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Genetic Diversity and Evolution

Punctuated evolution of myxoma virus: rapid and disjunct evolution of a recent viral lineage in Australia

Peter J. Kerr, John-Sebastian Eden, Francesca Di Giallonardo, David Peacock, June Liu, Tanja Strive, Andrew F. Read, Edward C. Holmes
Peter J. Kerr
CSIRO Health and Biosecurity, Canberra, Australian Capital Territory 2601, Australia.Marie Bashir Institute for Infectious Diseases and Biosecurity, School of Life and Environmental Sciences and Sydney Medical School, Charles Perkins Centre, University of Sydney, Sydney, New South Wales 2006, Australia.
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John-Sebastian Eden
Marie Bashir Institute for Infectious Diseases and Biosecurity, School of Life and Environmental Sciences and Sydney Medical School, Charles Perkins Centre, University of Sydney, Sydney, New South Wales 2006, Australia.Centre for Virus Research, Westmead Institute for Medical Research, Westmead, NSW 2145, Australia.
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Francesca Di Giallonardo
The Kirby Institute, University of New South Wales, Randwick, NSW 2052, Australia.
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David Peacock
Biosecurity SA, Adelaide 5001, South Australia.School of Animal and Veterinary Sciences, the University of Adelaide, Roseworthy, SA 5371, Australia.
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June Liu
CSIRO Health and Biosecurity, Canberra, Australian Capital Territory 2601, Australia.Department of Agriculture and Water Resources, 7 London Circuit, Canberra, Australian Capital Territory 2601, Australia.
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Tanja Strive
CSIRO Health and Biosecurity, Canberra, Australian Capital Territory 2601, Australia.Centre for Invasive Species Solutions, Bruce, Australian Capital Territory 2617, Australia.
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Andrew F. Read
Center for Infectious Disease Dynamics and Department of Biology, The Pennsylvania State University, University Park, Pennsylvania 16802, USA.Department of Entomology, The Pennsylvania State University, University Park, Pennsylvania 16802, USA.
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Edward C. Holmes
Marie Bashir Institute for Infectious Diseases and Biosecurity, School of Life and Environmental Sciences and Sydney Medical School, Charles Perkins Centre, University of Sydney, Sydney, New South Wales 2006, Australia.
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  • ORCID record for Edward C. Holmes
  • For correspondence: edward.holmes@sydney.edu.au
DOI: 10.1128/JVI.01994-18
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ABSTRACT

Myxoma virus (MYXV) has been evolving in a novel host species – European rabbits – in Australia since 1950. Previous studies of viruses sampled from 1950 to 1999 revealed a remarkably clock-like evolutionary process across all Australian lineages of MYXV. Through an analysis of 49 newly generated MYXV genome sequences isolated in Australia between 2008 and 2017 we show that MYXV evolution in Australia can be characterized by three lineages, one of which exhibited a greatly elevated rate of evolutionary change and a dramatic break-down of temporal structure. Phylogenetic analysis revealed that this apparently punctuated evolutionary event occurred between 1996 and 2012. The branch leading to the rapidly evolving lineage contained a relatively high number of non-synonymous substitutions, and viruses in this lineage reversed a mutation found in the progenitor standard laboratory strain (SLS) and all previous sequences that disrupts the reading frame of the M005L/R gene. Analysis of genes encoding proteins involved in DNA synthesis or RNA transcription did not reveal any mutations likely to cause rapid evolution. Although there was some evidence for recombination across the MYXV phylogeny, this was not associated with the increase in evolutionary rate. The period from 1996 to 2012 saw significant declines in wild rabbit numbers, due to the introduction of rabbit hemorrhagic disease and prolonged drought in south-eastern Australia, followed by the partial recovery of populations. It is therefore possible that a rapidly changing environment for virus transmission changed the selection pressures faced by MYXV, altering the course and pace of virus evolution.

IMPORTANCE The co-evolution of myxoma virus (MYXV) and European rabbits in Australia is one of the most important natural ‘experiments’ in evolutionary biology, providing insights into virus adaptation to new hosts and the evolution of virulence. Previous studies of MYXV evolution have also shown that the virus evolves both relatively rapidly and in a strongly clock-like manner. Using newly acquired MYXV genome sequences from Australia we show that the virus has experienced a dramatic change in evolutionary behavior over the last 20 years, with a break-down in clock-like structure, the appearance of a rapidly evolving virus lineage, and the accumulation of multiple non-synonymous and indel mutations. We suggest that this punctuated evolutionary event may reflect a change in selection pressures as rabbit numbers declined following the introduction of rabbit hemorrhagic disease virus and drought in the geographic regions inhabited by rabbits.

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Punctuated evolution of myxoma virus: rapid and disjunct evolution of a recent viral lineage in Australia
Peter J. Kerr, John-Sebastian Eden, Francesca Di Giallonardo, David Peacock, June Liu, Tanja Strive, Andrew F. Read, Edward C. Holmes
Journal of Virology Feb 2019, JVI.01994-18; DOI: 10.1128/JVI.01994-18

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Punctuated evolution of myxoma virus: rapid and disjunct evolution of a recent viral lineage in Australia
Peter J. Kerr, John-Sebastian Eden, Francesca Di Giallonardo, David Peacock, June Liu, Tanja Strive, Andrew F. Read, Edward C. Holmes
Journal of Virology Feb 2019, JVI.01994-18; DOI: 10.1128/JVI.01994-18
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