Thursday, 30 January 2014

Myxy Sticks, Rabbits And Rapid Evolution

When I was a child of about 10 or 11, the English countryside saw one of the most impressive cases of rapid evolution yet witnessed in a wild mammal. It took just about ten years. It was also witnessed in Australia and the rest of Europe. It was how the European rabbits (Oryctolagus cuniculus) and the myxoma virus co-evolved to accommodate one another.

I remember still how during the first onslaught of rabbit myxomatosis the countryside suddenly became full of pathetic 'myxy' rabbits staggering blindly (and deafly) about, their eyes and ears swollen and closed with hideous pustules, completely lost and disorientated to be squashed by cars, killed by dogs and cats and dispatched mercifully by us humans who carried our 'myxy sticks'. The foxes had a heyday and their population exploded for a year or two. I once killed twenty rabbits in the corner of a single field in a few minutes. You had to be careful how you handled a myxy stick as the wrong end was a gory, pusy mess. You could easily spot a distant myxy rabbit because the swelling exposed the pale under-fur making it look like they had pale bases to their ears and pale stripes over their eyes.

It looked for a while as though the ubiquitous rabbit, the farmers enemy and the friend to every villager who had a family to feed and who knew how to set a snare or work a ferret, was about to disappear forever. With a good ferret, if you knew where the best burrows were, you could get enough rabbits in an hour to feed a family for a week - and I knew the countryside around my small village like I knew the back of my hand. I also knew who I could sell a brace of rabbits to for a shilling each. I could skin, gut, and quarter up a rabbit in about ten minutes. By next year the burrow would be full of rabbits again as each female could rear a batch of half a dozen young every three months and the young would be breeding themselves almost before the next batch had left the nest. You had to know which burrows were ready for the next rabbit harvest.

During World War II when meat was rationed, many an English country family eked out their rations with rabbit stew.

Then myxomatosis looked set to end all that for ever.

Baby rabbits with eyes full of pus
This is the work of scientific us.

Spike Milligan
The myxoma virus is a poxvirus which caused an innocuous localised skin fibroma in two American relatives of the rabbit (Sylvilagus brasiliensis and Sylvilagus bachmani) but in O. cuniculus it is (or was) systemic and rapidly fatal. It is passed on in Europe by the rabbit flea - a species unique to rabbits and which pass between rabbits when they mate. Most English rabbits will have hundreds of fleas living on them. (How the rabbit flea coordinates it's reproduction with that of the rabbit is an interesting story in itself, but it must wait for another day).

Despite official denials, myxomatosis was deliberately introduced in Britain. With the vector being the rabbit flea, it could not have crossed the English Channel from France. Interestingly, the then owner of Lundy Island in the Bristol Channel had tried to introduce it to the island by putting a rabbit dead from myxomatosis down a rabbit burrow. It failed to take hold because, for some reason, Lundy Island rabbits have no rabbit fleas. On the mainland it's spread was rapid and devastating. Woods and fields soon became littered with the bleached bones of dead rabbits. Soon every field where once you could be sure of lifting your baby brother or sister up to see over the wall and watch the rabbits run for cover, was empty save for little clusters of white bones. And the fox population crashed accordingly.

Then, seemingly almost by magic there were a few rabbits again; then more. Then another wave of myxy wiped them out. The rabbits and the myxoma virus seemed to be finding some sort of balance. A few rabbits would be left to breed then, when the population built up, myxy would come and knock it back down again.

But gradually, rabbits gained the upper hand, each wave of myxomatosis seemed to take fewer and fewer until a myxy rabbit was a rarity - almost something to talk about. Soon the corners of fields were filled with rabbits and the old deserted burrows were re-inhabited. But now almost no-one in the countryside would look at a rabbit as something for the pot. The sight of myxy rabbits put people off eating them even though the myxoma virus is harmless to humans. No one would risk eating them and they dropped off the radar as a food source. You'd be hard-pressed now to find a 10 year-old who can work a ferret or skin and gut a rabbit in a few minutes. You'd probably be hard-pressed to find parents who would let them or could even teach them to.

The same thing was seen in Australia where European rabbits had been introduced. During the voyage there it seems they had lost their flea population but the virus vector was a species of mosquito which was enjoying an abundant new supply of blood as rabbit numbers ballooned, reaching plague proportions and seriously competing for grass with the sheep.

How this happened is one of the best illustrations of co-evolution between two species:

Myxoma virus is a poxvirus naturally found in two American leporid (rabbit) species (Sylvilagus brasiliensis and Sylvilagus bachmani) in which it causes an innocuous localised cutaneous fibroma. However, in European rabbits (Oryctolagus cuniculus) the same virus causes the lethal disseminated disease myxomatosis. The introduction of myxoma virus into the European rabbit population in Australia in 1950 initiated the best known example of what happens when a novel pathogen jumps into a completely naïve new mammalian host species. The short generation time of the rabbit and their vast numbers in Australia meant evolution could be studied in real time. The carefully documented emergence of attenuated strains of virus that were more effectively transmitted by the mosquito vector and the subsequent selection of rabbits with genetic resistance to myxomatosis is the paradigm for pathogen virulence and host-pathogen coevolution. This natural experiment was repeated with the release of a separate strain of myxoma virus in France in 1952. The subsequent spread of the virus throughout Europe and its coevolution with the rabbit essentially paralleled what occurred in Australia. Detailed molecular studies on myxoma virus have dissected the role of virulence genes in the pathogenesis of myxomatosis and when combined with genomic data and reverse genetics should in future enable the understanding of the molecular evolution of the virus as it adapted to its new host. This review describes the natural history and evolution of myxoma virus together with the molecular biology and experimental pathogenesis studies that are informing our understanding of evolution of emerging diseases.

Kerr PJ., Myxomatosis in Australia and Europe: a model for emerging infectious diseases;
Antiviral Res. 2012 Mar;93(3):387-415. doi: 10.1016/j.antiviral.2012.01.009. Epub 2012 Feb 8.

Under intense selection pressure, those few rabbits with an inherited genetic resistance survived to produce offspring carrying that genetic resistance. Meanwhile, under the selection pressure of increasing resistance, the myxoma virus also evolved and attenuated, making it more easily transmitted. Keeping it's host alive was a better strategy than killing it quickly before it could infect more rabbits, because that produced more copies of myxoma viruses. The same thing would have been seen in the world human population in response to the devastation of the Black Death in the Middle Ages. We evolved resistance and the bacillus causing it attenuated.

It almost goes without saying that the only known natural mechanism which can cause host and parasite species to accommodate one another like this is natural selection acting on small variations in the genome, so automatically favouring the variations which produce most descendants, and so increasing its frequency in the population gene-pool, no matter how unlikely that variation was to arise by chance in the first place.

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  1. I seem to recall that among the rabbit population of Cheshire a small number of animals tended not to burrow but to bed down amongst dense vegetation. These, we kids believed, were the ones which escaped the myxy onslaught. Do you know if there is any truth in this rudimentary attempt at scientific observation?

    1. Rob.

      I remember hearing that myself at the time in Oxfordshire. I don't know if it was true or just someone's guess, but I would have expected this changed behaviour to have become the norm if it accounted for survival under the circumstances, so it seems unlikely to me. I'm open to persuasion, though

    2. Were those rabbits or hares? Hares don't burrow, do they?

      I'd like to ask just why myxomatosis was deliberately introduced into England. After all, rabbits weren't an invasive foreign species, nor did they actually threaten agriculture to any significant extent, did they?

      The evolution of Plasmodium to be able to cope with anti-malarial drugs would probably fit into the recent rapid evolution extravaganza...

    3. Rabbits were a serious agricultural pest. They were an ancient introduced species, probably by the Romans but they were semi-domestic until about the 1400's and were kept in specially constructed warrens consisting of a wall built around a sandy bank in which they burrowed. For some reason they didn't become established as a wild species in Britain until then. The reasons why are not fully understood and may have been involved genetic change. I think they originated in Spain, Portugal and North-West Africa.


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