Host Phylogeny Determines Viral Persistence and Replication in Novel Hosts
Ben Longdon1,2*, Jarrod D. Hadfield1, Claire L. Webster1,2, Darren J. Obbard1,2#, Francis M. Jiggins3#
1 Institute of Evolutionary Biology, University of Edinburgh, Ashworth Labs, Edinburgh, United Kingdom, 2 Centre for Immunity, Infection and Evolution, University of Edinburgh, Ashworth Labs, Edinburgh, United Kingdom, 3 Department of Genetics, University of Cambridge, Cambridge, United Kingdom
Abstract
Pathogens switching to new hosts can result in the emergence of new infectious diseases, and determining which species are likely to be sources of such host shifts is essential to understanding disease threats to both humans and wildlife. However, the factors that determine whether a pathogen can infect a novel host are poorly understood. We have examined the ability of three host-specific RNA-viruses (Drosophila sigma viruses from the family Rhabdoviridae) to persist and replicate in 51 different species of Drosophilidae. Using a novel analytical approach we found that the host phylogeny could explain most of the variation in viral replication and persistence between different host species. This effect is partly driven by viruses reaching a higher titre in those novel hosts most closely related to the original host. However, there is also a strong effect of host phylogeny that is independent of the distance from the original host, with viral titres being similar in groups of related hosts. Most of this effect could be explained by variation in general susceptibility to all three sigma viruses, as there is a strong phylogenetic correlation in the titres of the three viruses. These results suggest that the source of new emerging diseases may often be predictable from the host phylogeny, but that the effect may be more complex than simply causing most host shifts to occur between closely related hosts.
Author Summary
Emerging infectious diseases such as SARS, HIV and swine-origin influenza have all been recently acquired by humans from other species. Understanding the reasons why parasites jump between different host species is essential to allow us to predict future threats and understand the causes of disease emergence. Here we ask how host-relatedness might determine when host-shifts can occur in the most important group of emerging diseases—RNA viruses. We show that the relationship between host species is the primary factor in determining a virus's ability to persist and replicate in a novel host following exposure. This can be broken down into two components. Firstly, species closely related to the virus's natural host are more susceptible than distantly related species. Secondly, independent of the distance effect, groups of closely related host species have similar levels of susceptibility. This has important implications for our understanding of disease-emergence, and until now the only large-scale studies of viruses have been correlative rather than experimental. We also found groups of related species that are susceptible to these viruses but are distantly related to the natural hosts, which may explain why viruses sometimes jump between distantly related species.
Citation: Longdon B, Hadfield JD, Webster CL, Obbard DJ, Jiggins FM (2011) Host Phylogeny Determines Viral Persistence and Replication in Novel Hosts. PLoS Pathog 7(9): e1002260. doi:10.1371/journal.ppat.1002260
Editor: David S. Schneider, Stanford University, United States of America
Received: April 14, 2011; Accepted: July 25, 2011; Published: September 22, 2011
Copyright: © 2011 Longdon et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was funded by a BBSRC PhD studentship awarded to BL, a NERC fellowship to JDH, a Royal Society Research Fellowship and Wellcome Trust Project Grant to FMJ and Wellcome Trust RCD Fellowship (085064/Z/08/Z) to DJO. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: B.Longdon@ed.ac.uk
# These authors contributed equally to this work.
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