Experimental evolution of an RNA virus in wild birds: evidence for host-dependent impacts on population structure and competitive fitness.
Within hosts, RNA viruses form populations that are genetically and phenotypically complex. Heterogeneity in RNA virus genomes arises due to error-prone replication and is reduced by stochastic and selective mechanisms that are incompletely understood. Defining how natural selection shapes RNA virus...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2015-05-01
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| Series: | PLoS Pathogens |
| Online Access: | http://europepmc.org/articles/PMC4439088?pdf=render |
| _version_ | 1818288144954425344 |
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| author | Nathan D Grubaugh Darci R Smith Doug E Brackney Angela M Bosco-Lauth Joseph R Fauver Corey L Campbell Todd A Felix Hannah Romo Nisha K Duggal Elizabeth A Dietrich Tyler Eike Jennifer E Beane Richard A Bowen William C Black Aaron C Brault Gregory D Ebel |
| author_facet | Nathan D Grubaugh Darci R Smith Doug E Brackney Angela M Bosco-Lauth Joseph R Fauver Corey L Campbell Todd A Felix Hannah Romo Nisha K Duggal Elizabeth A Dietrich Tyler Eike Jennifer E Beane Richard A Bowen William C Black Aaron C Brault Gregory D Ebel |
| author_sort | Nathan D Grubaugh |
| collection | DOAJ |
| description | Within hosts, RNA viruses form populations that are genetically and phenotypically complex. Heterogeneity in RNA virus genomes arises due to error-prone replication and is reduced by stochastic and selective mechanisms that are incompletely understood. Defining how natural selection shapes RNA virus populations is critical because it can inform treatment paradigms and enhance control efforts. We allowed West Nile virus (WNV) to replicate in wild-caught American crows, house sparrows and American robins to assess how natural selection shapes RNA virus populations in ecologically relevant hosts that differ in susceptibility to virus-induced mortality. After five sequential passages in each bird species, we examined the phenotype and population diversity of WNV through fitness competition assays and next generation sequencing. We demonstrate that fitness gains occur in a species-specific manner, with the greatest replicative fitness gains in robin-passaged WNV and the least in WNV passaged in crows. Sequencing data revealed that intrahost WNV populations were strongly influenced by purifying selection and the overall complexity of the viral populations was similar among passaged hosts. However, the selective pressures that control WNV populations seem to be bird species-dependent. Specifically, crow-passaged WNV populations contained the most unique mutations (~1.7× more than sparrows, ~3.4× more than robins) and defective genomes (~1.4× greater than sparrows, ~2.7× greater than robins), but the lowest average mutation frequency (about equal to sparrows, ~2.6× lower than robins). Therefore, our data suggest that WNV replication in the most disease-susceptible bird species is positively associated with virus mutational tolerance, likely via complementation, and negatively associated with the strength of selection. These differences in genetic composition most likely have distinct phenotypic consequences for the virus populations. Taken together, these results reveal important insights into how different hosts may contribute to the emergence of RNA viruses. |
| first_indexed | 2024-12-13T01:51:43Z |
| format | Article |
| id | doaj.art-067aa91bdc714381adb255765a07bcfe |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-12-13T01:51:43Z |
| publishDate | 2015-05-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-067aa91bdc714381adb255765a07bcfe2022-12-22T00:03:29ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742015-05-01115e100487410.1371/journal.ppat.1004874Experimental evolution of an RNA virus in wild birds: evidence for host-dependent impacts on population structure and competitive fitness.Nathan D GrubaughDarci R SmithDoug E BrackneyAngela M Bosco-LauthJoseph R FauverCorey L CampbellTodd A FelixHannah RomoNisha K DuggalElizabeth A DietrichTyler EikeJennifer E BeaneRichard A BowenWilliam C BlackAaron C BraultGregory D EbelWithin hosts, RNA viruses form populations that are genetically and phenotypically complex. Heterogeneity in RNA virus genomes arises due to error-prone replication and is reduced by stochastic and selective mechanisms that are incompletely understood. Defining how natural selection shapes RNA virus populations is critical because it can inform treatment paradigms and enhance control efforts. We allowed West Nile virus (WNV) to replicate in wild-caught American crows, house sparrows and American robins to assess how natural selection shapes RNA virus populations in ecologically relevant hosts that differ in susceptibility to virus-induced mortality. After five sequential passages in each bird species, we examined the phenotype and population diversity of WNV through fitness competition assays and next generation sequencing. We demonstrate that fitness gains occur in a species-specific manner, with the greatest replicative fitness gains in robin-passaged WNV and the least in WNV passaged in crows. Sequencing data revealed that intrahost WNV populations were strongly influenced by purifying selection and the overall complexity of the viral populations was similar among passaged hosts. However, the selective pressures that control WNV populations seem to be bird species-dependent. Specifically, crow-passaged WNV populations contained the most unique mutations (~1.7× more than sparrows, ~3.4× more than robins) and defective genomes (~1.4× greater than sparrows, ~2.7× greater than robins), but the lowest average mutation frequency (about equal to sparrows, ~2.6× lower than robins). Therefore, our data suggest that WNV replication in the most disease-susceptible bird species is positively associated with virus mutational tolerance, likely via complementation, and negatively associated with the strength of selection. These differences in genetic composition most likely have distinct phenotypic consequences for the virus populations. Taken together, these results reveal important insights into how different hosts may contribute to the emergence of RNA viruses.http://europepmc.org/articles/PMC4439088?pdf=render |
| spellingShingle | Nathan D Grubaugh Darci R Smith Doug E Brackney Angela M Bosco-Lauth Joseph R Fauver Corey L Campbell Todd A Felix Hannah Romo Nisha K Duggal Elizabeth A Dietrich Tyler Eike Jennifer E Beane Richard A Bowen William C Black Aaron C Brault Gregory D Ebel Experimental evolution of an RNA virus in wild birds: evidence for host-dependent impacts on population structure and competitive fitness. PLoS Pathogens |
| title | Experimental evolution of an RNA virus in wild birds: evidence for host-dependent impacts on population structure and competitive fitness. |
| title_full | Experimental evolution of an RNA virus in wild birds: evidence for host-dependent impacts on population structure and competitive fitness. |
| title_fullStr | Experimental evolution of an RNA virus in wild birds: evidence for host-dependent impacts on population structure and competitive fitness. |
| title_full_unstemmed | Experimental evolution of an RNA virus in wild birds: evidence for host-dependent impacts on population structure and competitive fitness. |
| title_short | Experimental evolution of an RNA virus in wild birds: evidence for host-dependent impacts on population structure and competitive fitness. |
| title_sort | experimental evolution of an rna virus in wild birds evidence for host dependent impacts on population structure and competitive fitness |
| url | http://europepmc.org/articles/PMC4439088?pdf=render |
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