Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients

  1. Kyra Hermanns
  2. Marco Marklewitz
  3. Florian Zirkel
  4. Anne Kopp
  5. Stephanie Kramer-Schadt
  6. Sandra Junglen  Is a corresponding author
  1. Charité-Universitätsmedizin Berlin, Germany
  2. University of Bonn Medical Centre, Germany
  3. Leibniz Institute for Zoo and Wildlife Research, Germany

Abstract

Previously unknown pathogens often emerge from primary ecosystems, but there is little knowledge on the mechanisms of emergence. Most studies analyzing the influence of land-use change on pathogen emergence focus on a single host-pathogen system and often observe contradictory effects. Here, we studied virus diversity and prevalence patterns in natural and disturbed ecosystems using a multi-host and multi-taxa approach. Mosquitoes sampled along a disturbance gradient in Côte d’Ivoire were tested by generic RT-PCR assays established for all major arbovirus and insect-specific virus taxa including novel viruses previously discovered in these samples based on cell culture isolates enabling an unbiased and comprehensive approach. The taxonomic composition of detected viruses was characterized and viral infection rates according to habitat and host were analyzed. We detected 331 viral sequences pertaining to 34 novel and 15 previously identified viruses of the families Flavi-, Rhabdo-, Reo-, Toga-, Mesoni- and Iflaviridae and the order Bunyavirales. Highest host and virus diversity was observed in pristine and intermediately disturbed habitats. The majority of the 49 viruses was detected with low prevalence. However, nine viruses were found frequently across different habitats of which five viruses increased in prevalence towards disturbed habitats, in congruence with the dilution effect hypothesis. These viruses were mainly associated with one specific mosquito species (Culex nebulosus), that increased in relative abundance from pristine (3%) to disturbed habitats (38%). Interestingly, the observed increased prevalence of these five viruses in disturbed habitats was not caused by higher host infection rates but by increased host abundance, an effect tentatively named abundance effect. Our data show that host species composition is critical for virus abundance. Environmental changes that lead to an uneven host community composition and to more individuals of a single species is a key driver of virus emergence.

Data availability

The viral sequence fragments and genomes as well as the potential non-retroviral integrated RNA virus sequences (NIRVS) were assigned the GenBank accession numbers MZ202249-MZ202305 and MZ399697- MZ399709, respectively.

Article and author information

Author details

  1. Kyra Hermanns

    Institute of Virology, Charité-Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Marco Marklewitz

    Institute of Virology, Charité-Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Florian Zirkel

    Institute of Virology, University of Bonn Medical Centre, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Anne Kopp

    Institute of Virology, Charité-Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Stephanie Kramer-Schadt

    Department of Ecological Dynamics, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9269-4446
  6. Sandra Junglen

    Institute of Virology, Charité-Universitätsmedizin Berlin, Berlin, Germany
    For correspondence
    sandra.junglen@charite.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3799-6011

Funding

Federal Ministry of Education and Research (01KI1716)

  • Sandra Junglen

German Research Foundation (JU2857/3-2)

  • Sandra Junglen

German Research Foundation (DR772/10-2)

  • Sandra Junglen

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

Reviewing Editor

  1. Isabel Rodriguez-Barraquer, University of California, San Francisco, United States

Version history

  1. Received: January 14, 2021
  2. Accepted: September 12, 2023
  3. Accepted Manuscript published: September 13, 2023 (version 1)

Copyright

© 2023, Hermanns 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.

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  1. Kyra Hermanns
  2. Marco Marklewitz
  3. Florian Zirkel
  4. Anne Kopp
  5. Stephanie Kramer-Schadt
  6. Sandra Junglen
(2023)
Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients
eLife 12:e66550.
https://doi.org/10.7554/eLife.66550

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