Genetic and non-genetic factors influencing KLH binding natural antibodies and specific antibody response to Newcastle disease in Kenyan chicken populations

Abstract

This study aimed at investigating the influence of genetic and non-genetic factors on immune traits to inform on possibilities of genetic improvement of disease resistance traits in local chicken of Kenya. Immune traits such as natural and specific antibodies are considered suitable indicators of an individual's health status and consequently, used as indicator traits of disease resistance. In this study, natural antibodies binding to Keyhole Limpet Hemocyanin (KLH-NAbs) was used to measure general disease resistance. Specific antibodies binding to Newcastle disease virus (NDV-IgG) post vaccination was used to measure specific disease resistance. Titers of KLH-NAbs isotypes (KLH-IgM, KLH-IgG and KLH-IgA) and NDV-IgG were measured in 1,540 chickens of different ages ranging from 12 to 56weeks. A general linear model was fitted to determine the effect of sex, generation, population type, phylogenetic cluster, line, genotype and age on the antibody traits. A multivariate animal mixed model was fitted to estimate heritability and genetic correlations among the antibody traits. The model constituted of non-genetic factors found to have a significant influence on the antibody traits as fixed effects, and animal and residual effects as random variables. Overall mean (±SE) concentration levels for KLH-IgM, KLH-IgG, KLH-IgA and NDV-IgG were 10.33±0.04, 9.08±0.02, 6.00±0.02 and 10.12±0.03, respectively. Sex, generation and age (linear covariate) significantly (p<0.05) influenced variation across all the antibody traits. Genotype effects (p<0.05) were present in all antibody traits, apart from KLH-IgA. Interaction between generation and line was significant (p<0.05) in KLH-IgM and NDV-IgG while nesting phylogenetic cluster within population significantly (p<0.05) influenced all antibody traits, apart from KLH-IgA. Heritability estimates for KLH-IgM, KLH-IgG, KLH-IgA and NDVIgG were 0.28±0.08, 0.14±0.06, 0.07±0.04 and 0.31±0.06, respectively. There were positive genetic correlations (0.40–0.61) among the KLH-NAbs while negative genetic correlations (−0.26 to −0.98) were observed between the KLH-NAbs 14390388, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jbg.12738 by EBMG ACCESS - KENYA, Wiley Online Library on [31/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License | MIYUMO et al. 107 1 | INTRODUCTION Indigenous chicken (IC) (Gallus gallus domesticus) plays significant roles in nutrition, food security and economic growth in many rural households in most countries in the tropical regions (Alders & Pym, 2009). In Kenya, IC account for about 80% of the total chicken population and is kept by over 75% of the rural households (Magothe et al., 2012). Their popularity, particularly among rural households, is attributed to their ability to produce under low-input systems and adapt to local environmental conditions (Olwande et al., 2010). Despite their adaptive ability, IC is predominantly raised under scavenging systems that are constrained in terms of, among other challenges, diseases that limit optimal utilization and expansion of the sub-sector (Lamont, 2010). For instance, depending on the season, disease prevalence and mortality rates, reduction in productivity and product condemnation of about 20%–100% are experienced at the farm level and these cumulatively translate to 10%–15% of annual economic losses (Okeno et al., 2011; Rist et al., 2015). With respect to climate change effects, environmental conditions are expected to favour pathogens and parasite proliferation resulting in increased disease occurrence. Among the various poultry diseases, Newcastle disease (NCD) which is endemic among chicken in the tropics is currently considered of importance because of the massive production and economic losses it causes in the industry (Alders et al., 2018). While bio-security measures combined with vaccinations have proved useful in controlling NCD, the effects are, in some cases, temporary and/or highly influenced by the environment (Zanella, 2016). Control by use of anti-microbial drugs, on the other hand, is beneficial but often misused leading to product safety concerns (Lamont, 2010). Furthermore, the reliance on free-range scavenging system among smallholder farmers' increases transmission rates of NCD between and within flocks (Lwelamira, 2012). These factors emphasize the importance of considering alternative measures to maintain or enhance disease resistance in chicken flocks. ****Selective breeding for disease resistance, as a control measure, offers an opportunity to enhance adaptability of IC, especially, under scavenging systems where they are exposed to a myriad of disease pathogens (Cheng et al., 2013; Lwelamira et al., 2009). Besides, disease resistance is ranked a trait of economic importance among IC farmers in Kenya (Okeno et al., 2012), an indication that the trait should be considered in breeding goals. Disease resistance is generally defined as the ability to prevent infection when exposed to a pathogen or control a pathogen's life cycle (Zanella, 2016). The trait, however, is not often absolute because of the complex biological networks and host-pathogen interactions that control disease resistance, and the high sensitivity to environmental stressors (Cheng et al., 2013). On the other hand, disease resistance measurement requires that animals are challenged with pathogens and this severely violates animal welfare, presents biosecurity risks and is economically costly (Zanella, 2016). To circumvent these limitations, health traits related to the immune function are suitable indicator traits for indirect improvement of disease resistance (Cheng et al., 2013). Success of their utilization is, however, dependent on whether the traits are related to disease resistance, easy and cheap to measure and of utmost importance, heritable. Natural antibodies (NAbs) binding keyhole limpet hemocyanin (KLH-NAbs) and specific antibodies (SpAbs) binding NCD virus (NDV-IgG) have been used extensively to measure general disease resistance and specific resistance against NCD, respectively (Lwelamira, 2012; Sun et al., 2013). Considering the intrinsic nature of innate humoral immunity, KLH-NAb titres is expected to vary among individuals (Mangino et al., 2017). Previous studies on chicken found that part of this variation was due to additive genetic effects and further estimated moderate to low (0.44–0.07) heritability for KLH-NAb isotypes (Berghof and NDV-IgG. Results from this study indicate that non-genetic effects due to biological and environmental factors influence natural and specific antibodies and should be accounted for to reduce bias and improve accuracy when evaluating the traits. Subsequently, the moderate heritability estimates in KLH-IgM and NDV-IgG suggest selection possibilities for genetic improvement of general and specific immunity, respectively, and consequently disease resistance. However, the negative correlations between KLH-NAbs and NDV-IgG indicate the need to consider a suitable approach that can optimally combine both traits in a multiple trait selection strategies.