Humanization of wildlife gut microbiota in urban environments

  1. Brian A Dillard  Is a corresponding author
  2. Albert K Chung
  3. Alex R Gunderson
  4. Shane C Campbell-Staton
  5. Andrew H Moeller  Is a corresponding author
  1. Cornell University, United States
  2. Princeton University, United States
  3. Tulane University, United States

Abstract

Urbanization is rapidly altering Earth’s environments, demanding investigation of the impacts on resident wildlife. Here, we show that urban populations of coyotes (Canis latrans), crested anole lizards (Anolis cristatellus), and white-crowned sparrows (Zonotrichia leucophrys) acquire gut microbiota constituents found in humans, including gut bacterial lineages associated with urbanization in humans. Comparisons of urban and rural wildlife and human populations revealed significant convergence of gut microbiota among urban populations relative to rural populations. All bacterial lineages overrepresented in urban wildlife relative to rural wildlife and differentially abundant between urban and rural humans were also overrepresented in urban humans relative to rural humans. Remarkably, the bacterial lineage most overrepresented in urban anoles was a Bacteroides sequence variant that was also the most significantly overrepresented in urban human populations. These results indicate parallel effects of urbanization on human and wildlife gut microbiota and suggest spillover of bacteria from humans into wildlife in cities.

Data availability

Sequencing data have been deposited in Data Dryad at https://dx.doi.org/10.5061/dryad.dfn2z353d

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Brian A Dillard

    Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, United States
    For correspondence
    bd429@cornell.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1845-2980
  2. Albert K Chung

    Princeton University, Princeton, NJ, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Alex R Gunderson

    Tulane University, Tulane, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Shane C Campbell-Staton

    Princeton University, Princeton, NJ, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Andrew H Moeller

    Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, United States
    For correspondence
    ahm226@cornell.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8377-4647

Funding

National Institute of General Medical Sciences (R35 GM138284)

  • Andrew H Moeller

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Peter J Turnbaugh, University of California, San Francisco, United States

Version history

  1. Received: December 14, 2021
  2. Preprint posted: January 6, 2022 (view preprint)
  3. Accepted: May 16, 2022
  4. Accepted Manuscript published: May 31, 2022 (version 1)
  5. Version of Record published: June 16, 2022 (version 2)

Copyright

© 2022, Dillard et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,936
    Page views
  • 740
    Downloads
  • 14
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Brian A Dillard
  2. Albert K Chung
  3. Alex R Gunderson
  4. Shane C Campbell-Staton
  5. Andrew H Moeller
(2022)
Humanization of wildlife gut microbiota in urban environments
eLife 11:e76381.
https://doi.org/10.7554/eLife.76381

Share this article

https://doi.org/10.7554/eLife.76381

Further reading

    1. Ecology
    2. Plant Biology
    Jamie Mitchel Waterman, Tristan Michael Cofer ... Matthias Erb
    Research Article

    Volatiles emitted by herbivore-attacked plants (senders) can enhance defenses in neighboring plants (receivers), however, the temporal dynamics of this phenomenon remain poorly studied. Using a custom-built, high-throughput proton transfer reaction time-of-flight mass spectrometry (PTR-ToF-MS) system, we explored temporal patterns of volatile transfer and responses between herbivore-attacked and undamaged maize plants. We found that continuous exposure to natural blends of herbivore-induced volatiles results in clocked temporal response patterns in neighboring plants, characterized by an induced terpene burst at the onset of the second day of exposure. This delayed burst is not explained by terpene accumulation during the night, but coincides with delayed jasmonate accumulation in receiver plants. The delayed burst occurs independent of day:night light transitions and cannot be fully explained by sender volatile dynamics. Instead, it is the result of a stress memory from volatile exposure during the first day and secondary exposure to bioactive volatiles on the second day. Our study reveals that prolonged exposure to natural blends of stress-induced volatiles results in a response that integrates priming and direct induction into a distinct and predictable temporal response pattern. This provides an answer to the long-standing question of whether stress volatiles predominantly induce or prime plant defenses in neighboring plants, by revealing that they can do both in sequence.

    1. Ecology
    Congnan Sun, Yoel Hassin ... Yossi Yovel
    Research Article

    Covid-19 lockdowns provided ecologists with a rare opportunity to examine how animals behave when humans are absent. Indeed many studies reported various effects of lockdowns on animal activity, especially in urban areas and other human-dominated habitats. We explored how Covid-19 lockdowns in Israel have influenced bird activity in an urban environment by using continuous acoustic recordings to monitor three common bird species that differ in their level of adaptation to the urban ecosystem: (1) the hooded crow, an urban exploiter, which depends heavily on anthropogenic resources; (2) the rose-ringed parakeet, an invasive alien species that has adapted to exploit human resources; and (3) the graceful prinia, an urban adapter, which is relatively shy of humans and can be found in urban habitats with shrubs and prairies. Acoustic recordings provided continuous monitoring of bird activity without an effect of the observer on the animal. We performed dense sampling of a 1.3 square km area in northern Tel-Aviv by placing 17 recorders for more than a month in different micro-habitats within this region including roads, residential areas and urban parks. We monitored both lockdown and no-lockdown periods. We portray a complex dynamic system where the activity of specific bird species depended on many environmental parameters and decreases or increases in a habitat-dependent manner during lockdown. Specifically, urban exploiter species decreased their activity in most urban habitats during lockdown, while human adapter species increased their activity during lockdown especially in parks where humans were absent. Our results also demonstrate the value of different habitats within urban environments for animal activity, specifically highlighting the importance of urban parks. These species- and habitat-specific changes in activity might explain the contradicting results reported by others who have not performed a habitat specific analysis.