Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients
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 stud...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2023-09-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/66550 |
| _version_ | 1797666969545080832 |
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| author | Kyra Hermanns Marco Marklewitz Florian Zirkel Anne Kopp Stephanie Kramer-Schadt Sandra Junglen |
| author_facet | Kyra Hermanns Marco Marklewitz Florian Zirkel Anne Kopp Stephanie Kramer-Schadt Sandra Junglen |
| author_sort | Kyra Hermanns |
| collection | DOAJ |
| description | 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), which 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 are a key driver of virus emergence. |
| first_indexed | 2024-03-11T20:06:21Z |
| format | Article |
| id | doaj.art-4ac6ab0be37e4f12aa99cae34b22de1e |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-11T20:06:21Z |
| publishDate | 2023-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-4ac6ab0be37e4f12aa99cae34b22de1e2023-10-03T16:02:18ZengeLife Sciences Publications LtdeLife2050-084X2023-09-011210.7554/eLife.66550Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradientsKyra Hermanns0Marco Marklewitz1Florian Zirkel2Anne Kopp3Stephanie Kramer-Schadt4https://orcid.org/0000-0002-9269-4446Sandra Junglen5https://orcid.org/0000-0002-3799-6011Institute of Virology, Charité - Universitätsmedizin Berlin, corporate member of Free University Berlin, Humboldt-Universtiy Berlin, and Berlin Institute of Health, Berlin, GermanyInstitute of Virology, Charité - Universitätsmedizin Berlin, corporate member of Free University Berlin, Humboldt-Universtiy Berlin, and Berlin Institute of Health, Berlin, GermanyInstitute of Virology, University of Bonn Medical Centre, Berlin, GermanyInstitute of Virology, Charité - Universitätsmedizin Berlin, corporate member of Free University Berlin, Humboldt-Universtiy Berlin, and Berlin Institute of Health, Berlin, GermanyDepartment of Ecological Dynamics, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany; Institute of Ecology, Technische Universität Berlin, Berlin, GermanyInstitute of Virology, Charité - Universitätsmedizin Berlin, corporate member of Free University Berlin, Humboldt-Universtiy Berlin, and Berlin Institute of Health, Berlin, GermanyPreviously 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), which 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 are a key driver of virus emergence.https://elifesciences.org/articles/66550arbovirusmosquitodisease ecologyinsect-specific viruscommunity composition |
| spellingShingle | Kyra Hermanns Marco Marklewitz Florian Zirkel Anne Kopp Stephanie Kramer-Schadt Sandra Junglen Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients eLife arbovirus mosquito disease ecology insect-specific virus community composition |
| title | Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients |
| title_full | Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients |
| title_fullStr | Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients |
| title_full_unstemmed | Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients |
| title_short | Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients |
| title_sort | mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients |
| topic | arbovirus mosquito disease ecology insect-specific virus community composition |
| url | https://elifesciences.org/articles/66550 |
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