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J Virol. 2019 Apr 3;93(8). pii: e01994-18. doi: 10.1128/JVI.01994-18. Print 2019 Apr 15.

Punctuated Evolution of Myxoma Virus: Rapid and Disjunct Evolution of a Recent Viral Lineage in Australia.

Kerr PJ1,2,3, Eden JS2,3,4, Di Giallonardo F5, Peacock D6,7, Liu J1,8, Strive T1,9, Read AF10,11,12, Holmes EC13,3.

Author information

1
CSIRO Health and Biosecurity, Canberra, Australian Capital Territory, Australia.
2
Marie Bashir Institute for Infectious Diseases and Biosecurity, School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia.
3
Sydney Medical School, Charles Perkins Centre, University of Sydney, Sydney, New South Wales, Australia.
4
Centre for Virus Research, Westmead Institute for Medical Research, Westmead, New South Wales, Australia.
5
The Kirby Institute, University of New South Wales, Randwick, New South Wales, Australia.
6
Biosecurity SA, Adelaide, South Australia, Australia.
7
School of Animal and Veterinary Sciences, the University of Adelaide, Roseworthy, South Australia, Australia.
8
Department of Agriculture and Water Resources, Canberra, Australian Capital Territory, Australia.
9
Centre for Invasive Species Solutions, Bruce, Australian Capital Territory, Australia.
10
Center for Infectious Disease Dynamics, The Pennsylvania State University, University Park, Pennsylvania, USA.
11
Department of Biology, The Pennsylvania State University, University Park, Pennsylvania, USA.
12
Department of Entomology, The Pennsylvania State University, University Park, Pennsylvania, USA.
13
Marie Bashir Institute for Infectious Diseases and Biosecurity, School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia edward.holmes@sydney.edu.au.

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 breakdown 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 nonsynonymous 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 the 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 southeastern 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 coevolution 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 breakdown in clock-like structure, the appearance of a rapidly evolving virus lineage, and the accumulation of multiple nonsynonymous 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.

KEYWORDS:

Australia; evolution; myxoma virus; natural selection; phylogeny; rabbit

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