Uropygial gland microbiota of nearctic-neotropical migrants vary with season and migration distance

Abstract

Symbiotic microbiota are important drivers of host behaviour, health, and fitness. While most studies focus on humans, model organisms, and domestic or economically important species, research investigating the role of host microbiota in wild populations is rapidly accumulating. Most studies focus on the gut microbiota; however, skin and other glandular microbiota also play an important role in shaping traits that may impact host fitness. The uropygial gland is an important source of chemical cues and harbours diverse microbes that could mediate chemical communication in birds, so determining the factors most important in shaping host microbiota should improve our understanding of microbially-mediated chemical communication. Hypothesizing that temporal, geographic, and taxonomic effects influence host microbiota, we evaluated the effects of season, migration distance, and taxonomy on the uropygial gland microbiota of 18 passerine species from 11 families. By sampling 473 birds at a single stopover location during spring and fall migration and using 16S rRNA sequencing, we demonstrate that season, followed by migration distance, had the strongest influence on uropygial gland microbial community composition. While statistically significant, taxonomic family and species had only weak effects on gland microbiota. Given that temporal effects on gland microbiota were nearly ubiquitous among the species we tested, determining the consequences of and mechanisms driving this seasonal variation are important next steps.

Keywords: Microbiome; Migration; Passerine; Preen gland; Seasonal variation; Uropygial gland.

Fig. 1

Barplot showing bacterial taxa identified from uropygial glands of 16 neotropical passerine species. The relative abundances of ASVs that shared the same level of identification (e.g., multiple ASVs identified as belonging to bacterial species within the same genus) were pooled. Data were filtered to include only taxa with a relative abundance of at least 5% in at least one species within season; taxa with less than 5% abundance in any one species within season are pooled as ‘Other’. Taxa denoted F- are those identified to family level, all other taxa were identified to genus. Fig S1 shows all taxa in 1% or greater abundance in at least one species within season

Fig. 2

PC1 and PC2 scores derived from relative abundances of passerine uropgyial gland bacterial amplicon sequence variants (ASVs) indicating variation between spring (green) and fall (gold) migration and with migration distance (circle: inter = intercontinental migrant, triangle: intra = intracontinental migrant). A version of this figure with loadings based on ASV relative abundances most strongly associated with PC1 and PC2 is available in the supplementary material (Fig. S2)

Fig. 3

PC2 and PC3 scores derived from relative abundances of passerine uropygial gland bacterial amplicon sequence variants (ASVs) indicating variation between spring (green) and fall (gold) migration and with migration distance (circle: inter = intercontinental migrant, triangle: intra = intracontinental migrant). A version of this figure with loadings based on ASV relative abundances most strongly associated with PC2 and PC3 is available in the supplementary material (Fig. S3)

Fig. 4

Bacterial taxa composing the microbial signature that best differentiates among uropygial gland swabs collected during spring and fall migration based on coda4microbiome analysis. The magnitude of the coefficients represents the contribution of each variable to the model (gold = positive, green = negative). Where possible, ASVs were identified to genus, but two could only be identified to order or family (O-Enterobacteriales, F-Rhodocyclaceae)

Fig. 5

Box and whisker plots of PC1 and PC2 scores derived for each species from relative abundances of passerine uropygial gland bacterial amplicon sequence variants (ASVs) indicating variation between spring and fall migration. Midline indicates median values, whiskers indicate minimum and maximum values. Asterisks denote significant differences at α = 0.05. See Table S3 for ANOVA output. Species photos courtesy of Brock and Sherri Fenton and used with permission. A version of this figure presented as PC biplots is available in the supplementary material (Fig. S5)