It’s Not Easy Being Mean

Credit: Kuhnmi

Phyllobates terribilis, The world’s most toxic frog. Credit: Kuhnmi

Venomous and poisonous animals capture the imagination of people across the globe. Whether through fear or fascination, toxic creatures (epitomised by reptiles and amphibians) have long been the object of interest amongst the public and scientists alike. This has lead to an incredible body of research on the benefits to individuals of having a chemical arsenal, often obvious such as avoiding meeting a grisly end in a predator’s stomach or catching prey of your own, and the consequences of those unlucky enough to be on the receiving end of a powerful defence which may leave an unfortunate human paralysed, rotting alive, or just plain dead. But, perhaps surprisingly, we have only recently begun to understand what having such weaponry means for the bigger picture: the ecology, evolution, and even conservation of species.

My work as an evolutionary biologist (and keen herpetologist) at the University of Liverpool has tried to provide an insight into these large-scale consequences of using chemical antipredator defences such as venoms and toxins. I specialise in using ‘phylogenies’ (or ‘phylogenetic trees’), which are essentially like family trees showing the relationships between different species. The reason they are so great is that they represent the evolutionary history of a group of species, the context in which everything about them has evolved, and capture information on the time at which events in their history happened too. When combined with lots of data (often gathered from published sources), phylogenies can let me get to the heart of big questions on big datasets across big time scales. I use phylogenies for all sorts of things, but for now I want to talk about the impact that chemical defences can have on the animals that possess them.

Ecology

First up, a confession. This part of my work was on mammals, not herptiles, but it did give me some good ideas to test on an even bigger scale in amphibians, so that’s my excuse! Second confession. This bit wasn’t on toxic defence as such, but on really smelly things, though these are still enough to get rid of a predator and still use chemicals so I’m going to count them. Anyway, why would we expect chemical defence to influence the ecology of a species?

Imagine a skunk wandering through the woods, minding its own business and chomping away on some yummy berries. Now imagine a cougar appearing from between the trees looking for a tasty meal. Now realise this exact situation has happened, as shown in this photo taken from a series captured by a camera trap in Alberta, Canada.

Credit: Waterton Lakes National Park/Parks Canada

Credit: Waterton Lakes National Park/Parks Canada

What actually happened here was that the cougar approached, the skunk did a handstand to advertise the fact that it’s a skunk, and the cougar (wisely) moved off elsewhere. The skunk could then get on with eating dinner. Many other prey animals would have had to run off and hide to avoid being eaten, and while that’s good in some ways (if you’re hiding you can’t be eaten), it does mean that you’re wasting valuable time that could be spent looking for food, or mates, or whatever else takes your fancy. The skunk on the other hand doesn’t have to worry so much about predators and can carry on feeding as a result of being too well defended for predators to mess with.

So if this situation is common, we might think that species with smelly anal glands that are discharged in defence against a predator might be able to exploit more of their environment. If you look at all sorts of ecological traits in the group of mammals called ‘musteloids’ (things like skunks, badgers, otters, raccoons, etc.), that’s exactly what you find. In my research, it turns out that species like skunks tend to have a broader diet and activity period (not restricted to either the day or the night) than species without such a defence. Along with other traits, this agrees with our idea that chemical defences can broaden the ecological niche of the species lucky enough to have them, perhaps even making them better able to compete with other species or exist where others can’t.

Evolution

At one level, evolutionary history can be thought of as a mix of speciation (formation of new species) and extinction events that combine to leave the diversity of life we see around us today. But not all species or, over longer time scales, ‘lineages’ (branches in the tree of life) are equally likely to form new species or go extinct, and the traits they possess can be important in deciding who lives and who dies. We have just discussed how chemical defences can lead to a wider range of ecological opportunities, but they are also inherently a trait involved in what are called ‘arms races’.

In arms races, we have each side desperately trying to overtake the other on the battlefield and this leads to a constantly adapting set of armaments. The same works in nature. Imagine a frog that evolves a potent toxin. This works well, but it gives predators an advantage if they can avoid this toxin (e.g. by evolving resistance or specialist behaviours) and eat that frog, because most other predators can’t. This then leads to an advantage to frogs that can evolve a way to get past this resistance, and the cycle continues. This situation is often likened to a quote by the Red Queen in Lewis Carroll’s novel Through the Looking Glass: “It takes all the running you can do, to keep in the same place”. In other words, predators and prey are constantly driving each other’s evolution but they never quite get the upper hand and ‘escape the race’.

Alice-Red-Queen

Why is this relevant? Well, it turns out that both increased ecological opportunity and arms race scenarios have long been thought to drive speciation. We would expect then that species with a chemical defence should experience evolutionary radiations, which are characterised by what is called ‘diversification rates’ (or the number of speciation events in a given time period minus the number of extinction events). I figured that amphibians provide a great opportunity to test this, because there are a lot of them, we know the evolutionary history for the group reasonably well, and there are lots of species that have a chemical antipredator defence (often poisons) and lots that don’t. I set about collecting as much data as possible from published sources and fit all sorts of complicated models (the mathematical kind not the artistic kind). This in essence is like assuming lots of different scenarios, describing those using equations, and then we can ask which model (or scenario) best explains the data.

In part, the initial idea was supported – toxic amphibians had much higher rates of speciation than those without a chemical defence. But it also turns out to be a bit more complicated than that. Not only do they have higher speciation rates, but they also have higher extinction rates. In other words, toxic amphibians might be more likely to form new species, but they are also even more likely to go extinct! When you work out the overall diversification rate, you find that extinction is affected more as chemically-defended amphibians have a lower diversification rate as a whole. This is bad. We still don’t fully understand why, but it is still bad. What makes it worse is that we also found that toxins are very easily (and are frequently) gained, but are actually surprisingly difficult to lose again. This makes sense because poisonous defence is great for an individual frog – predators can’t eat it – but it also means than once toxins are gained the animals are effectively ‘locked’ into a scenario that may spell doom for their lineage.

This was an unexpected but an interesting result and one that deserves further study.

Conservation

I suppose it’s obvious where we’re going with this now. If amphibians with a chemical defence are more likely to go extinct over evolutionary time, does the same thing hold in the present-day? Well, ongoing work suggests the answer is yes! Amphibians are, as most people are aware, highly threatened across the world and are in fact the most severely threatened group of vertebrates. One way to assess the current extinction risk of species is using the criteria devised by the IUCN in its Red Data Book, in which it assigns a conservation status (such as ‘endangered’, ‘critically endangered’, and ‘least concern’) to as many species as possible. What my research is beginning to show is that the results from my analyses on the evolution of amphibians can tell us something about modern extinction risk too. It seems that toxic amphibians are indeed more likely to be threatened than those without such a defence against predators. This might help to explain why so many of the iconic poison dart frogs (such as that pictured below) are faced with such a dire situation. In any case, it shows that how an animal protects itself can have important consequences for the future of its species, and that the venomous and poisonous animals, that inspire fear in so many people, deserve, and may even need, our care and attention. If not, some of the most beautiful creatures on the planet may be lost before our very eyes.

Phylobates

Credit: Kevin Arbuckle

profile picAbout the Author: Kevin is an evolutionary biologist at the University of Liverpool, working on a range of subjects including the evolution of venomous and poisonous animals. He obtained a masters degree in zoology from the University of Glasgow (working on projects such as the evolution of coral snake coloration and the efficacy of gut-loading as a part of captive feeding) and is just finishing a PhD at the University of Liverpool on the macroevolution of antipredator defences and convergent evolution. He makes frequent use of phylogenetic comparative methods but has wide-ranging research interests and has also worked on exotic animal husbandry, reproductive behaviour and life-history evolution, and the evolution of intelligence.  You can follow Kevin on Twitter here.

Image credits:

Kuhnmi’s Flickr stream. Photo used under license.

Waterton Lakes national Park Canada.

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