Abstract

The gastrointestinal tracts of animals contain diverse communities of microbes that provide a number of services to their hosts. There is recent concern that these communities may be lost as animals enter captive breeding programmes, due to changes in diet and/or exposure to environmental sources. However, empirical evidence documenting the effects of captivity and captive birth on gut communities is lacking. We conducted three studies to advance our knowledge in this area. First, we compared changes in microbial diversity of the gut communities of two species of woodrats (Neotoma albigula, a dietary generalist, and Neotoma stephensi, which specializes on juniper) before and after 6-9 months in captivity. Second, we investigated whether reintroduction of the natural diet of N. stephensi could restore microbial diversity. Third, we compared the microbial communities between offspring born in captivity and their mothers. We found that the dietary specialist, N. stephensi, lost a greater proportion of its native gut microbiota and overall diversity in response to captivity compared with N. albigula. Addition of the natural diet increased the proportion of the original microbiota but did not restore overall diversity in N. stephensi. Offspring of N. albigula more closely resembled their mothers compared with offspring-mother pairs of N. stephensi. This research suggests that the microbiota of dietary specialists may be more susceptible to captivity. Furthermore, this work highlights the need for further studies investigating the mechanisms underlying how loss of microbial diversity may vary between hosts and what an acceptable level of diversity loss may be to a host. This knowledge will aid conservation biologists in designing captive breeding programmes effective at maintaining microbial diversity. Sequence Accession Numbers: NCBI's Sequence Read Archive (SRA) - SRP033616.

Highlights

  • The gut microbial communities of animals are hyperdiverse and influence many aspects of their physiology, such as nutrition, immune development and even behaviour (Amato, 2013)

  • We found that the dietary specialist, N. stephensi, lost a greater proportion of its native gut microbiota and overall diversity in response to captivity compared with N. albigula

  • The birthing process represents the greatest microbial acquisition event in the lives of many species (Palmer et al, 2007; Dominguez-Bello et al, 2010; Funkhouser and Bordenstein, 2013). It is currently unknown whether the uniform conditions of captivity tend to homogenize microbial gut communities among individuals or species. We addressed this gap in knowledge using woodrats (Neotoma spp.), which are small, herbivorous rodents that serve as a model system to study interactions between dietary plant toxins and the gut microbiota (Dearing et al, 2000)

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Summary

Introduction

The gut microbial communities of animals are hyperdiverse and influence many aspects of their physiology, such as nutrition, immune development and even behaviour (Amato, 2013). The birthing process represents the greatest microbial acquisition event in the lives of many species (Palmer et al, 2007; Dominguez-Bello et al, 2010; Funkhouser and Bordenstein, 2013) It is currently unknown whether the uniform conditions of captivity tend to homogenize microbial gut communities among individuals or species. Given that a large proportion of microbes are acquired from mothers through the birth process and milk feeding in mammals (Palmer et al, 2007; Dominguez-Bello et al, 2010; Funkhouser and Bordenstein, 2013), we predicted that offspring would resemble their own mothers and species, suggesting that captive breeding programmes may retain wild microbiomes. We predicted that captive-born animals would perform as well as wild-caught individuals due to effective microbial transmission

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