Australasian Science: Australia's authority on science since 1938

It’s Evolution – But Not As We Know It

Cane toad

Perhaps some other process, not natural selection, is responsible for the evolved acceleration of the toad invasion.

By Rick Shine

The accelerating pace of the cane toad’s advance through tropical Australia has revealed a new mechanism of evolution.

Big ideas can appear when you least expect them, especially when you are busy working on some straightforward research project. That’s exactly what happened to me and my colleagues, Greg Brown and Ben Phillips, in the course of our ecological studies on the invasion of cane toads.

We discovered that the toad front has accelerated as it has travelled through Australia, and in trying to understand why we realised that the answer may lie in a new evolutionary process. The process – which we have dubbed “spatial sorting” – occurs in parallel with the mechanism of natural selection proposed by Charles Darwin, but it’s very different from anything that Darwin suggested.

The story began 75 years ago, when some agricultural scientists foolishly introduced giant South American cane toads to tropical coastal Queensland. The toads didn’t have much effect on the cane-eating beetles they were meant to control, but found Australia to their liking. They soon spread southwards along the coast into north-eastern New South Wales, and westwards across the Gulf of Carpentaria and through the Northern Territory. Last year they crossed the Western Australian border, and the toads are currently moving into the Kimberley.

The result has been devastating for some of the native animals that try to eat the toads, presumably mistaking them for native frogs. Australia doesn’t have any native toads, and the powerful defensive chemicals of cane toads have caused fatal heart attacks in many native predators.

Populations of several frog-eating predators have crashed when the toads have arrived, sometimes by more than 90% within a year. The worst-affected species are a marsupial (the northern quoll), goannas (especially the yellow-spotted monitor), bluetongue skinks, venomous snakes like king browns and death adders, and freshwater crocodiles in some areas.

I’m not really a toad biologist. Instead, I’ve spent most of my career studying the ecology of snakes. The main focus of my field studies on snakes is at Fogg Dam, a small floodplain in the Adelaide River region midway between Darwin and Kakadu National Park in the wet–dry tropics of the Northern Territory. My colleagues, students and I have conducted detailed research on a variety of snakes in this magnificent area for more than 20 years.

Cane toads were the last thing on my mind. I knew they were moving towards us, of course, but all the experts had predicted that toads wouldn’t reach the Darwin area for several decades – and I didn’t expect to be studying tropical snakes by then.

In about 2000, however, it became clear that the toads were going to reach Fogg Dam within about 5 years – much sooner than anyone had expected. This was terrible news in one sense – my beloved snakes were at huge risk if even half the stories about the impact of cane toads were true.

On the other hand, the toads’ impending arrival was an incredible research opportunity. With our 20 years of background data we could see what this noxious invader actually did to a complex tropical ecosystem.

I applied to the Australian Research Council for funding that would allow me – and my newly-expanded research group, which calls itself “Team Bufo” – to look at the toads’ biology and ecological impact in detail. We obtained the funding and were ready as the toads came closer.

Greg Brown was out driving and walking roads in our study area every night, and he found the first toad on 2 February 2005. They came in small numbers at first – by the end of the wet season in June 2005 he had only found 80 – but the trickle turned into an avalanche so that Greg had captured more than 1700 toads by June 2006.

Every one of those first few toads, and many thereafter, were fitted with waistbelts containing small radiotransmitters. We then released them so that we could see how far they moved and what habitats they used.

Greg did the tracking, and immediately discovered something very peculiar and utterly untoadlike. The cane toads at the invasion front were incredible long-distance athletes, often travelling almost 2 km per night when the ground was damp enough to allow them to travel.

No other toad in the world has been recorded to travel anything like these distances, and in Queensland, where they were first released, cane toads are pretty much stay-at-home creatures. They certainly wander about at times, sometimes making quite long moves, but tracking by Ross Alford and Lin Schwarzkopf from James Cook University had revealed that a Queensland toad moves less than 10 metres per night on average. Our Northern Territory toads were travelling ten times that far, and that’s why they got to Fogg Dam so much sooner than anybody had expected them to.

If toads have dramatically sped up in recent years then the rate they have invaded should have increased steadily during that period. Fortunately, that’s an easy prediction to test because a lot of people have gone to a lot of trouble to document the toads’ Australian invasion progress in great detail. And just as we’d expect from the behaviour of toads in different parts of their range, the rate that toads have spread has increased from around 10–15 km/year in the decades after toads were released, up to about 55–60 km/year now.

Are toads moving quickly now just because it’s easier to move through the Northern Territory than through Queensland? Ben Phillips tested that idea by catching toads from sites across the toads’ Australian range and tracking them at our Fogg Dam study area.

The Cairns toads didn’t move anything like as far as toads collected from the invasion front, so it was something about the toads and not the landscape.

John Llewelyn showed that the toads collected from the invasion front were more athletic (they had much better stamina). Long-legged animals dominated the invasion front and travelled further each night than shorter-legged toads.

Could we really have evolved a long-legged, athletic toad from a couch potato ancestor in just 75 years? For that to be true, the characteristics would have be genetically based rather than just induced by local conditions.

So Ben Phillips took on the herculean task of breeding toads from each of the populations, then raising their offspring under identical conditions at Fogg Dam. Sure enough, when the toads were old enough to radio-track, Ben found that the offspring resembled their parents in dispersal rates. The mobile toads from the Territory produced mobile progeny, whereas the couch potatoes from Queensland produced offspring that would rather sit around than disperse.

So we really do have a case of the evolution of rapid dispersal in only 75 years. But why?

The only mechanism that modern biology can offer to explain such a directional evolution is natural selection, an idea that really hasn’t changed too much since Charles Darwin first suggested it in 1859. Darwin pointed out that if individuals vary in some characteristic (like dispersal rate), and some of those variations make an individual more likely to survive and reproduce, then we’d expect to see those variations become more and more common in the population. Any other characteristics that made organisms less likely to survive and reproduce would gradually disappear because there were fewer and fewer individuals with those traits each generation.

Under this explanation, the reason that faster dispersal has evolved in Australian cane toads is because the individual toads that moved fastest got some kind of advantage as a result. Perhaps toads at the very front of the invasion get access to more food because there are few other toads around to compete with them for all those juicy bugs? So, goes the argument, slow toads are less likely to survive and breed, and we see the evolution of faster and faster toads, all of them hurtling westwards across tropical Australia to boldly go where no toad has gone before.

This is all possible, and natural selection has proven to be incredibly powerful at causing evolution, but we started to wonder if there might be another explanation. The point that made us stop and think was whether or not toads get any individual benefit in survival and/or reproduction from being quicker than other toads.

We don’t seem to see such benefits. A toad on the frontline may well get a bit more food than those further back, but it also is exposed to more predators.

Remember that the toads kill many of the predators as soon as they arrive because the toad is so toxic that the predator dies of a heart attack. But many other predator species don’t die, and therefore remain common, but they soon learn that toads make a terrible meal and leave them off the menu.

This means that the risk of being killed by a predator is much higher for toads on the frontline. Indeed, our radio-tracking showed that the faster a toad moved, the more likely it was to get killed.

Cathy Shilton, a veterinary pathologist who works with Team Bufo, noticed another peculiar thing that suggests it isn’t all fun for a toad at the invasion front. Cathy found very high rates of extreme spinal arthritis in the toads at the front – especially the fast-moving, long-legged ones.

We think that these animals have weakened immune systems, so they can’t fight off bacteria that help to cause arthritis in inflamed joints. Basically, these toads just aren’t built to be long-distance runners, and their bodies are collapsing under the strain.

Furthermore, we haven’t seen much reproduction by the invasion-front toads – they are so busy racing through the study area that they rarely stop to spawn. It’s really pretty strange. The Fogg Dam floodplain looks like Toad Heaven – with lots of water, and lots of bugs to eat – yet these invasion-front toads just keep moving through without stopping.

In combination, these observations made Greg, Ben and I wonder if maybe there wasn’t any advantage to dispersing faster. Perhaps some other process, not natural selection, was responsible for the evolved acceleration of the toad invasion.

The problem was that just about every biologist thinks that natural selection is the one and only mechanism that causes directional evolutionary change. Fortunately, Ben’s familiarity with mathematical modelling brought to light another possibility that had been talked about by mathematicians but had never been seriously considered as a genuine alternative to Darwin’s idea of natural selection. Indeed, the idea was so poorly understood that it didn’t even have a name. We’ve called it “spatial sorting”.

The idea runs like this. The toad’s invasion across the Australian tropics has been a footrace. The toads were released on the east coast and have been spreading west ever since. At the end of each generation, the individuals at the frontline will be the ones that have travelled furthest. Toads that have moved more slowly, or have travelled in circles, are left behind.

From Ben’s toad-breeding research we know there is a genetic basis to variation in dispersal rates among toads. This means that genes that make toads quicker – say, by influencing speed or directionality of movement – will end up accumulating at the invasion front. Genes for being a slowpoke will be left behind in the long-colonised areas of the toads’ range.

The same spatial sorting of genes will occur every generation. Every new mutation that makes toads move more quickly will find its way to the front while every mutation that slows toads down will drop back from the front.

This process is cumulative. At the frontline, the fastest male toads breed with the fastest female toads because there are no slowpokes to breed with as they are all many kilometres further back. So at least some of the resulting baby toads will inherit fast-dispersal genes from both mum and dad, and thus be even quicker than their parents.

Unlike Darwin’s idea of natural selection, this process doesn’t require faster dispersal to be an advantage to any toad so it’s very different from anything that Darwin talked about. Genes become sorted non-randomly through space rather than changing in relative frequency through time.

Our ideas about “spatial sorting” were recently published in the Proceedings of the National Academy of Sciences, and our paper is making many evolutionary biologists contemplate the idea that natural selection isn’t the only process capable of causing evolutionary change.

Natural selection has ruled the roost for 150 years, ever since Darwin suggested it, and there’s no doubt that it’s the major mechanism that has created the diversity of life on Earth today. However, the cane toads’ accelerating march across tropical Australia suggests that natural selection may not be the only process that can cause evolution.

The much-reviled cane toad may end up as the poster boy for spatial sorting, just as the Galapagos finches are an enduring symbol of Darwin’s ideas about natural selection.

Rick Shine is a Professor in Biology at the University of Sydney.