Gut bacterial composition shows sex-specific shifts during breeding season in ex situ managed black-footed ferrets

Alexandra L DeCandia; Laura Adeduro; Piper Thacher; Adrienne Crosier; Paul Marinari; Robyn Bortner; Della Garelle; Travis Livieri; Rachel Santymire; Pierre Comizzoli; Michael Maslanka; Jesús E Maldonado; Klaus-Peter Koepfli; Carly Muletz-Wolz; Sally L Bornbusch

doi:10.1093/jhered/esad065

Gut bacterial composition shows sex-specific shifts during breeding season in ex situ managed black-footed ferrets

J Hered. 2023 Oct 27:esad065. doi: 10.1093/jhered/esad065. Online ahead of print.

Authors

Alexandra L DeCandia^{1

2}, Laura Adeduro¹, Piper Thacher^{2

3}, Adrienne Crosier⁴, Paul Marinari⁴, Robyn Bortner⁵, Della Garelle⁵, Travis Livieri⁶, Rachel Santymire⁷, Pierre Comizzoli⁸, Michael Maslanka⁹, Jesús E Maldonado², Klaus-Peter Koepfli^{3

8}, Carly Muletz-Wolz², Sally L Bornbusch^{2

9}

Affiliations

¹ Biology Department, Georgetown University, Washington, DC, USA.
² Center for Conservation Genomics, Smithsonian's National Zoo & Conservation Biology Institute, Washington, DC, USA.
³ Smithsonian-Mason School of Conservation, George Mason University, Front Royal, VA, USA.
⁴ Center for Animal Care Sciences, Smithsonian's National Zoo & Conservation Biology Institute, Front Royal, VA, USA.
⁵ National Black-Footed Ferret Conservation Center, Carr, CO, USA.
⁶ Prairie Wildlife Research, Stevens Point, WI, USA.
⁷ Biology Department, Georgia State University, Atlanta, GA, USA.
⁸ Center for Species Survival, Smithsonian's National Zoo & Conservation Biology Institute, Front Royal, VA, USA.
⁹ Department of Nutrition Science, Smithsonian's National Zoo & Conservation Biology Institute, Washington, DC, USA.

PMID: 37886904
DOI: 10.1093/jhered/esad065

Abstract

The gut microbiome of mammals engages in a dynamic relationship with the body and contributes to numerous physiological processes integral to overall health. Understanding the factors shaping animal-associated bacterial communities is therefore paramount to the maintenance and management in ex situ wildlife populations. Here, we characterized the gut microbiome of 48 endangered black-footed ferrets (Mustela nigripes) housed at Smithsonian's National Zoo and Conservation Biology Institute (Front Royal, Virginia, USA). We collected longitudinal fecal samples from males and females across two distinct reproductive seasons to consider the role of host sex and reproductive physiology in shaping bacterial communities, as measured using 16S rRNA amplicon sequencing. Within each sex, gut microbial composition differed between breeding and non-breeding seasons, with five bacterial taxa emerging as differentially abundant. Between sexes, female and male microbiomes were similar during non-breeding season but significantly different during breeding season, which may result from sex-specific physiological changes associated with breeding. Finally, we found low overall diversity consistent with other mammalian carnivores alongside high relative abundances of potentially pathogenic microbes such as Clostridium, Escherichia, Paeniclostridium, and (to a lesser degree) Enterococcus - all of which have been associated with gastrointestinal or reproductive distress in mammalian hosts, including black-footed ferrets. We recommend further study of these microbes and possible therapeutic interventions to promote more balanced microbial communities. These results have important implications for ex situ management practices that can improve the gut microbial health and long-term viability of black-footed ferrets.

Keywords: Clostridium; ex situ conservation; dysbiosis; mammalian gut microbiome; reproduction; sex differences.