Developing an empirical model for spillover and emergence: Orsay virus host range in Caenorhabditis

Clara L. Shaw, David A. Kennedy

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

A lack of tractable experimental systems in which to test hypotheses about the ecological and evolutionary drivers of disease spillover and emergence has limited our understanding of these processes. Here we introduce a promising system: Caenorhabditis hosts and Orsay virus, a positive-sense single-stranded RNA virus that naturally infects C. elegans. We assayed species across the Caenorhabditis tree and found Orsay virus susceptibility in 21 of 84 wild strains belonging to 14 of 44 species. Confirming patterns documented in other systems, we detected effects of host phylogeny on susceptibility. We then tested whether susceptible strains were capable of transmitting Orsay virus by transplanting exposed hosts and determining whether they transmitted infection to conspecifics during serial passage. We found no evidence of transmission in 10 strains (virus undetectable after passaging in all replicates), evidence of low-level transmission in 5 strains (virus lost between passage 1 and 5 in at least one replicate) and evidence of sustained transmission in 6 strains (including all three experimental C. elegans strains) in at least one replicate. Transmission was strongly associated with viral amplification in exposed populations. Variation in Orsay virus susceptibility and transmission among Caenorhabditis strains suggests that the system could be powerful for studying spillover and emergence.

Original languageEnglish (US)
Article number20221165
JournalProceedings of the Royal Society B: Biological Sciences
Volume289
Issue number1983
DOIs
StatePublished - Sep 28 2022
Externally publishedYes

Bibliographical note

Funding Information:
This work was supported by National Science Foundation grants DEB-1754692 and DEB-2211322. The funders had no role in study design, data collection and analysis, decision to publish or preparation of this article. Acknowledgements

Funding Information:
We thank M.-A. Félix and A. Richaud for Caenorhabditis strains and for technical advice. Some strains were provided by the CGC, which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440). We thank A. J. Belville for help with supplemental experiments, A. Aluquin for help with viral extractions, B. Tuschhoff, C. Geyer and A. Wood for statistical and computational assistance, A. Bhattacharya, H. Dutra, B. McGraw, E. Hansen and A. Read for discussion, and L. Stevens for technical guidance on working with phylogenetic data. We are also grateful to M.-A. Félix and two anonymous reviewers for comments on earlier drafts of this manuscript.

Publisher Copyright:
© 2022 The Author(s).

Keywords

  • Caenorhabditis
  • emergence
  • host jump
  • host range
  • Orsay virus
  • spillover

PubMed: MeSH publication types

  • Journal Article
  • Research Support, U.S. Gov't, Non-P.H.S.

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