Morphological and genetic factors shape the microbiome of a seabird species (Oceanodroma leucorhoa) more than environmental and social factors

Abstract

Background: The microbiome provides multiple benefits to animal hosts that can profoundly impact health and behavior. Microbiomes are well-characterized in humans and other animals in controlled settings, yet assessments of wild bird microbial communities remain vastly understudied. This is particularly true for pelagic seabirds with unique life histories that differ from terrestrial bird species. This study was designed to examine how morphological, genetic, environmental, and social factors affect the microbiome of a burrow-nesting seabird species, Leach's storm petrel (Oceanodroma leucorhoa). These seabirds are highly olfactory and may rely on microbiome-mediated odor cues during mate selection. Composition and structure of bacterial communities associated with the uropygial gland and brood patch were assessed using 16S rRNA amplicon-based Illumina Mi-Seq analysis and compared to burrow-associated bacterial communities. This is the first study to examine microbial diversity associated with multiple body sites on a seabird species.

Results: Results indicate that sex and skin site contribute most to bacterial community variation in Leach's storm petrels and that major histocompatibility complex (MHC) genotype may impact the composition of bacterial assemblages in males. In contrast to terrestrial birds and other animals, environmental and social interactions do not significantly influence storm petrel-associated bacterial assemblages. Thus, individual morphological and genetic influences outweighed environmental and social factors on microbiome composition.

Conclusions: Contrary to observations of terrestrial birds, microbiomes of Leach's storm petrels vary most by the sex of the bird and by the body site sampled, rather than environmental surroundings or social behavior.

Keywords: Brood patch; Leach’s storm petrel; Skin microbiome; Uropygial gland.

Fig. 1

Relative abundance of bird-associated bacterial communities by phylum (a) and most abundant families (b). Both body sites were characterized by highly abundant Proteobacteria, Bacteroidetes, Firmicutes, and Actinobacteria. Families represent the top 20 most abundant OTUs. Colors of the families in b correspond to the phyla represented in a. Proteobacteria are marked as (β) Betaproteobacteria, (α) Alphaproteobacteria, and (γ) Gammaproteobacteria. Remaining families not represented in this figure are listed in Additional file 9: Table S4

Fig. 2

PCoA of female uropygial gland, female brood patch, male uropygial gland, and male brood patch bacterial communities based on weighted UniFrac dissimilarity. Green circles represent DAB2 heterozygous individuals, blue squares represent DAB2 homozygous individuals, and gray triangles represent individuals lacking genotype data. Morphological and genetic factors are represented by arrows, and the length of each arrow is proportional to the explanatory power of each variable. Female wing chord length explained 50% of variation in brood patch bacterial community structure (R ² = 0.500, p = 0.024, n = 14). DAB2 homozygosity explained 72% of variation in male uropygial gland community structure (weighted UniFrac pseudo-F = 1.859, p = 0.015, n = 8), although sample size was small for this analysis. Wing chord was too small to represent for female uropygial gland analysis