Divergent host genetic architectures drive breed-specific modulation of the caecal microbiome in chickens

Background: Enteric microbiota are crucial for animal health and performance, but their role is often challenging to determine. Host genetics appear to influence gut microbial communities, even among individuals in similar environments. This study aimed to identify host genetic variation associated with the caecal microbiota in two chicken breeds: the indigenous Indian Kadaknath and commercial Cobb400 broilers. Blood and caecal contents were collected from 300 chickens per breed in Western India. Genotyping was performed using the 600K Affymetrix Axiom HD single nucleotide polymorphism (SNP) array, and caecal microbiota were characterized using 16S rRNA gene sequencing. A subset of 40 chicken underwent whole genome sequencing for deeper genetic insights. SNP-based heritability estimates and genome-wide association studies (GWAS) were conducted separately for both breeds to explore the genetic background of caecal microbial structure (alpha and beta diversity) and the host’s influence on the establishment of different bacterial genera in the caeca, with a focus on potential pathogens. Results: The GWAS in Kadaknath chickens identified 108 significant SNPs across 26 Gallus gallus chromosomes (GGC1–GGC23, GGC27, and GGC28), associated with heritable caecal microbial traits, including microbiota structure and the abundance of specific genera. SNP-based heritability estimates ranged from 0.12 to 0.76, with the nearest genes predominantly involved in immune response and cell signaling pathways. In Cobb400 chickens, 71 significant SNPs were identified across 22 chromosomes (GGC1–GGC5, GGC7–GGC11, GGC14, GGC17–GGC22, GGC25–GGC28, and GGCZ), linked to heritable caecal microbial traits with heritability estimates from 0.16 to 0.61. Genes nearest to these SNPs were primarily associated with microbial regulation, growth processes, and adaptation under stress conditions. These findings underscore the role of host genetic variation in shaping caecal microbiota composition and diversity in indigenous and commercial chicken breeds and reveal breed-specific genetic architectures underlying caecal microbiota-related traits. Conclusion: This study provides valuable insights into the genetic basis of host-microbiome interactions in chickens, highlighting distinct breed-specific genetic influences on caecal microbiota composition. These findings have the potential to inform future genomic selection strategies aimed at enhancing protective or productive gut microbial populations while reducing reliance on antibiotics in poultry production.