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DNA Analysis Solves the Mystery of the Rabbit Invasion of Australia

COVID and monkeypox seem to have come out of nowhere and exploded across continents. But the phenomenon of natural selection acting on genetic variants – of viruses or organisms – that have an advantage in a certain place and time is ages old. The rabbits of Australia provide a powerful example of natural selection run amok, favoring a particularly robust mix of domestic and wild traits against an environmental backdrop of plenty of food and a paucity of predators.

The animals that have overrun the continent eat almost any plant, their appetites reverberating along food webs, costing an estimated $200 million a year. Over decades, interventions to control their numbers – from rabbit-proof fences to intentional infections with nasty viruses to shooting – have all failed. “In Australia, the rabbit has survived drought, fire, flood, diseases, predators, poisons and other stratagems devised by man and remains this country’s most serious vertebrate pest,” wrote Brian Coman in “Tooth and Nail: The Story of the Rabbit in Australia.”

Now researchers from the University of Cambridge and CIBIO Institute in Portugal have wed genetics to history to illuminate the precise source of Australia’s problem. Their report is in the Proceedings of the National Academy of Sciences.

“The colonisation of Australia by the European rabbit is one of the most iconic and devastating biological invasions in recorded history. Here, we show that despite numerous introductions over a 70-year period, this invasion was triggered by a single release of a few animals that spread thousands of kilometres across the continent,” the researchers write.

Feral rabbits – once-domestic animals relocated, where novel behaviors emerge – remain a problem in Australia, where they number more than 150 million. It’s an interesting mammal, in terms of the relationships to us. “The rabbit has, in various times and places, been a treasured pet, a commercial farm animal, a valued subject of the hunt, a major ecological force and an economic pest,” wrote Coman, to which I’d add a valuable model organism in the lab.

Thirteen Rascally Rabbits

The rabbit invasion of Australia began with a mixing of genomes – sex – among 13 animals shipped from England in 1859. But those weren’t the first rabbits – just the first to take over.

Historical records trace the pioneer rabbits to 1788, when the First Fleet of 11 ships – six convict transports, three ships of goods, and two Royal Navy vessels – brought the founding European and African settlers from Portsmouth, England, to Botany Bay, New South Wales. Among the 1400 humans were five silver grey domestic bunnies. These pets were taken to Sydney, supposedly never released into the wild.

At least 90 times after that, domestic rabbits came to Australia, but the populations stayed small. Then in 1859 wild rabbits nosed into a shipment of domestics and all hell broke loose.

The animals spread 100 kilometers a year for the next half-century, munching their way through native plants and starving the indigenous herbivores and then carnivores that had evolved there over millions of years. The new genetic analysis reveals that it was specific genes that spawned the fastest colonization rate for an introduced mammal ever recorded.

What happened in and after 1859 to propel these particular wild rabbits into reproductive overdrive? DNA provides the answer. But first, more backstory.

Local lore as well as the historical record trace the origin of Australia’s ‘rabbit plague’ to Thomas Austin, master of the Barwon Park estate Winchelsea, southwest of Melbourne.

On October 6, 1859, Thomas’s brother William, who lived at the family estate in Baltonsborough, Somerset, England, sent the 13 rabbits to Australia. It was a mixed bunch. ”Wild rabbits were by no means common ‘round Baltonsborough. It was only with great difficulty that he managed to get six; these were half-grown specimens taken from their nests and tamed. To make up the number he bought seven grey rabbits that the villagers had kept in hutches, either as pets or to eat,” recalled William’s granddaughter Joan Palmer. Eighty days later, on Christmas, two dozen rabbits arrived in Australia – they’d clearly bred on the journey.

The domestic and wild rabbit genomes mixing on this particular trip from England brewed a gene combination that enabled the animals to explode in numbers once let loose into the vast new land full of food from the new pastoral practices. One such trait from the domestic camp was the colored coat that provided protection across the land, and the burgeoning rabbit population came to be called “the grey blanket.”

Within three years, the animals had expanded to thousands. In 1865, Austin killed 20,000 rabbits at his estate, alarmed by the “extraordinary fecundity of the English rabbit.” A year later, hunters bagged 14,000 more there.

“Austin’s rabbits” spread, finding plentiful food and no predators. From 1880 to 1894, they took over New South Wales, Queensland, and Western Australia. An article from the National Museum Australia provides context: It took rabbits 700 years to spread throughout Britain, but 50 years to colonize two-thirds of Australia, which is about 25 times larger.

By the late 1940s the animals numbered 600 million, despite many people eating them during the depression and war years. Robust harvests following abundant rainfall fed the rabbits, while men who could build more fences were in short supply.

DNA Analysis Reveals 5 Founding Females – Echoing History

The researchers sequenced the exomes (the protein-encoding parts of the genome) of 187 rabbits. Most were wild, from Australia, Tasmania, and New Zealand, but a few were from France and Britain. The analysis included nearly 2 million gene variants.

The animals had been caught between 1865 and 2018. They’d become pests in New Zealand and Tasmania in the decades following their introduction too. The common denominator among the Australian, New Zealand, and Tasmanian rabbits, the investigators conclude, “was the arrival of a new genotype that was better adapted to the natural environment,” which is arid and semi-arid.

“We managed to trace the ancestry of Australia’s invasive population right back to the South-West of England, where Austin’s family collected the rabbits in 1859. Our findings show that despite the numerous introductions across Australia, it was a single batch of English rabbits that triggered this devastating biological invasion, the effects of which are still being felt today,” said lead author Joel Alves.

The genetic diversity of the rabbits fell as the animals migrated away from Barwon Park and natural selection favored the gene variants that accelerated growth and fitness. In the lexicon of Darwin, “fitness” means reproductive success.

If an environmental change beginning in 1859 was the only force that had spurred the rabbit population explosion, such as agriculture, then several small rabbit populations would have expanded across the continent. But the petering out of pre-1859 rabbits and the new DNA evidence argue against that explanation, pointing to a single event that led to a hardy, adaptive genome.

What traits could have propelled the rabbits’ success? Animals introduced earlier had the hallmarks of pets: floppy ears, complex coat coloring, and tameness. But Austin’s rabbits also brought in a combination of traits that conferred a changed body shape that enabled the animals to withstand a much greater temperature range – which enabled them to take over and eat nearly any plant. The historical record indicates that Austin’s rabbit shipment was the only one to include wild animals.

Even more compelling evidence comes from analysis of mitochondrial DNA, which is passed from mothers to all offspring. Remember “mitochondrial Eve” from 1987? She was the theoretical most recent woman from whom all living humans descend, deduced from comparing mitochondrial DNA from 147 people from 5 diverse populations. Similar analysis of rabbit mitochondrial DNA indicated 5 female rabbits having seeded the millions of invasive descendants – and that matches, precisely, the historical record of Austin’s original 13 rabbits, which included 5 wild females.

In all my years of science writing, I can’t think of a more elegant example of converging genetic and historical evidence.

What happened after Austin’s rabbits reached Australia was a phenomenon called “allele surfing.” An allele is an older term for gene variant. When the alleles conferring grey color and a svelte body came to Australia, the geographic expansion triggered a sudden amplification of the alleles conferring these traits because the characteristics were, and continue to be, so adaptive. In other words, alleles that were rare in the ancestral British population exploded under the environmental conditions in Australia.

Summed up Alves:

“More than 150 years have passed since Thomas Austin asked his brother to send him some wild rabbits from their family property in England. Unbeknown to him, this request caused a cascade of events that changed forever the landscape of an entire continent and resulted in the greatest pastoral pest of the 20th century.

These findings matter because biological invasions are a major threat to global biodiversity and if you want to prevent them you need to understand what makes them succeed. Environmental change may have made Australia vulnerable to invasion, but it was the genetic makeup of a small batch of wild rabbits that ignited one of the most iconic biological invasions of all time. This serves as a reminder that the actions of just one person, or a few people, can have a devastating environmental impact.”

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