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 bacterial communities are shaped will ultimately shed light on potential tradeoffs associated with alternative behavioral strategies and socially-transmitted microbes.

Highlights

  • Host-associated microbial communities can contribute to the overall health of their animal hosts [1,2,3,4], and many factors, including behavior and physiology, can impact the composition of these complex communities [1, 5,6,7]

  • We asked two main questions: (1) do the cloacal bacterial communities differ between female and male tree swallows within a population? and (2) do pair-bonded social partners share more similar cloacal bacterial communities than expected by chance? For the first question, we hypothesized that the cloacal bacterial communities of females and males would differ due to physiological differences that exist between the sexes during the breeding season, such as differences in hormonal profiles [20] and immune activity [21]

  • We assessed (1) whether the cloacal bacterial communities differed between female and male tree swallows within a population, and (2) whether pair-bonded social partners shared more similar cloacal bacterial communities than expected by chance

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Summary

Introduction

Host-associated microbial communities can contribute to the overall health of their animal hosts [1,2,3,4], and many factors, including behavior and physiology, can impact the composition of these complex communities [1, 5,6,7]. Given that cloacal contact during copulation can result in the transmission of microbes between individuals [10] and that pair-bonded social partners maintain a relatively close relationship throughout the breeding season, it has been hypothesized that pair-bonded social partners share more similarity in their cloacal microbial communities compared to others in the same population [13, 16,17,18,19]. This hypothesis has been tested in several systems, and has generally been supported. Two observational studies on barn swallows (Hirundo rustica) in Europe found that cloacal bacterial communities of pair-bonded social partners were more similar to each other than to other individuals in the population or than expected by chance [16, 17]; the effect size was small in one of the studies [16]

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