IM Interview - The Great Accidental Evolution Experiment

The scoop: Natural selection and evolution are in overdrive in some parts of Australia. Evolutionary biologist Rick Shine of the University of Sydney never expected to be in the middle of one of the most amazing – and totally accidental – evolutionary experiments in the world. But he is. His darling snakes and lizards are evolving at rates never before thought possible beyond bacteria. The cause: The invasion of toxic cane toads. A few years ago the hopping menace of eastern Australia reached his long-time field study area just outside of Darwin. What has happened since has global implications for wildlife.

LarryO': You work is on snakes, ecology and evolution, is that correct?

Rick Shine: Yes, I grew up as one of those terrible little boys that carried lizards around in their pockets, and graduated to snakes when I got to high school.

I never got over my fascination with reptiles, and I've conducted research on the ecology and evolution of snakes throughout my career - mostly in the field rather than the laboratory.

LarryO': How did you get involved in the cane toad matter?

Rick Shine: I'm a passionate believer in the importance of long-term ecological studies if we are to ever really understand how natural ecosystems operate - and especially, address processes only accessible for study with long-term data sets.

Climate change is an obvious example. So, early in my career - in the early 1980's - I set up a study on snakes of the Adelaide River floodplain in the tropical Northern Territory - quite close to the city of Darwin.

The wet-dry tropics are fantastic for reptile diversity and abundance, and I and my co-workers conducted a diverse array of studies over a couple of decades.

But then the cane toads arrived.

There are no native toads in Australia, but cane-growers brought the South American cane toad Bufo marinus to eastern Australia in 1935, and released these large warty beasts in the hope that they would eat beetles threatening the sugar cane crop. The toads were a failure at that job, but thrived and soon began expanding their range. They now cover most of topical Australia- and reached my study site near Darwin in 2004.

Because Australia doesn't have any native toads, the chemical defences - poisons - produced by cane toads are different from those produced by native frogs.

So, if a frog-eating Aussie snake grabs a toad by mistake, he's likely to be a dead snake very quickly. With the huge background data on the ecology of this system, my study rapidly expanded to include the impact of the invasive toads on my beloved snakes.

LarryO': So what happened to your snakes when the toads arrived?

Rick Shine: Like most things in science, it all turned out to be more complicated than we had guessed beforehand.

A lot of the snakes were not really affected - they simply recognized that toads were not the same as frogs, so left them alone. Other snakes tried to eat toads - and a few of of them turned out to be capable of dealing with the toad's poison, and lots of others couldn't. But the snakes that foolishly tried to eat toads didn't necessarily die - some did, but others spat out the toad, and rapidly learned not to eat them.

So in the end, we were left with a relatively small number of predator species that were at real risk of dying in large numbers when the toads arrived.

The chief victims were big lizards (especially goannas, or monitor lizards), and some of the venomous snakes, like King Browns and Death Adders. For some of these guys, the toads were a catastrophe - predator populations decreased by about 90 percent in a few species, and it was common to find a freshly-dead snake or lizard lying in the bush with a toad in its mouth.

Fortunately, many of those super-vulnerable species seem to recover populations pretty quickly. In areas where toads have been present for 50 years or so, the goannas and some of the snakes have made impressive comebacks. Ben Phillips' work shows that blacksnakes have changed, for example, in at least three ways that render them safe in the presence of toads.

First, the snakes have evolved not to eat toads - snakes from toad-infested areas still happily munch a frog if given the chance, but leave toads alone. We can't teach blacksnakes to do this in the lab, so it seems to be a "hard-wired" - genetically-based - response.

Second, the snakes from toad-infested areas are more resistant to the toad's poisons.

And third, snakes from toad-infested areas tend to have small heads compared to their body size, relative to the same species of snake from areas where toads don't occur.

Basically, if you're a small-headed snake you can't swallow a toad big enough to kill you - so evolution has favoured a head-size reduction as the toads arrived.

LarryO': What has this taught us about how quickly animals can adapt to changes?

Rick Shine: Yep. It's classical Natural Selection, just as Charlie Darwin envisaged.

So long as you've got variation within the predator species - say, in whether or not you try to eat a toad - and that variation is heritable (genetically based), we're likely to see rapid evolutionary change if the pressure is strong enough. In the case of blacksnakes and toads, it's all pretty clear.

When the toads arrive, most snakes try to eat the toads, and those animals die. The only snakes that survive are the ones that - by pure genetic accident - have genes that say "don't eat toads".

We've actually measured selection on this trait in our study population of Death Adders - the individual snakes that try to eat a toad in captivity are the ones most likely to die after we release them into a floodplain containing toads.

So, in that case the only snakes that are still alive a year or two after toad invasion are the ones that have genes telling them not to eat toads.

They breed, their offspring inherit that dietary specialisation, and after a few generations the population recovers - but their behaviour has shifted in a way that enables them to deal with this new challenge.

LarryO': Does this give you any hope regarding species threatened by climate change? Or is that an entirely different matter?

Rick Shine: I've become a bit more upbeat about the resilience of natural systems, I have to admit.

The speed of the predator's adaptive response to toad invasion is quite remarkable. I'm sure the same kind of thing will happen with climate change - but whether that change in climate occurs slowly enough, or there is enough genetic variation to really aid survival in a world that changes in this way, are tough issues.

Presumably some species will flourish, others will disappear, and the ones in the middle will start adapting. Some of them may change fast enough to cope, and others not. It's a huge unplanned experiment, and it would take a real optimist to predict we won't seem some pretty awful casualties.

LarryO': Experiments on top of experiments. Has this all changed your research direction?

Rick Shine: Absolutely!

Basically, evolution started to permeate our thinking... maybe we need to incorporate an evolutionary perspective in thinking about the impact of threatening processes (like cane toads or climate change), not just the conventional steady-state "ecology" approach. So the data on predator evolution made us look a bit more closely at the toads themselves - and sure enough, they provide an even more dramatic example of rapid evolutionary change.

Cane toads were released in eastern Australia in 1936, and have sprinted westwards across the continent - they are now most of the way across. That's basically one giant footrace - and so we might expect that evolutionary pressures would be at work - favouring characteristics that enable toads to invade faster than their fellow toads.

If so, the invasion front should consist of toads with distinctive shapes and behaviors that enable them to disperse more quickly - and that's exactly what's happened.

The invasion-front toads not only are bigger than the ones in "old" population established many years ago - the invasion-front toads also have much longer legs (which makes them quicker) and they are much more active animals.

Radio-tracking shows that invasion-front toads often travel a kilometre or more each night, whereas the toads on the east coast tend to sit around and not move anything like as much.

So evolution has modified the toads as well as their victims, and I suspect that close attention will reveal similarly dramatic evolutionary shifts in many issues that have traditionally been thought of as "ecological" not "evolutionary" questions.

LarryO': Sounds like I should check back in with you for updates. I'll let you get on with it then. Thanks very much for your time today.

Rick Shine: No probs. Cheers, Rick

Article posted March 2, 2009.