Parallel evolution between genomic segments of seasonal human influenza viruses reveals RNA-RNA relationships
Abstract
The influenza A virus (IAV) genome consists of eight negative-sense viral RNA (vRNA) segments that are selectively assembled into progeny virus particles through RNA-RNA interactions. To explore putative intersegmental RNA-RNA relationships, we quantified similarity between phylogenetic trees comprising each vRNA segment from seasonal human IAV. Intersegmental tree similarity differed between subtype and lineage. While intersegmental relationships were largely conserved over time in H3N2 viruses, they diverged in H1N1 strains isolated before and after the 2009 pandemic. Surprisingly, intersegmental relationships were not driven solely by protein sequence, suggesting that IAV evolution could also be driven by RNA-RNA interactions. Finally, we used confocal microscopy to determine that colocalization of highly coevolved vRNA segments is enriched over other assembly intermediates at the nuclear periphery during productive viral infection. This study illustrates how putative RNA interactions underlying selective assembly of IAV can be interrogated with phylogenetics.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Scripts have been deposited to GitHub as described in the manuscript. Summary tables have been provided for Figures 2-7 and figure supplements.
-
Influenza Research Database: An integrated bioinformatics resource for influenza virus researchInfluenza Research Database, doi: 10.1093/nar/gkw857.
Article and author information
Author details
Funding
National Institute of Allergy and Infectious Diseases (T32 AI049820)
- Jennifer E Jones
Center for Evolutionary Biology and Medicine, University of Pittsburgh
- Jennifer E Jones
National Institute of Allergy and Infectious Diseases (R01 AI139063)
- Seema S Lakdawala
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Jones 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.
Metrics
-
- 2,176
- views
-
- 315
- downloads
-
- 15
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Evolutionary Biology
- Epidemiology and Global Health
- Microbiology and Infectious Disease
- Genetics and Genomics
eLife is pleased to present a Special Issue to highlight recent advances in the growing and increasingly interdisciplinary field of evolutionary medicine.
-
- Evolutionary Biology
Eyespot patterns have evolved in many prey species. These patterns were traditionally explained by the eye mimicry hypothesis, which proposes that eyespots resembling vertebrate eyes function as predator avoidance. However, it is possible that eyespots do not mimic eyes: according to the conspicuousness hypothesis, eyespots are just one form of vivid signals where only conspicuousness matters. They might work simply through neophobia or unfamiliarity, without necessarily implying aposematism or the unprofitability to potential predators. To test these hypotheses and explore factors influencing predators’ responses, we conducted a meta-analysis with 33 empirical papers that focused on bird responses to both real lepidopterans and artificial targets with conspicuous patterns (i.e. eyespots and non-eyespots). Supporting the latter hypothesis, the results showed no clear difference in predator avoidance efficacy between eyespots and non-eyespots. When comparing geometric pattern characteristics, bigger pattern sizes and smaller numbers of patterns were more effective in preventing avian predation. This finding indicates that single concentric patterns have stronger deterring effects than paired ones. Taken together, our study supports the conspicuousness hypothesis more than the eye mimicry hypothesis. Due to the number and species coverage of published studies so far, the generalisability of our conclusion may be limited. The findings highlight that pattern conspicuousness is key to eliciting avian avoidance responses, shedding a different light on this classic example of signal evolution.