Preen gland microbiota covary with major histocompatibility complex genotype in a songbird

Abstract

Pathogen-mediated selection at the major histocompatibility complex (MHC) is thought to promote MHC-based mate choice in vertebrates. Mounting evidence implicates odour in conveying MHC genotype, but the underlying mechanisms remain uncertain. MHC effects on odour may be mediated by odour-producing symbiotic microbes whose community structure is shaped by MHC genotype. In birds, preen oil is a primary source of body odour and similarity at MHC predicts similarity in preen oil composition. Hypothesizing that this relationship is mediated by symbiotic microbes, we characterized MHC genotype, preen gland microbial communities and preen oil chemistry of song sparrows (Melospiza melodia). Consistent with the microbial mediation hypothesis, pairwise similarity at MHC predicted similarity in preen gland microbiota. Counter to this hypothesis, overall microbial similarity did not predict chemical similarity of preen oil. However, permutation testing identified a maximally predictive set of microbial taxa that best reflect MHC genotype, and another set of taxa that best predict preen oil chemical composition. The relative strengths of relationships between MHC and microbes, microbes and preen oil, and MHC and preen oil suggest that MHC may affect host odour both directly and indirectly. Thus, birds may assess MHC genotypes based on both host-associated and microbially mediated odours.