Cloacal bacterial communities of tree swallows (Tachycineta bicolor): Similarity within a population, but not between pair-bonded social partners

Abstract

Host-associated microbial communities can influence the overall health of their animal hosts, and many factors, including behavior and physiology, can impact the formation of these complex communities. Bacteria within these communities can be transmitted socially between individuals via indirect (e.g., shared environments) or direct (e.g., physical contact) pathways. Limited research has been done to investigate how social interactions that occur in the context of mating shape host-associated microbial communities. To gain a better understanding of these interactions and, more specifically, to assess how mating behavior shapes an animal's microbiome, we studied the cloacal bacterial communities of a socially monogamous yet genetically polygynous songbird, the North American tree swallow (Tachycineta bicolor). We address two questions: (1) do the cloacal bacterial communities differ between female and male tree swallows within a population? and (2) do pair-bonded social partners exhibit more similar cloacal bacterial communities than expected by chance? To answer these questions, we sampled the cloacal microbiome of adults during the breeding season and then used culture-independent, 16S rRNA gene amplicon sequencing to assess bacterial communities. Overall, we found that the cloacal bacterial communities of females and males were similar, and that the communities of pair-bonded social partners were not more similar than expected by chance. Our results suggest that social monogamy does not correlate with an increased similarity in cloacal bacterial community diversity or structure. As social partners were not assessed at the same time, it is possible that breeding stage differences masked social effects on bacterial community diversity and structure. Further, given that tree swallows exhibit high variation in rates of extra-pair activity, considering extra-pair activity when assessing cloacal microbial communities may be important for understanding how these bacterial communities are shaped. Further insight into how PLOS ONE | https://doi.Cloacal bacterial communities of tree swallows (Tachycineta bicolor): Similarity within a population, but not between pair-bonded social partners. PLoS ONE 15(2): e0228982. https://doi.

Assessing age, breeding stage, and mating activity as drivers of variation in the reproductive microbiome of female tree swallows

“…Moreover, in barn swallows ( Hirundo rustica ), a socially monogamous species that exhibits extra‐pair mating activity, social partners exhibited more similar cloacal bacterial communities than expected by chance, though one study acknowledged a low effect size with regard to this pattern (Ambrosini et al., 2019 ; Kreisinger et al., 2015 ). In contrast, the cloacal bacterial communities of tree swallow ( Tachycineta bicolor ) social partners were not more similar than expected by chance (Hernandez et al., 2020 ). However, these studies have not focused on variation in sexual activity and the number of sexual partners, two factors that are hypothesized to contribute to variation in cloacal microbiome diversity.…”

“…We processed bacterial DNA samples as in Hernandez et al. ( 2020 ) for bacterial DNA extraction, amplification, and sequencing. Briefly, we extracted DNA from cloacal swabs using the DNeasy Blood and Tissue Kit protocol.…”

“…In contrast, the cloacal bacterial communities of tree swallow (Tachycineta bicolor) social partners were not more similar than expected by chance (Hernandez et al, 2020). However, these studies have not focused on variation in sexual activity and the number of sexual partners, two factors that are hypothesized to contribute to variation in cloacal microbiome diversity.…”

“…In birds, most studies examining the impact of mating behavior on reproductive microbiomes have selectively targeted a limited set of bacteria in social partners (Hupton et al., 2003 ; Lombardo & Thorpe, 2000 ; Stewart & Rambo, 2000 ) or have focused on interspecific comparisons of species with divergent mating systems using culture‐dependent approaches (e.g., monogamous vs. polygamous: Poiani & Gwozdz, 2002 ; Poiani & Wilks, 2000a , 2000b ). Culture‐independent work exploring how the reproductive microbiome is shaped with respect to mating has focused on genetically monogamous systems and/or pair‐bonded social partners (Ambrosini et al., 2019 ; Hernandez et al., 2020 ; Kreisinger et al., 2015 ; White et al., 2010 ). For instance, pairs of genetically monogamous black‐legged kittiwakes ( Rissa tridactyla ) exhibit similar cloacal bacterial communities when allowed to copulate, and this similarity was reduced when pairs were experimentally blocked from mating (White et al., 2010 ).…”

Antibiotic perturbation of gut bacteria does not significantly alter host responses to ocular disease in a songbird species

“…For cloacal swab bacterial community assessment, we amplified the V4 region of bacterial 16S rRNA gene with the 515F/806R primers ( Caporaso et al, 2012 ) as previously described ( Thomason et al, 2017 ; Hernandez et al, 2020 ; Weitzman et al, 2021 ), and amplicons were sequenced using a 250 bp single-end strategy on an Illumina MiSeq at the Dana Farber Cancer Center of Harvard University. Forward reads were demultiplexed in QIIME2 ( Bolyen et al, 2019 ) and processed with the DADA2 package with R version 4.0.2 in RStudio version 1.3.1093 ( R Development Core Team, 2015 ; Callahan et al, 2016 ; RStudioTeam, 2020 )).…”