Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Historical Records of Australian Science Historical Records of Australian Science Society
The history of science, pure and applied, in Australia, New Zealand and the southwest Pacific
Shopping Cart: ( empty )
You are here: Home > Journals > HR > HR24010
RESEARCH ARTICLE
Online Early

Problems with Fenner and Marshall’s method of estimating myxoma virus virulence delayed a closer understanding of rabbit-virus coevolution

Brian Cooke https://orcid.org/0000-0001-7430-1824 A *
+ Author Affiliations
- Author Affiliations

A Rabbit Free Australia, PO Box 145, Collinswood, SA 5081, Australia.

* Correspondence to: briancooke.rfa@gmail.com

Historical Records of Australian Science https://doi.org/10.1071/HR24010
Published online: 4 October 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the Australian Academy of Science.

Abstract

When myxoma virus was first released in Australia it was seen not only as a means of controlling rabbits but also an opportunity to understand the evolution of a disease in a new host. The virus quickly attenuated into less virulent variants while simultaneously rabbits built heritable resistance to the disease. Nonetheless, rather than rabbits quickly outstripping virus virulence, myxoma viruses have adapted and kept pace with increases in rabbit resistance by increasing in virulence and other attributes necessary for remaining highly transmissible. As well as benefitting the biological control of pest rabbits, this previously unrevealed chapter details the evolution of myxomatosis while also documenting the delays in reaching a consensus on the coevolution of myxoma virus virulence and rabbit resistance.

Keywords: biological arms race, European rabbit, European rabbit fleas, evolution, myxoma virus, Oryctolagus cuniculus, resistance, virus lineages.

References

Anderson, W. (2017) Nowhere to run, rabbit: the cold-war calculus of disease ecology, History and Philosophy of the Life Sciences, 39, 13.
| Crossref | Google Scholar |

Aragão, H. B. (1943) O virus do mixoma no coelho do mato (Sylvilagus minensis), su transmissão pelos Aedes scapularis e aegtypti, Memorias do Instituto Oswaldo Cruz, 38, 93-99 [In Portuguese].
| Google Scholar |

Best, S. M., and Kerr, P. J. (2000) Coevolution of host and virus: the pathogenesis of virulent and attenuated strains of myxoma virus in resistant and susceptible European rabbits, Virology, 267, 36-48.
| Crossref | Google Scholar | PubMed |

Burnet, F. M. (1952) Myxomatosis as a method of biological control against the Australian rabbit, American Journal of Public Health Nations Health, 42, 1522-1526.
| Crossref | Google Scholar | PubMed |

Cooke, B. D. (1983) Changes in the age-structure and size of populations of wild rabbits in South Australia, following the Introduction of European Rabbit Fleas, Spilopsyllus cuniculi (Dale), as vectors of myxomatosis, Wildlife Research, 10, 105-120.
| Crossref | Google Scholar |

Cooke, B. D. (2023) Fifty-year review: European rabbit fleas, Spilopsyllus cuniculi (Dale, 1878) (Siphonaptera: Pulicidae), enhanced the efficacy of myxomatosis for controlling Australian rabbits, Wildlife Research, 50, 4-15.
| Crossref | Google Scholar |

Cooke, B. D., McPhee, S., Robinson, A. J., and Capucci, L. (2002) Rabbit haemorrhagic disease: does a pre-existing RHDV-like virus reduce the effectiveness of RHD as a biological control in Australia? Wildlife Research, 29, 673-682.
| Crossref | Google Scholar |

Cooke, B. D., Duncan, R. P., McDonald, I., Liu, J., Capucci, L., Mutze, G. J., and Strive, G. J. M. T. (2018) Prior exposure to non-pathogenic calicivirus RCV-A1 reduces both infection rate and mortality from rabbit haemorrhagic disease in a population of wild rabbits in Australia, Transboundary and Emerging Diseases, 65(2), e470-e477.
| Crossref | Google Scholar | PubMed |

Cooke, B. D., Taggart, P., and Patel, K. (2023) Quantifying resistance to myxomatosis in wild rabbits produces novel evolutionary insights, Epidemiology and Infection, 151, e182.
| Crossref | Google Scholar | PubMed |

Dawkins, R., and Krebs, J. R. (1979) Arms races between and within species, Proceedings of the Royal Society of London. Series B. Biological Sciences, 205, 489-511.
| Crossref | Google Scholar | PubMed |

Di Giallonardo, F., and Holmes, E. C. (2015) Viral biocontrol: grand experiments in disease emergence and evolution, Trends in Microbiology, 23, 83-90 Epub 31 October 2014.
| Crossref | Google Scholar | PubMed |

Douglas, G. W. (1965) A review of myxomatosis in Victoria, Journal of Agriculture Victoria, 63, 557-562.
| Google Scholar |

Dwyer, G., Levin, S. A., and Buttel, L. (1990) A simulation model of the population dynamics and evolution of myxomatosis, Ecological Monographs, 60, 423-447.
| Crossref | Google Scholar |

Edmonds, J. W., Nolan, I. F., Shepherd, R. C., and Gocs, A. (1975) Myxomatosis: the virulence of field strains of myxoma virus in a population of wild rabbits (Oryctolagus cuniculus L.) with high resistance to myxomatosis, Journal of Hygiene, 74, 417-418.
| Crossref | Google Scholar | PubMed |

Eldredge, N. and Gould, S. J. (1972) ‘Punctuated Equilibria: an alternative to Phyletic Gradualism’, in Models in Paleobiology, ed. T. J. M. Schopf, Freeman Cooper, San Francisco. pp. 82–115.

Elsworth, P. G, Kovaliski, J., and Cooke, B. D. (2012) Rabbit haemorrhagic disease: are Australian rabbits (Oryctolagus cuniculus) evolving resistance to infection with Czech CAPM 351 RHDV? Epidemiology and Infection, 140, 1972-1981.
| Crossref | Google Scholar | PubMed |

Elsworth, P., Cooke, B. D., Kovaliski, J., Sinclair, R., Holmes, E. C., and Strive, T. (2014) Increased virulence of rabbit haemorrhagic disease virus associated with genetic resistance in wild Australian rabbits (Oryctolagus cuniculus), Virology, 464–465, 415-423.
| Crossref | Google Scholar | PubMed |

Fenner, F. and Fantini, B. (1999) Biological Control of Vertebrate Pests: The History of Myxomatosis, an Experiment in Evolution, CABI Publishing, Wallingford.

Fenner, F., and Marshall, I. D. (1957) A comparison of the virulence for European rabbits (Oryctolagus cuniculus) of strains of myxoma virus recovered in the field in Australia, Europe and America, Journal of Hygiene, 55, 149-191.
| Crossref | Google Scholar | PubMed |

Fenner, F., Day, M. F., and Woodroofe, G. M. (1956) Epidemiological consequences of the mechanical transmission of myxomatosis by mosquitoes, Journal of Hygiene, 54, 284-303.
| Crossref | Google Scholar | PubMed |

Fordham, D. A., Sinclair, R. G., Peacock, D. E., Mutze, G. J., Kovaliski, J., Cassey, P., Capucci, L., and Brook, B. W. (2012) European rabbit survival and recruitment are linked to epidemiological and environmental conditions in their exotic range, Austral Ecology, 37, 945-957.
| Crossref | Google Scholar |

Kaplan, E. L., and Meier, P. (1958) Nonparametric estimation from incomplete observations, Journal of the American Statistical Association, 53, 457-481.
| Crossref | Google Scholar |

Kerr, P., and McFadden, G. (2002) Immune responses to myxoma virus, Viral Immunology, 15, 229-246.
| Crossref | Google Scholar | PubMed |

Kerr, P. J., Perkins, H. D., Inglis, B., Stagg, R., McLaughlin, E., Collins, S. V., and Van Leeuwen, B. H. (2004) Expression of rabbit IL-4 by recombinant myxoma viruses enhances virulence and overcomes genetic resistance to myxomatosis, Virology, 324, 117-128.
| Crossref | Google Scholar | PubMed |

Kerr, P. J., Ghedin, E., DePasse, J. V., Fitch, A., Cattadori, I. M., Hudson, P. J., Tscharke, D. C., Read, F. A., and Holmes, E. C. (2012) Evolutionary history and attenuation of Myxoma virus on two continents, PLoS Pathogens, 8, e1002950.
| Crossref | Google Scholar |

Kerr, P. J., Cattadori, I. M., Liu, J., Sim, D. G., Dodds, J. W., Brooks, J. W., Kennett, M. J., Holmes, E. C., and Read, A. F. (2017) Next step in the ongoing arms race between myxoma virus and wild rabbits in Australia is a novel disease phenotype, Proceedings of the National Academy of Science U S A, 114, 9397-9402.
| Crossref | Google Scholar | PubMed |

Kerr, P. J., Eden, J-S., Di Giallonardo, F., Peacock, D., Liu, J., Strive, T., Read, A. F., and Holmes, E. C. (2019) Punctuated evolution of Myxoma virus: rapid and disjunct evolution of a recent viral lineage in Australia, Journal of Virology, 93(8), 10.1128/jvi.01994-18.
| Crossref | Google Scholar | PubMed |

Kerr, P. J, Cattadori, I. M., Sim, D., Liu, J., Holmes, E. C., and Read, A. F. (2022) Divergent evolutionary pathways of myxoma virus in Australia: virulence phenotypes in susceptible and partially resistant rabbits indicate possible selection for transmissibility, Journal of Virology, 96, e0088622.
| Crossref | Google Scholar | PubMed |

King, D. R. and Wheeler, S. H. (1979) ‘Ecology of the rabbit in Western Australia’, in Proceedings of the World Lagomorph Conference, eds K. Myers, C. D. MacInnes, University of Guelph, ON, Canada, pp. 858–869.

Liu, J., Fordham, D. A, Cooke, B. D., Cox, T., Mutze, G., and Strive, T. (2014) Distribution and prevalence of the Australian non-pathogenic rabbit calicivirus is correlated with rainfall and temperature, PLoS One, 9(12), e113976.
| Crossref | Google Scholar | PubMed |

MacLachlan, N. J. and Dubovi, E. J. (eds) (2016) ‘Chapter 7’, in Poxviridae Fenner’s Veterinary Virology, 5th edn, Academic Press, London.

Marshall, I. D. (1959) The influence of ambient temperature on the course of myxomatosis in rabbits, Journal of Hygiene, 57(4), 484-497.
| Crossref | Google Scholar | PubMed |

Marshall, I. D., and Fenner, F. (1958) Studies in the epidemiology of infectious myxomatosis of rabbits: V. Changes in the innate resistance of Australian wild rabbits exposed to myxomatosis, Journal of Hygiene, 56, 288-302.
| Crossref | Google Scholar | PubMed |

Marshall, I. D., and Fenner, F. (1960) Studies in the epidemiology of infectious myxomatosis of rabbits: VII. The virulence of strains of myxoma virus recovered from Australian wild rabbits between 1951 and 1959, Journal of Hygiene, 58, 485-488.
| Crossref | Google Scholar | PubMed |

Martin, C. J. (1936) Observations on Myxomatosis cuniculi (Sanarelli) made with a view to the use of the virus for the control of rabbit plagues, Council for Scientific and Industrial Research Bulletin No. 26. pp. 1–28.

Parer, I. (1995) Relationship between survival rate and survival-time of rabbits, Oryctolagus-cuniculus (L), challenged with myxoma virus, Australian Journal of Zoology, 43, 303-311.
| Crossref | Google Scholar |

Pirie, N. W. (1966) John Burdon Sanderson Haldane. 1892-1964, Biographical Memoirs of Fellows of the Royal Society, 12, 219-249 Available at http://www.jstor.org/stable/769532.
| Google Scholar |

Rendel, J. M. (1971) Myxomatosis in the Australian rabbit population, Search, 2, 89-94.
| Google Scholar |

Richardson, B. J, Phillips, S., Hayes, R. A., Sindhe, S., and Cooke, B. D. (2007) Aspects of the biology of the European rabbit (Oryctolagus cuniculus) and rabbit haemorrhagic disease virus (RHDV) in coastal eastern Australia, Wildlife Research, 34, 398-407.
| Crossref | Google Scholar |

Shepherd, R. C., and Edmonds, J. W. (1978) Myxomatosis: changes in the epidemiology of myxomatosis coincident with the establishment of the European rabbit flea Spilopsyllus cuniculi (Dale) in the Mallee region of Victoria, Journal of Hygiene, 81, 399-403.
| Crossref | Google Scholar | PubMed |

Sobey, W. R., and Conolly, D. (1971) Myxomatosis: the introduction of the European rabbit flea Spilopsyllus cuniculi (Dale) into wild rabbit populations in Australia, Journal of Hygiene, 69, 331-346.
| Crossref | Google Scholar | PubMed |

Strive, T., Wright, J., Kovaliski, J., Botti, G., and Capucci, L. (2010) The non-pathogenic Australian lagovirus RCV-A1 causes a prolonged infection and elicits partial cross-protection to rabbit haemorrhagic disease virus, Virology, 398, 125-134.
| Crossref | Google Scholar | PubMed |

Van Valen, L. (1973) A new evolutionary law, Evolutionary Theory, 1, 1-30.
| Google Scholar |

Ward, C. (2011) James Meadows (Jim) Rendel [1905-2001], CSIROpedia, https://csiropedia.csiro.au/rendel-james-meadows/, accessed January 2024.