Co-evolution of the humoral immune and serotonergic systems in chickens selected for high or low blood antibody titer response to sheep red blood cells

Serotonin is a potent immunomodulatory neurohormone. Activities of the serotonergic and immune systems are often reported together in poultry studies with unidirectional analyses focused on serotonergic signaling mediating immune response. Considering serotonin's relevance across a range of immune-related poultry topics, elucidation of whether the immune system affects the serotonergic system can provide valuable insights into the bi-directionality of poultry neuroendocrine-immune interactions. The present study sought to determine whether selection for divergence in blood antibody titers to a non-pathogenic antigen coincides with parallel changes in the chicken's serotonergic system over the life of the bird. We utilized generations 49 and 50 male and female White Leghorn chickens (n = 10-12/chickens/line/sex/age) that have been selected long-term for high (HAS) or low (LAS) blood antibody response to intravenous sheep red blood cell injection. Because serotonin is predominantly produced in the gut and acts as an interkingdom signaling molecule, the first experiment sampled cecal tissue and luminal content samples from male and female HAS and LAS chickens at 293 days of age. In the second experiment, cecal tissue and luminal content, as well as plasma, were collected from HAS and LAS chickens at 28 and 56 days of age. Serotonin and its main metabolite, 5-hydroxyindoleacetic acid (5-HIAA), concentrations were determined in cecal tissue, luminal content, and plasma samples. Immunoglobulins IgA and IgY concentrations were analyzed in cecal luminal content or plasma, respectively. The HAS chickens had lower (p < 0.05) cecal IgA concentrations but higher (p < 0.05) plasma IgY concentrations than LAS chickens, suggesting a compensatory response within the intestinal tract following selection for high or low blood antibody titers. Serotonin and 5-HIAA concentrations in the ceca and plasma diverged (p < 0.05) in a pattern that mirrored ceca IgA and plasma IgY differences according to genetic line. The results from this study demonstrate that evolutionary selection pressure for humoral immune response in chickens causes responses in the serotonergic system at both enteric and systemic levels.