IgM, IgA, IgG, the total KLH-binding (IgT) NAb titers, total antibody concentrations of the isotypes IgM, IgA, IgG, and the total antibodies concentration in plasma. GWAS were performed using 57,636 single-nucleotide polymorphisms (SNP). One chromosomal region on chromosome 4 was associated with KLH-binding IgT NAb, and total IgM concentration, and especially with KLH-binding IgM NAb. The region of interest was fine mapped by imputing the region of the study population to whole genome sequence, and subsequently performing an association study using the imputed sequence variants. 16 candidate genes were identified, of which FAM114A1, Toll-like receptor 1 family member B (TLR1B), TLR1A, Krüppel-like factor 3 (KLF3) showed the strongest associations. SNP located in coding regions of the candidate genes were checked for predicted changes in protein functioning. One SNP (at 69,965,939 base pairs) received the maximum impact score from two independent prediction tools, which makes this SNP the most likely causal variant. This SNP is located in TLR1A, which suggests a fundamental role of TLR1A on regulation of IgM levels (i.e., KLH-binding IgM NAb, and total IgM concentration), or B cells biology, or both. This study contributes to increased understanding of (genetic) regulation of KLH-binding NAb levels, and total antibody concentrations.