Multigenerational selection for high or low antibody response to sheep red blood cells modulates the chicken cecal microbiome and its relationship to the immune and serotonergic systems.

The chicken cecal microbiome has an important role in regulating immune function, health, resilience to foodborne pathogen carriage, and myriad other factors important in poultry production. However, in chickens, the effects of long-term immune modulation through selective breeding on gut microbiome composition and function remain understudied. The present study aimed to investigate how the multigenerational selection of chickens for high (HAS) or low (LAS) antibody response to sheep red blood cells (SRBC) influences cecal microbiome diversity, community composition, and functional capacity across different ages. Data from both lines and sexes were obtained in generation 49 at 293 days of age and in generation 50 at 28 and 56 days of age. The LAS chickens exhibited greater microbial diversity and abundance, particularly at 56 days (p < 0.05), than HAS. Microbial community composition also varied between the two lines, with age and line influencing microbiome structure across developmental stages and sexes (p < 0.05). Functional profiling revealed that metabolic activity of the LAS microbiome was different compared to the HAS microbiome, with pathways enriched in L-tryptophan biosynthesis, as well as carbon metabolism and degradation processes, suggesting that selection on the humoral immune system fostered alterations in microbial functional capacity. Correlation and co-occurrence analyses with serotonin, 5-hydroxyindoleacetic acid, IgA, and IgY revealed associations between microbial taxa and the neuroendocrine-immune axis, particularly in LAS (p < 0.05), including bacterial taxa known to be involved in serotonergic signaling, such as Clostridia, and immunoglobulin concentrations, including Oscillospiraceae. Overall, these results show that long-term selection for differential antibody responses has lasting impacts on cecal microbiome diversity, community structure, and functional potential. This study provides insights into the evolutionary relationship between the cecal microbiome and its relation to the chicken neuroendocrine-immune axis. Together, the findings of this study suggest specific bacterial taxa adapted to the chicken may be leveraged to affect host humoral immune and serotonergic systems to potentially bolster gut health and increase foodborne pathogen resistance.