Shine Lab

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Scientific Publications

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The cane toad invasion

2006

Phillips, B. L., G. P. Brown, J. Webb, and R. Shine. 2006. Invasion and the evolution of speed in toads. Nature 439:803.

In the first few decades after toads were released in Queensland, they expanded their range at about 10 km per year. That rate then began to increase, and now averages about 55 km per year. We show that toads with relatively long legs (compared to their body length) move faster and further than shorter-legged toads of the same body size; and that the invasion front is composed of very mobile, long-legged toads. Thus, toads have changed dramatically, through rapid evolution, in the course of only about 50 generations in Australia.

toad with 5 legs

Brown, G. P., B. L. Phillips, J. K. Webb, and R. Shine. 2006. Toad on the road: use of roads as dispersal corridors by cane toads (Bufo marinus) at an invasion front in tropical Australia. Biological Conservation 133:88-94.

As noted above, invasion-front toads are in a real hurry to move, and so don’t waste their time struggling through thick vegetation. Instead, they take advantage of the roads (and cattle paths, etc) that we humans have so thoughtfully provided for them. Most of our radio-tracked toads zipped along the highway rather than moving through dense vegetation. When they reached crossroads, their paths of movement often took a right-angle turn because they would rather follow roads, even if the direction isn't exactly perfect, than try bashing through the scrub. By the way, this also means that people tend to overestimate the abundance of toads - because they prefer open spaces, they are much easier to see than are native frogs (that are smaller, and hide in vegetation most of the time).

toad on highway

2007

Phillips, B. L., G. P. Brown, M. Greenlees, J. K. Webb, and R. Shine. 2007. Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia. Austral Ecology 32:169-176.

We radio-tracked toads at the invasion front (on the Adelaide River floodplain), by putting small waistbands on the toads and attaching miniature transmitters. Then, Greg was able to go out and locate the toads every day. This is a really useful method, because otherwise the toads are pretty much invisible within the landscape unless they gather beside a pool to start breeding. The tracking showed that the toads move quite amazing distances, and in incredibly consistent directions. We also mapped the advance of the toad front through Kakadu and towards Darwin, and found very similar rates of progress of the front as estimated by the radio-tracking. This is probably one of the most astonishing results from our fieldwork: the invasion-front toads move hundreds of metres every night, an incredible achievement for a small amphibian. Of course, this makes the front almost impossible to stop - if you miss even a single toad, it will be many kilometres past you within a few weeks or perhaps, in a few days.



2008

Urban, M., B. L. Phillips, D. K. Skelly, and R. Shine. 2008. A toad more traveled: the heterogeneous invasion dynamics of cane toads in Australia. American Naturalist 171:E134-E148.

How fast have cane toads traveled through Australia since their release in 1935, and why have they moved more quickly through some areas than others? We have incredibly detailed information about the rate that toads have spread, because people really notice toads and so, have been able to record when they turn up. We put all this information together with data on climates and landforms etc, to try to work out what factors affect toad invasion speeds. The biggest factor turns out to be the gradual acceleration of the toad front through time - they have evolved to disperse more rapidly (with longer legs and different behaviours) and thus move westwards about five times faster than in the early years of toad invasion.

lots of toads

Phillips, B. L., G. P. Brown, J. M. J. Travis, and R. Shine. 2008. Reid's paradox revisited: the evolution of dispersal kernels during range expansion. American Naturalist 172:S34-S48.

There is lots of recent interest in the effects of climate change, and one interesting issue is how quickly animals and plants could move across the landscape to colonise a newly-available area. This happened after the last Ice Age, for example, as glaciers retreated - how quickly could plants and animals move into the new space? Many years ago, Reid noticed a puzzle - species seemed to move much faster than we would expect from the rates that we measure animals and plants dispersing under today's conditions. We show, with some mathematical modeling and studies on movements of radio-tracked toads, that the answer lies in the amount of variation in movement distances. Toads at the invasion front have more variable movement distances per day, and this allows some of them to move much further than we would expect from the "average" values.

Shilton, C. M., G. P. Brown, S. Benedict, and R. Shine. 2008. Spinal arthropathy associated with Ochrobactrum anthropi in free-ranging cane toads (Chaunus [Bufo] marinus) in Australia. Veterinary Pathology 45:85-94.

In other work, we showed that the cane toad invasion front has moved faster and faster across tropical Australia, due to rapid evolutionary changes. Our radio-tracking has confirmed incredible rates of dispersal in invasion-front toads - often more than a kilometer in a single night. How can a toad move so far? Wouldn't this put extreme pressure on their bodies - after all, toads look to be built for comfort not for speed, and no other frog species worldwide moves so far and so fast. Sure enough, the invasion-front toads are paying a price - many of them develop severe spinal arthritis, reflecting their inability to stop a common bacteria from infecting their spinal joints.

toad on road

2009

Alford, R. A., G. P. Brown, L. Schwarzkopf, B. Phillips, and R. Shine. 2009. Comparisons through time and space suggest rapid evolution of dispersal behaviour in an invasive species. Wildlife Research 36:23-28.

In previous work, we showed that cane toads are moving faster and faster through tropical Australia, and that one of the reasons for that acceleration is the evolution of longer legs (that enable toads to move quicker). But of course, how fast a cane toad can disperse depends on its behaviour as well as its running speed. Fortunately, Ross Alford and Lin Schwarzkopf had radio-tracked cane toads in Queensland several years ago, so we were able to combine our results with theirs to see what behaviours have changed over the course of the toads' Australian invasion. As we expected, the invasion-front toads move a lot further every day, and tend to move whenever conditions are suitable - whereas the Queensland toads end up staying a lot closer to home.

 

White, A. W., and R. Shine. 2009. The extra-limital spread of an invasive species via "stowaway"dispersal: toad to nowhere? Animal Conservation 12:38-45.

Working closely with a community group in Sydney, we have examined records of cane toads that have found their way outside the main range. It turns out that most of these toads have hitched a ride with building and landscaping materials - and that the numbers of adult toads reaching Sydney are very high. Clearly, we need to be doing something about cutting down the numbers of hitch-hikers, to prevent toads expanding their range even more rapidly than they are already achieving.

toad in brick

2011

Shine, R., G. P. Brown, and B. L. Phillips. 2011. An evolutionary process that assembles phenotypes through space rather than time. Proceedings of the National Academy of Sciences USA 108:5708-5711 (selected by ‘Faculty of 1000’).

Shine, R., G. P. Brown, and B. L. Phillips. 2011. Spatial sorting, assortative mating, and natural selection. Proceedings of the National Academy of Sciences USA 108:E348.

These two papers explore the process that has resulted in cane toads evolving to move faster and faster across tropical Australia. Unlike conventional evolution, that is driven by natural selection, we think that the accelerated toad invasion results from “spatial sorting”. Genes for moving faster and further become concentrated at the increasingly fast-moving invasion front.

spatial sorting fig

2012

Shine, R. 2012. Invasive species as drivers of evolutionary change: cane toads in tropical Australia. Evolutionary Applications 5:107-116.

This paper reviews the evidence that we have gathered about how cane toads in Australia have caused rapid evolutionary change. The changes have occurred in toads themselves, in their parasites, and in the native species with which the toads interact.

Llewellyn, D., M. B. Thompson, B. L. Phillips, G. P. Brown, and R. Shine. 2012. Reduced investment in immune function in invasion-front populations of the cane toad (Rhinella marina) in Australia. Biological Invasions 14:999-1008.

Following on from earlier work where we found that invasion-front toads appear to have weakened immune systems, David actually measured the energy investment into the immune response in cane toads whose parents were collected from a range of areas – some from long-colonised regions, some from the invasion front. As predicted, the invasion-front toads invested less energy into the immune response.

Kelehear, C., G. P. Brown, and R. Shine. 2012. Rapid evolution of parasite life-history traits on an expanding range-edge. Ecology Letters 15:329-337.

Its not just toads and their predators that have evolved – the toads’ parasites also have changed. Crystal showed that parasites from invasion-front toads have larger body sizes in the stages that live outside the host – probably because low numbers of toads at the invasion front make it hard for parasites to find a new host, so they have to live longer in the soil.


2013

Brown, G., C. Kelehear, and R. Shine. 2013. The early toad gets the worm: cane toads at an invasion front benefit from higher prey availability. Journal of Animal Ecology 82:854-862.

Why has the cane toad invasion front accelerated over the time since toads arrived in Australia? One possible explanation is that there has been an evolutionary advantage to the toads that are the first to arrive in an area – perhaps because there is less competition from other toads, and hence more food. Our studies at Fogg Dam confirm that the first toads to arrive did indeed eat more, and grow faster, than the toads that arrived in the same area a few years later.


Lindstrom, T., G. P. Brown, S. A. Sisson, B. L. Phillips, and R. Shine. 2013. Rapid shifts in dispersal behavior on an expanding range edge. Proceedings of the National Academy of Science USA 110:13452-13456.

In earlier studies, we showed that cane toads have invaded faster and faster since they were first released into Australia; and that those changes are due to evolution (that is, offspring inherit their parent’s dispersal speed). But until now, we hadn’t looked at what happens to the dispersal rate of toads as the invasion front passes through. We radio-tracked toads at Fogg Dam for several years after they first arrived, and our analyses reveal that toads were moving a lot further in the first couple of years (at the invasion front) than they have subsequently. The general message from this study is that if we want to understand how quickly a species can spread into new territory, we need to actually measure what happens at the expanding range edge – animals there will probably move a lot quicker and further than we expect from studies of the same species at the range core.

toad with telemetry belt

2014

Brown, G. P., and R. Shine. 2014. Immune response varies with rate of dispersal in invasive cane toads (Rhinella marina). PLoS One 9:e99734.

An invading animal is subject to many new pressures, and its immune system may be directly modified by consistent long-distance movement. Greg tracked toads at Middle Point, and found consistent differences in immune-system function between individuals that dispersed a long way, and those that didn’t move very far.


McCann, S., M. J. Greenlees, D. Newell, and R. Shine. 2014. Rapid acclimation to cold allows the cane toad (Rhinella marina) to invade montane areas within its Australian range. Functional Ecology 28:1166-1174.

Cane toads are spreading into montane regions near the NSW-Queensland border that have been thought to be too cold for these tropical amphibians. How can they do it? Sam McCann showed that toads in high cold sites select open areas where they can stay warm by basking, and that their physiology shifts rapidly when they are exposed to cold. Even a few hours at low temperatures enables a toad to function well at those temperatures. These results suggest that cane toads may be able to spread further south in Australia than has been predicted by previous studies.


Brown, G. P., B. L. Phillips, and R. Shine. 2014. The straight and narrow path: the evolution of straight-line dispersal at a cane-toad invasion front. Proceedings of the Royal Society (London) B 281:20141385.

Our radio-tracking studies showed that toads in the invasion path tend to keep on moving in the same direction day after day. This enables them to disperse much further than if they moved in a more meandering path (as do toads from long-colonised areas in Queensland). We bred toads from different areas and raised their offspring under standard conditions at our field station near Darwin. After they reached adult size, we released and radio-tracked these progeny. Remarkably, the offspring of invasion-front toads were just as directional in their movements as their parents had been, whereas the offspring of Queensland toads resembled their own meandering parents in this respect. So, that heritability shows that we are looking at a case of genuine evolutionary change, not just an effect of the local environment. Toads at the invasion front really ARE different!


2015

Brown, G. B, B. L. Phillips, S. Dubey, and R. Shine. 2015. Invader immunology: invasion history alters immune-system function in cane toads (Rhinella marina) in tropical Australia. Ecology Letters 18:57-65.

An animal at the forefront of an invasion experiences many stresses – it is heading into unknown country, with new challenges, and moving long distances every day. We show that even when we look at progeny that have been raised under standard conditions, the immune systems of toads have been altered by invasion. Animals from the invasion front have very different kinds of immune responses than animals from long-colonised areas. This paper adds to our conclusion that toads in Australia exhibit very rapid evolutionary changes.


Brown, G. P., B. L. Phillips, and R. Shine. 2015. Directional dispersal has not evolved during the cane toad invasion. Functional Ecology 29:830-838.

By breeding cane toads from different areas at our field station near Darwin, we have shown that the toads have rapidly evolved characteristics (changes in shape, physiology, behaviour etc) that enable them to invade more rapidly into new areas. We thought that perhaps the toads have evolved to disperse in a westerly direction (since that is the way the front has been expanding for 80 years) but in fact, this hasn’t happened. The offspring of invasion-front (Northern Territory) toads are no more likely to travel westwards than the offspring of Queensland toads.


Rollins, L. A., M. F. Richardson, and R. Shine. 2015. A genetic perspective on rapid evolution in cane toads. Molecular Ecology 24:2264-2276.

From 101 cane toads brought to Australia in 1935, the toad population has expanded massively, and evolved rapidly to become more effective invaders. How have they done this, starting from such limited genetic variation? This paper explores some of our recent results on gene expression in toads from different parts of Australia.


Chan, M., R. Shine, G. P. Brown, and P. S. Kim. 2015. Mathematical modelling of spatial sorting and evolution in a host-parasite system. Journal of Theoretical Biology 380:530-541.

Why have toads evolved to disperse more and more rapidly across Australia? In this paper we use mathematical models to tease apart some of the evolutionary processes at work in that acceleration.


Brown, G. P., C. Kelehear, C. M. Shilton, B. L. Phillips, and R. Shine. 2015. Stress and immunity at the invasion front: a comparison across cane toad (Rhinella marina) populations. Biological Journal of the Linnean Society 116:748-760.

Invading new territory is stressful; how has it affected toad immune systems? Our surveys revealed a complex pattern with populations of toads from different areas showing quite different types of immune responses.


Hudson, C. H., B. L. Phillips, G. P. Brown, and R. Shine. 2015. Virgins in the vanguard: low reproductive frequency in invasion-front cane toads. Biological Journal of the Linnean Society 116:743-747.

Stopping to reproduce slows you down and takes away energy that you could otherwise spend on dispersing. As a result, cane toads at the invasion front rarely reproduce – even after we catch them and keep them in standardised conditions at our field station.


2016

Ducatez, S., M. Crossland, and R. Shine. 2016. Differences in developmental strategies between long-settled and invasion front populations of the cane toad in Australia. Journal of Evolutionary Biology 29:335-343.

Even when they are raised under standard conditions in the laboratory, the tadpoles of toads from Queensland and Western Australia respond very differently to the stress of reduced food availability or higher densities of other tadpoles. Broadly, the Western Australian tadpoles are more sensitive.


Hudson, C. M., G. P. Brown, and R. Shine. 2016. It is lonely at the front: contrasting evolutionary trajectories in male and female invaders. Royal Society Open Science 3:160687.

The body shapes of cane toads have evolved as the species has spread across Australia. One shift involves the degree of sexual difference in body shape. Male and female toads started out having quite different leg lengths relative to body length, but 80 generations of a footrace across the tropics has largely eliminated that sex difference.


Pettit, L., M. J. Greenlees, and R. Shine. 2016. The behavioural consequences of translocation: how do invasive cane toads (Rhinella marina) respond to transport and release to novel environments? Behavioral Ecology and Sociobiology 71:1-14.

One frequent way that toads reach new areas in Australia is by hitching a ride with produce or landscaping materials on trucks. How does that translocation affect a toad’s behaviour when it arrives at its new home? Lachlan looked in detail at this question by experimentally moving toads around, and he found major effects.


Hudson, C. M., M. R. McCurry, P. Lundgren, C. R. McHenry, and R. Shine. 2016. Constructing an invasion machine: the rapid evolution of a dispersal-enhancing phenotype during the cane toad invasion of Australia. PLoS One 11:e0156950.

Cam used high-tech 3D imaging methods to look at how toad skeletons have changes during the toads’ Australian invasion. Many components of the toad body have changed dramatically, from limb sizes to head shapes. It’s a case of remarkably rapid evolutionary change.


Hudson, C. M., G. P. Brown, and R. Shine. 2016. Athletic anurans: the impacts of morphology, ecology and evolution on climbing ability in invasive cane toads. Biological Journal of the Linnean Society 119:992-999.

Cane toads don’t look very athletic, but we have found them climbing cliffs and even bushes. Toads from some areas do this more often than toads from other areas. Our tests in the lab showed that males are better climbers than females (probably because they have longer limbs), but that the geographic variation in climbing ability is likely to be the result of learning not genetics.


Lillie, M., J. Cui, R. Shine, and K. Belov. 2016. Molecular characterization of MHC class II in the Australian invasive cane toad reveals multiple splice variants. Immunogenetics 68:449-460.

This genetics analysis clarifies the mechanisms involved in the shifting pattern of immune-system function within invasive cane toads.


Pettit, L. J., M. J. Greenlees, and R. Shine. 2016. Is the enhanced dispersal rate seen at invasion fronts a behaviourally plastic response to encountering novel ecological conditions? Biology Letters 12:20160539.

Cane toads in Western Australia disperse almost ten times faster than toads in Queensland. Could this be due, at least partly, to the toads encountering novel conditions? By translocating toads in NSW, Lachlan found that a toad released in an unknown area massively increases its rate of dispersal.


2017

Gruber, J., G. P. Brown, M. Whiting, and R. Shine. 2017. Geographic divergence in dispersal-related behaviour in cane toads from range-front versus range-core populations in Australia. Behavioral Ecology and Sociobiology 71:38.

Jodie measured the behaviour of toads in standard laboratory trials, and found that toads from the invasion front in Western Australia were bolder and more active than toads from long-colonised areas in Queensland. Bold exploratory behaviour probably helps an invasion-front toad to boldly go where no toad has gone before.


Pizzatto, L., C. Both, G. P. Brown, and R. Shine. 2017. The accelerating invasion: dispersal rates of cane toads at an invasion front compared to an already-colonised area. Evolutionary Ecology 31:533-545.

In science, it’s a good idea to replicate studies in different places to check the generality of previous results. We already knew that when the toads reached Darwin they were dispersing much faster than they had earlier in the invasion, in Queensland. Several years later Ligia radio-tracked toads in Western Australia, and showed the same result. Toads at the invasion front consistently disperse much faster than toads in long-colonised regions.


Pettit, L., M. Greenlees, and R. Shine. 2017. The impact of transportation and translocation on dispersal behaviour in the invasive cane toad. Oecologia 184:411-422.

How does translocation (say, on a truck) affect the behaviour of a toad that finds itself in a new home? Lachlan’s study showed that those effects depend both on translocation alone, and on the amount of stress involved in the transport process.


Kosmala, G., G. P. Brown, K. Christian, and R. Shine. 2017. Locomotor performance of cane toads differs between native-range and invasive populations. Royal Society Open Science 4:170517.

Under standard conditions, cane toads from Australian populations have much higher locomotor ability than the same species from South America (their native home) or Hawai’i (a stepping-stone population for the Aussie toads).


Hudson, C. M., G. P. Brown, and R. Shine. 2017. Evolutionary shifts in anti-predator responses of invasive cane toads (Rhinella marina). Behavioral Ecology and Sociobiology 71:134.

A cane toad’s response to “attack” by a predator differs depending on where the toad comes from; and offspring tend to inherit the responses of their parents.


Cane toad research photo credits: Christa Beckmann, Haley Bowcock, Greg Brown, Elisa Cabrera-Guzman, Travis Child, Michael Crossland, Matthew Greenlees, Mattias Hagman, Crystal Kelehear, John Llewelyn, David Nelson, Stephanie O'Donnell, Ben Phillips, Ligia Pizzatto, Sam Price-Rees, Cathy Shilton, Ruchira Somaweera, Peter Street, Georgia Ward-Fear, Jonathan Webb