Experimental Evolution of an RNA Virus in Wild Birds: Evidence for Host-Dependent Impacts on Population Structure and Competitive Fitness

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 Brault, Gregory D. Ebel

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
Article numbere1004874
JournalPLoS Pathogens
Volume11
Issue number5
DOIs
StatePublished - Jan 1 2015
Externally publishedYes

Fingerprint

RNA Viruses
West Nile virus
Birds
Songbirds
Sparrows
Population
Crows
Genetic Selection
Bird Diseases
Genome
Viruses
Satellite Viruses
Mutation Rate
Virus Replication
Phenotype
Mutation
Mortality

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Immunology
  • Molecular Biology
  • Genetics
  • Virology

Cite this

Grubaugh, N. D., Smith, D. R., Brackney, D. E., Bosco-Lauth, A. M., Fauver, J. R., Campbell, C. L., ... Ebel, G. D. (2015). Experimental Evolution of an RNA Virus in Wild Birds: Evidence for Host-Dependent Impacts on Population Structure and Competitive Fitness. PLoS Pathogens, 11(5), [e1004874]. https://doi.org/10.1371/journal.ppat.1004874

Experimental Evolution of an RNA Virus in Wild Birds : Evidence for Host-Dependent Impacts on Population Structure and Competitive Fitness. / Grubaugh, Nathan D.; Smith, Darci R.; Brackney, Doug E.; Bosco-Lauth, Angela M.; Fauver, Joseph R.; Campbell, Corey L.; Felix, Todd A.; Romo, Hannah; Duggal, Nisha K.; Dietrich, Elizabeth A.; Eike, Tyler; Beane, Jennifer E.; Bowen, Richard A.; Black, William C.; Brault, Aaron; Ebel, Gregory D.

In: PLoS Pathogens, Vol. 11, No. 5, e1004874, 01.01.2015.

Research output: Contribution to journalArticle

Grubaugh, ND, Smith, DR, Brackney, DE, Bosco-Lauth, AM, Fauver, JR, Campbell, CL, Felix, TA, Romo, H, Duggal, NK, Dietrich, EA, Eike, T, Beane, JE, Bowen, RA, Black, WC, Brault, A & Ebel, GD 2015, 'Experimental Evolution of an RNA Virus in Wild Birds: Evidence for Host-Dependent Impacts on Population Structure and Competitive Fitness', PLoS Pathogens, vol. 11, no. 5, e1004874. https://doi.org/10.1371/journal.ppat.1004874
Grubaugh, Nathan D. ; Smith, Darci R. ; Brackney, Doug E. ; Bosco-Lauth, Angela M. ; Fauver, Joseph R. ; Campbell, Corey L. ; Felix, Todd A. ; Romo, Hannah ; Duggal, Nisha K. ; Dietrich, Elizabeth A. ; Eike, Tyler ; Beane, Jennifer E. ; Bowen, Richard A. ; Black, William C. ; Brault, Aaron ; Ebel, Gregory D. / Experimental Evolution of an RNA Virus in Wild Birds : Evidence for Host-Dependent Impacts on Population Structure and Competitive Fitness. In: PLoS Pathogens. 2015 ; Vol. 11, No. 5.
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