Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients
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
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
- Isabel Rodriguez-Barraquer, University of California, San Francisco, United States
Version history
- Received: January 14, 2021
- Preprint posted: February 6, 2021 (view preprint)
- Accepted: September 12, 2023
- Accepted Manuscript published: September 13, 2023 (version 1)
- Version of Record published: October 3, 2023 (version 2)
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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