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Myxoma virus and Rabbits in Australia

Overview:

Summary

In the 1700s, European colonialists brought rabbits from Europe to Australia. While their goal was to establish a small rabbit population for hunting, the population of rabbits quickly exploded. The local ecology was devastated, including farms. In response, Australia has tried to control the rabbit population through various measures. One such measure was a form of biological warfare. In the 1950s, Australian officials infected rabbits with a virus, hoping that it would kill off the invasive species.

Myxoma virus is a poxvirus that is able to infect both South American and European rabbits. South American rabbits (Tapetis) are commonly infected by the Myxoma virus in the wild. When infected, Tapetis show few symptoms. However, the same is not the case for European rabbits. European rabbits infected with Myxoma virus experience skin tumors, fevers, fatigue, and death. In short, the virus is much more virulent in European rabbits than in South American Tapetis. Upon making this discovery, scientists decided to infect wild European rabbits in Australia with the virus.

The release of the virus was initially very successful. The rabbit population dropped from 600 million to 100 million rabbits within a couple of years. In fact, 99% of rabbits that became infected with the virus in the year after it was released died within a few weeks of becoming infected. However, after this initial success, the plan flopped. More and more infected rabbits started to survive infection. The population stopped declining and started growing again. What happened?

Coevolution

When the scientists released Myxoma virus into the rabbit population they introduced a new selective pressure to the rabbit population, driving the evolution of resistance in the rabbit population. While most rabbits died, any rabbit that managed to survive infection, or avoid it altogether, were left to reproduce. Any genetic variants in these rabbits that that had contributed to their ability to survive the virus became more common over time.

However, the rabbits were not the only population to evolve. Just as their coexistence with the Myxoma virus drove evolution in the rabbit population, coexistence with rabbits led to evolution the Myxoma virus. This coevolution between Australian rabbits and the Myxoma virus has not been simple, though. Understanding how these two populations have influenced each other’s' evolutionary trajectories - and ultimately why rabbit populations are still flourishing in Australia to this day- requires discussing one more layer of evolutionary complexity: virulence-transmission trade-offs.

Virulence-Transmission trade-offs

When considering natural selection in viruses, two aspects of the viral lifecycle are particularly important. The first is a virus’s ability to replicate within their host. The second is the virus’s ability to transmit from one host to another. In some cases, traits that improve a virus’s ability to replicate within the host interferes with its ability to transmit between hosts, and vice versa. To the extent that this is true, it is often said that a virulence-transmission trade-off exists. This type of trade-off plays an important role in the coevolutionary history between Myxoma virus and rabbits in Australia.

Upon its initial release, the Myxoma virus was extremely virulent. It had a case fatality rate approaching 100%, meaning the virus killed nearly every rabbit it infected. This death was rapid. Infected rabbits often died within 20 days of becoming infected. However, the rapid death caused by the virus was not necessarily good news for the virus. The reason for this has to do with how the Myxoma virus transmits from rabbit to rabbit. The Myxoma virus is transmitted by mosquitos, making the likelihood of transmission dependent on how often mosquitos bite infected rabbits. One way to increase the likelihood a mosquito bites an infected rabbit, and thus the likelihood a virus transmits to a new host, is to increase the total number of days a rabbit is infectious. Unfortunately for the virus, mosquitos don’t bite dead rabbits, and the quick deaths caused by the virus limited its ability to transmit.

The evolution of resistance to Myxoma was not the only reason the scientists’ rabbit eradication plan failed; ongoing selection for less virulent viruses that were better at transmitting between hosts also contributed to a drop in case fatality rates. The scientists’ controlling agent lost its efficiency.

The virus did not become completely harmless, though. Understanding why requires thinking about the selective pressures that exist when a virus replicates inside of its host. All else being equal, a virus that replicates quickly causes more damage to the host than one which replicates more slowly. Unfortunately for the host, natural selection favors faster replication. Thus, while selective pressures on transmission drive virulence down, selective pressures that take place within the host drive it up. The necessity to balance these two fitness components has led to a constant selective force toward an optimal virulence, one that is neither too high nor too low.

Cultural practices

Australian officials would have benefited from more evolutionary knowledge before deciding to release the virus into the wild. There are currently around 200 million rabbits in Australia; this rabbit population is still dealing with the Myxoma virus that was released 70 years ago. Perhaps a more complex plan that took coevolution and virulence-transmission trade-offs would have promoted better population control. In this case, hindsight is 20/20. However, many modern-day plans for large scale interventions require evolutionary knowledge foresight into how these plans may fail. Unfortunately, a sufficient appreciation of evolution is often lacking.

Principles this example illustrates:

Coevolution and Trade-offs:

The complexity of this coevolutionary dynamics between the Myxoma virus and rabbits scales quickly. This complexity offers an opportunity to ask students to work through problems that forces them to consider how coevolution between the virus and rabbits might change under different scenarios. For example, the optimal virulence for Myxoma virus is not actually a single value. Instead, it varies across time and space. It will change based on different ecological parameters. Students can be asked to consider how optimal virulence may change over time as rabbit populations evolved greater viral immunity? This question could be pushed to have students tie proximate mechanisms to ultimate outcomes by having them consider different mechanisms that could grant greater viral immunity (e.g. mechanisms that interfere with transmission in different ways). Students can also be asked to consider other ecological parameters important to this process, like mosquito ecology. Specifically, how might optimal virulence change as mosquito populations change? Students can be pressed further to consider how climate change might impact mosquito ecology, and consider how climate change may alter host-pathogen coevolution for the Myxoma virus as well as other pathogens.

Cultural practices:

The story of Australian rabbits and the Myxoma virus illustrates how evolution can interfere with best-laid plans, especially when those plans fail to consider evolution. Students can be asked to consider other interventions and evaluate whether evolution would lead to failure. Further, they can evaluate potential ways to make the intervention work. Some examples of interventions students can consider are: phage therapy for treating bacterial infections, the release of genetically modified mosquitos to combat disease transmission, or the use of insecticides.

Study design:

While not discussed above, the research that determined the coevolution of greater immunity in rabbits and lower virulence in the virus is an elegant system that can be helpful for students to learn study design. In brief, researchers sampled Myxoma virus from wild rabbits each year and stored them. Years later, they evaluated the virulence levels of their virus samples by infecting laboratory rabbits and examining how virulence changed each year. Students can consider what ‘control’ is when it comes to a research study, and why this procedure was necessary. Similarly, students can be asked about ways in which they could confirm whether rabbits evolved greater immunity over time.

Additional resources:

Readings

  1. http://science.psu.edu/news-and-events/2017-news/Read8-2017
  2. https://www.the-scientist.com/multimedia/infographic-evolving-virulence-30813
  3. https://www.the-scientist.com/features/do-pathogens-gain-virulence-as-hosts-become-more-resistant-30219
  4. https://www.theatlantic.com/science/archive/2017/08/rabbit-virus-arms-race/536796/

Videos


Journal articles

  1. Alves, J. M., Carneiro, M., Cheng, J. Y., de Matos, A. L., Rahman, M. M., Loog, L., ... & Strive, T. (2019). Parallel adaptation of rabbit populations to myxoma virus. Science363(6433), 1319-1326.
  2. Kerr, P. J., Cattadori, I. M., Liu, J., Sim, D. G., Dodds, J. W., Brooks, J. W., Kennett, M. J., Holmes, E. C., & 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 Sciences of the United States of America114(35), 9397–9402. https://doi.org/10.1073/pnas.1710336114

  3. Fenner, F. J. (1983). The Florey Lecture, 1983-Biological control, as exemplified by smallpox eradication and myxomatosis. Proceedings of the Royal Society of London. Series B. Biological Sciences218(1212), 259-285.

Teaching materials:

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